![Worldwide distribution and species diversity of Dysphanieae (green = Dysphania [incl. Cycloloma], blue = Neomonolepis, lilac = Suckleya, beige = Teloxys). Species numbers refer to species currently known. Only native species and native areas are included.](https://www.researchgate.net/profile/Pertti-Uotila/publication/349985630/figure/fig1/AS:1000592918974464@1615571350097/Worldwide-distribution-and-species-diversity-of-Dysphanieae-green-Dysphania-incl_Q320.jpg)
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Phylogeny, biogeography and systematics of Dysphanieae
(Amaranthaceae)
Pertti Uotila,
1
Alexander P. Sukhorukov,
2,3
Nadine Bobon,
4
John McDonald,
5
Anastasiya A. Krinitsina
2,6
& Gudrun Kadereit
7
1Botany Unit, Finnish Museum of Natural History, University of Helsinki, 00014 University of Helsinki, Finland
2Department of Higher Plants, Biological Faculty, Lomonosov Moscow State University, 119234, Moscow, Russia
3Laboratory Herbarium (TK), Tomsk State University, Lenin St. 36, 634050, Tomsk, Russia
4Institut für Entwicklungsbiologie und Neurobiologie der Johannes Gutenberg-Universität Mainz, 55128 Mainz, Germany
5Discipline of Ecology and Evolutionary Biology, School of Biological Sciences, University of Adelaide, Adelaide, 5005 Australia
6I.M. Sechenov First Moscow State Medical University, Pharmaceutical Natural Science Department, Izmailovsky Boulevard
8, 105043, Moscow, Russia
7Lehrstuhl für Systematik, Biodiversität & Evolution der Pflanzen, Ludwig-Maximilians-Universität München, Menzinger Str.
67, 80638 München, Germany
Address for correspondence: Pertti Uotila, pertti.uotila@helsinki.fi
DOI https://doi.org/10.1002/tax.12458
Abstract After a rather turbulent taxonomic history, Dysphanieae (Chenopodioideae, Amaranthaceae) were established to contain
five genera, four of which are monospecific (Cycloloma,Neomonolepis,Suckleya,Teloxys) and geographically restricted, and the fifth
genus, Dysphania, having a nearly worldwide distribution and comprising ca. 50 species. This study investigates the phylogeny, bio-
geography and taxonomy of Dysphanieae. We studied specimens from 32 herbaria to infer morphological differences and distribution
areas of the species and sampled 121 accessions representing 39 accepted species of the tribe for molecular phylogenetic analyses. The
molecular phylogeny tested generic relationships of the tribe and infrageneric relationships of Dysphania on the basis of two plastid
DNA markers (atpB-rbcL spacer, rpl16 intron) and two nuclear ribosomal markers(ETS, ITS) and was also used for an ancestral area
reconstruction with BioGeoBEARS. Three of the monospecific genera (Neomonolepis,Suckleya,Teloxys) form a basal grade and
appear to be relictual lineages of the tribe, while Cycloloma is nested within Dysphania. The ancestral area reconstruction favors a
widespread ancestry for Dysphanieae, and the relictual lineages in Asia (Teloxys) and North America (Neomonolepis,Suckleya) might
be explained by a wide distribution across Beringia during the Late Oligocene/Early Miocene. Dysphania likely originated in North
America; however, the simultaneous diversification into three major clades, an Asian/African, an American and an Australian/African
clade, indicates a widespread ancestor at the crown node of Dysphania. Our taxonomic revision results in four accepted genera in
Dysphanieae, Dysphania,Neomonolepis,Suckleya and Teloxys. The sectional subdivision for Dysphania is revised. We subdivide
the genus into five sections, D. sect. Adenois (13 spp.), D. sect. Botryoides (10 spp.), D. sect. Dysphania (17 spp.), D. sect. Incisa
(2 spp.) and D. sect. Margaritaria (4 spp.); three strongly deviating species remain unplaced and need further attention.
Keywords Cycloloma;Dysphania; infrageneric classification; long-distance dispersal; molecular clock; molecular phylogeny;
Neomonolepis;Suckleya; taxonomy; Teloxys
Supporting Information may be found online in the Supporting Information section at the end of the article.
■INTRODUCTION
Dysphanieae is a tribe of subfam. Chenopodioideae be-
longing to the now widely circumscribed Amaranthaceae (incl.
Chenopodiaceae: Morales-Briones & al., 2020). According to
extensive molecular studies, it includes the genus Dysphania
R.Br. and four monotypic genera: Cycloloma Moq., Neomo-
nolepis Sukhor., Suckleya A.Gray and Teloxys Moq. (Kadereit
& al., 2010; Fuentes-Bazan & al., 2012a,b; Sukhorukov & al.,
2018a). The vast majority of the members of Dysphanieae
were previously part of Chenopodium L. s.l., with many spe-
cies transferred from Chenopodium to Dysphania by Mosya-
kin & Clemants (2002, 2008), Verloove & Lambinon (2006)
and Uotila (2013). Further investigations based on morpho-
logical and carpological data allowed the description of new spe-
cies of Dysphania from the Himalayas and Tibet (Sukhorukov,
2012b, 2014; Uotila, 2013; Sukhorukov & al., 2015), and
Australia (Dillon & Markey, 2017), and to confirm or contradict
Article history: Received: 18 Jun 2020 | returned for (first) revision: 4 Aug 2020 | (last) revision received: 30 Nov 2020 | accepted: 3 Dec 2020
Associate Editor: Levent Can | © 2021 The Authors.
TAXON published by John Wiley & Sons Ltd on behalf of International Association for Plant Taxonomy.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,
provided the original work is properly cited.
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TAXON 00 (00) •1–26 Uotila & al. •Systematics of Dysphanieae
SYSTEMATICS AND PHYLOGENY
the species status of some taxa (Sukhorukov & al., 2018b,
2019a,b). To date, Dysphania is one of the largest genera in
Chenopodioideae, comprising ca. 50 species (Sukhorukov
&al.,2018b).
Dysphanieae is geographically widespread on all conti-
nents excluding Antarctica, with predominant distribution in
the subtropics and tropical mountainous deserts (Fig. 1). The
greatest species diversity, all Dysphania, is in Australia and
New Zealand with 17 native and three naturalized species
(Wilson, 1984; Shepherd & Wilson, 2008). In North America,
there are seven native species in four genera, including the
monospecific Cycloloma (Mosyakin, 2003), Neomonolepis
(Holmgren, 2003, as part of Monolepis)andSuckleya (Chu,
2003), and eight naturalized species in two genera, including
Teloxy s (Clemants & Mosyakin, 2003). In South America (plus
Tristan da Cunha), there are at least 12 native species and three
aliens (including Cycloloma) documented (Aellen, 1973; Simón,
1996; Múlgura & Marticorena, 2008). The centre of diversity of
Dysphania in Asia has been recently revealed in the Himalayas
and Tibet, where eight native and two alien species occur
(Uotila, 2013; Sukhorukov, 2014; Sukhorukov & Kushunina,
2014; Sukhorukov & al., 2015); in addition, one native species
is widespread in South-West Asia (Uotila, 2013), and two more
aliens have been reported from Iran (Rahiminejad & al., 2004),
Japan (Clemants, 2006) and India (Ramayya & Rajagopal,
1969; Ravi & Anilkumar, 1990). Teloxys is widespread in the
deserts of Central Asia, with many records in temperate Eurasia
(e.g., Iljin & Aellen, 1936; Grubov, 1966; Sukhorukov, 2014).
From the Arabian Peninsula, only three native and two intro-
duced species are mentioned by Boulos (1996). The number
of species given for Africa is relatively low: five native and four
introducedspecies (three native and three introduced species in
tropical Africa: Brenan, 1954; Lebrun & Stork, 1991; Friis &
Gilbert, 2000; Sukhorukov & al., 2018b; one native and two
introduced species in North Africa: Dobignard & Chatelain,
2011). Europe is the region poorest in native species including
only Dysphania botrys (L.) Mosyakin & Clemants, but with a
number of other Dysphanieae (Cycloloma,Dysphania,Teloxys)
naturalized to at least some degree (Aellen, 1960; Uotila, 2001,
2011; Sukhorukov, 2014).
Almost all morphological characters of Dysphanieae
(Fig. 2) are similar to many other members of Chenopodioi-
deae; e.g., flat leaves, thyrsoid inflorescences, mostly three
to five free or more or less fused perianth segments, short
(0.2–0.3 mm) anthers, thin parenchymatous pericarp, subglo-
bose to lenticular seeds with copious perisperm and usually
annular embryo. However, most Dysphanieae, i.e., the species
of Dysphania, are known to produce glandular white hairs
and/or yellow or orange subsessile glands; these glands con-
tain essential oils that provide a characteristic aromatic odour,
often persisting in herbarium specimens for years. Four other
genera, Cycloloma,Neomonolepis,Suckleya and Teloxys, are
reported to lack such glands or glandular hairs, but Suckleya
and Teloxys bear papillae that are rare in almost all other
Chenopodioideae (Reimann & Breckle, 1988; Simón, 1997;
Sukhorukov, 2012a, 2014). Pollen morphology is relatively
Fig. 1. Worldwide distribution and species diversity of Dysphanieae (green = Dysphania [incl. Cycloloma], blue = Neomonolepis, lilac = Suckleya,
beige = Teloxys). Species numbers refer to species currently known. Only native species and native areas are included.
2Version of Record
Uotila & al. •Systematics of Dysphanieae TAXON 00 (00) •1–26
uniform in all Chenopodioideae, and species of Dysphanieae
and Chenopodieae fall into the same group (e.g., Perveen
& Qaiser, 2012). Mosyakin & Tsymbalyuk (2004) studied pol-
len of nine species of Dysphanieae and observed that pollen
grains in Dysphania are morphologically rather uniform, but
some species and groups of species can still be distinguished
by their pollen morphology. Although Dysphania shares the
same floral histogenesis with Chenopodieae (Mahabale &
Solanky, 1954; Eckardt, 1967, 1968), a set of reproductive
characters of Dysphanieae in its recent circumscription differ-
entiates it from almost all other Chenopodioideae (Fuentes-
Bazan & al., 2012b). Fruits and seeds of Dysphanieae are dis-
tinguished by different hairs and papillae (if present) on the
pericarp surface and absence of cell wall stalactites in the exo-
testal layer of the seed coat (Sukhorukov & Zhang, 2013).
Two basic chromosome numbers have been reported for
Dysphanieae, x= 8 and x=9. Both Suckleya suckleyana
(Torr.) Rydb. (Bassett & Crompton, 1970) and Teloxys aristat a
(L.) Moq. (e.g., Probatova & al., 2004; Ankova & Zykova,
2018) have x= 9 and are diploids with 2n=18.Cycloloma atri-
plicifolium (Spreng.) J.M.Coult. is reported to have a tetraploid
number 2n= 36 (Löve & Löve, 1982).
Fig. 2. Representative species of Dysphanieae. A, Population of Cycloloma atriplicifolium;B, Detail of the infructescence of C. atriplicifolium;
U.S.A., Indiana Dunes State Park, 25 August 2012, M. Huft; C,Dysphania ambrosioides; India, Uttarakhand State, Dehradun, February 2017,
A. Sukhorukov (reproduced by the written permission of PhytoKeys Editorial Office); D,D. graveolens; Mexico, Teotihuacan, September 2018,
A. Sukhorukov; E,D. multifida; U.S.A., California, 2004, J. DiTomaso; F,D. neglecta; Nepal, Mid-West, Mugu Distr., September 2013,
A. Sukhorukov; G,D. pumilio; Switzerland, Geneva, October 2019, P. Uotila; H,Suckleya suckleyana; Canada, Alberta Prov., Fort Macleod,
21 August 2005, R. Bielesch; I,Teloxys aristata; Russia, Irkutsk Prov., August 2017, E. Bayandina.
Version of Record 3
TAXON 00 (00) •1–26 Uotila & al. •Systematics of Dysphanieae
As to Dysphania, only small numbers of taxa have been
studied, and, in addition, single counts only are available of
several taxa. Further, misidentifications are common, and so-
matic polyploidy is possible (see Palomino & al., 1990), so
the figures should be interpreted with caution, and not all
reports have been accepted below. Most counts from Ameri-
can Dysphania species show the basic number x= 8. The tet-
raploid number 2n= 32 has been reported for D. multifida (L.)
Mosyakin & Clemants and D. ambrosioides (L.) Mosyakin &
Clemants (Grozeva & Cvetanova, 2013 and references therein),
D. chilensis (Schrad.) Mosyakin & Clemants (Voroshilov,
1942), D. venturii (Aellen) Mosyakin & Clemants (Giusti,
1988) and for D. graveolens (Willd.) Mosyakin & Clemants
(e.g., Giusti, 1970; Keener, 1970). The octoploid number
2n= 64 has been counted for D. anthelmintica (L.) Mosyakin
& Clemants (Voroshilov, 1942; Kawatani & Ohno, 1950) and
D. retusa (Juss. ex Moq.) Mosyakin & Clemants (Giusti,
1970). However, several counts indicate x= 9: the tetraploid
number 2n=36forD. multifida from Bulgaria (Grozeva &
Cvetanova, 2013) and the hexaploid number 2n=54for
D. mandonii (S.Watson) Mosyakin & Clemants (Giusti, 1970).
Reliable diploid counts do not seem to exist of American taxa.
Numerous counts of the Eurasiatic D. botrys and African/
Arabian D. schraderiana (Schult.) Mosyakin & Clemants
resulted in x=9and2n= 18 (e.g., Grozeva & Cvetanova, 2013
and references therein). A report of D. procera (Hochst. ex
Moq.) Mosyakin & Clemants from Africa gives the tetraploid
number 2n= 36 (Auquier & Renard, 1975). The two studied
Australian species are diploids, with both x= 8 and x=9
reported: D. pumilio (R.Br.) Mosyakin & Clemants with 2n=
16 (Giusti, 1970; Keener, 1974) and 2n=18 (many recent
counts, e.g., Rahiminejad & al., 2004; Grozeva & Cvetanova,
2013), and D. carinata (R.Br.) Mosyakin & Clemants with
2n= 16 (Kawatani & Ohno, 1962).
Some species of Dysphania produce secondary metabo-
lites that play a role for human health, albeit in very different
ways. Dysphania ambrosioides (Mexican tea), for example,
contains essential oils used as tea, spice or in traditional medi-
cine with numerous applications (e.g., Boutkhil & al., 2009
and references therein). Ascaridol is a major component of
the essential oil and shows amoebicidal activity (Ávila-Blanco
& al., 2014). Dysphania botrys is a traditional as well as a
potentially new medicinal plant that might be explored for can-
cer treatment (Morteza-Semnani, 2015). Other species of Dys-
phania,D. glomulifera (Nees) Paul G.Wilson and D. littoralis
R.Br., were shown to contain high concentrations of cyanid
(McKenzie & al., 2007). The concentration in Dysphania
plants, especially during dry seasons, is high enough to kill cat-
tle and sheep after consuming less than 200 g of fresh plant
(McKenzie & al., 2007).
Taxonomic history of Dysphania and related genera. —
Dysphania was described by Robert Brown as a genus “related
to chenopods”and consisted of one species, D. littoralis (Brown,
1810). Simultaneously with Dysphania, Brown (1810) des-
cribed a new section Orthosporum R.Br. for Australian spe-
cies of Chenopodium with a vertical seed embryo. Taxa of
Ch. sect. Orthosporum were said to differ from Dysphania in
the number of perianth lobes and stamens. Spach (1836) em-
phasised the aromatic odour of certain chenopods and placed
them in two genera, Ambrina Spach and Botrydium Spach.
In Moquin-Tandon (1840), the “hairy”taxa of the tribe Anser-
ineae were recognized as several genera, such as Ambrina,
Cycloloma and Roubieva Moq., but none of the “hairy”species
was included in Chenopodium. However, Moquin-Tandon
(1840) did not mention Australian taxa of Chenopodium sect.
Orthosporum. Later, he regarded seed orientation position as
a key character in the subtribal classification of tribus Cheno-
podieae (≡Anserineae) (Moquin-Tandon, 1849). The genera
with vertical seeds were included in subtribe ‘Bliteae’and those
with horizontal seeds in subtribe ‘Beteae’, independent of the
type of indumentum (Table 1).
The placement of the genus Dysphania has been uncertain
and far from constant (Table 1). Bentham & Hooker (1880)
placed it in Illecebraceae (now a part of extended Caryophylla-
ceae: Greenberg & Donoghue, 2011). Pax (1889) described
Dysphanieae as a tribe of Caryophyllaceae subfam. Alsinoi-
deae and included only Dysphania with three species. Later,
Pax (1927) claimed that Dysphania is intermediate between
Chenopodiaceae and Caryophyllaceae, describing it as a family
on its own, Dysphaniaceae. However, Aellen (1930a) pointed
out that Dysphania has a close relationship to Chenopodium,
and placed Dysphania as a section in Chenopodium, which
already included Ch.sect.Orthosporum from Australia. He
also divided Dysphania into two sections of Chenopodium by
describing a new Ch.sect.Tetrasep al ae Aellen for species with
four sepals, i.e., D.rhadinostachya (F.Muell.) A.J.Scott and
D. inflata (Aellen) A.J.Scott (= D. rhadinostachya subsp.
inflata (Aellen) Paul G.Wilson), and reducing Ch.sect.Dys-
phania to include only the species with three sepals (Aellen,
1930b). He proposed that Ch.sect.Tet ra sepal ae is a link
between Ch.sect.Dysphania and Ch.sect.Orthosporum.
Black (1934) accepted Aellen’s concept, but also raised the
possibility of maintainig Dysphania as a genus that included
the sections Orthosporum and Tetras epalae. However, further
taxonomic development led in an opposite direction: Pax &
Hoffmann (1934) accepted the family Dysphaniaceae. Aellen
(1961) subsequently changed his mind and treated his previ-
ous section at family level. Family status was later rendered
superfluous by Eckardt (1967), who included Dysphania in
Chenopodiaceae and regarded its generic status separate from
Chenopodium as debatable. However, Scott (1978a) again rec-
ognized Dysphania as a separate genus and divided it into three
sections (D.sect.Dysphania,sect.Tetrasepalae (Aellen) A.J.
Scott, sect. Caudatae A.J.Scott) on the basis of the number of
perianth segments and the orientation of the seed embryo. Even
Kühn & al. (1993) accepted Dysphania as a genus in its tradi-
tional delimitation.
The four genera of the Anserineae (Moquin-Tandon, 1840)
were added by Standley (1916), who described one more “glan-
dular-pubescent”genus within Chenopodiaceae, Meiomeria
Standl. Since then, the hairy species were treated in various
ways as separate genera and sections or as a subgenus of
4Version of Record
Uotila & al. •Systematics of Dysphanieae TAXON 00 (00) •1–26
Chenopodium (Table 1). Roubieva and Meiomeria were later in-
cluded in Chenopodium as sections. Cycloloma kept its generic
rank, but was included in subfam. Camphorosmioideae by
Scott (1978b), mainly because of the horizontal wing on the
perianth segments, and was followed by Kühn & al. (1993).
However, Mosyakin (2003) noted that the development of
the wing in Cycloloma seems to be different from the mode
of development of a similar wing (or other appendages) in taxa
of Camphorosmioideae and expressed an opinion that Cyclo-
loma is more closely related to Chenopodium in the broad
sense. Teloxys was sometimes included in Chenopodium as a
subsection or section (e.g., Iljin & Aellen, 1936; Aellen, 1960;
Table 1. Historical overview of classifications in the present Dysphanieae (Amaranthaceae). –Genera and sections belong to Chenopodiaceae tr.
Chenopodieae if not otherwise stated (marked with bold). (Continued to the right on next page.)
