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Mycology
An International Journal on Fungal Biology
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Quasipucciniastrum agrimoniae, gen. et sp. nov. on
Agrimonia (Rosaceae) from China
Xiao-Hua Qi, Lei Cai & Peng Zhao
To cite this article: Xiao-Hua Qi, Lei Cai & Peng Zhao (2019): Quasipucciniastrum
agrimoniae, gen. et sp. nov. on Agrimonia (Rosaceae) from China, Mycology, DOI:
10.1080/21501203.2019.1610522
To link to this article: https://doi.org/10.1080/21501203.2019.1610522
© 2019 The Author(s). Published by Informa
UK Limited, trading as Taylor & Francis
Group.
Published online: 30 Apr 2019.
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Quasipucciniastrum agrimoniae,gen.etsp.nov.onAgrimonia (Rosaceae) from China
Xiao-Hua Qi
a,b
, Lei Cai
a
and Peng Zhao
a
a
State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, China;
b
University of Chinese Academy
of Sciences, Beijing, China
ABSTRACT
A new rust genus, Quasipucciniastrum, typified by Q. agrimoniae sp. nov., is proposed based on
distinct morphological characters and phylogenetic placement. This genus is characterised by its
uredinial ostiolar peridial cells with rough surface and sessile, multicellular teliospores with
apparently thickened apical wall. Molecular phylogenetic analyses using internal transcribed
spacer regions and intervening 5.8S nrRNA gene (ITS) and the large subunit (LSU) rDNA revealed
that this genus is sister to the genus Cronartium (Cronartiaceae), but morphologically it is distinct
from Cronartium in the sessile teliospores that are divided by vertical septa. Morphologically,
Quasipucciniastrum should be compared to Pucciniastrum (Pucciniastraceae) in its multicellular
teliospores, but they were phylogenetically distant.
ARTICLE HISTORY
Received 31 March 2019
Accepted 17 April 2019
KEYWORDS
Agrimony; Cronartiaceae;
molecular phylogeny;
morphology;
Pucciniastraceae
Introduction
Agrimonia Ldb. species, known as “common agri-
mony”, are perennial herbaceous flowering plants
widely distributed in the temperate regions of the
Northern Hemisphere, and they have been com-
monly planted for ornamentation and medicinal
use (Lu 2001). Common agrimony is economically
and horticulturally important, but their growths
have been frequently threatened by rust diseases.
Hitherto, seven rust species have been recorded on
Agrimonia species (Farr and Rossman 2018), among
which, Pucciniastrum agrimoniae (Dietel) Tranzschel
(Pucciniastraceae) and its synonymies, P. agrimoniae-
eupatoriae (DC.) Lagerh. (Pucciniastraceae),
Thekopsora agrimoniae Dietel (Pucciniastraceae),
Uredo agrimoniae J. Schröt. (Anamorphic genera)
are frequently assigned names (Tai 1979; Zhuang
1983,2001,2005; Guo 1989; Zhang et al. 1997; Cao
and Li 1999; Zhuang and Wei 1999; Cao et al. 2000),
or in fewer cases as Melampsora agrimoniae Dietel
(Melampsoraceae), Puccinia agrimoniae (Arthur)
Arthur (Pucciniaceae) and Uropyxis agrimoniae
Arthur (Uropyxidaceae) (Arthur 1910; Maneval 1937).
During our study on rust fungi in China,
a morphologically distinct species was found on
Agrimonia pilosa. It produces Milesia-type uredinia
and ostiolar peridial cells with rough surface, and
have subglobose teliospores divided by vertical
septa. These characters are to some extent, similar
to Pucciniastrum spp. (Pucciniastraceae), but the
rDNA ITS and LSU sequences showed its close rela-
tionship to genus Cronartium Fr. (Cronartiaceae)
rather than Pucciniastrum. Our critical morphological
and molecular comparisons of this fungus with
Cronartium, Pucciniastrum and other related genera
suggested that this rust fungus represents a new
genus herein described as Quasipucciniastrum agri-
moniae gen. et sp. nov.
Materials and methods
Fungal specimens
A total of 204 dried herbarium specimens on
Agrimonia pilosa were loaned from the Mycological
Herbarium of Institute of Microbiology, CAS, China
(HMAS). Several fresh specimens on Agrimonia spe-
cies were collected from different provinces in China
during last three years. Herbarium specimens of
Cronartium and Peridermium (Link) J.C. Schmidt &
Kunze involved in this study were loaned from
University of Florida Herbarium, USA (FLAS), HMAS,
University of Michigan Herbarium, USA (MICH) and
New York Botanical Garden, USA (NY). In this study,
the Roman numerals of II and III referred to uredinial
and telial stages in the rust fungi.