Moquin-Tandon,
1840
(Anserineae)
Moquin-Tandon,
1849
Bentham & Hooker,
1880
(Euchenopodieae)
Pax, 1889
(Caryophyllaceae)
Volkens, 1893
(Chenopodiaceae) Standley, 1916
Pax & Hoffmann, 1934
(Dysphaniaceae)
Ulbrich, 1934
(Chenopodioideae)
Dysphania
(Chenopodieae
subtr. ‘Bliteae’)
Dysphania
(Illecebraceae
tr. Pollichieae)
Dysphania
(Caryophyllaceae
subfam. Alsinoideae)
Dysphania
(Dysphaniaceae)
Blitum
sect. Orthosporum
(Chenopodieae
subtr. ‘Bliteae’)
Chenopodium
sect. Orthosporum
Chenopodium
sect. Orthosporum
Chenopodium
[unranked] Carinata
Chenopodium
sect. Orthosporum
Chenopodium
sect. Tetrasepala
Ambrina
sect. Adenoïs
(Anserineae)
Chenopodium
sect. Ambrina
Chenopodium
sect. Ambrina
Chenopodium
[unranked]
Ambrosioidia
Chenopodium
sect. Ambrina
Roubieva
(Anserineae)
Roubieva
(Chenopodieae
subtr. ‘Bliteae’)
Roubieva Roubieva Chenopodium
sect. Roubieva
Cycloloma
(Anserineae)
Cycloloma
(Chenopodieae
subtr. ‘Beteae’)
Cycloloma Cycloloma Cycloloma Cycloloma
Ambrina
sect. Botryoïs
(Anserineae)
Chenopodium
sect. Botryoïs
(Chenopodieae
subtr. ‘Beteae’)
Chenopodium
sect. Botrydium
Chenopodium
sect. Botrydium
Chenopodium
[unranked] Botryes
Chenopodium
sect. Botryoides
Chenopodium
[unranked] Incisa
Meiomeria Meiomeria
Monolepis p.p. Monolepis p.p. Monolepis p.p.
Suckleya
(Atripliceae)
Suckleya
(Atripliceae)
Suckleya
(Atripliceae)
Suckleya
(Atripliceae)
Teloxys
(Anserineae)
Teloxys
(Chenopodieae
subtr. ‘Beteae’)
Chenopodium
[unranked] Aristata
Teloxys
Version of Record 5
TAXON 00 (00) •1–26 Uotila & al. •Systematics of Dysphanieae
Mosyakin, 1993). Furthermore, Moldenke (1946) described a
new genus Neobotrydium Moldenke that was substituted for
the illegitimate name Botrydium, with the single species
N. botrys (L.) Moldenke (≡Dysphania botrys).
Weber (1985) concluded that the glandular taxa of Che-
nopodium should be treated as a separate genus together with
Teloxys, but did not consider Dysphania at all. Wilson (1983),
after carefully studying the Australian species, discussed
again the lack of clear differences between Chenopodium sect.
Orthosporum and Dysphania, but he retained the generic divi-
sion (Wilson, 1984). Later, disagreeing with Weber’s sugges-
tion that sect. Orthosporum should be placed in Teloxys,he
wrote: “I consider the two groups to be generically distinct
and that the American species should be placed in Teloxys
Table 1. Continued from the left from previous page.
Aellen, 1961
(Dysphaniaceae)
Aellen, 1960
(Chenopodiaceae)
Scott, 1978a
(Chenopodieae)
Scott, 1978b
(Camphorosmeae)
Simón, 1996
(Chenopodium
subg. Ambrosia)
Mosyakin &
Clemants, 2002
(Chenopodiaceae)
Zhu & Sanderson,
2017
This study
(Amaranthaceae
tr. Dysphanieae)
Dysphania
(Dysphaniaceae)
Dysphania
sect. Dysphania +
sect. Caudatae
Dysphania
sect. Dysphania
Dysphania
(Neobotrydieae)
Dysphania
sect. Dysphania
Chenopodium
sect. Orthosporum
Chenopodium
subg. Ambrosia
sect. Orthosporum
Chenopodium
subg. Ambrosia
sect. Orthosporum
Dysphania
sect. Orthospora
Chenopodium
sect. Tetrasepala
Dysphania
sect. Tetrasepala
Chenopodium
sect. Ambrina
Chenopodium
subg. Ambrosia
sect. Ambrina
Chenopodium
subg. Ambrosia
sect. Adenois
subsect. Adenois
Dysphania
sect. Adenois
Ambrina
(Neobotrydieae)
Dysphania
sect. Adenois
Chenopodium
sect. Roubieva
Chenopodium
subg. Ambrosia
sect. Roubieva
Chenopodium
subg. Ambrosia
sect. Adenois
subsect. Roubieva
Dysphania
sect. Roubieva
Roubieva
(Neobotrydieae)
Cycloloma Cycloloma
(Camphorosmeae)
Cycloloma
(Neobotrydieae)
Chenopodium
sect. Botryoides
subsect. Botrys
Chenopodium
subg. Ambrosia
sect. Botryoides
subsect. Botrys
Chenopodium
subg. Ambrosia
sect. Botryoides
subsect. Botrys
Dysphania
sect. Botryoides
subsect. Botrys
Neobotrydium
(Neobotrydieae)
Dysphania
sect. Botryoides
Dysphania
sect. Botryoides
subsect. Incisa
Dysphania
sect. Incisa
Chenopodium
subg. Ambrosia
sect. Margaritaria
Chenopodium
subg. Ambrosia
sect. Margaritaria
Dysphania
sect. Margaritaria
Chenopodium
subg. Ambrosia
sect. Meiomeria
Chenopodium
subg. Ambrosia
sect. Meiomeria
unplaced
Monolepis p.p. Monolepis p.p.
(Chenopodieae)
Neomonolepis
Suckleya
(Chenopodieae subtr.
Suckleyinae)
Suckleya
Chenopodium
sect. Botryoides
subsect. Teloxys
Chenopodium
subg. Ambrosia
sect. Botryoides
subsect. Teloxys
Chenopodium
subg. Ambrosia
sect. Botryoides
subsect. Teloxys
Dysphania
sect. Botryoides
subsect. Teloxys
Teloxys
(Neobotrydieae)
Teloxys
6Version of Record
Uotila & al. •Systematics of Dysphanieae TAXON 00 (00) •1–26
and the Australian in Dysphania (or Dysphania and Ortho-
sporum)”(Wilson, 1987: 79).
Mosyakin & Clemants (2002, 2008) concluded that all
species of Chenopodium with glandular hairs as well as Tel-
oxys belong in Dysphania. Finally, based on morphological
characters (indumentum, inflorescence details, seed embryo
position), Zhang & Zhu (2016) and Zhu & Sanderson (2017)
reinstated Ambrina,Neobotrydium and Roubieva at generic
rank, and Zhu & Sanderson (2017) included them, with
Cycloloma and Dysphania, in tribe Neobotrydieae G.L.Chu.
Kadereit & al. (2010) showed that the monotypic genus
Suckleya, earlier generally included in Atripliceae, belongs
to Dysphanieae, and Sukhorukov & al. (2018a) moved Mono-
lepis spathulata A.Gray, a species of the small genus Mono-
lepis Schrad. (at that time part of Blitum L.) to Dysphanieae
as a monotypic genus Neomonolepis.
Objectives of this study. —The aims of this study are to
(1) provide a robust phylogenetic tree of Dysphanieae based
on two nuclear ribosomal and two plastid DNA markers in-
cluding species representing all four genera of the tribe as well
as a representative number of species from all sections of Dys-
phania, (2) conduct a biogeographical analysis of the tribe,
(3) test the current generic classification of Dysphanieae, and
(4) suggest a new infrageneric classification of Dysphania.
■MATERIALS AND METHODS
Plant material, sampling and outgroups. —We used
leaf fragments taken from herbarium specimens or from mate-
rial collected during recent field trips and dried in silica gel.
Altogether 121 accessions were included in the phylogenetic
analyses representing all genera, sections and 39 accepted
species of Dysphanieae. Voucher information for all accessions
is given in Appendix 1. Our sampling covers ~80 % of the cur-
rently recognized species of Dysphanieae according to recent
taxonomic treatments. We included multiple accessions for
problematic or widespread species to test their monophyly. Rep-
resentatives of all three genera of Axyrideae, Axyris (five acces-
sions representing two species), Ceratocarpus (three accessions
representing C. arenarius) and Krascheninnikovia (five acces-
sions representing the two subspecies of K. ceratoides) were
included as outgroups according to Kadereit & al. (2010)
(Appendix 1). Appendix 1 alsogives an overview of sequences
newly generated for this study and sequences included from
previous molecular studies with GenBank accession numbers.
Sequencing and phylogenetic inference. —Total DNA
was extracted from 20 mg dried leaf-material using the DNeasy
Plant Mini Kit (QIAGEN, Venlo, Netherlands) following
the manufacturer’s specifications. PCR was carried out in a
T-Professional or T-Gradient Thermocycler (Biometra, Jena,
Germany). Table 2 gives the details of primer sequences, PCR
recipe and cycler programme for each marker. PCR products
were checked on 1% agarose gels and purified subsequently
using the NucleoSpin Gel and PCR clean-up-Kit (Macherey-
Nagel, Düren, Germany) following the manufacturers manual.
DNA sequences were obtained using the Big Dye Terminator
v.3.1 Cycle Sequencing Kit (Applied Biosystems, Thermo
Fisher Scientific, Schwerte, Germany) in combination with
the primers detailed in Table 2 following a purification step
using Illustra Sephadex G-50 Fine DNA Grade (Cytiva, Thermo
Fisher Scientific, Schwerte, Germany). DNA fragments were
sequenced using an automatic capillary sequencer GA3130XL
(Applied Biosystems) following the Sanger method. Forward
and reverse sequences were edited and merged to consensus
sequences, then compiled in preliminary alignments using
Sequencher v.4.1.4 (Gene Codes Corporation). All prelimi-
nary marker alignments were then subjected to automatic
alignment using MAFFT (v.7.402) on CIPRES. The align-
ments were checked once more and corrected manually where
needed. For the combined alignment, see supplementary
Appendix S1.
The chloroplast dataset consisting of the atpB-rbcL spacer
and rpl16 intron sequences and the nuclear dataset consisting
of ITS (internal transcribed spacer) and ETS (external tran-
scribed spacer) were initially analysed separately. For all acces-
sions that had been successfully sequenced for both partitions
(plastid and nuclear), a combined analysis was conducted. For
all three datasets (plastid, nuclear, combined), the best substitu-
tion model was inferred using jModeltest (v.2.1.6) on CIPRES
Science Gateway v.3.3 (https://www.phylo.org, Miller & al.,
2010). Maximum likelihood phylogenetic analyses were then
performed using RAxML-HPC2 on XSEDE (v.8.2.12) includ-
ing bootstrapping (Stamatakis, 2014) with GTR+Γ+I for the
nuclear dataset, GTR+Γfor the plastid dataset and HKY+Γ+I
for the combined dataset selected as the best substitution
models under the Akaike information criterion.
Divergence times were estimated using a Bayesian uncor-
related lognormal relaxed clock under a birth–death speciation
process (Nee & al., 1994; Gernhard, 2008). This tree is based
on the combined data matrix with only one accession per spe-
cies included. For each aligned locus, the best substitution
model was determined using PartitionFinder v.2 (Lanfear &
al., 2017). The GTR+Γ+I model was suggested as the most ap-
propriate model for the ETS and atpB-rbcL datasets, while the
GTR+Γmodel was selected for the ITS and rpl16 datasets. A
secondary calibration was used as dating prior, being obtained
from Kadereit & al. (2012), that constrains the age estimate
for the most recent common ancestor (MRCA) of Dysphanieae
at 34 Ma (95% highest posterior density [HPD]: 18.24–
38.63 Ma). We selected a normal distribution prior for the sec-
ondary calibration with a standard deviation of 8, equivalent to
the 95% HPD estimate of Kadereit & al. (2012). This calibra-
tion was chosen because it includes the early-branching line-
ages Tel oxys and Suckleya, five representatives of Dysphania
and a wide outgroup sampling of Amaranthaceae s.l. The age
estimate found in this study covers mean node ages for the stem
of Dysphanieae found in other studies (Morales-Briones &
al., 2020: 33.9 myr; Kadereit & al., 2010: 37.1 myr [plastid
data] and 25.1 myr [nuclear data]). Two independent MCMC
analyses were run, each of 20 million generations, sampling
every 20,000. Input files were generated with BEAUti v.2.4.5
Version of Record 7
TAXON 00 (00) •1–26 Uotila & al. •Systematics of Dysphanieae
(Bouckaert & al., 2014) and analyses ran using BEAST v.2.4.5
(Bayesian Evolutionary Analysis by Sampling Trees; Bouckaert
& al., 2014) on the CIPRES Science Gateway v.3.3 (https://
www.phylo.org, Miller & al., 2010). Output log files were
analysed using Tracer v.1.6 (Rambaut & Drummond, 2013)
to assess convergence and effective sample size of all parame-
ters. As “burn-in”, 25% of samples were removed prior to
combining the independent runs using LogCombiner v.2.4.5
(Bouckaert & al., 2014). The MCC tree was generated using
TreeAnnotator v.2.4.5 (Bouckaert & al., 2014).
Ancestral area analysis. —Species distribution was
assessed from literature, the online database Australasian
Virtual Herbarium (https://avh.chah.org.au/) and study of her-
barium specimens housed in AD, AQ, B, BCN, BEI, BM, C,
E, G, GLM, H, HAL, K, KAS, LE, M, MJG, MO, MPU,
MSB, MW, NSW, P, PERTH, S, STU, TARI, TUH, UPS,
W, WU and Z. Eight broad geographic regions reflecting the
worldwide distribution of Dysphanieae were coded as follows:
A = Asia: Siberia and Mongolia; B = Asia: Himalayas and
Tibet; C = Asia: Irano-Turanian Region and Mediterranean;
Table 2. Primer sequences, PCR recipe and cycler program for each marker.
Marker Primer
Primer sequence
5′–3′Author PCR recipe (all in μl) Cycler program
ITS F: ITS18S CCT TMT CAT YTA GAG
GAA GGA G
Blattner,
1999
ddH2O: 16.33
MgCl
2
[25 mM]: 2.5
σ-Buffer: 2.5
dNTPs (10 mM each): 0.5
σ-Taq Enzym DNA-Polymerase: 0.17
DNA: 1.0
Primer (F + R): 0.5 (20 μM) each
DMSO: 1.0
94C, 1 min
35 cycles
94C, 30 s
52C, 50 s
72C, 1 min
94C, 30 s
52C, 72 s
72C, 8 min
10C, ∞
R: ITS28S CCG CTT ATT CAT ATG
CTT AAA
ITS1 F: ITS A GGA AGG AGA AGT CGT
AAC AAG G
Blattner,
1999
ddH2O: 16.58
MgCl
2
[25 mM]: 1.5
σ-Buffer: 2.5
dNTPs (10 mM each): 0.25
σ-Taq Enzym DNA-Polymerase: 0.17
DNA: 2.0
Primer (F + R): 0.5 (50 μM) each
DMSO: 1.0
94C, 1 min
35 cycles
94C, 20 s
55C, 30 s
72C, 1 min
94C, 20 s
55C, 80 s
72C, 8 min
10C, ∞
R: ITS C GCA ATT CAC ACC AAG
TAT CGC
ITS2 F: ITS B CTT TTC CTC CGC TTA
TTG ATA TG
R: ITS D CTC TCG GCA ACG GAT
ATC TCG
ETS F: ETS 18S II CTC TAA CTG ATT TAA
TGA GCC ATT CGC A
Zacharias
& Baldwin,
2010
ddH2O: 16.25
MgCl
2
[25 mM]: 2.5
σ-Buffer: 2.5
dNTPs (10 mM each): 0.25
σ-Taq Enzym DNA-Polymerase: 0.25
DNA: 2.0
Primer (F + R): 0.5 (50 μM) each
DMSO: 0.25
94C, 1 min
35 cycles
94C, 30 s
52C, 50 s
72C, 1 min
94C, 30 s
52C, 72 s
72C, 8 min
10C, ∞
R: ETS
Atriplex Int.
CGT GTG AGT GGT GAT
TGG TT
atpB-rbcL
spacer
F: atpB-rbcL
spacer F
GAA GTA GTA GGA TTG
ATT CTC
Xu & al.,
2000
ddH2O: 18.6
MgCl
2
[25 mM]: 1.2
σ-Buffer: 2.5
dNTPs (10 mM each): 0.25
σ-Taq Enzym DNA-Polymerase: 0.2
DNA: 1.0
Primer (F + R): 0.5 (50 μM) each
DMSO: 0.25
94C, 1 min
35 cycles
94C, 30 s
52C, 50 s
72C, 1 min
94C, 30 s
52C, 72 s
72C, 8 min
10C, ∞
R: atpB.rbcL
spacer R
CAA CAC TTG CTT TAG
TCT CTG
rpl16
intron
F: rplF71
R: rplR1516
GCT ATG CTT AGT GTG
TGA CTC GTT G
CCC TTC ATT CTT CCT
CTA TGT TG
Shaw & al.,
2005
ddH2O: 17.8
MgCl
2
[25 mM]: 2
σ-Buffer: 2.5
dNTPs (10 mM each): 0.25
σ-Taq Enzym DNA-Polymerase: 0.2
DNA: 1.0
Primer (F + R): 0.5 (50 μM) each
DMSO: 0.25
Temp., time, ramp [C/s]
80C, 5 min, 5.0
35 cycles
95C, 1 min, 5.0
50C, 1 min, 0.3
65C, 4 min, 5.0
65C, 5 min
8C, ∞
8Version of Record
Uotila & al. •Systematics of Dysphanieae TAXON 00 (00) •1–26
Table 3. Distribution areas of species of Dysphanieae included in the molecular and biogeographical analyses and the coding used for the analysis
with BioGeoBears.
Species Sequence_ID Distribution Coding
Axyris amaranthoides L. AxamarAC647_3015 Siberia and Mongolia A
A. prostrata L. Axpros0118 Himalayas and Tibet B
Ceratocarpus arenarius L. CearenAC649_3050 Irano-Turanian Region C
Dysphania ambrosioides (L.) Mosyakin & Clemants Dyambr2786 South America F
D. anthelmintica (L.) Mosyakin & Clemants Dyanth2795 Southern U.S.A., Mexico and West Indies D
D. atriplicifolia (Spreng.) G.Kadereit, Sukhor. & Uotila Cy2791 Mexico, U.S.A. and southern Canada D
D. bhutanica Sukhor. Dybhut2998 Himalayas and Tibet B
D. botrys (L.) Mosyakin & Clemants Dybotr2999 Irano-Turanian Region and Mediterranean C
D. carinata (R.Br.) Mosyakin & Clemants Dycari3425 Eastern Australia E
D. chilensis (Schrad.) Mosyakin & Clemants Dychil2796 South America F
D. congestiflora S.J.Dillon & A.S.Markey Dycofl3501 Western Australia E
D. congolana (Hauman) Mosyakin & Clemants Dycong3306 East and Central Africa G
D. cristata (F.Muell.) Mosyakin & Clemants Dycris3528 Australia E
D. geoffreyi Sukhor. Dygeof3309 Himalayas and Tibet B
D. glandulosa Paul G.Wilson Dyglan3537 Western Australia E
D. glomulifera (Nees) Paul G.Wilson Dyglom3523 Australia E
D. graveolens (Willd.) Mosyakin & Clemants Dygrav2073 Mexico and southern U.S.A. D
D. himalaica Uotila Dyhima2773 Himalayas and Tibet B
D. kalpari Paul G.Wilson Dykalp3508 Central Australia E
D. littoralis R.Br. Dylitt3432 Eastern Australia E
D. mandonii (S.Watson) Mosyakin & Clemants Dymand2781 Peru, Bolivia, northern Argentina and
northern Chile
F
D. melanocarpa (J.M.Black) Mosyakin & Clemants Dymela3409 Australia E
D. multifida (L.) Mosyakin & Clemants Dymult2789 South America F
D. multiflora (Moq.) G.Kadereit, Sukhor. & Uotila Dymufl3014 Himalayas B
D. neglecta Sukhor. Dynegl3010 Himalayas B
D. nepalensis (Colla) Mosyakin & Clemants Dynepa3011 Hindukush –Himalayas, and China B
D. plantaginella F.Muell. Dyplan3522 Australia E
D. platycarpa Paul G.Wilson Dyplat3411 Central Australia E
D. procera (Hochst. ex Moq.) Mosyakin & Clemants Dyproc2772 East and Central Africa, South Arabia G
D. pseudomultiflora (Murr) Verloove & Lambinon Dypseu2783 Southern Africa H
D. pumilio (R.Br.) Mosyakin & Clemants Dypumi3513 Australia E
D. rhadinostachya (F.Muell.) A.J.Scott Dyrhad3414 Australia E
D. saxatilis (Paul G.Wilson) Mosyakin & Clemants Dysaxa3517 Western Australia E
D. schraderiana (Schult.) Mosyakin & Clemants Dyschr3048 East and Central Africa, South Arabia G
D. simulans F.Muell. & Tate Dysimu3421 Central Australia E
D. sphaerosperma Paul G.Wilson Dyspha3530 Central and Western Australia E
D. tibetica (A.J.Li) Uotila Dytibe2769 Himalayas and Tibet B
D. truncata (Paul G.Wilson) Mosyakin & Clemants Dytrun3424 Central Australia E
(Continues)
Version of Record 9
TAXON 00 (00) •1–26 Uotila & al. •Systematics of Dysphanieae
D = North America incl. Mexico; E = Australia; F = South
America; G = East and Central Africa, South Arabia; H =
Southern Africa (Table 3, Fig. 1). Ancestral range estimation
(ARE) was conducted using the time-calibrated tree represent-
ing 39 species of Dysphanieae and 5 of Axyrideae included in
this analysis with only one accession per species using Bio-
GeoBEARS (Matzke, 2013, 2014) in R v.3.3.2 (R Core
Team, 2016). We ran the analysis under a dispersal-extinction
cladogenesis (DEC) model, dispersal-vicariance (DIVALIKE)
model and BAYAREA (BAYAREALIKE) model. We did
not consider a second run adding the parameter “j”(founder-
event speciation) for each biogeographic model because of
the conceptual and statistical problems of this parameter out-
lined by Ree & Sanmartín (2018). Out of the three models
explored in this study, the DIVALIKE model was the best fit
based on the Akaike information criterion and likelihood ratio
test results. The analyses were unconstrained (without possible
dispersal routes or ancestral areas assumed apriori). In three
independent runs, we allowed the inferred ancestor to occupy
a maximum of two, three and four areas, respectively, even
though the maximum number of areas occupied by any extant
species was one.
Morphological studies. —Our studies included macro-mor-
phological characters from the herbaria listed above. Micro-
morphological and anatomical features studied included peri-
carp and perianth (for methods, see Sukhorukov, 2014) and
trichomes. For the latter, we used SEM microscopy in the lab-
oratory of Electron Microscopy at the Lomonosov Moscow
State University.
■RESULTS
Phylogenetic inference. —The plastid marker alignment
consisted of 116 accessions and 1569 bp, the nuclear marker
alignment had 120 accessions and 1262 bp and the combined
alignment, which consisted only of those accessions represen-
ted in both separate datasets, had 107 accessions and 2831 bp
(suppl. Appendix S1). The phylogenetic tree resulting from
the combined dataset (Fig. 3) shows an overall better resolu-
tion than the trees resulting from the individual datasets (plas-
tid tree, suppl. Fig. S1; nuclear tree, suppl. Fig. S2). There are
only few instances of topological conflict between the plastid
and nuclear trees that received considerable bootstrap support
(BS > 75). However, these have implications for the backbone
of the Dysphanieae tree and are therefore mentioned in detail
below.
Dysphanieae, comprising Dysphania (incl. Cycloloma),
Neomonolepis,Suckleya and Teloxys, is well supported (BS
100) in the ML trees of all three datasets (Fig. 3, suppl. Figs.
S1, S2). Teloxys and Neomonolepis are successively sister to
the remainder of Dysphanieae with Teloxys branching first
in the plastid tree (suppl. Fig. S1) and second in the nuclear
tree (suppl. Fig. S2). As a result of this topological conflict,
the sister-group relationship of Teloxys to the remainder of
Dysphanieae (incl. Neomonolepis) received low support in the
combined analysis because the monophyly of the remainder of
Dysphanieae (incl. Neomonolepis) was only weakly supported
(BS 64; Fig. 3). Excluding these two conflicting monotypic
genera from the analyses does not change the topology of the
remaining clades. Suckleya and Dysphania are sister genera
(BS 80; Fig. 3) in all analyses, and Cycloloma is always nested
in Dysphania as sister to a clade comprising species from South
and North America (Fig. 3, suppl. Figs. S1, S2). Within Dys-
phania, overall resolution and support of the tree resulting from
the combined dataset is improved, in comparison to the tree
topologies resulting from the separate datasets, indicating that
they show a congruent phylogenetic signal. Conflict affecting
the backbone of Dysphania is found in the position of a branch
consisting of D. graveolens and D.mandonii. There are three
major clades in Dysphania: An Asian/African clade consisting
of nine species (clade 1 in Fig. 3), an American clade including
seven species (clade 2 in Fig. 3) and an Australian/African
clade with 20 species (clade 3 in Fig. 3). While clades 1 and
3 are well supported, clade 2 receives only low support due to
the conflicting position of the D.graveolens/D. mandonii
branch. This branch resolves as sister to clade 1 in the plastid
tree (BS 72; suppl. Fig. S1) and as part of clade 2 in the
Table 3. Continued.
Species Sequence_ID Distribution Coding
D. valida Paul G.Wilson Dyvali3433 Eastern Australia E
Krascheninnikovia ceratoides (L.) Gueldenst. subsp.
ceratoides
KrceraAC608_0012 Siberia –Irano-Turanian Region C
K. ceratoides subsp. lanata (Pursh) H.Heklau KrcerassplanaAC628_1887 Western U.S.A. and Canada D
Neomonolepis spathulata (A.Gray) Sukhor. MoSPATH Southwestern U.S.A. and northwestern
Mexico
D
Suckleya suckleyana (Torr.) Rydb. Susuck2000 Central U.S.A. D
Teloxys aristata (L.) Moq. Tearis0293 Siberia and Mongolia A
A, Asia: Siberia and Mongolia; B, Asia: Himalayas and Tibet; C, Asia: Irano-Turanian Region and Mediterranean; D, North America incl. Mexico;
E, Australia; F, South America; G, East and Central Africa, South Arabia; H, Southern Africa.
10 Version of Record
Uotila & al. •Systematics of Dysphanieae TAXON 00 (00) •1–26
nuclear tree (BS 59; suppl. Fig. S2). Although this conflicting
topology received only low support, it likely prevents a resol-
ved backbone within Dysphania, which means that the phylo-
genetic relationships of the three major clades remain unclear.
Clade 2 consists of species from South and North America
and also includes the North American Cycloloma atriplici-
folium. Differentiation is poor between the morphologically
similar Dysphania ambrosioides and D. chilensis.TheAus-
tralian/African clade 3 consists of 17 Australian species with
3 African species (D. congolana (Hauman) Mosyakin & Cle-
mants, D. pseudomultiflora (Murr) Verloove & Lambinon,
D. schraderiana) nested among them. Apart from clade 1,
which is unresolved at the backbone, the Dysphania clades
show considerable internal resolution.
Ancestral area analysis. —In the biogeographical analy-
sis, the reduced and dated tree showed the same topology as
the combined ML tree (Figs. 3, 4). According to our dating,
the Dysphanieae started to diversify ca. 18 million years ago
Dysphania
Outgroup
Axyrideae
clade 3
clade 1 clade 2
Suckleya
Neomonolepis
Teloxys
Dysphanieae
Dy. graveolens 2080
Kr. ceratoides subsp. lanata AC626_1887
Dy. ambrosioides 3426
Dy. graveolens 2073
Dy. multiflora 3014
Su. suckleyana 1999
Te. aristata 2778_3002
Dy. mandonii 2770
Kr. ceratoides subsp. ceratoides AC608_0012
Dy. neglecta 3010
Dy. geoffreyi 3309
Dy. botrys 0116
Dy. procera 3001
Te. aristata 0293
Dy. nepalensis 3000
Dy. chilensis 2796
Dy. himalaica 2773
Su. suckleyana 2001
Ce. arenaria AC649_3050
Dy. botrys 2999
Dy. chilensis 2792
Ax. amaranthoides AC647_3015
Dy. multifida 2774
Dy. ambrosioides 2786
Dy. multifida 2789
Ax. prostrata 0118
Dy. botrys 3046
Dy. nepalensis 3011
Dy. chilensis 2793
Su. suckleyana 2000
Dy. nepalensis 2785
Dy. nepalensis 3047
Ne. spathulata
Dy. geoffreyi 3308
Dy. bhutanica 2998
Dy. mandonii 2781
Dy. ambrosioides 2066
Dy. multifida 2775
Dy. tibetica 2769
Dy. ambrosioides 0822
Dy. multifida 2081
Cy. atriplicifolium 2791
Ax. prostrata 3003
Dy. ambrosioides 2787
Dy. ambrosioides 2790
Dy. procera 2772
Dy. graveolens 2079
Dy. anthelmintica 2795
Dy. botrys 2798
Dy. botrys 2777
100
100
100
100
64
86
100
65
100
98
100
99
100 63
100
100
100
93
53
64
100
97
98
100
91
91
100
96
80
100
100
100
64
100
100
72
continue Fig. 3B
A
Fig. 3. Phylogenetic tree resulting from a maximum likelihood analysis of combined plastid and nuclear data of 101 Dysphanieae samples repre-
senting 39 species of the tribe. Representatives of Axyrideae serve as outgroup. Bootstrap support values >50 are given above branches.
Version of Record 11
TAXON 00 (00) •1–26 Uotila & al. •Systematics of Dysphanieae
and Dysphania 10 million years ago. The DIVALIKE model
received the best likelihood scores compared to the other
models in all three runs, and the lowest when four ancestral
areas were allowed (−56.56; versus −66.37.12 for DEC and
−116.88 for BAYAREALIKE). The reconstructed ancestral
area for the stem node of Dysphanieae was Asia (areas A–C)
and North America (D) with the ancestral areas ABCD recei-
ving the highest score of 53.2 and ACD = 17.6; see Fig. 4);
for the crown node, it was Siberia, Mongolia/North America
(AD) with the highest score of 100. The ancestral area of
the stem node of Dysphania showed the highest score for
North America (D = 98.8), while the ancestral area of the
crown node of Dysphania remains uncertain with BDEG
receiving the highest score of 34.2. Within the American
clade of Dysphania (clade 2), South America seems to have
been colonized twice from North America, and within the
Dysphania
clade 3
Dysphanieae
Dy. sphaerosperma 3529
Dy. simulans 3420
Dy. truncata 3423
Dy. pumilio 3514
Dy. glomulifera 0277
Dy. truncata 3424
Dy. plantaginella 3534
Dy. carinata 3425
Dy. glomulifera 3523
Dy. kalpari 0528
Dy. rhadinostachya 0525
Dy. platycarpa 3412
Dy. sphaerosperma 3510
Dy. valida 3433
Dy. pumilio 3519
Dy. melanocarpa 3410
Dy. pseudomultiflora 2783
Dy. glandulosa 3535
Dy. pumilio 3513
Dy. truncata 3422
Dy. melanocarpa 3408
Dy. glomulifera 3524
Dy. glandulosa 3525
Dy. littoralis 3434
Dy. cristata 3310
Dy. saxatilis 3518
Dy. simulans 3421
Dy. congolana 3306
Dy. cristata 3526
Dy. sphaerosperma 3531
Dy. kalpari 3508
Dy. rhadinostachya 3414
Dy. carinata 2776
Dy. cristata 3528
Dy. pseudomultiflora 2784
Dy. plantaginella 3509
Dy. valida 3441
Dy. littoralis 3432
Dy. platycarpa 3411
Dy. sphaerosperma 3530
Dy. melanocarpa 3409
Dy. glandulosa 3537
Dy. congestiflora 3501
Dy. melanocarpa 3527
Dy. congolana 2771
Dy. kalpari 3520
Dy. glandulosa 3536
Dy. sphaerosperma 3521
Dy. simulans 3419
Dy. simulans 3511
Dy. saxatilis 3517
Dy. simulans 3512
Dy. plantaginella 3522
Dy. platycarpa 3413
Dy. kalpari 3415
Dy. pumilio 2788
Dy. schraderiana 3048
61
51
69
68
95
52
50
57
83
83
100
100
63
52
97
81
98
76
95
99
52
66
100
100
63
88
81
69
57
85
100
97
100
54
92
74
58
57
100
73
100
97
86
99
63
91
100
56
100
100
69
52
continue
Fig. 3A
B
Fig. 3. Continued.
12 Version of Record
Uotila & al. •Systematics of Dysphanieae TAXON 00 (00) •1–26
3.0
0.05.010.015.020.025.0
Dy. littoralis 3432
Dy. congolana 3306
Cy. atriplicifolium 2791
Te. aristata 0293
Ax. prostrata 0118
Su. suckleyana 2000
Dy. glomulifera 3523
Dy. pseudomultiflora 2783
Dy. schraderiana 3048
Dy. neglecta 3010
Dy. rhadinostachya 3414
Dy. simulans 3421
Dy. multiflora 3014
Dy. ambrosioides 2786
Ax. amaranthoides AC647_3015
Dy. graveolens 2073
Kr. ceratoides subsp. ceratoides AC608_0012
Dy. valida 3433
Dy. geoffreyi 3309
Ne. spathulata
Dy. mandonii 2781
Dy. multifida 2789
Dy. tibetica 2769
Kr. ceratoides subsp. lanata AC626_1887
Dy. pumilio 3513
Dy. himalaica 2773
Dy. kalpari 3508
Dy. saxatilis 3517
Dy. botrys 2999
Dy. congestiflora 3501
Dy. chilensis 2796
Dy. bhutanica 2998
Ce. arenarius AC649_3050
Dy. anthelmintica 2795
Dy. carinata 3425
Dy. plantaginella 3522
Dy. nepalensis 3011
Dy. sphaerosperma 3530
Dy. platycarpa 3411
Dy. melanocarpa 3409
Dy. glandulosa 3537
Dy. truncata 3424
Dy. cristata 3528
Dy. procera 2772
1
1
1
1
1
1
1
1
1
1
1
1
1
0.99
0.92
0.99
0.99
0.63
0.64
0.82
0.88
1
1
1
1
1
1
1
0.79
1
0.74
1
1
1
0.83
0.79
F 100
DF 100
D 100
CD 100
C 95.1
AB 100
G 98.2
GH 100
E 100
E 98.9
DE 98.8
DF 100
D
100
AD 100
B 100
BG 100
D 99.1
D 98.8
EG 98.9
BC 58.8
ABC 24.8
AC 13.5
ABD 8.2
BCD 5.9
ACD 17.6
ABC 5.9
ABCD 53.2
BDE 25.9BDEG 34.2
DEG 25.9
DG 5.1BD 5.1
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
H
G
G
E
F
F
F
D
D
D
F
B
B
C
B
B
B
B
B
G
D
D
A
C
D
C
A
B
E
G
F
H
C
Asia: Siberia and Mongolia
Asia: Himalaya and Tibet
Asia: Irano-Turanian Region and Mediterranean
North America incl. Mexico
Australia
South America
East and Central Africa, South Arabia
Southern Africa
A
B
D
Areas
Fig. 4. Results of the ancestral range estimation (ARE) under the DIVALIKE model and with a maximum of four ancestral areas allowed, run with
BioGeoBEARS based on a time-calibrated tree representing 44 species and subspecies of Dysphanieae with only one accession per species. Num-
bers above branches represent posterior probabilities.
Version of Record 13
TAXON 00 (00) •1–26 Uotila & al. •Systematics of Dysphanieae
Australian clade of Dysphania (clade 3), Africa has been
colonized from Australia (Fig. 4). For the Asian clade
(clade 1 in Fig. 3), the Himalayas/Tibet and East and Cen-
tral Africa and South Arabia were inferred as ancestral;
however, internal resolution of this clade is lower compared
to the other two.
■DISCUSSION
Phylogenetic history and diversification of Dyspha-
nieae. —Molecular phylogenetic studies of Chenopodioideae
consistently agreed that the tribe Dysphanieae included the
genera Cycloloma,Dysphania,Suckleya and Teloxys (Kade-
reit & al., 2010, 2012; Fuentes-Bazan & al., 2012a; Morales-
Briones & al., 2020). Only recently, it was discovered that
one more genus, Neomonolepis, also belongs to Dysphanieae
(Sukhorukov & al., 2018a). These previous results are sup-
ported here with a substantially broadened sampling of the
large genus Dysphania (Fig. 3). While the monophyly of Dys-
phanieae is always well supported (including our study), there
is either low support or conflict between nuclear and chloro-
plast data concerning the branching order of the first two
lineages, Teloxys and Neomonolepis. Both are monospecific
genera of small, annual, non-aromatic herbs. While the native
distribution range of Teloxys is Central Asia, Neomonolepis
is found in the southwestern United States and Mexico (Baja
California; Fig. 1). The following, successively branching lin-
eage is the monospecific annual genus Suckleya, which is dis-
tributed through the southern-central United States (Fig. 1).
With a view to the ancestral area reconstruction, which favo-
ured a North American/Asian stem and a North American/
Siberian-Mongolian distribution for the crown node of Dys-
phanieae, we interpret these three old and species-poor line-
ages as relictual decendants of an ancestral lineage with a
wider distribution across Beringia. The stem and crown of
the Dysphanieae date back to the Late Oligocene and Early
Miocene, respectively (Fig. 4), a period when warm-temperate
groups migrated via the Beringia Land Bridge. The disjunct
distribution of early-branching Dysphanieae (Fig. 4) is there-
fore consistent with the availability of the Bering Land Bridge
(Wen, 1999; Sanmartín & al., 2001) and supported by other
taxa with an Asian/North American disjunction of similar age
(Wen & al., 2016 and references therein).
Although we allowed a maximum of four combined areas,
the ancestral area analysis showed a high score for North Amer-
ica (D = 98.8) for the stem node of Dysphania. From its ances-
tral area in North America (Fig. 4), the genus spread worldwide.
A broad ancestral range at the crown nodeof Dysphania would
probably explain the simultaneous diversification on different
continents (Fig. 3), viz. North Africa/Asia (clade 1), America
(clade 2) and Australia (clade 3). The phylogeny reveals that
the North American Dysphanieae as well as the African Dys-
phanieae are not monophyletic. Native to North America are
the already mentioned relictual old Dysphanieae lineages Neo-
monolepis and Suckleya with closest relatives in Central Asia
and also the much younger Cycloloma atriplicifolium,which
seems to have originated during the Late Miocene from within
a North American Dysphania clade and will hence be included
in Dysphania. Native to Africa is a Late Miocene lineage con-
sisting only of Dysphania procera, which is sister to the Asian
Dysphania species, and a Pliocene lineage originating from
Australia consisting of three species, one of which is distributed
in South Africa. This younger African lineage is sister to the
Australian species D. saxatilis (Paul G.Wilson) Mosyakin &
Clemants. From a geographical point of view this might be
surprising, but easy to accept on the basis of morphological
characters. Already Wilson (1983) had difficulty placing his
new species Chenopodium saxatile Paul G.Wilson in any of
the existing Australian sections. He compared it also with the
African Chenopodium congolanum (Hauman) Brenan, recog-
nizing several common features. The biogeographical analysis
allows two interpretations for this Australian/African clade.
Either the ancestor of the three African species dispersed from
Australia to Africa, in which case the typical morphology of
this lineage evolved in Australia, or the ancestor of the lineage
comprising D. saxatile and the three African species dispersed
from Australia to Africa. In the latter case, morphological traits
of this group could have evolved in Africa, and D. saxatile rep-
resents a dispersal event back to Australia.
The phylogenetic trees (Figs. 3, 4) resulting from the
combined analysis of plastid and nuclear data resolves all
American species of Dysphania in one clade depicting the
phylogenetic signal of the nuclear data (suppl. Fig. S2). The
ancestral area reconstruction suggests that within Dysphania
South America was reached during the Pliocene/Quaternary
two times independently within the two subclades: 1, D. man-
donii and D. graveolens,and2,D. ambrosioides,D. chilensis,
D. multifida,D. anthelmintica,Cycloloma atriplicifolium. Mor-
phological data support the distinction of the two subclades.
Main differences between the species of these subclades exist
in the type of inflorescence, perianth characters and pericarp
surface. The species of subclade 1 have paniculate inflores-
cences, flowers in loose, compound dichasial cymes, abortive
at the tip of ultimate branches, the perianth opened in fruit-
ing stage, perianth lobes with prominent appendages on the
back and the pericarp smooth and glabrous. By contrast, spe-
cies in subclade 2 have spiciform inflorescences, all flowers
developed, ± dense glomerules (flowers seldom single), the
perianthclosedinfruitingstageandthepericarpcovered
with yellow glandular hairs, sometimes together with simple
hairs.