CONTACT Lei Cai cail@im.ac.cn
MYCOLOGY
https://doi.org/10.1080/21501203.2019.1610522
© 2019 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted
use, distribution, and reproduction in any medium, provided the original work is properly cited.
Published online 30 Apr 2019
Morphological examinations
Morphological characteristics of all specimens were
observed using a dissecting microscope (DM), the
light microscope (LM) and the scanning electron
microscope (SEM). The methods for morphological
analyses as outlined by Zhao et al. (2013), Zhao et al.
(2014), 2017) were followed. Fifty measurements of
sori and spores from each specimen were recorded,
and morphological characteristics in uredinial and
telial stages, i.e. the position of uredinia and telia,
the ornamentation and dimension of urediniospores,
the dimension and shape of ostiolar cells, the position
and shape of peridial cells, the dimension of telios-
pores, the position and shape of teliospores were
examined.
DNA extraction, amplification and sequencing
For the fungal specimens, several sori from each
specimen were excised and DNA were extracted
from all studied herbarium specimens using Gentra
Puregene Tissue Kit (Qiagen, Valencia, CA) according
to the manufacturer’s instructions. From the crude
extracts, 1–3μl DNA templates were directly used for
the polymerase chain reaction (PCR) amplification of
the internal transcribed spacer regions and interven-
ing 5.8S nrRNA gene (ITS) and the large subunit (LSU)
rDNA. rDNA ITS regions were amplified using the
primer pairs ITS1F (Gardes and Bruns 1993)/ITS4
(White et al. 1990), Rust2inv (Aime 2006)/ITS4BR
(Feau et al. 2009), and fragment of LSU was amplified
using the primer pairs ITS4BRf/LR6 (Vilgalys and
Hester 1990), LR1R/LR3 and LR3R/LR6 (Vilgalys and
Hester 1990). PCR was performed under the follow-
ing conditions: denaturation at 95°C for 5 min; fol-
lowed by 35 cycles of denaturation at 95°C for 45 s,
annealing at 55°C for 1 min and elongation at 72°C
for 1 min, finally with an extension step at 72°C for
10 min. Purification and sequencing of PCR ampli-
cons were carried out at the Tianyi Huiyuan
Company, Beijing.
Molecular phylogeny
Full-length ITS and partial LSU regions were
amplified from 23 specimens, and we included 16
specimens from genus Cronartium and Peridermium
for comparable studies because they have high
similarity to rust fungus on Agrimonia in rDNA
sequences. Their herbarium numbers, host plants,
geographical origins and GenBank accession num-
bers are listed in Table 1. Besides, a total of 148
sequences from closely related species were
retrieved from GenBank for phylogenetic comparison
(Table 2). Pileolaria terebinthi (DC.) Castagne was
used as outgroup. In the final dataset, ITS and LSU
were concatenated and the final alignment includes
124 specimens with a length of 1836 characters (743
for ITS, 1093 for 28S).
Sequences were manually aligned by using
BioEdit 7.0.9 (Hall 1999), and multiple alignments
were performed using MAFFT 7 (Katoh and
Standley 2013). Gaps were treated as missing data
for all analyses. The Akaike Information Criteria (AIC)
in Modeltest 3.7 (Posada and Crandall 1998) was
used to estimate the best-fit substitution models,
and GTR+I + G was selected as the best evolutionary
model. Maximum Likelihood (ML) analyses were per-
formed using RAxML 8.0.0 (Stamatakis and Alachiotis
2010), and Bayesian Markov chain Monte Carlo
(MCMC) analyses were performed by MrBayes 3.1.2
(Huelsenbeck and Ronquist 2001). Supported values
of ML and Bayesian posterior probability (Bpp) were
indicated in the phylogenetic tree.
Results
Molecular phylogeny
The combined ITS and LSU dataset included 106
sequences of ITS and 123 sequence of LSU from 125
rust samples. The dataset comprised aligned length of
1836 characters, of which, 1162 characters are con-
stant, and 640 are variable with 533 parsimony infor-
mative sites. Both ML and Bayesian inference resulted
in a highly concordant topology (Figure 1). Our speci-
mens on Agrimonia pilosa constituted a strongly sup-
ported clade (ML/Bpp = 93/0.98), close to Cronartium,
Endocronartium Y. Hirats. of the family Cronartiaceae.