The morphological circumscription of Dysphanieae. —
After a rather turbulent taxonomic history (see Introduction
and Table 1), Mosyakin & Clemants (2002, 2008) suggested
assembling all species of Chenopodium with glandular hairs
as well as Teloxys in Dysphania. The molecular results clearly
indicate that they were correct in recognizing Dysphania and
Teloxys as a natural lineage, albeit not as congeneric since also
Suckleya and Neomonolepis belong to this lineage. Together,
these four genera make up the tribe Dysphanieae, which can be
distinguished from other Chenopodioideae by a combination
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Uotila & al. •Systematics of Dysphanieae TAXON 00 (00) •1–26
of diverse trichomes (Fig. 5). It seems that only Neomonole-
pis, which is a glabrous herb, is a clear exception to this, and
this monospecific genus is sister to all other Dysphanieae
according to the nuclear sequence data (suppl. Fig. S2). Con-
trary to other Dysphanieae, flowers of Neomonolepis and Suck-
leya are unisexual, and the perianth of the female flowers of
Neomonolepis abortive.
Subsessile, yellow- or orange-coloured glands containing
essential oils are found in almost all species of Dysphania
(Fig. 5A). As to Cycloloma atriplicifolium (combined into Dys-
phania below), we discovered in the course of this study that
this species has short-stipitate, white glandular hairs (lacking
essential oils) of the same shape as in Dysphania (Fig. 5B).
They are easily overlooked, being scattered and mainly present
on young parts of the stem, flower bases and perianths. Because
Cy. atriplicifolium is nested among species with oil-containing
glandular hairs, we assume that in Cy. atriplicifolium the oil
secretion was lost. The inflated unicellular trichomes (Fig. 5C),
mentioned by Chu & al. (1991) as a peculiar character of Suck-
leya, are in fact intermixed with multi-celled glandular hairs.
Teloxys aristata is described as a glabrous herb (Iljin & Aellen,
1936; Grubov, 1966), but is hairy at the base of the stem, the
number of cells varying from one (Fig. 5D) to several, and
the apical cell is inflated. In Dysphania,manyspecieshavein
addition to the glands often also other types of trichomes (multi-
cellular glandular and simple hairs, and papillae) (Simón, 1997;
Sukhorukov, 2012a,b, 2014; Sukhorukov & Zhang, 2013;
Sukhorukov & al., 2015).
■TAXONOMIC TREATMENT
Our molecular and morphological study is the first com-
prehensive attempt to disentangle phylogenetic relationships
within Dysphanieae and to translate these findings into a mod-
ern taxonomic treatment. Our results strongly confirm the
acceptance of only four genera within the tribe –Dysphania,
Neomonolepis,Suckleya and Teloxys. The characters men-
tioned by Zhang & Zhu (2016) and Zhu & Sanderson (2017),
e.g., the shape of the subsessile glands (“gland-grains”), or
position of seed embryo (horizontal vs. vertical) in Ambrina,
Neobotrydium and Dysphania are not genus-specific, and there
are no distinct characters supporting the existence of Ambrina,
Roubieva and Neobotrydium (Sukhorukov & al., 2018b).
Below we provide an updated circumscription of Dysphanieae,
with an improved generic key and nomenclatural synonymies.
A new sectional subdivision of the largest genus Dysphania is
also included.
Key to genera
1. Plants glabrous; flowers unisexual, female flowers with
reduced perianth ....................................... Neomonolepis
Fig. 5. SEM images of gland and hair types in Dysphanieae. A, Subsessile glands on the perianth of Dysphania graveolens; Mexico, September
2018, A. Sukhorukov s.n. (MW); B, Short, multicellular glandular hairs on the stem of D. atriplicifolia; Romania, Turda, G. & J. Wolff 1018
(MW); C, A papilla on the stem of Suckleya suckleyana; U.S.A., New Mexico, July 1984, Hill 14611 (GH); D, A papilla on the stem of Teloxys
aristata; Russia, Tambov Prov., August 2001, A. Sukhorukov s.n. (MW).
Version of Record 15
TAXON 00 (00) •1–26 Uotila & al. •Systematics of Dysphanieae
1. Plants pubescent, at least in basal parts or in inflores-
cence; flowers bisexual, unisexual or polygamous, all
flowers with properly developed perianth ......................2
2. Flowers strictly unisexual (plants monoecious); perianth
of female flowers zygomorphic, enlarged, flattened and
triangular in fruit stage; seeds ca. 3 mm ........... Suckleya
2. Flowers bisexual or polygamous; perianth actinomor-
phic, not enlarged and flattened in fruit stage; seeds
0.3–1.6 mm ................................................................. 3
3. Plants not aromatic, with papillae and short multicellular
white hairs mostly localized on lower parts of the stem;
branches usually bifurcate, terminating with long arista;
all flowers solitary ............................................... Teloxys
3. Plants mostly aromatic, with glandular hairs and usually
yellow or orange subsessile glands, and multicellular sim-
ple hairs; branches mostly not bifurcate, if bifurcate, short
and not terminating with long arista; flowers in simple or
compound cymes or dense glomerules...........Dysphania
Dysphanieae Pax in Engler & Prantl, Nat. Pflanzenfam.
3(1b): 92. 1889 ≡Dysphaniaceae Pax in Bot. Jahrb. Syst.
61: 230. 1927 –Type: Dysphania R.Br.
= Suckleyinae G.L.Chu & Stutz in Amer. J. Bot. 78(1): 65.
1991 –Type: Suckleya A.Gray.
= Neobotrydieae G.L.Chu in Chu & Sanderson, Gen. New
Evol. System World Chenopod.: 72. 2017 –Type: Neo-
botrydium Moldenke.
Dysphania R.Br., Prodr.: 411. 1810 –Type: Dysphania litto-
ralis R.Br.
=Roubieva Moq. in Ann. Sci. Nat., Bot., ser. 2, 1: 292. 1834 ≡
Ambrina Spach, Hist. Nat. Vég. 5: 295. 1836, nom.
superfl. & illeg. –Type: Roubieva multifida (L.) Moq.
(≡Dysphania multifida (L.) Mosyakin & Clemants).
=Cyclolepis Moq. in Ann. Sci. Nat., Bot., sér. 2, 1: 203. 1834,
nom. illeg., non Gillies ex D.Don 1832 ≡Cycloloma Moq.,
Chenop. Monogr. Enum.: 17. 1840 –Type: Сycloloma pla-
typhyllum (Michx.) Moq. (= C. atriplicifolium (Spreng.)
J.M.Coult. ≡Dysphania atriplicifolia comb. nov.).
=Botrydium Spach, Hist. Nat. Vég. 5: 298. 1836, nom. illeg.,
non Wallr. 1815 ≡Neobotrydium Moldenke in Amer.
Midl. Naturalist 35: 330. 1946 –Type: Neobotrydium
botrys (L.) Moldenke (≡Dysphania botrys (L.) Mosyakin
& Clemants).
=Meiomeria Standl. in Britton & al., N. Amer. Fl. 21: 7. 1916
–Type: Meiomeria stellata Standl. (≡Dysphania stellata
(Standl.) Mosyakin & Clemants).
Description. –Annuals or short-lived perennial herbs,
more or less covered with simple multicellular hairs and
stalked glandular hairs/subsessile glands, sometimes glabres-
cent, usually aromatic. Stems rarely somewhat woody in lower
part, erect, ascending, decumbent or prostrate, branched(rarely
± simple), not jointed, not spiny, not fleshy. Leaves alternate,
usually petiolate; blade lanceolate, oblanceolate, ovate or ellip-
tic, entire or lobed to pinnatisect, margins entire, sinuate, den-
tate or serrate, base cuneate to truncate, apex obtuse, acute or
acuminate. Inflorescences terminal, loosely paniculate, of sim-
ple or compound dichasial cymes, or spiciform and of dense
axillary glomerules; glomerules may be subtended by reduced
leaves (sometimes referred to as “leaflike bracts”). Flowers
bisexual or sometimes polygamous (at least functionally). Peri-
anth segments 1–5, rarely 6–9(D. stellata), free or variously
connate from the base, flat to variously keeled with longitudi-
nal or rarely (D. atriplicifolia) transverse outgrowths. Stamens
0–5. Ovary superior; style short or ± absent, stigmas 1–5, fili-
form. Fruits 1-seeded, often enclosed in perianth; pericarp
adherent or non-adherent, membranous, smooth, papillate,
with glands, glandular hairs or rarely with simple hairs (D. atri-
plicifolia). Seeds horizontal or vertical (rarely oblique), glo-
bose to lenticular or ellipsoidal; seed coat reddish brown or
black, smooth to rugose, rarely reticulate with deep pits (D. dis-
secta); outer cell walls of the testal layer without stalactites;
embryo annular or almost straight, with copious farinose
perisperm.
Note. –The inclusion of Cycloloma within Dysphania is
stated for the first time, and two peculiarities of Cycloloma –
circular wing-like outgrowth on the perianth evidently enhanc-
ing anemochory, and presence of long simple hairs on the peri-
carp, missing in all Chenopodioideae –emend the description
of Dysphania.
1. Dysphania sect. Adenois (Moq.) Mosyakin & Clemants in
Ukrayins’k. Bot. Zhurn. 59(4): 382. 2002 ≡Ambrina sect.
Adenois Moq., Chenop. Monogr. Enum.: 39. 1840 ≡Che-
nopodium [unranked] Ambrosioidia Standl. in Britton
& al., N. Amer. Fl. 21: 26. 1916 ≡Chenopodium [subg.
Ambrosia] sect. Adenois (Moq.) L.E.Simón in Anales
Jard. Bot. Madrid 54: 138. 1996 –Type (designated by
Simón in Anales Jard. Bot. Madrid 54: 138. 1996): Che-
nopodium ambrosioides L. (≡Dysphania ambrosioides
(L.) Mosyakin & Clemants).
=Roubieva Moq. in Ann. Sci. Nat., Bot., sér. 2, 1: 292. 1834 ≡
Ambrina Spach, Hist. Nat. Vég. 5: 295. 1836, nom.
superfl. & illeg. ≡Chenopodium sect. Ambrina Benth.
& Hook.f., Gen. Pl. 3(1): 51. 1880 ≡Chenopodium sect.
Roubieva (Moq.) Rouy in Rouy & Foucaud, Fl. France
12: 53. 1910 ≡Chenopodium [subg. Ambrosia sect. Ade-
nois] subsect. Roubieva (Moq.) L.E.Simón in Anales
Jard. Bot. Madrid 54: 138. 1996 ≡Dysphania sect. Rou-
bieva (Moq.) Mosyakin & Clemants in Ukrayins’k. Bot.
Zhurn. 59(4): 382. 2002 –Type: Roubieva multifida (L.)
Moq. (≡Dysphania multifida (L.) Mosyakin & Clemants).
=Chenopodium sect. Nigrescentia Aellen in Acta Bot. Acad.
Sci. Hung. 19: 3. 1973 –Type: Chenopodium burkartii
(Aellen) Worosch. (≡Dysphania burkartii (Aellen)
Mosyakin & Clemants).
Description. –Annuals or perennials, with subsessile
glands and glandular and multicellular simple hairs. Stems
sometimes woody in the lower part, erect to ascending or pro-
cumbent, variously branched. Leaves short-petiolate (in inflo-
rescence sessile); blades entire, lobed or pinnatifid, oblong-
ovate, oblong or lanceolate, margins almost entire to sinuate or
16 Version of Record
Uotila & al. •Systematics of Dysphanieae TAXON 00 (00) •1–26
dentate, base cuneate, apex acute or fairly obtuse. Inflorescences
more or less spiciform, leafy, or branches leafless; flowers clus-
tered in dense sessile glomerules, sometimes some flowers sol-
itary. Perianth segments (3–)4–5, basally connate for 1/4–3/4
of their length, cucullate, or fused to form sac surrounding
the fruit, abaxially rounded or keeled, rarely with transverse
wing, glabrous or with glands or multicellular hairs. Stamens
4–5. Stigmas 2–5. Pericarp ± loose. Seeds mostly horizontal,
sometimes vertical, up to 1.3 mm, subglobose to obovoid; seed
coat black, smooth or indistinctly sculptured.
Included species. –13 species: Dysphania ambrosioides
(L.) Mosyakin & Clemants (2n= 32), D. anthelmintica (L.)
Mosyakin & Clemants (2n= 64), D. atriplicifolia (Spreng.)
G.Kadereit, Sukhor. & Uotila, comb. nov. (≡Salsola atriplici-
folia Spreng., Nachtr. Bot. Gart. Halle: 35. 1801 ≡Cycloloma
atriplicifolium (Spreng.) J.M.Coult. in Mem. Torrey Bot. Club
5: 143. 1894) (2n=36),D. bonariensis (Hook.f.) Mosyakin
& Clemants ex Sukhor. (not analysed), D. burkartii (Aellen)
Mosyakin & Clemants (not analysed), D. chilensis (Schrad.)
Mosyakin & Clemants (2n=32),D. microcarpa (Phil.) Mosya-
kin & Clemants (not analysed), D. multifida (L.) Mosyakin &
Clemants (2n= 32), D. oblanceolata (Speg.) Mosyakin
& Clemants (not analysed), D. retusa (Juss. ex Moq.) Mosyakin
& Clemants (2n= 64) (not analysed), D. sooana (Aellen)
Mosyakin & Clemants (not analysed), D. tomentosa (Thouars)
Mosyakin & Clemants (not analysed) and D. venturii (Aellen)
Mosyakin & Clemants (2n= 32) (not analysed). –Dysphania
anthelmintica and D. atriplicifolia are distributed in North
America, D. tomentosa on Tristan da Cunha, the other species
in South America. Dysphania ambrosioides is widespread as
naturalized species in the tropics and subtropics including
southern North America, and D. multifida in southern North
America, the Mediterranean Europe, Australia, northern and
southern Africa. Dysphania chilensis is reported as natural-
ized in coastal areas of the southwestern U.S.A. (e.g., Clem-
ants & Mosyakin, 2003).
Notes. –In the molecular anlaysis, Dysphania atripicifolia
was sister to the other species of D.sect.Adenois; in addition, it
has unique morphological charaters within the genus, which
might allow to recognize a subsection for it. However, there
are several American species, three of them morphologically
distinctive, that were not included in our analysis, and due to
lack of this information, no further division of D.sect.Adenois
was adopted. Dysphania anthelmintica, sometimes considered
only a variety of the polymorphic species D. ambrosioides,
proved to be sister to the remaining taxa of the group, i.e.,
D. ambrosioides,D. chilensis and D. multifida.Dysphania
anthelmintica is morphologically much closer to the two first
species than to D. multifida.However,D. anthelmintica is quite
well distinguished from D. ambrosioides and D. chilensis by
regularly lobed leaves and leafless branches of the inflores-
cence. Furthermore, according to the few chromosome counts
available, it might be octoploid, whereas the others are tetra-
ploids. Even their native areas appear different: D. anthelmin-
tica grows in North America round the Gulf of Mexico,
D. chilensis originates from the southern part of South
America, while the indigenous area of D. ambrosioides is
probably in South America. Dysphania ambrosioides and
D. anthelmintica have been cultivated as medicinal plants, but
many of the plants cultivated under the name Chenopodium
anthelminticum L. or Dysphania anthelmintica seem to be
misidentified and belong to D. ambrosioides.
The molecular difference between Dysphania multifida
and D. ambrosioides +D. chilensis agrees with their consider-
able morphological differences in leaf shape and perianth
characters, which in earlier treatments led to their placements
in different sections or even in different genera. Dysphania
bonariensis and D. microcarpa share a flattened, elongated
and hardened, always closed perianth with D. multifida.
Dysphania ambrosioides and D. chilensis are morpholog-
ically close to each other. Dysphania ambrosioides is poly-
morphic and obviously taxonomically heterogeneous, while
D. chilensis has been sometimes misunderstood. Further, there
are several species, not included in our analysis, that are mor-
phologically fairly similar to D. ambrosioides,asD. oblan-
ceolata and D. tomentosa.Dysphania burkartii,D. retusa,
D. sooana and D. venturii are morphologically well-separate
from D. ambrosioides even though usually placed near it, for
instance, Aellen (1973) included them into D. sect. Ambrina,
except for D. burkartii (as Chenopodium burkartii), which
was placed in a monotypic D.sect.Nigrescentia mainly because
it turns blackish when pressed. Additional morphological and
molecular studies are needed for proper understanding of the
variation and taxonomy of this section.
2. Dysphania sect. Botryoides (C.A.Mey.) Mosyakin & Clem-
ants in Ukrayins’k. Bot. Zhurn. 59(4): 383. 2002 ≡Cheno-
podium sect. Botryoides C.A.Mey. in Ledebour, Fl. Altaic.
1: 410. 1829 ≡Chenopodium sect. Botrys W.D.J.Koch,
Syn. Fl. Germ. Helv.: 607. 1837 ≡Ambrina sect. Botryois
Moq., Chenop. Monogr. Enum.: 36. 1840 ≡Chenopo-
dium sect. Botryois Moq. in Candolle, Prodr. 13(2): 72.
1849 ≡Chenopodium [unranked] Botryes Standl. in Brit-
ton & al., N. Amer. Fl. 21: 25. 1916 ≡Chenopodium
[sect. Botryoides]subsect.Botrys(W.D.J.Koch) Aellen
& Iljin in Komarov, Fl. URSS 6: 46. 1936 ≡Dysphania
subsect. Botrys (W.D.J.Koch) Mosyakin & Clemants in
Ukrayins’k. Bot. Zhurn. 59(4): 383. 2002 –Type: Cheno-
podium botrys L. (≡Dysphania botrys (L.) Mosyakin
&Clemants).
=Botrydium Spach, Hist. Nat. Vég. 5: 298. 1836, nom. illeg.,
non Wallr. 1815 ≡Chenopodium sect. Botrydium Benth.
& Hook.f., Gen. Pl. 3(1): 51. 1880 ≡Neobotrydium Mol-
denke in Amer. Midl. Naturalist 35: 330. 1946 –Type:
Neobotrydium botrys (L.) Moldenke (≡Dysphania botrys
(L.) Mosyakin & Clemants).
Description. –Annuals, with multicellular simple and
glandular hairs and subsessile glands. Stems mostly erect, bran-
ched. Leaves with fairly short petiole; blades ovate to elliptic,
shallowly to deeply lobate, lyrate-sinuate, sinuate-dentate,
erose-dentate, or pinnatifid, occasionally entire, base cuneate
to truncate, apex ± obtuse. Inflorescence mainly terminal,
Version of Record 17
TAXON 00 (00) •1–26 Uotila & al. •Systematics of Dysphanieae
mostly leafless, loosely paniculate, composed of compound
small dichasial cymes and solitary flowers; rarely ultimate
branches bifurcate, sterile (D. tibetica). Perianth segments
free to variously connate, more or less navicular, flat to swol-
len abaxially, with glandular hairs/subsessile glands and often
multicellular hairs, sometimes narrow lobes. Stamens (1–)5.
Stigmas 2. Pericarp ± adherent. Seeds mostly horizontal, some-
times vertical, rarely oblique, 0.5–1.1 mm, orbicular or sligh-
tly ovate in outline, lenticular, margin obtuse to truncate; seed
coat brown, red or black, smooth or faintly reticulate.
Included species. –10 species: Dysphania bhutanica
Sukhor., D. botrys (L.) Mosyakin & Clemants (2n= 18),
D. geoffreyi Sukhor., D. himalaica Uotila, D. kitiae Uotila (not
analysed), D. multiflora (Moq.) G.Kadereit, Sukhor. & Uotila,
comb. nov. (≡Chenopodium multiflorum Moq. in Candolle,
Prodr. 13(2): 75. 1849), D. neglecta Sukhor., D. nepalensis
(Colla) Mosyakin & Clemants, D. procera (Hochst. ex Moq.)