Genera Hyalopsora Magnus, Melampsorella J. Schröt.,
Melampsoridium Kleb., Milesia F.B. White, Naohidemyces
S. Sato, Katsuya & Y. Hirats., Pucciniastrum, Thekopsora
Magnus and Uredinopsis Magnus from the family
Pucciniastraceae, which produce Milesia-type uredinia
and multicellular teliospores, clustered together but
are phylogenetically distant from our rust specimens
on A. pilosa.
2X.-H. QI ET AL.
Taxonomy
Quasipucciniastrum X.H. Qi, P. Zhao & L. Cai, gen.
nov.
MycoBank no.: MB828669
Etymology
Quasipucciniastrum (Lat.) referring to the morpholo-
gical characters (uredinial and telial stages) similar to
genus Puccinistrum.
Type species
Quasipucciniastrum agrimoniae X.H. Qi, P. Zhao & L. Cai
Generic diagnosis
Spermogonia and aecia unknown. Uredinia hypo-
phyllous, subepidermal, round, scattered or
crowded in groups, Milesia-type, erumpent with
peridium opening by a pore delimited by well-
developed, globose and verrucose ostiolar cells,
peridialcellssmall,irregular.Urediniosporesborne
singly, no pedicels, ovoid, globoid or ellipsoid,
spore wall colourless, echinulate. Telia hypophyl-
lous, subepidermal, one spore deep, light yellow.
Teliospores subglobose, sessile, multicellular, sepa-
rated by vertical or oblique septa, wall apparently
thickened at apex.
Table 1. Herbarium specimens used for molecular phylogenetic analyses.
GenBank accession no. Collection
Species Host Locality and data of Specimen no.
a
LSU ITS
Cronartium coleosporioides Castilleja linariaefolia Montana USA, 1914 MICH253346 MK208284 MK193824
C. comandrae Comandra umbellata Wisconsin USA, 1955 MICH253364 MK208293 MK193825
C. comandrae C. richardsiana Canda NY00267638 MK208294 MK193826
C. comandrae C. pallida USA NY03106200 MK208295 MK193827
C. flaccidum Paeonia lactiflora Ussuriysk Russia, 2003 HMAS89229 MK208286 MK193819
C. flaccidum P. lactiflora Jilin China, 2003 HMAS89231 MK208289 MK193822
C. flaccidum Pinus tabulaeformis Inner Mongolia China, 1984 HMAS82784 MK208287 MK193818
C. flaccidum P.taiwanensis Henan China, 1981 HMAS44164 MK208288 MK193816
C. flaccidum Quercus aquifolioides Tibet China, 2010 HMAS242642 MK208290 MK193821
C. flaccidum Q. aquifolioides Tibet China, 2010 HMAS242641 MK208291 MK193820
C. quercuum Q. glandulifera Jiangxi China, 1996 HMAS82717 MK208292 MK193817
C. ribicola Ribes nigrum USA NY00267051 MK208296 MK193828
C. ribicola Pinus strobus Ontario Canada, 1952 NY00267053 MK208298 MK193829
C. ribicola Pedicularis yezoensis Nagano Japan, 1990 HMAS66843 MK208297 MK193830
C. strobilinum Pinus taeda Florida USA, 1982 FLAS-F-53,222 MK208285 MK193823
Peridermium filamentosum Pinus ponderosa Arizona USA, 1957 MICH300081 MK208299 MK193831
Quasipucciniastrum agrimoniae Agrimonia pilosa Beijing China, 1998 HMAS82312 MK208264 MK193835
Q. agrimoniae A. pilosa Gansu China, 1992 HMAS67301 MK208261 MK193832
Q. agrimoniae A. pilosa Gansu China, 1992 HMAS67302 MK208273 MK193844
Q. agrimoniae A. pilosa Gansu China, 1992 HMAS67306 MK208262 MK193833
Q. agrimoniae A. pilosa Gansu China, 1992 HMAS67309 MK208263 MK193834
Q. agrimoniae A. pilosa Gansu China, 2003 HMAS134791 MK208268 MK193839
Q. agrimoniae A. pilosa Guangxi China, 1997 HMAS77430 MK208271 MK193842
Q. agrimoniae A. pilosa Guizhou China, 2015 HMAS248096 MK208283 MK193854
Q. agrimoniae A. pilosa Heilongjiang China, 2003 HMAS89584 MK208277 MK193848
Q. agrimoniae A. pilosa Heilongjiang China, 2004 HMAS136005 MK208274 MK193845
Q. agrimoniae A. pilosa Heilongjiang China, 2015 HMAS248094 MK208280 MK193851
Q. agrimoniae A. pilosa Heilongjiang China, 2015 HMAS248095 MK208281 MK193852
Q. agrimoniae A. pilosa Inner Mongolia China, 2000 HMAS172175 MK208272 MK193843
Q. agrimoniae A. pilosa Ningxia China, 2000 HMAS172172 MK208270 MK193841
Q. agrimoniae A. pilosa Ningxia China, 2000 HMAS172173 MK208265 MK193836
Q. agrimoniae A. pilosa Sichuan China, 2016 HMAS248093 MK208279 MK193850
Q. agrimoniae A. pilosa Sichuan China, 1989 HMAS63888 MK208266 MK193837
Q. agrimoniae A. pilosa Sichuan China, 1989 HMAS63892 MK208275 MK193846
Q. agrimoniae A. pilosa Sichuan China, 2010 HMAS243033 MK208276 MK193847
Q. agrimoniae A. pilosa Yunnan China, 2007 HMAS199430 MK208269 MK193840
Q. agrimoniae A. pilosa Yunnan China, 2011 HMAS248097 MK208282 MK193853
Q. agrimoniae A. pilosa Tibet China, 2011 HMAAS244481 MK208267 MK193838
Q. agrimoniae A. pilosa Yunnan China, 2016 HMAS248092 MK208278 MK193849
a
FLAS-F: University of Florida Herbarium, USA; HMAS: Fungarium, Chinese Academy of Sciences, China; MICH: University of Michigan Herbarium, USA; NY:
New York Botanical Garden, USA.
MYCOLOGY 3
Table 2. Sequence data retrieved from GenBank and used for phylogenetic analyses.
GenBank accession no.
Species Host plants ITS LSU Reference
Chrysomyxa arctostaphyli Arctostaphylos sp. DQ200930.1 AY700192.1 Matheny et al. (2007)
C. chiogenis Gaultheria hispidula GU049452.1 GU049532.1 Feau et al. (2011)
C. ledi Picea abies HM037711.1 HM037707.1 Kaitera et al. (2010)
C. ledicola P. mariana GU049417.1 GU049520.1 Feau et al. (2011)
C. nagodhii Rhododendron groenlandicum GU049431.1 GU049524.1 Feau et al. (2011)
C. neoglandulosi Ledum glandulosum GU049498.1 GU049550.1 Feau et al. (2011)
C. piperiana L. macrophyllum GU049497.1 GU049565.1 Feau et al. (2011)
C. rhododendri L. lapponicum GU049467.1 GU049560.1 Feau et al. (2011)
C. rhododendri Rhododendron ferrugineum GU049471.1 GU049570.1 Feau et al. (2011)
C. vaccinii Vaccinium parvifolium GU049463.1 GU049561.1 Feau et al. (2011)
C. woroninii Ledum groenlandicum GU049462.1 GU049540.1 Feau et al. (2011)
Coleosporium. cacaliae Adenostyles alliariae KY810462.1 KY810462.1 Beenken et al. (2017)
Col. campanulae Campanula rapunculoides KY810465.1 KY810465.1 Beenken et al. (2017)
Col. euphrasiae Rhinanthus alectorolophus KY810469.1 KY810469.1 Beenken et al. (2017)
Col. inulae Inula salicina KY810470.1 KY810470.1 Beenken et al. (2017)
Col. ipomoeae Ipomoea sp MF769624.1 MF769639.1 McTaggart and Aime (2018)
Col. petasitidis Petasites hybridus KY810471.1 KY810471.1 Beenken et al. (2017)
Col. plumeriae Plumeria sp MF769629.1 GU145555.1 McTaggart and Aime (2018) Holcomb and Aime (2010)
Col. senecionis Jacobaea alpina KY810472.1 KY810472.1 Beenken et al. (2017)
Col. senecionis Senecio ovatus KY810473.1 KY810473.1 Beenken et al. (2017)
Col. solidaginis Solidago virgaurea KY810481.1 KY810481.1 Beenken et al. (2017)
Col. solidaginis S. gigantea KY810483.1 KY810483.1 Beenken et al. (2017)