Mosyakin & Clemants (2n=36),D. tibetica (A.J.Li) Uotila. –
Most species are distributed mainly in the Himalayas and adja-
cent China; C. botrys occurs in Central Asia to the Arabian
Peninsula and Mediterranean Europe and Africa, and D. pro-
cera in eastern Africa and the adjacent Arabian Peninsula.
Notes. –Up to now Dysphania sect. Botryoides included
also a few American taxa, usually as D. subsect. Incisa.Remov-
ing this group does not cause marked changes in the morpho-
logical description of D.sect.Botryoides, the most important
change being the absence of sterile inflorescence branches end-
ing with a knot of an abortive flower. Furthermore, the area of
D.sect.Botryoides is now limited to Asia (including the Ara-
bian Peninsula), East Africa (D. procera) and North Africa
and southern Europe (D. botrys). The latter species occurs as
introduced in North America. Even though D. kitiae has several
special features, as deeply divided leaves and a strong keel in
the apical part of the perianth, it seems to belong to D.sect.
Botryoides. Recognizing D. multiflora at species rank was con-
firmed by molecular characters but supposed on the basis of
leafy inflorescences; it was earlier included in the polymorphic
D. nepalensis (e.g., Uotila, 2013; Sukhorukov & Kushunina,
2014; Sukhorukov & al., 2019a).
3. Dysphania sect. Dysphania ≡Chenopodium sect. Dyspha-
nia (R.Br.) Aellen in Bot. Jahrb. Syst. 63: 486. 1930 –
Type: Dysphania littoralis R.Br.
=Chenopodium sect. Orthosporum R.Br., Prodr.: 407. 1810
≡Dysphania sect. Orthospora (R.Br.) Mosyakin &
Clemants in Ukrayins’k. Bot. Zhurn. 59(4): 382. 2002
–Type (designated by Ulbrich in Engler & Prantl, Nat.
Pflanzenfam., ed. 2, 16c: 494. 1934): Chenopodium cari-
natum R.Br. (≡Dysphania carinata (R.Br.) Mosyakin
& Clemants).
=Chenopodium [unranked] Carinata Standl. in Britton & al.,
N. Amer. Fl. 21: 27. 1916 –Type: Chenopodium carina-
tum R.Br. (≡Dysphania carinata (R.Br.) Mosyakin &
Clemants).
=Chenopodium sect. Tetrasepalae Aellen in Bot. Jahrb. Syst.
63: 490. 1930 ≡Dysphania sect. Tetrasepalae (Aellen)
A.J.Scott in Bot. Jahrb. Syst. 100: 218. 1978 –Type (des-
ignated by Scott in Bot. Jahrb. Syst. 100: 218. 1978): Dys-
phania inflata (Aellen) A.J.Scott (= D. rhadinostachya
subsp. inflata (Aellen) Paul G.Wilson).
=Dysphania sect. Caudatae A.J.Scott in Bot. Jahrb. Syst.
100: 218. 1978 –Type: Dysphania plantaginella
F.Muell.
Description. –Annual or short-lived perennials, with
multicellular simple and glandular hairs and glands. Stems
prostrate, procumbent or erect. Leaves almost sessile to fairly
short petiolate; blade elliptic to ovate, entire or variously
lobed, margin entire to sinuous, base cuneate or truncate, apex
obtuse. Inflorescence spiciform, axillary and terminal, of com-
pact, ± sessile glomerules. Flowers bisexual or functionally
female. Perianth segments 1–5, free to variously connate, cucul-
late to navicular, in fruit stage swollen or enlarged and hard-
ened, sometimes prominently keeled or winged, glabrous,
variously glandular or with multicellular hairs. Stamens 0–2.
Stigmas 1–2, short. Pericarp mostly ± adherent. Seeds verti-
cal, oblique or horizontal, globular, ellipsoidal or lenticular,
0.3–0.6 mm; seed coat smooth.
Included species. –17 species: Dysphania carinata (R.Br.)
Mosyakin & Clemants, D. congestiflora S.J.Dillon & A.S.Mar-
key, D. cristata (F.Muell.) Mosyakin & Clemants, D. glandu-
losa Paul G.Wilson, D. glomulifera (Nees) Paul G.Wilson,
D. kalpari Paul G.Wilson, D. littoralis R.Br., D. melanocarpa
(J.M.Black) Mosyakin & Clemants, D. plantaginella F.Muell.,
D. platycarpa Paul G.Wilson, D. pumilio (R.Br.) Mosyakin
&Clemants(2n= 16, 18), D. pusilla (Hook.f.) Mosyakin
& Clemants (not analysed), D. rhadinostachya (F.Muell.)
A.J.Scott, D. simulans F.Muell. & Tate, D. sphaerosperma
Paul G.Wilson, D. truncata (Paul G.Wilson) Mosyakin &
Clemants, D. valida Paul G.Wilson. –All species are endemic
to Australia, excluding D. pusilla, which is probably endemic
to New Zealand; D. pumilio and D. carinata are frequently
naturalized in other continents, D. pumilio also in New
Zealand.
Notes. –The exclusion of Dysphania saxatile from the
other Australian taxa makes D. sect. Dysphania morphologi-
cally more homogeneous, e.g., in inflorescence morphology.
Dysphania pusilla is the only species of the section not ana-
lysed by us. It is regarded as morphologically related to D. pu-
milio (Wilson, 1983; Webb & al., 1988; De Lange, 2020),
even though rather different in habit, leaf form, seeds size and
number of perianth segments (usually only 4 segments instead
of usually 5 in D. pumilio). Also, preliminary DNA data based
on one marker (nrDNA ITS) places it with D. pumilio
(De Lange, 2020).
4. Dysphania sect. Incisa (Standl.) G.Kadereit, Sukhor. &
Uotila, comb. & stat. nov. ≡Chenopodium [unranked]
Incisa Standl. in Britton & al., N. Amer. Fl. 21: 25. 1916
≡Dysphania [sect. Botryoides] subsect. Incisa (Standl.)
Mosyakin & Clemants in Ukrayins’k. Bot. Zhurn. 59(4):
383. 2002 –Type: Chenopodium incisum Poir. (= Dys-
phania graveolens (Willd.) Mosyakin & Clemants).
18 Version of Record
Uotila & al. •Systematics of Dysphanieae TAXON 00 (00) •1–26
Description. –Annuals, with subsessile glands and thin
multicellular simple hairs. Stems erect, branched. Leaves with
rather short petiole; blade lanceolate to ovate or elliptic, sinuate-
pinnatifid or laciniate-pinnatifid to deeply dentate, sinuate or
entire, base truncate or cuneate, apex obtuse to acuminate. Inflo-
rescence paniculate, axillary and terminal, loose, of dichasial
few-flowered cymes and single flowers, often with ultimate
branches ending with a small knot (abortive flower). Perianth
segments 5, basally shortly connate, abaxially fairly flat but
often with prominent appendage(s) in the apical part, with sub-
sessile glands. Stamens 0–5. Stigmas 2. Pericarp rugose, adher-
ent. Seeds horizontal, 0.5–0.8 mm, depressed-globose; seed
coat dark brown.
Included species. –2 species: Dysphania graveolens
(Willd.) Mosyakin & Clemants (2n= 32) in southern North
America and D. mandonii (S.Watson) Mosyakin & Clemants
(2n= 54) in South America (Argentina, Bolivia, Chile, Peru).
Notes. –Dysphania graveolens and Teloxys aristata
resemble each other in having long sterile ultimate branches
of the inflorescence. This similarity led Aellen (1960) to in-
clude D. graveolens (as Chenopodium graveolens Willd.) in
Chenopodium sect. Botryoides subsect. Teloxys (Moq.) Aellen
& Iljin (now genus Teloxys). Also Dysphania tibetica from
D. sect. Botryoides has sterile ultimate inflorescence branches
(Uotila, 2013). This character seems to have developed con-
vergently in different lineages of the tribe and led to a some-
what different result: In D. sect. Incisa, the ultimate branches
are terminated by an abortive flower visible as a knot; in
D. tibetica, the sterile branches are short, somewhat hooked;
and in Teloxys, they are long, needle-like aristae. Morpholog-
ically, the species of D. sect. Incisa are relatively similar to
those of D.sect.Botryoides and more dissimilar with the
other American section D. sect. Adenois. Scott (1978a) mer-
ged D. sect. Incisa under D. subsect. Botrys, and Mosyakin
& Clemants (2008) regarded it as a subsection in D. sect.
Botryoides.
5. Dysphania sect. Margaritaria (Brenan) G.Kadereit,
Sukhor. & Uotila, comb. nov. ≡Chenopodium sect. Mar-
garitaria Brenan in Kew. Bull. 11: 166. 1956 –Type:
Chenopodium congolanum (Hauman) Brenan (≡Dyspha-
nia congolana (Hauman) Mosyakin & Clemants).
Description. –Annuals, with multicellular simple hairs
and subsessile glands. Stems mostly erect, sometimes pros-
trate, branched mostly in lower part, branches often long,
spreading. Leaves short-petiolate; blade lanceolate to ovate
or elliptic, deeply pinnatifid to entire with sinuate to lobed
margins, base cuneate, apex obtuse to subacute. Inflorescence
axillary and terminal, narrowly paniculate, composed of com-
pound dichasial cymes and solitary flowers. Perianth segments
4 or 5, free near to the base, navicular, abaxially somewhat
swollen to cristately keeled, with subsessile glands or multi-
cellular hairs. Stamens 0–5. Stigmas 2. Pericarp thin, adherent
to the seed, sometimes glandular. Seeds vertical or horizontal,
0.6–1.0 mm, lenticular to semiglobose; seed coat black or
brown, finely and reticulately rugulose or smooth.
Included species. –4 species: Dysphania congolana
(Hauman) Mosyakin & Clemants, D. pseudomultiflora (Murr)
Verloove & Lambinon, D. saxatilis (Paul G.Wilson) Mosyakin
& Clemants, D. schraderiana (Schult.) Mosyakin & Clemants
(2n=18).–Dysphania saxatilis is a West-Australian species
largely inhabiting rocky places like hillslopes, hill tops and
escarpments of tablelands; the three others are in Africa, with
differing distribution patterns: foothills and mountains of trop-
ical Africa (D. congolana; Sukhorukov & al., 2016), southern
Africa (D. pseudomultiflora; Sukhorukov & al., 2019b), and
foothills and mountains of eastern Africa and southwestern
mountains of the Arabian Peninsula, with secondary distribu-
tion in Europe and West Asia (D. schraderiana).
Notes. –Brenan (1956) considered that the tropical African
Chenopodium congolanum is in some respects a morphological
link between C.sect.Botryoides and C.sect.Orthosporum and
proposed a new section C.sect.Margaritaria for it. Wilson
(1983) was uncertain of the placement of Chenopodium saxa-
tile and considered options between Dysphania s.str. and
Chenopodium sect. Orthosporum, sect. Botryoides and sect.
Margaritaria. He solved the difficulty by emending C. sect.
Orthosporum to cover also C. saxatile, e.g., by accepting also
4 perianth segments and 2 stamens, and allowing more open
lateral branches of the inflorescence. Zhang & Zhu (2016)
moved Dysphania saxatile to Neobotrydium.
Dysphania sect. Margaritaria is small but morphologi-
cally heterogeneous. Dysphania pseudomultiflora and
D. schraderiana are fairly similar with usually pinnatifid
leaves, mostly leafless inflorescence, 5 carinate to cristate
perianth segments and horizontal seeds. By contrast,
D. congolana and D. saxatile have less-lobed leaves, leafy
inflorescences, four somewhat swollen perianth segments,
and vertical seeds. Some other characters break this group-
ing. The perianth segments of D. saxatile have multicellular
simple hairs but no glands, while in the other species simple
hairs are missing but glands are present. Dysphania congo-
lana has a smooth pericarp, while the other species have
papillate pericarp.
Neomonolepis Sukhor. in PhytoKeys 109: 121. 2018 –Type:
Neomonolepis spathulata (A.Gray) Sukhor. (≡Monolepis
spathulata A.Gray ≡Blitum spathulatum (A.Gray)
S.Fuentes, Uotila & Borsch).
Description. –Non-aromatic, small, glabrous, annuals.
Stem branched or not, lateral branches (if present) ascending.
Leaves short-petiolate to sessile; blade spathulate-oblong, mar-
gin entire. Inflorescence leafy (bracts similar to stem leaves)
composed of axillary, small glomerules; flowers sessile or short-
ly pedicellate, with unisexual, pistillate and staminate flowers
mixed in small glomerules. Male flowers with 2-lobed hyaline
perianth, stamens 1–2, anthers 0.10–0.15 mm long. Female
flowers with reduced perianth, stigmas 2(–3). Fruits ca. 0.5 mm,
almost globose; pericarp blackish, papillate, easily ruptured.
Seeds vertical, 0.4 × 0.3 mm; seed coat reddish, smooth, with
tiny irregular pits, outer cell walls of the testal layer with sta-
lactites. Embryo vertical.
Version of Record 19
TAXON 00 (00) •1–26 Uotila & al. •Systematics of Dysphanieae
One species, Neomonolepis spathulata (A.Gray) Sukhor.;
western North America (Holmgren, 2003).
Suckleya A.Gray in Proc. Amer. Acad. Arts 11: 103. 1876 –
Type: Suckleya suckleyana (Torr.) Rydb. (≡Obione suck-
leyana Torr.).
Description. –Annuals, with inflated papillate cells and
multicellular glandular hairs, lacking essential oils (Fig. 5C).
Stems prostrate or ascending, diffusely branched. Leaves usu-
ally fairly long-petiolate; blade rhombic-ovate to suborbicular,
repand-dentate. Inflorescence of axillary glomerules; flowers
unisexual, monoecious, with pistillate and staminate flowers
mixed in glomerules. Staminate flowers usually with 4 free
perianth segments, 4 stamens and sometimes rudimentary
ovary. Pistillate flowers zygomorphic, with 4 somewhat fleshy
perianth segments, which become fused, enlarged and com-
pressed in fruit; ovary ovoid, stigmas 2. Fruit enclosed by
the enlarged perianth, ovate to triangular-ovate, compressed;
pericarp thin, adnate to the seed. Seeds vertical, to 3 mm; seed
coat brown, smooth; outer cell walls of the testal layer without
stalactites. Embryo subannular, surrounding the copious peri-
sperm, radicle superior.
Suckleya has a zygomorphic female perianth and flat-
tened fruits that differentiate it from other Dysphanieae.
One species, Suckleya suckleyana (Torr.) Rydb. (2n=18);
midwestern U.S.A. and southern Alberta, Canada (Chu &
al., 1991; Chu, 2003).
Teloxys Moq. in Ann. Sci. Nat., Bot., ser. 2, 1: 289. 1834 ≡
Chenopodium sect. Teloxys (Moq.) Beck in Reichenbach,
Icon. Fl. Germ. Helv. 24: 116. 1908 ≡Chenopodium
[unranked] Aristata Standl. in Britton & al., N. Amer. Fl.
21: 25. 1916 ≡Chenopodium [sect. Botryoides]subsect.
Teloxys (Moq.) Aellen & Iljin in Komarov, Fl. URSS 6:
47. 1936 ≡Dysphania [sect. Botryoides] subsect. Telox ys
(Moq.) Mosyakin & Clemants in Ukrayins’k. Bot. Zhurn.
59(4): 383. 2002 –Type: Teloxys aristata (L.) Moq. (≡Che-
nopodium aristatum L.).
Description. –Non-aromatic, small annuals, richly
branched and tumble-weed in habit, the stem base covered
with papillae and multicellular simple hairs (Fig. 5D), other
parts ± glabrous. Leaves subsessile; blade up to 6 cm, linear,
narrowly oblong or spathulate, often folded on the ventral side,
margin entire. Inflorescence terminal, paniculate; flowers ses-
sile or short-pedicellate in loose dichotomous cymes, ultimate
branches usually sterile, terminating with acicular apices,
sometimes (in wet habitats) without acicular apices. Perianth
segments 5, free to base, hyaline, sometimes pinkish, glabrous,
abaxially subcarinate. Styles 2(3). Fruit compressed-spheri-
cal; pericarp tightly adjoining the seed and separating from
it when rubbed, smooth. Seeds horizontal, 0.7–0.8 mm, mar-
gin keeled, seed coat reddish-black, smooth; outer cell walls
of the testal layer without stalactites. Embryo horizontal, rarely
obliquely or vertically orientated.
One species, Teloxys aristata (L.) Moq. (2n= 18);
distributed in Central Asia and more or less established
as an alien in many parts of temperate Eurasia and North
America.
Uncertain placements. —Most of the Dysphanieae
species that were not included in our analysis are morpholog-
ically so closely related to the studied species of Dysphania
that it is possible to list them in the present sectional division
of Dysphania. However, three American species of Dyspha-
nieae have specialized morphological features that indicate
that they obviously belong to Dysphania, but their placements
in the present sectional grouping remain uncertain. They are
briefly discussed here.
Dysphania minuata (Aellen) Mosyakin & Clemants (≡Che-
nopodium minuatum Aellen).
Aellen (1973) described Chenopodium minuatum as a
member of C.sect.Ambrina, but later Simón (1996) pro-
posed to transfer the species to the African C. sect. Marga-
ritaria. In addition to some morphological features similar
to C. congolanum, she pointed out possible phytogeogra-
phic relationships across the Atlantic Ocean: Chenopodium
minuatum was described and known only from the Atlantic
coastal regions of eastern Brazil (Simón, 1995); however, it is
probably more widespread in tropical South America. A fairly
robust specimen from northern Peru (Prov. Piura, Piura, 1865,
R. Spruce, BM!, G!), seems to belong to D. minuata. Sukhor-
ukov & al. (2016) did not consider D. minuata closely related
to the African D.congolana despite the morphological simi-
larity in leaf shape and vertical seed embryo position. However,
D. minuata deviates from the South American D.sect.Adenois
in leaf characters, branching of the inflorescence and hairy peri-
anth, and its placement pends molecular confirmation.
Dysphania dissecta (Moq.) Mosyakin & Clemants (≡Amb-
rina dissecta Moq. ≡Chenopodium dissectum (Moq.)
Standl. = Chenopodium bipinnatifidum Moric. ex Moq.).
Small, branched annual with glandular and multicellular
hairs. Leaves sparsely pinnatisect, lobes linear, as wide as the
rachis, with few very short secondary lobes, apex and lobes
obtuse. Flowers dense on short paniculate branches in leaf axils,
subsessile. Perianth segments 5, deeply split, not contiguous,
abaxially swollen in fruit stage. Seeds ca. 1 mm, globose, with
prominently reticulate surface, pits deep. Similar seeds are not
known in other Dysphanieae. Dysphania dissecta is known
from Mexico, in mountainous areas from the State of Puebla
to the State of Coahuila. Standley (1916) placed Chenopodium
dissectum, together with C. botrys,inhisC. [unranked] Botryes;
instead, Mosyakin & Clemants (2008) included D. dissecta in
Dysphania subsect. Incisa, together with D. graveolens and
D. mandonii.
Dysphania stellata (S.Watson) Mosyakin & Clemants (≡
Chenopodium stellatum S.Watson ≡Meiomeria stellata
(S.Watson) Standl.).
Small, branched annual with glandular and multicellular
hairs. Leaves subsessile, linear, entire, obtuse. Flowers densely
20 Version of Record
Uotila & al. •Systematics of Dysphanieae TAXON 00 (00) •1–26
on spiciform branches in leaf axils, subsessile; perianth seg-
ments 6–9 (Fig. 6A), almost free, concave, linear, not contig-
uous, strongly swollen abaxially and becoming winged and
dentate in fruit. Pericarp with tubular papillae. Seeds verti-
cal, 0.3–0.4 mm. Flowers deviate from other Dysphanieae
in particular as to the high number of perianth segments.
Additionally, this species drastically differs in having tubu-
lar pericarp papillae (Fig. 6B) that are not mentioned in any
American Dysphania (only D. dissecta was not studied).
Such papillae are very similar to those of D. schraderiana
(Sukhorukov, 2014: plate 8, fig. 6). Watson (1883) stated
that the species is allied to Chenopodium carinatum (≡Dys-
phania carinata). Standley (1916) described a new genus
Meiomeria for it, which was generally accepted since Scott
(1978a) transferred it back to Chenopodium as the monotypic
C. sect. Meiomeria. When transferred to Dysphania Mosya-
kin & Clemants (2008) did not place it in any section.