Col. tussilaginis Tussilago farfara KY810485.1 KY810485.1 Beenken et al. (2017)
Cronartium conigenum Pinus leiophylla L76486.1 –Vogler and Bruns (1998)
Cro. ribicola –DQ533975.1 AF522166.1 –
Endocronartium harknessii Pinus sp. DQ206982.1 AY700193.1 Matheny et al. (2007)
Hyalopsora polypodii Cystopteris fragilis –AF426229.1 Maier et al. (2003)
H. polypodii Deparia petersenii –KJ698627.1 –
Melampsorella caryophyllacearum Caryophyllaceae Cerastium –MG907233.1 Aime et al. (2018)
M. caryophyllacearum Abies alba –AF426232.1 Maier et al. (2003)
M. betulinum Betula pubescens KF031556.1 KF031539.1 McKenzie et al. (2013)
M. betulinum Alnus cordata KF031559.1 KF031544.1 McKenzie et al. (2013)
M. betulinum Betula nana KF031562.1 KF031549.1 McKenzie et al. (2013)
M. hiratsukanum Alnus incana KF031554.1 KF031541.1 McKenzie et al. (2013)
M. hiratsukanum A. rhombifolia KC313889.1 KC313888.1 Blomquist et al. (2014)
Milesina philippinensis Nephrolepis sp. –KM249868.1 McTaggart et al. (2014)
Milesina sp. Pinaceae Abies –MG907234.1 Aime et al. (2018)
M. vogesiaca Polystichum aculeatum –MG907235.1 Aime et al. (2018)
Naohidemyces vaccinii Vaccinium ovatum –DQ354563.1 Aime (2006)
N. vaccinii Vaccinum –KJ698628.1 Padamsee et al. (2014)
Peridermium harknessii Pinus contorta L76506.1 –Vogler and Bruns (1998)
Pileolaria terebinthi Pistacia atlantica HM639742.1 HM639742.1 Alaei et al. (2012)
P. terebinthi P. atlantica HM639743.1 HM639743.1 Alaei et al. (2012)
Pucciniastrum actinidiae Actinidia arguta AB221446.1 AB221403.1 Liang (2006)
P. actinidiae A. rufa AB221448.1 AB221405.1 Liang (2006)
P. boehmeriae Boehmeria tricuspis AB221450.1 AB221393.1 Liang (2006)
P. boehmeriae B. platanifolia AB221451.1 AB221391.1 Liang (2006)
P. corni Cornus kuosa AB221437.1 AB221409.1 Liang (2006)
P. corni C. kuosa AB221436.1 AB221408.1 Liang (2006)
P. fagi Fagus crenata AB221425.1 AB221378.1 Liang (2006)
P. fagi F. crenata AB221420.1 AB221374.1 Liang (2006)
P. fagi F. crenata AB221424.1 AB221375.1 Liang (2006)
P. fagi F. japonica AB221421.1 AB221376.1 Liang (2006)
P. fagi F. crenata AB221423.1 AB221377.1 Liang (2006)
P. hikosanense Acer rufinerve AB221441.1 AB221388.1 Liang (2006)
P. hikosanense A. rufinerve AB221440.1 AB221389.1 Liang (2006)
P. hydrangeae-petiolaris Hydrangea petiolaris AB221438.1 AB221384.1 Liang (2006)
P. hydrangeae-petiolaris H. petiolaris AB221439.1 AB221385.1 Liang (2006)
P. kusanoi Clethra barbinervis AB221429.1 AB221400.1 Liang (2006)
P. kusanoi C. barbinervis AB221426.1 AB221402.1 Liang (2006)
P. kusanoi C.abarbinervis AB221430.1 AB221401.1 Liang (2006)
P. kusanoi C. barbinervis AB221427.1 AB221399.1 Liang (2006)
P. kusanoi Clethra barbinervis AB221428.1 AB221398.1 Liang (2006)
P. miyabeanum Viburnum furcatum AB221443.1 AB221397.1 Liang (2006)
P. miyabeanum V. furcatum AB221442.1 AB221394.1 Liang (2006)
P. styracinum Styrax japonica AB221433.1 AB221417.1 Liang (2006)
P. styracinum S. japonica AB221432.1 AB221418.1 Liang (2006)
P. styracinum S. japonica AB221431.1 AB221416.1 Liang (2006)
P. tiliae Tilia mandshurica AB221455.1 AB221412.1 Liang (2006)
P. tiliae T. japonica AB221453.1 AB221414.1 Liang (2006)
(Continued)
4X.-H. QI ET AL.
Notes
The new genus Quasipucciniastrum is characterised by
its Milesia-type uredinia with well-developed ostiolar
cells, well-developed peridial cells, hypophyllous telia
producing subglobose teliospores which is divided by
vertical and oblique septa under host epidermis. This
genus resembles Pucciniastrum (Pucciniastraceae,
Pucciniales) but differs in producing hypophyllous
telia, subglobose teliospores with apparently thickened
apical wall. Within family Pucciniastraceae, other gen-
era clearly differed from Quasipucciniastrum in uredi-
nial ostiole and teliospores. Genera Calyptospora,
Hyalopsora, Milesina and Uredinopsis differ from this
new genus in the type of ostiole, position of telia and
type of teliospores, while Melampsorella and
Melampsoridium differ from Quasipucciniastrum mainly
in their unicellular teliospores without septa (Cummins
and Hiratsuka 2003). In addition, Melampsorella has
Milesia-type uredinia with discrete ostiole, which also
clearly differs from Quasipucciniastrum. Phylogenetic
results supported the separation of
Quasipucciniastrum from Pucciniastrum, Melampsorella
and other genera in the family Pucciniastraceae
(Figure 1).
Quasipucciniastrum agrimoniae X.H. Qi, P. Zhao &
L. Cai, sp. nov. (Figure 2)
MycoBank no.: MB828670
Typification
CHINA. HEILONGJIANG: Greater Higgnan Mountains,
Tahe, II, III on A. pilosa, 6 September 2015, P. Zhao
(Holotype designated here, HMAS248095),
GenBank: ITS = MK208281; LSU = MK193852.
Etymology
Named after the host plant of the type specimen.
Description from holotype
Spermogonia and aecia unknown. Uredinia hypophyl-
lous, subepidermal, round, pale-yellow, scattered or
rarely grouped, 0.1–0.4 mm in diameter, erumpent
with peridium with well-developed ostiolar cells, usually
six to nine, arranged at the apex of uredinia. Peridial cells
small, irregular, walls smooth. Ostiolar cells well-
developed, oblong or ellipsoid, with rough surface.
Urediniospores borne singly, no pedicels, scattered, glo-
boid, ovoid or ellipsoid, 16.5–22 × 12.5–17.3 µm, wall
0.7–2.1 µm thick, evenly echinulate without smooth area
on surface, spinules 0.5–1.2 µm in length, and the dis-
tance between spinules 1.1 and 2.2 µm, germ bizonated.
Telia hypophyllous, subepidermal, one spore deep, light
yellow. Teliospores consisting of several cells adhering
laterally under the epidermal cells, sessile, subglobose,
18.5–36.1 × 13.7–29.9 µm, 2–6 celled, mainly with verti-
cal septa, walls apparently thickened at apex, up to
4.6 µm.
Additional specimens examined: CHINA. BEIJING:
Dongling Mountain, II, III on Agrimonia pilosa,
16 September 1998, J.Y. Zhuang (HMAS82312);
CHINA. GANSU: Gan Nan, Diebu, II, III on A. pilosa,
10 September 1992, J.Y. Zhuang (HMAS67301);
CHINA. GANSU: Gan Nan, Diebu, II, III on A. pilosa,
12 September 1992, J.Y. Zhuang (HMAS67302);
CHINA. GANSU: Gan Nan, Zhouqu, II, III on A. pilosa,
Table 2. (Continued).
GenBank accession no.
Species Host plants ITS LSU Reference
P. tiliae T. japonica AB221454.1 AB221415.1 Liang (2006)
P. yoshinagai Stewartia monadelphagene AB221435.1 AB221410.1 Liang (2006)
P. yoshinagai S. monadelphagene AB221434.1 AB221411.1 Liang (2006)
Quasipucciniastrum agrimoniae Agrimonia eupatoria –AF426234.1 Maier et al. (2003)
Q. agrimoniae –KJ486537.1 KJ725376.1 Yang (2015)
Q. agrimoniae –KJ486536.1 KJ725375.1 Yang (2015)
Q. agrimoniae Agrimonia sp. –MG907236.1 Aime et al. (2018)
Thekopsora guttata Galium odoratum –AF426231.1 Maier et al. (2003)
T. minima Ericaceae Vaccinium –MG907243.1 Aime et al. (2018)
T. minima Vaccinium corymbosum –KY991374.1 Shands et al. (Unpublished)
T. symphyti Symphytum officinale –AF426230.1 Maier et al. (2003)
Uredinopsis osmundae Dryopteridaceae Athyrium –MG907244.1 –
U. osmundae Osmundaceae Osmunda –MG907245.1 –
U. pteridis Pteridium esculentum –KM249869.1 McTaggart et al. (2014)
Uredinopsis sp. ––AF522181.1 –
(–): No information from GenBank.