■AUTHOR CONTRIBUTIONS
PU, APS and GK designed the project. JMD, PU, APS and GK
contributed samples. NB, AAK and GK conducted labwork and mole-
cular data analyses. PU and APS conducted morphological analyses.
PU, APS and GK contributed to the biogeographical and taxonomic
part. PU, APS and GK wrote the draft; all authors approved and con-
tributed to the final version of the paper. —PU, https://orcid.org/0000-
0002-3707-0454; APS, https://orcid.org/0000-0003-2220-826X; AAK,
https://orcid.org/0000-0002-0653-3655; GK, https://orcid.org/0000-
0003-0094-8769
■ACKNOWLEDGEMENTS
We would like to thank the curators and personnel of the following
herbaria: AD, AQ, B, BCN, BEI, BM, C, E, G, GLM, H, HAL, K,
KAS, LE, M, MJG, MO, MPU, MSB, MW, NSW, P, PERTH, S, STU,
TARI, TUH, UPS, W, WU and Z for providing loans and for assistance
during visits. We are also grateful to Helen Vonow (AD), Kelly Shep-
herd (PERTH), Karina Knight and John Huisman (WA), and Ailsa Hol-
land (BRI) for additional DNA samples, and to two bachelor students,
Karin Fehr and Kristina Lust, for generating part of the sequences dur-
ing their projects. We thank Steven Dillon (PERTH) and Peter Lang
(AD), who reexamined the identity of some samples from Australia.
We are grateful to Michael Huft (Dysphania atriplicifolia), Joseph
DiTomaso (D. multifida), Robert Bielesch (Suckleya suckleyana), and
Elena Bayandina (Teloxys aristata) for the excellent images of living
plants. We thank Marie Claire Veranso (Mainz) for assistence with Bio-
GeoBEARS and Alexander N. Sennikov (H) for valuable help in
nomenclature. We thank Sergei M. Mosyakin (KW) for useful sugges-
tions that improved the paper. Alexander Sukhorukov and Anastasiya
Krinitsina thank the Russian Foundation for Basic Research (project
18-04-00029), Moscow State University Grant for Leading Scientific
Schools “Depository of the Living Systems”, Russian Academic Excel-
lence Project 5-100, Sechenov University (AK) and Tomsk State Uni-
versity competitiveness improvement programme (AS) for financial
support. Pertti Uotila thanks The Otto A. Malm Foundation and Conser-
vatoire Jardin et Botaniques Genevé for financial support for recent her-
barium visits.
■LITERATURE CITED
Aellen, P. 1930a. Die systematische Stellung und Gliederung der
R. Brownischen Gattung Dysphania. Bot. Jahrb. Syst. 63: 482–490.
Aellen, P. 1930b. Eine neue Sektion der Gattung Chenopodium (Sect.
Tetrasepala). Bot. Jahrb. Syst. 63: 490–492.
Aellen, P. 1960. Chenopodiaceae (1. & 2. Teil). Pp. 533–692 in:
Hegi, G. (ed.), Illustrierte Flora von Mitteleuropa, vol. 3 (2/2–
3). Ed. K.-H. Rechinger. Munich: Hanser.
Aellen, P. 1961. Dysphaniaceae. P. 748 in: Hegi, G., Illustrierte Flora
von Mitteleuropa, vol. 3 (2/4). Ed. K.-H. Rechinger. Munich: Hanser.
Aellen, P. 1973. Formenkreis von Chenopodium L. sect. Ambrina
(Spach) Benth. & Hook. und sect. Nigrescentia Aellen. Acta
Bot. Acad. Sci. Hung. 19(1–4): 1–12.
Ankova, T.V. & Zykova E.Y. 2018. [Report]. P. 1041 in: Marhold,
K. & Kucˇera, J. (eds.), IAPT chromosome data 27. Taxon 67:
1041–1047. https://doi.org/10.12705/675.24
Auquier, P. & Renard, R. 1975: Nombres chromosomiques de quelques
Angiospermes du Rwanda, Burundi et Kivu (Zaire). I. Bull. Jard.
Bot. Natl. Belg. 45: 421–445. https://doi.org/10.2307/3667493
Fig. 6. SEM images of the perianth and pericarp ultrasculpture of Dysphania stellata.A, Perianth in fruit stage with 9 winged segments; B, Papillae
on the pericarp; Mexico, Coahuila, 1800, E. Palmer 1155 (LE).
Version of Record 21
TAXON 00 (00) •1–26 Uotila & al. •Systematics of Dysphanieae
Ávila-Blanco, M.E., Rodríguez, M.G., Moreno Duque, J.L.,
Muñoz-Ortega, M. & Ventura-Juárez, J. 2014. Amoebicidal
activity of essential oil of Dysphania ambrosioides (L.) Mosyakin
& Clemants in an amoebic liver abscess hamster model. Evidence-
Based Complementary and Alternative Medicine 2014: 930208.
https://doi.org/10.1155/2014/930208
Bassett, I. & Crompton, C. 1970. [Report]. P. 437 in: Löve, Á. (ed.),
IOPB chromosome number reports XXVII. Taxon 19: 437–442.
https://doi.org/10.1002/j.1996-8175.1970.tb03047.x
Bentham, G. & Hooker, J.D. 1880. Genera plantarum, vol. 3(1).
London: Reeve. https://doi.org/10.5962/bhl.title.747
Black, J.M. 1934. Additions to the flora of South Australia. Trans.
& Proc. Roy. Soc. South Australia 58: 168–186.
Blattner, F.R. 1999. Direct amplification of the entire ITS region from
poorly preserved plant material using recombinant PCR. BioTech-
niques 27: 1180–1186. https://doi.org/10.2144/99276st04
Bouckaert, R., Heled, J., Kühnert, D., Vaughan, T., Wu, C.H., Xie, D.,
Suchard, M.A. & Drummond, A.J. 2014. BEAST 2: A software
platform for Bayesian evolutionary analysis. PLoS Computat. Biol.
10: e1003537. https://doi.org/10.1371/journal.pcbi.1003537
Boulos, L. 1996. Chenopodiaceae. Pp. 233–283 in: Miller, A.G. &
Cope, T.A. (eds.), Flora of the Arabian Peninsula and Socotra,
vol. 1. Edinburgh: Royal Botanic Garden Edinburgh; Richmond,
U.K.: Royal Botanic Gardens Kew.
Boutkhil, S., Idrissi, M.E., Amechrouq, A., Chbicheb, A., Chakir, S.
& Badaoui, K.E. 2009. Chemical composition and antimicrobial
activity of crude, aqueous, ethanol extracts and essential oils of Dys-
phania ambrosioides (L.) Mosyakin & Clemants. Acta Bot. Gallica
156(2): 201–209. https://doi.org/10.1080/12538078.2009.10516151
Brenan, J.P.M. 1954. Flora of Tropical East Africa, vol. 7, Chenopo-
diaceae. London: The Crown Agents for the Colonies.
Brenan, J.P.M. 1956. A new section of the genus Chenopodium from
Africa. Kew Bull. 11: 165–167. https://doi.org/10.2307/4109408
Brown, R. 1810. Prodromus florae Novae Hollandiae et Insulae Van-
Diemen. Londini [London]: typis Richardi Taylor & socii.
https://doi.org/10.5962/bhl.title.52309
Chu, G. 2003. Suckleya. P. 260 in: Flora of North America Editorial
Committee (eds.), Flora of North America, North of Mexico,
vol. 4. New York & Oxford: Oxford University Press.
Chu, G.L., Stutz, H.C. & Sanderson, S.C. 1991. Morphology and
taxonomic position of Suckleya suckleyana (Chenopodiaceae).
Amer. J. Bot. 78: 63–68. https://doi.org/10.2307/2445228
Clemants, S.E. 2006. Chenopodiaceae. Pp. 212–221 in: Iwatsuki, K.,
Boufford, D.E. & Ohba, H. (eds.), Flora of Japan, vol. 2a.
Tokyo: Kodansha.
Clemants, S.E. & Mosyakin, S.L. 2003. Dysphania. Pp. 275–300 in:
Flora of North America Editorial Committee (eds.), Flora of
North America, North of Mexico, vol. 4. New York & Oxford:
Oxford University Press.
De Lange, P.J. 2020. Dysphania pusilla Fact Sheet (content continu-
ously updated). New Zealand Plant Conservation Network. https://
www.nzpcn.org.nz/flora/species/dysphania-pusilla/ (accessed Apr
2020).
Dillon, S.J. & Markey, A.S. 2017. Dysphania congestiflora (Cheno-
podiaceae), a new species from Western Australia. Nuytsia 27:
133–138. https://florabase.dpaw.wa.gov.au/nuytsia/article/793
Dobignard, A. & Chatelain, C. 2011. Index synonymique de la flore
d’Afrique du Nord, vol. 2. Geneva: Conservatoire et Jardin botani-
ques de la Ville de Genève.
Eckardt, T. 1967. Vergleich von Dysphania mit Chenopodium und mit
Illecebraceae. Bauhinia 3: 327–344.
Eckardt, T. 1968. Zur Blütenmorphologie von Dysphania plantagi-
nella Muell. Phytomorphology 17: 165–172.
Friis, I. & Gilbert, M.G. 2000. Chenopodiaceae (incl. Salicorniaceae
and Salsolaceae). Pp. 277–298 in: Edwards, S., Tadesse, M.,
Demissew, S. & Hedberg, I. (eds.), Flora of Ethiopia & Eritrea,
vol. 2(1). Addis Ababa & Uppsala: University of Uppsala.
Fuentes-Bazan, S., Mansion, G. & Borsch, T. 2012a. Towards a spe-
cies level tree of the globally diverse genus Chenopodium.Molec.
Phylogen. Evol. 62: 359–374. https://doi.org/10.1016/j.ympev.
2011.10.006
Fuentes-Bazan, S., Uotila, P. & Borsch, T. 2012b. A novel phylogeny-
based generic classification for Chenopodium sensu lato, and a
tribal rearrangement of Chenopodioideae (Chenopodiaceae). Will-
denowia 42: 5–24. https://doi.org/10.3372/wi.42.42101
Gernhard, T. 2008. The conditioned reconstructed process. J. Theor.
Biol. 253: 769–778. https://doi.org/10.1016/j.jtbi.2008.04.005
Giusti, L. 1970. El género Chenopodium en Argentina. 1: Números de
chromosomas. Darwiniana 16: 98–105.
Giusti, L. 1988. El número de cromosomas de tres especies. Lilloa 37:
153–154.
Greenberg, A.K. & Donoghue, M.J. 2011. Molecular systematics and
character evolution in Caryophyllaceae. Taxon 6: 1637–1652.
https://doi.org/10.1002/tax.606009
Grozeva, N.H. & Cvetanova, Y.G. 2013. Karyological and morpho-
logical variations within the genus Dysphania (Chenopodiaceae)
in Bulgaria. Acta Bot. Croat. 72: 49–69. https://doi.org/10.2478/
v10184-012-0017-5
Grubov, V.I. 1966. Plants of Central Asia, vol. 2. Leningrad: Nauka.
Holmgren, N.H. 2003. Monolepis. Pp. 300–301 in: Flora of North
America Editorial Committee (ed s.), Flora of North America, North
of Mexico, vol. 4. New York & Oxford: Oxford University Press.
Iljin, M.M. & Aellen, P. 1936. Chenopodium.Pp.41–73 in: Shishkin,
B.K. (ed.), Flora URSS, vol. 6. Leningrad: Nauka. [in Russian]
Kadereit, G., Zacharias, E., Mavrodiev, E. & Sukhorukov, A.P.
2010. Molecular phylogeny of Atripliceae (Chenopodioideae,
Chenopodiaceae): Implications for systematics, biogeography,
flower and fruit evolution, and the origin of C
4
photosynthesis.
Amer. J. Bot. 97: 1664–1687. https://doi.org/10.3732/ajb.1000169
Kadereit, G., Ackerly, D. & Pirie, M.D. 2012. A broader model for C
4
photosynthesis evolution in plants inferred from the goosefoot
family (Chenopodiaceae s.s.). Proc. Roy. Soc. London, Ser.B, Biol.
Sci. 279: 3304–3311. https://doi.org/10.1098/rspb.2012.0440
Kawatani, T. & Ohno, T. 1950. Chromosome numbers of genus Che-
nopodium,I.Jap. J. Genet. 25: 177–180. https://doi.org/10.1266/
jjg.25.177
Kawatani, T. & Ohno, T. 1962. Chromosome numbers of genus Chenopo-
dium, III. Jap. J. Genet. 37: 78–79. https://doi.org/10.1266/jjg.37.78
Keener, C.S. 1970. Documented plant chromosome numbers 70:1.
Sida 3: 533–536.
Keener, C.S. 1974. Documented plant chromosome numbers 1974:1.
Sida 5: 290–291.
Kühn, U., Bittrich, V., Carolin, R., Freitag, H., Hedge, I.C.,
Uotila, P. & Wilson, P. 1993. Chenopodiaceae. Pp. 253–281 in:
Kubitzki, K., Rohwer, J.G. & Bittrich, V. (eds.), The families and
genera of vascular plants, vol. 2. Berlin: Springer. https://doi.org/
10.1007/978-3-662-02899-5_26
Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T. & Calcott, B.
2017. PartitionFinder 2: New methods for selecting partitioned
models of evolution for molecular and morphological phyloge-
netic analyses, Molec. Biol. Evol. 34: 772–773. https://doi.org/
10.1093/molbev/msw260
Lebrun, J.-P. & Stork, A.L. 1991. Énumération des plantes à fleurs
d’Afrique tropicale,vol.1,Généralités et Annonaceae à Euphor-
biaceae et Pandanaceae. Geneva: Conservatoire et Jardin botani-
ques de la Ville de Genève.
Löve, Á. & Löve, D. 1982. [Report]. P. 122 in: Löve, Á. (ed.), IOPB
chromosome number reports LCCIV. Taxon 31: 119–128. https://
doi.org/10.1002/j.1996-8175.1982.tb02346.x
Mahabale, T.S. & Solanky, I.N. 1954. Studies in the Chenopodiaceae:
Embryology of Chenopodium ambrosioides L. J. Univ. Bombay
22: 31–42.
Matzke, N.J. 2013. Probabilistic historical biogeography: New models
for founder-event speciation, imperfect detection, and fossils allow
22 Version of Record
Uotila & al. •Systematics of Dysphanieae TAXON 00 (00) •1–26
improved accuracy and model-testing. Frontiers Biogeogr. 5(4):
242–248. https://doi.org/10.21425/F5FBG19694
Matzke, N.J. 2014. Model selection in historical biogeography reveals
that founder-event speciation is a crucial process in island clades.
Syst. Biol. 63: 951–970. https://doi.org/10.1093/sysbio/syu056
McKenzie, R.A., Burren, B.G., Noble, J.W. & Thomas, M.B. 2007.
Cyanide poisoning in cattle from Dysphania glomulifera (red
crumbweed): Using the internet for rapid plant identification and
diagnostic advice: Case Report. Austral. Vet. J. 85(12): 505–509.
https://doi.org/10.1111/j.1751-0813.2007.00216.x
Miller, M.A., Pfeiffer, W. & Schwartz, T. 2010. Creating the CIPRES
Science Gateway for inference of large phylogenetic trees.
Pp. 45–52 in: Proceedings of the Gateway Computing Environ-
ments Workshop (GCE), New Orleans, Louisiana, 14 Nov 2010.
Piscataway: IEEE. https://doi.org/10.1109/GCE.2010.5676129
Moldenke, H.N. 1946. A contribution to our knowledge of the wild and
cultivated flora of Pennsylvania. Amer. Midl. Naturalist 35(2):
289–399. https://doi.org/10.2307/2421669
Moquin-Tandon, A. 1840. Chenopodearum monographica enumera-
tio. Parisiis [Paris]: apud P.-J. Loss. https://doi.org/10.5962/bhl.
title.15484
Moquin-Tandon, A. 1849. Salsolaceae. Pp. 41–219 in: Candolle, A.P.
de (ed.), Prodromus systematis naturalis regni vegetabilis,vol.13
(2). Parisiis [Paris]: sumptibus Victoris Masson. https://doi.org/
10.5962/bhl.title.286
Morales-Briones, D.F., Kadereit, G., Tefarikis, D.T., Moore, M.J.,
Smith, S.A., Brockington, S.F., Timoneda, A., Yim, W.C.,
Cushman, J.C. & Yang, Y. 2020. Disentangling sources of gene
tree discordance in phylogenomic datasets: Testing ancient hybrid-
izations in Amaranthaceae s.l. Syst. Biol.: syaa066. https://doi.org/
10.1093/sysbio/syaa066
Morteza-Semnani, K. 2015. A review on Chenopodium botrys L.:
Traditional uses, chemical composition and biological activities.
Pharm. Biomed. Res. 1: 1–9. https://doi.org/10.18869/acadpub.
pbr.1.2.1
Mosyakin, S.L. 1993. An outline of a system for Chenopodium L. (spe-
cies of Europe, North and Central Asia). Ukrayins’k. Bot. Zhurn.
50(5): 71–77.
Mosyakin, S.L. 2003. Cycloloma. Pp. 264–265 in: Flora of North Amer-
ica Editorial Committee (eds.), Flora of North America, North of
Mexico, vol. 4. New York & Oxford: Oxford University Press.
Mosyakin, S.L. & Clemants, S.E. 2002. New nomenclatural combina-
tions in Dysphania R.Br. (Chenopodiaceae): Taxa occurring in
North America. Ukrayins’k. Bot. Zhurn. 59(4): 380–385.
Mosyakin, S.L. & Clemants, S.E. 2008. Further transfers of glandular-
pubescent species from Chenopodium subgen. Ambrosia to Dys-
phania (Chenopodiaceae). J. Bot. Res. Inst. Texas 2: 425–431.
Mosyakin, S.L. & Tsymbalyuk, Z.M. 2004. Palynomorphological
peculiarities of the genus Dysphania R.Br. emend. Mosyakin &
Clemants (Chenopodiaceae Vent.). Ukrayins’k. Bot. Zhurn. 61(6):
3–13.
Múlgura, M.E. & Marticorena, A. 2008. Chenopodiaceae. Pp.
1909–1929 in: Zuloaga, F.O., Morrone, O. & Belgrano, M.J.
(eds.), Catálogo de las plantas vasculares del Cono Sur (Argentina,
Sur de Brasil, Chile, Paraguay y Uruguay),vol.2.St.Louis:Missouri
Botanical Garden.
Nee, S., May, R.M. & Harvey, P.H. 1994. The reconstructed evolu-
tionary process. Philos. Trans., Ser. B 344: 305–311. https://doi.
org/10.1098/rstb.1994.0068
Palomino, G., Segura, M., Bye, R. & Mercado, P. 1990. Cytogenetic
distinction between Teloxys and Chenopodium (Chenopodiaceae).
S. W. Naturalist 35: 351–353. https://doi.org/10.2307/3671957
Pax, F. 1889. Caryophyllaceae. Pp. 61–94 in: Engler, A. & Prantl, K.
(eds.), Die natürlichen Pflanzenfamilien, 1st ed., vol. 3(1B).
Leipzig: Engelmann.
Pax, F. 1927. Zur Phylogenie der Caryophyllacee. Bot. Jahrb. Syst. 61:
223–241.
Pax, F. & Hoffmann, K. 1934. Dysphaniaceae. Pp. 272–274 in: Pax, F.
& Harms, H. (eds.), Die natürlichen Pflanzenfamilien, 2nd ed.,
vol. 16c. Berlin: Duncker & Humblot.
Perveen, A. & Qaiser, M. 2012. Pollen flora of Pakistan –LXX: Che-
nopodiaceae. Pakistan J. Bot. 44(4): 1325–1333.
Probatova, N.S., Rudyka, E.G., Kozhevnikov, A.E. & Kozhevni-
kova, Z.V. 2004. Chromosome numbers of some representatives
of the flora of the Primorsky Territory. Bot. Zhurn. (Moscow &
Leningrad) 89: 1209–1217.
Rahiminejad, M.R., Ghaemmaghami, L. & Sahebi, J. 2004. Cheno-
podium pumilio (Chenopodiaceae) new to the flora of Iran. Willde-
nowia 34: 183–186. https://doi.org/10.3372/wi.34.34115
Ramayya, N. & Rajagopal, T. 1969. Chenopodium pumilio R.Br. –
An addition to the Indian flora with an enlarged key to the South
Indian species of the genus. Curr. Sci. 7: 173–175.