MYCOLOGY 5
5 September 1992, J.Y. Zhuang (HMAS67306); CHINA.
GANSU: Lan Zhou, Yongdeng, II, III on A. pilosa,
11 October 2003, J.Y. Zhuang (HMAS134791); CHINA.
GANSU: Long Nan, Wenxian, II, III on A. pilosa,
21 September 1992, J.Y. Zhuang (HMAS67309);
CHINA. GUIZHOU: Qian Nan, Maolan, II, III on A. pilosa,
21 June 2015, P. Zhao (HMAS248096); CHINA.
HEILONGJIANG: Greater Higgnan Mountains,
Jiagedaqi District, II, III on A. pilosa, 9 September 2015,
P. Zhao (HMAS248094); CHINA. HEILONGJIANG: Khakan
Nature Reserve, II, III on A. pilosa, 9 August 2003, J.Y.
Zhuang (HMAS89584); CHINA. HEILONGJIANG: Mu Dan
Jiang, II, III on A. pilosa, 9 August 2004, J.Y. Zhuang
(HMAS136005); CHINA. INNER MONGOLIA: Tong Liao,
Horqin, II, III on A. pilosa, 18 September 2000, J.Y.
Zhuang (HMAS172175); CHINA. NINGXIA: Jin Yuan, II,
III on A. pilosa, 31 August 2000, J.Y. Zhuang
(HMAS172172); CHINA. NINGXIA: Jin Yuan, II, III on
0.05
Melampsorella caryophyllacearum on Abies alba AF426232
Coleosporium plumeriae on Plumeria sp. GU145555 MF769629
Naohidemyces vaccinii on Vaccinum KJ698628
Cronartium orientale on Quercus aquifolioides HMAS242642
Quasipucciniastrum agrimoniae on Agrimonia pilosa HMAS136005
Pucciniastrum styracinum on Styrax japonica AB221418 AB221432
Hyalopsora polypodii on Cystopteris fragilis AF426229
Pucciniastrum miyabeanum on Viburnum furcatum AB221397 AB221443
Coleosporium solidaginis on Solidago gigantea KY810483
Chrysomyxa vaccinii on Vaccinium parvifolium GU049463 GU049561
Pucciniastrum tiliae on Tilia japonica AB221414 AB221453
Cronartium flaccidum on Paeonia lactiflora HMAS89229
Pucciniastrum fagi on Fagus crenata AB221375 AB221424
Cronartium orientale on Quercus aquifolioides HMAS242641
Chrysomyxa ledi on Abies sp. HM037711 HM037707
Quasipucciniastrum agrimoniae on Agrimonia pilosa KJ486536 KJ725375
Cronartium flaccidum on Pinus taiwanensis HMAS44164
Pucciniastrum kusanoi on Clethra barbinervis AB221398 AB221428
Quasipucciniastrum agrimoniae on Agrimonia pilosa HMAS67302
Cronartium ribicola on Pedicularis yezoensis HMAS66843
Quasipucciniastrum agrimoniae on Agrimonia pilosa HMAS243033
Coleosporium tussilaginis on Tussilago farfara KY810485
Melampsoridium betulinum on Betula pubescens KF031539 KF031556
Pucciniastrum styracinum on Styrax japonica AB221416 AB221431
Pucciniastrum actinidiae on Actinidia rufa AB221405 AB221448
Peridermium filamentosum on Pinus ponderosa MICH300081
Chrysomyxa piperiana on Ledum macrophyllum GU049497 GU049565
Pucciniastrum boehmeriae on Boehmeria tricuspis AB221393 AB221450
Pucciniastrum corni on Cornus kuosa AB221409 AB221437
Coleosporium solidaginis on Solidago virgaurea KY810481
Thekopsora minima on Vaccinium corymbosum KY991374 SKY991375
Pucciniastrum fagi on Fagus japonica AB221376 AB221421
Coleosporium campanulae on Campanula apunculoides KY810465
Pucciniastrum kusanoi on Clethra barbinervis AB221402 AB221426
Quasipucciniastrum agrimoniae on Agrimonia pilosa HMAS67301
Cronartium ribicola on Ribes nigrum NY00267051
Chrysomyxa woroninii on Ledum groenlandicum GU049462 GU049540