Rambaut, A. & Drummond, A.J. 2013. Tracer, version 1.6. http://
tree.bio.ed.ac.uk/software/tracer/
Ravi, N. & Anilkumar, N. 1990. Chenopodium truncatum Paul G.
Wilson (Chenopodiaceae) –A new record from India. J. Econ.
Taxon. Bot. 14: 109–110.
R Core Team 2016. R: A language and environment for statistical
computing. R Foundation for Statistical Computing, Vienna, Aus-
tria. https://www.R-project.org
Ree, R.H. & Sanmartín, I. 2018. Conceptual and statistical problems
with the DEC+J model of founder-event speciation and its com-
parison with DEC via model selection. J. Biogeogr. 45: 741–
749. https://doi.org/10.1111/jbi.13173
Reimann, C. & Breckle, S.W. 1988. Anatomie und Entwicklung der
Blasenhaare von Chenopodium-Arten. Flora 180: 275–288.
https://doi.org/10.1016/S0367-2530(17)30323-7
Sanmartín, I., Enghoff, H. & Ronquist, F. 2001. Patterns of animal
dispersal, vicariance and diversification in the Holarctic. Biol. J.
Linn. Soc. 73: 345–390. https://doi.org/10.1111/j.1095-8312.
2001.tb01368.x
Scott, A.J. 1978a. A review of the classification of Chenopodium L.
and related genera (Chenopodiaceae). Bot. Jahrb. Syst. 100(2):
205–220.
Scott, A.J. 1978b. A revision of the Camphorosmioideae (Chenopo-
diaceae). Feddes Repert. 89: 101–119. https://doi.org/10.1002/
fedr.4910890202
Shaw, J., Lickey, E.B., Beck, J.T., Farmer, S.B., Liu, W., Miller, J.
& Small, R.L. 2005. The tortoise and the hare II: relative utility of
21 noncoding chloroplast DNA sequences for phylogenetic analy-
sis. Amer. J. Bot. 92: 142–166. https://doi.org/10.3732/ajb.92.1.142
Shepherd, K.A. & Wilson, P.G. 2008. New combinations in the genus
Dysphania (Chenopodiaceae). Nuytsia 18: 267–272.
Simón, L.E. 1995. Essai sur l’histoire paleobiogéographique du genre
Chenopodium L. sousgenre Ambrosia A. J. Scott. Biogeographica
(Paris) 71(3): 127–142.
Simón, L.E. 1996. Notas sobre Chenopodium L. subgen. Ambrosia
A.J. Scott (Chenopodiaceae). 1. Taxonomía. 2. Fitogeografía:
Áreas disyuntas. Anales Jard. Bot. Madrid 54: 137–148.
Simón, L.E. 1997. Variations des charactères foliares chez Chenopo-
dium subg. Ambrosia sect. Adenois (Chenopodiaceae) en Améri-
que du Sud: Valeur taxonomique & évolutive. Adansonia, sér. 3,
19(2): 293–320.
Spach, E. 1836. Histoire naturelle des végétaux: Phaneérogames,vol.
5. Paris: Librairie Encyclopédique de Roret. https://doi.org/10.
5962/bhl.title.44839
Stamatakis, A. 2014. RAxML version 8: A tool for phylogenetic anal-
ysis and post-analysis of large phylogenies. Bioinformatics 30:
1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Standley, P.C. 1916. North American Flora, vol. 21(1), Chenopodiales;
Chenopodiaceae. New York: The New York Botanical Garden.
Sukhorukov, A.P. 2012a. The analysis of the reproductive characters
of the Dysphania groups (Chenopodiaceae/Amaranthaceae clade)
with reference of the geographical isolation. Pp. 64–67 in: Sytin,
Version of Record 23
TAXON 00 (00) •1–26 Uotila & al. •Systematics of Dysphanieae
A.K., Pilipenko, V.N., Lactionov,A.P., Afa nasyev, V.E. & Mavro-
diev, E.V. (eds.), Analytical approaches in floristic studies and
methods of biogeography. Astrakhan: Astrakhan University.
Sukhorukov, A.P. 2012b. Taxonomic notes on Dysphania and Atriplex
(Chenopodiaceae). Willdenowia 42: 169–180. https://doi.org/10.
3372/wi.42.42202
Sukhorukov, A.P. 2014. The carpology of the Chenopodiaceae with
reference to the phylogeny, systematics and diagnostics of its rep-
resentatives. Tula: Grif & K.
Sukhorukov, A.P. & Kushunina, M. 2014. Taxonomic revision of
Chenopodiaceae in Nepal. Phytotaxa 191(1): 10–44. https://doi.
org/10.11646/phytotaxa.191.1.2
Sukhorukov, A.P. & Zhang, M. 2013. Fruit and seed anatomy of
Chenopodium and related genera (Chenopodioideae, Chenopo-
diaceae/Amaranthaceae): Implications for evolution and taxon-
omy. PLoS ONE 8: e61906. https://doi.org/10.1371/journal.pone.
0061906
Sukhorukov, A.P., Zhang, M. & Kushunina, M. 2015. A new species
of Dysphania (Chenopodioideae, Chenopodiaceae) from South-
West Tibet and East Himalaya. Phytotaxa 203(2): 138–146. https://
doi.org/10.11646/phytotaxa.203.2.3
Sukhorukov, A.P., Kushunina, M. & Verloove, F. 2016. Notes on
Atriplex,Oxybasis and Dysphania (Chenopodiaceae) in West-
Central Tropical Africa. Pl. Ecol. Evol. 149(2): 249–256. https://
doi.org/10.5091/plecevo.2016.1181
Sukhorukov, A.P., Nilova, M.V., Krinitsina A.A., Zaika, M.A.,
Erst, A.S. & Shepherd, K.A. 2018a. Molecular phylogenetic
data and seed coat anatomy resolve the generic position of some
critical Chenopodioideae (Chenopodiaceae –Amaranthaceae) with
reduced perianth segments. PhytoKeys 109: 103–128. https://doi.
org/10.3897/phytokeys.109.28956
Sukhorukov, A.P., Kushunina, M., El Mokni, R., Sáez Goñalons, L.,
El Aouni, M.H. & Daniel, T.F. 2018b. Chorological and taxo-
nomic notes on African plants, 3. Bot. Lett. 165(2): 228–240.
https://doi.org/10.1080/23818107.2018.1465467
Sukhorukov, A.P., Liu, P.L. & Kushunina, M. 2019a. Taxonomic
revision of Chenopodiaceae in Himalaya and Tibet. PhytoKeys
116: 1–141. https://doi.org/10.3897/phytokeys.116.27301
Sukhorukov, A.P., Kushunina, M., El Mokni, R., Ardenghi, N.M.
G., Verloove, F., Uotila, P., Baider, C., Bruyns, P. & Klak, C.
2019b. Chorological and taxonomic notes on African plants, 4:
Caryophyllales. Bot. Lett. 166(4): 401–416. https://doi.org/10.
1080/23818107.2019.1652848
Ulbrich, E. 1934. Chenopodiaceae. Pp. 379–584 in: Pax, F. & Harms,
H. (eds.), Die natürlichen Pflanzenfamilien, 2nd ed., vol. 16c.
Berlin: Duncker & Humblot.
Uotila, P. 2001. Chenopodium. Pp. 4–31 in: Jonsell, B. (ed.), Flora
Nordica, vol. 2. Stockholm: The Bergius Foundation.
Uotila, P. 2011. Chenopodiaceae (pro parte majore). In: Euro+Med
Plantbase –the information resource for Euro-Mediterranean
plant diversity. Published on the Internet http://ww2.bgbm.org/
EuroPlusMed/ (accessed 1 Nov 2014).
Uotila, P. 2013. Dysphania sect. Botryoides (Amaranthaceae s.lat.) in
Asia. Willdenowia 43: 65–80. https://doi.org/10.3372/wi.43.43107
Verloove, F. & Lambinon, J.J. 2006. The non-native vascular flora of
Belgium: A new nothospecies, and three new combinations. Syst.
Geogr. Pl. 76: 217–220.
Volkens, G. 1893. Chenopodiaceae. Pp. 36–91 in: Engler, A. & Harms,
H. (eds.), Die natürlichen Pflanzenfamilien, 1st ed., vol. 3(1a).
Leipzig: Engelmann.
Voroshilov [Woroschilov, Voroschilov], V.N. 1942. Obzor vidov
Chenopodium L. iz sektsii Ambrina (Spach) Hook. fil. [Revision
of the species of Chenopodium L. of the sect. Ambrina (Spach)
Hook. fil.]. Bot. Zhurn. (Moscow & Leningrad) 27(3/4): 33–47.
Watson, S. 1883. Contributions to American Botany. Proc. Amer.
Acad. Arts, n.s., 10: 96–196. https://doi.org/10.2307/25138689
Webb, C.J., Sykes, W.R. & Garnock-Jones, P.J. 1988. Flora of
New Zealand, vol. 4. Christchurch: Botany Division D.S.I.R.
Weber, W.A. 1985. The genus Teloxys (Chenopodiaceae). Phytologia
58(7): 477–478. https://doi.org/10.5962/bhl.part.14762
Wen, J. 1999. Evolution of eastern Asian and eastern North American
disjunct distributions in flowering plants. Annual Rev. Ecol. Syst.
30: 421–455. https://doi.org/10.1146/annurev.ecolsys.30.1.421
Wen, J., Nie, Z.-L. & Ickert-Bond, S.M. 2016. Intercontinental dis-
junctions between eastern Asia and western Nor th America in vas-
cular plants highlight the biogeographic importance of the Bering
land bridge from Late Cretaceous to Neogene. J. Syst. Evol. 54:
469–490. https://doi.org/10.1111/jse.12222
Wilson, P.G. 1983. A taxonomic revision of the tribe Chenopodieae
(Chenopodiaceae) in Australia. Nuytsia 4: 135–262.
Wilson, P.G. 1984. Chenopodiaceae. Pp. 81–317 in: George, A.S.
(ed.), Flora of Australia, vol. 4. Canberra: Australian Government
Publishing Service.
Wilson, P.G. 1987. Generic status in the Chenopodiaceae. Newslett.
Austral. Syst. Bot. 53: 78–85.
Xu, D.H., Abe, J., Sakai, M., Kanazawa,A. & Shimamoto, Y. 2000.
Sequence variation of non-coding regions of chloroplast DNA
of soybean and related wild species and its implications for the
evolution of different chloroplast haplotypes. Theor. Appl. Genet.
101: 724–732. https://doi.org/10.1007/s001220051537
Zacharias, E.H. & Baldwin, B.G. 2010. A molecular phylogeny of
North American Atripliceae (Chenopodiaceae), with implications
for floral and photosynthetic pathway evolution. Syst. Bot. 35:
839–857. https://doi.org/10.1600/036364410X539907
Zhang, M. & Zhu [Chu], G. 2016. Resurrection of the genus Botry-
dium Spach (Chenopodiaceae), with a description of four new spe-
cies from China, Peru and Burundi. Pl. Diversity 38: 322–329.
https://doi.org/10.1016/j.pld.2016.10.005
Zhu [Chu], G.-L. & Sanderson, S.C. 2017. Genera and a new evolu-
tionary system of world Chenopodiaceae. Beijing: Science Press.
Appendix 1. Sequence identification numbers and isolate numbers, voucher details and GenBank accession numbers of taxa sampled. Names follow new
taxonomy.
Taxon name with taxonomic authority, Seq_ID, Isolate number, ITS, ETS, atpB-rbcL spacer, rpl16 intron GenBank accession numbers for samples for which
sequences have been taken from GenBank only. An asterisk (*) indicates a sample included in biogeography analysis. A dash (–) indicates missing data.
Axyris amaranthoides L., AxamarAC647, AC647, HE577370, –,–,–;Axyris prostrata L., AxprosAC529, AC529, HE577369, –,–,–;Ceratocarpus
arenarius L., CearenAC649, AC649, HE577365, –,–,–;Ceratocarpus arenarius, CearenAC531, AC531, HE577364, –,–,–;Krascheninnikovia ceratoides
(L.) Gueldenst., KrceraAC608, AC608, HE577366, –,–,–,*(combined with Chen0012); Krascheninnikovia ceratoides, Krcera0012, Chen0012, –,–,
MK635457, –,*(combined with CearenAC531); Krascheninnikovia ceratoides subsp. lanata (Pursh) H.Heklau, KrcerassplanaAC626, AC626, HE577368,
–,–,–.
24 Version of Record
Uotila & al. •Systematics of Dysphanieae TAXON 00 (00) •1–26
Appendix 1. Continued.
Taxon name with taxonomic authority, Seq_ID, Isolate number, country: largest political subdivision/locality, collector(s) + number (Herbarium and
voucher sheet number), ITS, ETS, atpB-rbcL spacer, rpl16 intron GenBank accession numbers for newly sequenced specimens. An asterisk (*) indicates a sam-
ple included in biogeography analysis. A dash (–) indicates missing data. States of Australia and U.S.A. given with official abbreviations. BG = Botanical
Garden.
Axyris amaranthoides L., Axamar3015, Chen3015, Mongolia: North Mongolia, W. Hilbig 246/83 (HAL 56454), –, MK692777, MK635354, –,*;Axyris
prostrata L., Axpros0118, Chen0118, Mongolia: Gobi Altai, G. & S. Miehe 96-140-04 (KAS), MK802948, –, MK635355, MK784573, *;Axyris prostrata,
Axpros3003, Chen3003, Mongolia: Central Mongolia, W. Hilbig & Z. Schamsran s.n. (HAL 48537), –, MK692778, MK635356, MK784574; Ceratocarpus
arenarius L., Cearen3050, Chen3050, Mongolia: Khovd Prov., W. Hilbig & Z. Schamsran s.n. (HAL 101082), –, MK692779, MK635357, –,*;Dysphania
ambrosioides (L.) Mosyakin & Clemants, Dyambr0822, Chen0822, Portugal: Azores/Sao Miguel (seed sample from Berlin-Dahlem BG leg. Royl 6394, cult.
in BG Mainz), –, (MJG), MK802950, –, MK635361, MK784576; Dysphania ambrosioides, Dyambr2786, Chen2786, Tanzania: Tanga Prov./West Usambara,
K. Vainio-Mattila, K. Lahti & O. Vainio 96-151 (H 1692978), MK802952, MK692781, MK635363, MK784578, *;Dysphania ambrosioides, Dyambr2790,
Chen2790, Japan: Tokyo (seed sample from Tokyo BG, cult. in Helsinki BG), P. Uotila 29969 (H 1393031), MK802954, MK692783, MK635365, MK784580;
Dysphania ambrosioides, Dyambr2066, Chen2066, U.S.A.: CA/Butte County, Lowell Ahart 9413 (JEPS), MK802951, –, MK635362, MK784577; Dysphania
ambrosioides, Dyambr3426, Chen3426, India: Himachal Pradesh/20 km SW of Dehra Dun, P. Uotila 17666 (H 1101255), MK802955, MK692784,
MK635366, MK784581; Dysphania ambrosioides, Dyambr3504, Chen3504, Argentine: Mendoza/Malargüe, C.B. Passera s.n. (MERL 37468), MK802956,
MK692785, –,–;Dysphania ambrosioides, Dyambr2787, Chen2787, England: Surrey/Kew (seed sample from Royal BG Kew, cult. in Helsinki BG), P. Uo ti la
28757 (H 1260955), MK802953, MK692782, MK635364, MK784579; Dysphania anthelmintica (L.) Mosyakin & Clemants, Dyanth2795, Chen2795, U.S.A.:
NC/Conine Creek, H.E. Ahlee 52014 & J.G. Haesloop (H 1036364), MK802957, –, MK635367, MK784582, *;Dysphania atriplicifolia (Spreng.) G.Kadereit,
Uotila & Sukhor., Cyatri2791, Chen2791, U.S.A.: MN/Houston Co., S.R. Ziegler & M.F. Leykom 1838 (H 1206836), MK802949, MK692780, MK635358,
MK784575, *;Dysphania atriplicifolia, Cyatri2892, Chen2892, U.S.A.: IL/Henderson Co., T.G. Lammers 7464 (F), –,–, MK635359, –;Dysphania atriplicifolia,
Cyatri2893, Chen2893, U.S.A.: WI/Vernon Co., S.R. Ziegler & M.F. Leykom 1616 (H 1206837), –,–, MK635360, –;Dysphania bhutanica Sukhor., Dybhut2998,
Chen2998, Bhutan: Thimphu, A.J.C. Grierson & D.G. Long 2828 (K), MK802958, MK692786, MK635368, MK784583, *;Dysphania botrys (L.) Mosyakin
& Clemants, Dybotr0116, Chen0116, Turkey: Konya/road to Karapinar, H. Freitag & Adigüzel 28769 (KAS), MK802959, –, MK635369, MK784584; Dyspha-
nia botrys, Dybotr2798, Chen2798, Kyrgyzstan: Jalal-Abad region/Kyzyl-Jar, P. Uotila 47905 (H 1747524), MK802961, –, MK635370, –;Dysphania botrys,
Dybotr2777, Chen2777, Austria: Niederösterreich/Vöslau, W. Till 90228 (WU), MK802960, –,–, MK784585; Dysphania botrys, Dybotr2999,Chen2999, Kyr-
gyzstan: Jalal-Abad Region, P. Uotila 47502 (MW), MK802962, MK692787, MK635371, MK784586, *;Dysphania botrys, Dybotr3046, Chen3046, Russia:
Kursk prov./Zheleznogorsk, N.I. Degtyarev s.n. (MW), MK802964, MK692789, MK635373, MK784588; Dysphania carinata (R.Br.) Mosyakin & Clemants,
Dycari3425, Chen3425, South Africa: Johannesburg/Soweto, I. Sahi s.n. (H 1763504), MK802966, MK692790, MK635375, MK784590, *;Dysphania carinata,
Dycari2776, Chen2776, Yemen: Lahij/55 km from Habilayn towards Labus, M. Thulin, M. Ghebrehiwet & A.N. Gifri 9264 (UPS 125313), MK802965, –,
MK635374, MK784589; Dysphania chilensis (Schrad.) Mosyakin & Clemants, Dychil2796, Chen2796, Chile: Región de Maule/Tricao, M. Valdes
(Hernández 204) (H 1690741), MK802967, MK692793, MK635378, MK784591, *;Dysphania chilensis, Dychil2792, Chen2792, Chile: Región de Maule/Cor-
dillera de los Andes, C. Hernández 203 (H 1690734), –, MK692791, MK635376, –;Dysphania chilensis, Dychil2793, Chen2793, Chile: Santiago/Laguna de
Aculéo, C. Hernández 210 (H 1690732), –, MK692792, MK635377, –;Dysphania congestiflora S.J.Dillon & A.S.Markey, Dycofl3501, Chen3501,
Australia: WA, A. Markey & S. Dillon FM 9709 (PERTH 08730105), MK802968, MK692794, MK635379, –,*;Dysphania congolana (Hauman) Mosyakin
& Clemants, Dycong2771, Chen2771, Ethiopia: Gojjam Region/near Sekela, M. Thulin & A. Hunde 3970 (H 1377076 & UPS), MK802969, –, MK635380,
MK784592; Dysphania congolana, Dycong3306, Chen3306, Burundi: Prov. Muramwya/Bugarama, M. Reekmans 11051 (BR), MK802970, MK692795,
MK635381, MK784593, *;Dysphania congolana, Dycong3307, Chen3307, Burundi, M. Reekmans 11227 (BR), –, MK692796, –,–;Dysphania cristata
(F.Muell.) Mosyakin & Clemants, Dycris0256, Chen0256, Australia: NSW/Coonamble, S. Jacobs 8653 (NSW 491980), –,–, MK635382, MK784594; Dysphania
cristata, Dycris3310,Chen3310, Australia: SA/32.05090S 140.15977E, J. McDonald 1409/26B (MJG 020875), –, MK692797, MK635383, MK784595; Dys-
phania cristata, Dycris3526, Chen3526, Australia: WA/Giralia Station at S end of Exmouth Gulf, M. Maier GIR 107-X (PERTH 07451172), MK802972,
MK692798, MK635384, MK784596; Dysphania cristata, Dycris3528, Chen3528, Australia: WA/Lake Mason Station 56 km NNE of Sandstone, D.J. Edinger
& G. Marsh, DJE4638A (PERTH 06872980), MK802973, MK692799, MK635385, MK784597, *;Dysphaniageoffreyi Sukhor., Dygeof3308, Chen3308, Bhu-
tan: Upper Mo Chu distr., Sinclair & Long s.n. (E 00151629), MK802974, MK692800, MK635386, –;Dysphania geoffreyi, Dygeof3309, Chen3309, China:
Yunnan/Nada, Chungtien-Lijiang-Dali- Expedition 324 (K), MK802975, MK692801, MK635387, MK784598, *;Dysphania glandulosa Paul G.Wilson,
Dyglan3535, Chen3535, Australia, WA/13.2 km from Yalgoo, G. Byrne 3563 (PERTH 08387729), MK802977, MK692803, MK635389, MK784600; Dyspha-
nia glandulosa, Dyglan3536, Chen3536, Australia: WA/12.7 km E of Mt. Narryer Station Homestead, A.S. George 17439 (PERTH 05981301), MK802978,
MK692804, MK635390, –;Dysphania glandulosa, Dyglan3537, Chen3537, Australia: WA/Meekatharra, G. Byrne 308 (PERTH 07153201), MK802979,
MK692805, MK635391, MK784601, *;Dysphania glandulosa, Dyglan3525, Chen3525, Australia: WA/Gidgee Road, D.J. Edinger & G. Marsh DJE 4862
(PERTH 06930026), MK802976, MK692802, MK635388, MK784599; Dysphania glomulifera (Nees) Paul G.Wilson, Dyglom0277, Chen0277, Australia:
NSW/Hermidale, S. Jacobs 8738 (NSW 490542), MK802980, –, MK635392, MK784602; Dysphania glomulifera, Dyglom3523, Chen3523, Australia:
WA/Gibson Desert, C.P. Campbell 2429 (PERTH 06288871), MK802981, MK692806, MK635393, MK784603, *;Dysphania glomulifera, Dyglom3524,
Chen3524, Australia: WA/Doolgunna Station Gascoyne, D.J. Edinger 4337(PERTH 07112580), MK802982, MK692807, MK635394, MK784604; Dysphania
graveolens (Willd.) Mosyakin & Clemants, Dygrav2073, Chen2073, Mexico: Veracruz/Perote, M. Nee 32944 (JEPS & UC), MK802983, –, MK635395,
MK784605, *;Dysphania graveolens, Dygrav2079, Chen2079, U.S.A.: NM/Luna Co., J. Travis Columbus 525 (JEPS & UC), MK802984, –, MK635396, –;
Dysphania graveolens, Dygrav2080, Chen2080, U.S.A.: AZ/Mohave Co., L.C. Higgins 24017 (JEPS & UC), MK802985, –, MK635397, MK784606; Dysphania
himalaica Uotila, Dyhima2773, Chen2773, India: Ladakh/Rupshu, L.Klimeš99-27-9a (H 1757588), MK802986, –, MK635398, –,*;Dysphania kalpari Paul G.