Thekopsora guttata on Galium odoratum AF426231
Cronartium ribicola on Pinus strobus NY00267053
Pucciniastrum boehmeriae on Boehmeria platanifolia AB221391 AB221451
Pucciniastrum yoshinagai on Stewartia monadelphagene AB221410 AB221435
Melampsoridium betulinum on Alnus cordata KF031544 KF031559
Pucciniastrum corni on Cornus kuosa AB221408 AB221436
Quasipucciniastrum agrimoniae on Agrimonia pilosa HMAS63888
Milesina philippinensis on Nephrolepis sp. KM249868
Quasipucciniastrum agrimoniae on Agrimonia pilosa HMAS67309
Quasipucciniastrum agrimoniae on Agrimonia pilosa HMAS63892
Cronartium conigenum on Pinus leiophylla L76486
Quasipucciniastrum agrimoniae on Agrimonia pilosa HMAS82312
Quasipucciniastrum agrimoniae on Agrimonia pilosa HMAS244481
Chrysomyxa ledicola on Picea mariana GU049417 GU049520
Coleosporium inulae on Inula salicina KY810470
Quasipucciniastrum agrimoniae on Agrimonia pilosa HMAS248097
Pucciniastrum hydrangeae on Hydrangea petiolaris AB221384 AB221438
Pucciniastrum tiliae on Tilia japonica AB221415 AB221454
Pucciniastrum styracinum on Styrax japonica AB221417 AB221433
Coleosporium cacaliae on Adenostyles alliariae KY810462
Cronartium quercuum on Quercus glandulifera HMAS82717
Peridermium harknessii on Pinus contorta L76506
Melampsorella caryophyllacearum on Caryophyllaceae Cerastium MG907233
Uredinopsis sp. AF522181
Chrysomyxa rhododendri on Ledum lapponicum GU049467 GU049560
Uredinopsis pteridis on Pteridium esculentum KM249869
Quasipucciniastrum agrimoniae on Agrimonia pilosa HMAS89584
Pucciniastrum kusanoi on Clethra barbinervis AB221401 AB221430
Cronartium comandrae on Comandra pallida NY03106200
Chrysomyxa neoglandulosi on Ledum glandulosum GU049498 GU049550
Quasipucciniastrum agrimoniae on Agrimonia pilosa AF426234
Quasipucciniastrum agrimoniae on Agrimonia pilosa HMAS248096
Cronartium flaccidum on Pinus tabulaeformis HMAS82784
Thekopsora minima on Ericaceae Vaccinium MG907243
Quasipucciniastrum agrimoniae on Agrimonia pilosa HMAS199430
Pileolaria terebinthi on Pistacia atlantica HM639743
Quasipucciniastrum agrimoniae on Agrimonia pilosa HMAS172172
Quasipucciniastrum agrimoniae on Agrimonia pilosa HMAS248094
Coleosporium petasitidis on Petasites hybridus KY810471
Chrysomyxa rhododendri on Rhododendron ferrugineum GU049471 GU049570
Naohidemyces vaccinii on Vaccinium ovatum DQ354563
Quasipucciniastrum agrimoniae on Agrimonia pilosa KJ486537 KJ725376
Cronartium coleosporioides on Castilleja linariaefolia MICH253346
Cronartium comandrae on Comandra richardsiana NY00267638
Melampsoridium hiratsukanum on Alnus rhombifolia KC313889 KC313888
Uredinopsis osmundae on Athyrium sp. MG907244
Uredinopsis osmundae on Osmunda sp. MG907245
Quasipucciniastrum agrimoniae on Agrimonia pilosa HMAS248095
Melampsoridium alni on Alnus mandshurica KF031534 KF031557
Thekopsora symphyti on Symphytum officinale AF426230
Coleosporium senecionis on Senecio ovatus KY810473
Hyalopsora polypodii on Deparia petersenii KJ698627
Chrysomyxa nagodhii on Rhododendron groenlandicum GU049431 GU049524
Pileolaria terebinthi on