Wilson, Dykalp0276, Chen0276, Australia: NSW/ca. 75 km N of Bourke, S.W.L. Jacobs 8734 (NSW 490547), –,–,–, MK784607; Dysphania kalpari,
Dykalp0528, Chen0528, Australia: WA/Austin, S.W.L. Jacobs 9185 (MJG 018697 & NSW 594047), MK802987, –, MK635399, MK784608; Dysphania kalpari,
Dykalp3508, Chen3508, Australia:WA/Mt. Methwin, N. Gibson 6872 & al. (PERTH 08795010), MK802989, MK692809, MK635401, MK784610, *;Dysphania
kalpari, Dykalp3520, Chen3520, Australia: WA/2724′S120
38′E, G. Byrne 2232 (PERTH 07809360), MK802990, MK692810, MK635402, MK784611; Dys-
phania kalpari, Dykalp3415, Chen3415, Australia: WA/Austin, A.A. Mitchell 1518 (AD 234148), MK802988, MK692808, MK635400, MK784609; Dysphania
littoralis R.Br., Dylitt3432, Chen3432, Australia: Qld./Idalia National Park, R.J. Fensham 6182 (AQ 876272), MK802991, MK692811,MK635403, MK784612, *;
Dysphania littoralis, Dylitt3434, Chen3434, Australia: Qld/N of Yeppoon, A.R. Bean 31614 (AQ 823544), MK802992, MK692812, MK635404, MK784613;
Dysphania mandonii (S.Watson) Mosyakin & Clemants, Dymand2770, Chen2770, Bolivia: La Paz/Bautista Saavedra Prov. J. Krach 8378 (H 1661944),
MK802993, –, MK635405, MK784614; Dysphania mandonii, Dymand2781, Chen2781, Bolivia: La Paz/José Ramón Loayza Prov., St. G. Beck 22974
(H 1704706), MK802994, MK692813, MK635406, MK784615, *;Dysphania melanocarpa (J.M.Black) Mosyakin & Clemants, Dymela3408, Chen3408,
Australia: SA/Gairdner-Torrens,H.P.Vonow & N.R. Neagle BS721-452 (AD 241113), MK802995,MK692814, MK635407, MK784616;Dysphania melanocarpa,
Dymela3409, Chen3409, Australia: SA/E of mainSerpentine Lakes, D.E. Murfet7693 (AD 267507), MK802996, MK692815, MK635408, MK784617,*;Dyspha-
nia melanocarpa, Dymela3410, Chen3410, Australia: SA/W from Mt Hoare, P.D. Canty BS23-39262 (AD 120888), MK802997, MK692816, MK635409,
MK784618; Dysphania melanocarpa, Dymela3527, Chen3527, Australia: WA/E of Mt. Royal, W.A. Thompson & N.N. Sheehy 629 (PERTH 08571945),
MK802999, MK692818, MK635410, MK784619; Dysphania melanocarpa, Dymela3429, Chen3429, Australia: WA/W of Yeo Camp, H.R. Tölken 6046
Version of Record 25
TAXON 00 (00) •1–26 Uotila & al. •Systematics of Dysphanieae
Appendix 1. Continued.
(H 1559880), MK802998, MK692817, –,–;Dysphania multifida (L.) Mosyakin & Clemants,Dymult2774, Chen2774, Greece: Makedonia/Halkidiki, M. Koistinen
1997/285 (H 1720089), MK803001, –, MK635413, –;Dysphania multifida, Dymult2789, Chen2789, Chile: Región de Maule/San Miguel de Colín, C. Hernández
208 (H 1690726), MK803003, MK692820, MK635415, –,*;Dysphania multifida, Dymult2775, Chen2775, Spain: Malaga/Fuengirola, P. Uotila 42552
(H 1695061), MK803002, –, MK635414, MK784621; Dysphania multifida, Dymult2081, Chen2081, U.S.A.: CA/Butte County, V.H. Oswald 9981 (JEPS),
MK803000, –, MK635412, –;Dysphania multiflora (Moq.) G.Kadereit, Sukhor. & Uotila, Dymufl3014, Chen3014, Nepal: Jumla/Jumla village, A. Sukhorukov
s.n.(MW),–, MK692819, MK635411, MK784620, *;Dysphania neglecta Sukhor., Dynegl3010, Chen3010, Nepal: Jumla/Nigregar, A. Sukhorukov s.n.(MW),
MK802963, MK692788, MK635372, MK784587, *;Dysphania nepalensis (Colla) Mosyakin & Clemants, Dynepa2785, Chen2785, Nepal: Mustang/Mukhtinath
village, A. Sukhorukov s.n. (H 1750722), MK803004, –, MK635416, MK784622; Dysphania nepalensis, Dynepa3000, Chen3000, India: Kashmir/Leh,
H. Hartmann 4015 (G), MK803005, –, MK635417, –;Dysphania nepalensis, Dynepa3047, Chen3047, China: Qinghai/Gonghe, T.N. Ho & al. (E 00067214),
MK803007, –, MK635419, MK784623; Dysphania nepalensis, Dynepa3011, Chen3011, Bhutan: Bumthang, Ch. Parker 7118 (E), MK803006, MK692821,
MK635418, –,*;Dysphania plantaginella F.Muell., Dyplan3509, Chen3509, Australia: WA/Yamada rockhole, N. Gibson 6871 & al. (PERTH 08794855),
MK803008, MK692822, MK635420, MK784624; Dysphania plantaginella, Dyplan3522, Chen3522, Australia: WA/Tent Island Nature Reserve, N. Godfrey
NG 57/15 (PERTH 08752850), MK803009, MK692823, MK635421, MK784625, *;Dysphania plantaginella, Dyplan3532, Chen3532, Australia: WA/Giralia
Station, M. Maier, K. McCreery & B. Muir GIRB-08 (PERTH 07515758), –,–, MK635422, –;Dysphania plantaginella, Dyplan3533, Chen3533, Australia:
WA/Ord River, T. Handasyde & A.N. Start, TH 00 227 (PERTH 06193331), –,MK692824,–,–;Dysp hania plantaginella, Dyplan3534, Chen3534, Australia:
WA/Oyster stacks car park, J. English 157 (PERTH 07694474), –, MK692825, MK635423, MK784626; Dysphania platycarpa Paul G.Wilson, Dyplat3411,
Chen3411, Australia: SA/29 km S of Innamincka, D.J.Duval,D.Murfet,T.Croft,P.Winter&M.Thorpe864(AD 214659), MK803010, MK692826,
MK635424, MK784627, *;Dysphania platycarpa, Dyplat3412, Chen3412, Australia: SA/Mt. Sarah Station, R. Bates 46907 (AD 99815056), MK803011,
MK692827, MK635425, MK784628; Dysphania platycarpa, Dyplat3413, Chen3413, Australia: SA/Goyder Lagoon, R. Bates 71698 (AD 206499), MK803012,
MK692828,–, MK784 629; Dysphania proce ra (Hochst. ex Moq.) Mosyakin & Clemants, Dyproc2772, Chen2772, Burundi: Gankuzo/Gitwenge (seed sample from
Liege BG, cult. in Helsinki BG), P. Uotila 33696 (H 1590138), MK803013, MK692829, MK635426, MK784630; Dysphania procera, Dyproc3001, Chen3001
(=chen3012, 3013), Yemen: Shahará, J.R. Wood 2502 (BM & E), MK803014, –, MK635427, MK784631, *;Dysphania pseudomultiflora (Murr) Verloove
& Lambinon, Dypseu2783, Chen2783, South Africa: Transvaal/Pretoria, K.A. Dahlstrand 1288 (H 103920 0), –, MK692830, MK635428, MK784632, *;Dysphania
pseudomultiflora, Dypseu2784, chen2784, Namibia: Windhoek, M. Juva s.n. (H 1731422), –,–,–, MK784633; Dysphania pseudomultiflora,Dypseu3305,
Chen3305, South Africa: Eastern Cape/Albany, R.D.A. Bayliss 8675 (BR-16053632), –, MK692831, –,–;Dysphania pumilio (R.Br.) Mosyakin & Clemants,
Dypumi2788, Chen2788, Australia: Tas/East Coast, W.M. C urt is (H 1669458), MK803015, –, MK635430, –;Dysphania pumilio, Dypumi0255, Chen0255,
Australia: NSW/Coonamble, S. Jacobs 8651 (NSW 491981), –,–, MK635429, MK784634; Dysphania pumilio, Dypumi3049, Chen3049, Czech Republic: Mora-
via, F. Dvořăks.n. (MW), MK803016, MK692832, –,–;Dysphania pumilio, Dypumi3513, Chen3513, Australia: WA/Manjimup, R.J. Cranfield 14546 (PERTH
05600154), MK803017, MK692833, MK635431, MK784635, *;Dysphania pumilio, Dypumi3514, Chen3514, Australia: WA/Watheroo National Park, G.J.
Keighery (PERTH 05703662), MK803018, MK692834, MK635432, MK784636; Dysphania pumilio, Dypumi3519, Chen3519, Australia: WA/Manjimup town
centre, R.J. Cranfield 26678 (PERTH 08461422), MK803019, MK692835, MK635433, MK784637; Dysphania rhadinostachya (F.Muell.) A.J.Scott, Dyr-
had0525,Chen0525, Australia:WA/118 km NNE of Carnarvon, S. Jacobs 9167 (MJG 018698 & NSW 594049), MK803020, –, MK635434, MK784638; Dyspha-
nia rhadinostachya, Dyrhad3414, Chen3414, Australia: SA/Lake Eyre, D.J. Duval, D. Murfet, T. Croft, P. Winter, M. Thorpe 891 (AD 214625), MK803021,
MK692836, MK635435, MK784639, *;Dysphania rhadinostachya, Dyrhad3416, Chen3416, Australia: WA/Carnarvon, R. & K. Chinnock 16 (AD 98701214),
MK803022, MK692837, –,–;Dysphania saxatilis (Paul G.Wilson) Mosyakin & Clemants, Dysaxa3418, Chen3418, Australia: WA/ Von Treuer Tableland,
H.R. Tolken 6152 (AD 98006341), MK803023, MK692838, –,–;Dysphania saxatilis, Dysaxa3430u3417, Chen3430 (H) & Chen3417 (AD), Australia:
WA/124.6 km W of Neale Junction, H.R. Tolken 6042 (H 1559839 & AD 98004534), MK803024, MK692839, –,–;Dysphania saxatilis, Dysaxa3517, Chen3517,
Australia: WA/SE of Yalgoo, A. Markey & S. Dillon 5469 (PERTH 08488738), MK803025, MK692840, MK635436, MK784640, *;Dysphania saxatilis,Dys-
axa3518, Chen3518, Australia: WA/SW of Tom Price, J. Fairhead & P. Anderson BES 00424 (PERTH 08431000), MK803026, MK692841, MK635437,
MK784641; Dysphania schraderiana(S chult.) Mosyakin & Clemants, DyschrAC387, AC387, Ethiopia: –,M. Wondafrash 2255 (B), HE577349, –,–,–;Dysphania
schraderiana, Dyschr2794, Chen2794, Russia: Moscow distr. (seed sample from BG of Inst. Pl. Med., Vilar, cult. in Helsinki BG), P. Uotila 28695 (H 1259578), –,–,
MK635438, –;Dysphania schraderiana, Dyschr3048, Chen3048, Russia: Moscow/Botanical Garden, Yu. Al exeev s .n. (MW), MK803027, MK692842, MK635439,
MK784642, *;Dysphania simulans F.Muell. & Tate, Dysimu3419, Chen3419, Australia: SA/Clayton station, H.P. Vonow 2353 & al. (AD 99736045), MK803028,
MK692843, MK635440, MK784643; Dysphania simulans, Dysimu3420, Chen3420,Australia: SA/Lake Eyre,F.J. Badman 5158 (AD 99235095), –, MK692844,
MK635441, MK784644; Dysphania simulans, Dysimu3421, Chen3421, Australia: SA/Salt-gypsum lake off the Oodnadatta Track, R. Bates RB46908
(AD 9981505 7), MK803029, MK6928 45, MK635442, MK78464 5, *;Dysphania simulans, Dysimu3511, Chen3511, Australia: WA/S sideof Lake Kerrylyn Tate,
N. Gibson 6869& al. (PERTH 08794839), MK803030, MK692846, MK635443, MK784646; Dysphaniasimulans, Dysimu3512, Chen3512, Australia: WA/Sam-
phire Tate, R.J. Cranfield 5980 (PERTH 02586347), –, MK692847, MK635444, –;Dysphania simulans, Dysimu3515, Chen3515, Australia: WA/Lorna
Glen Station Tate, D.J. Edinger & G. Marsh DJE 3321 (PERTH 06464858), –,–, MK635445, –;Dysphania spec., Dyspec3503, Chen3503, Argentina: Men-
doza/Uspallata, F.A. Raig 11429 (MERL 42014), –, MK692848, –,–;Dysphania sphaerosperma Paul G.Wilson, Dyspha3510, Chen3510, Australia: WA/Lake
Kerrylyn, N. Gibson 6870 & al. (PERTH 08794847), MK803031, MK692849, MK635446, MK784647; Dysphania sphaerosperma, Dyspha3521, Chen3521,
Australia: WA/SE of Cane River Homestead, D.J. Edinger 1607 (PERTH 05435870), MK803032, MK692850, MK635447, MK784648; Dysphania sphaero-
sperma, Dyspha3529, Chen3529, Australia: WA/NW of Mt. Amy, S. Dillon, A. Markey CR 9199 (PERTH 08432473), MK803033, MK692851, MK635448,
MK784649; Dysphania sphaerosperma, Dyspha3530, Chen3530, Australia: WA/Pilbara, N.G. Walsh 6573 & al. (PERTH 08085706), MK803034,
MK692852, MK635449, MK784650, *;Dysphania sphaerosperma, Dyspha3531, Chen3531, Australia: WA/6.5 km NE of Mt. Turner, M. Maier BES
00001 (PERTH 08437173), MK803035, MK692853, MK635450, MK784651; Dysphania tibetica (A.J.Li) Uotila, Dytibe2769, Chen2769, India: Ladakh/Rup-
shu, L. Klimešs.n. (H 1757589), MK803036, –, MK635451, –,*;Dysphania truncata (Paul G.Wilson) Mosyakin & Clemants, Dytrun3422, Chen3422,
Australia: SA/Innamincka Regional Reserve, M. Barnett BS612-319 (AD 224049), MK803037, MK692854, MK635452, MK784652; Dysphania truncata,
Dytrun3423, Chen3423, Australia: SA/Cordillo Downs, D.J. Duval, M.J. Thorpe & T.S. Te 1217 (AD 224912), MK803038, MK692855, MK635453,
MK784653; Dysphania truncata, Dytrun3424, Chen3424, Australia: SA/off Borefield Road, R. Bates 46881 (AD 99909269), MK803039, MK692856,
MK635454, MK784654, *;Dysphania valida Paul G.Wilson, Dyvali3433, Chen3433, Australia: Qld/30 km S of Morven on Boatman road, J.L. Silcock JLS
1107 (AQ 825529), MK803040, MK692857, MK635455, MK784655, *;Dysphania valida, Dyvali3441, Chen3441, Australia: Qld/E of Windorah, A.R. Bean
30223 (AQ 822308), MK803041, MK692858, MK635456, MK784656; Krascheninnikovia ceratoides, Krcera3051, Chen3051, Mongolia: Govi-Altai Prov.,
E. Jäger (HAL 57753), –,–, MK635458, –;Krascheninnikovia ceratoides subsp. lanata (Pursh) H.Heklau, Krcerassplana1887, Chen1887, U.S.A.:NM/San
Miguel, J.B. Nelson 23554 & al. (HAL 100339), –, MK692859, MK635459, –,*;Neomonolepis spathulata (A.Gray) Sukhor., MoSPATH, MoSPATH,
U.S.A.: CA/Susanville, I.Yu. Koropachinsky & al. 404 (MHA), MH675518, –, MH152575, *;Suckleya suckleyana (Torr.) Rydb., Susuck2000, Chen2000,
U.S.A.: NM/Tres Piedras, J.E. Larson 6492 (RM), MK803042, MK692861, –, MK784658, *;Suckleya suckleyana, Susuck2001, Chen2001, U.S.A.: NM, B.E. Nel-
son 66396 (RM), –, MK692862, –, MK784659; Suckleya suckleyana, Susuck1999, Chen1999, U.S.A.: WY, B.E.Nelson 56487 (F), –, MK692860, –, MK784657;
Teloxys aristata (L.) Moq., Tearis0293, Chen0293, Mongolia: Ulaanbaatar, B.B. Neuffer & H. Hurka 11.727 (KAS), MK803043, –, MK635460, MK784660, *;
Teloxys aristata, Tearis2778, Chen2778, Russia: Altai Republic/Altai near river Chuya (Cuja), A. Tribsch & F. Essl 9924 (WU), MK803044, –,–, MK784661; Te l-
oxys aristata, Tearis3002, Chen3002, Mongolia: Zentralaimak, W. Hilbig, Z. Schamsran (HAL 45266), –,–, MK635461, –.
26 Version of Record
Uotila & al. •Systematics of Dysphanieae TAXON 00 (00) •1–26
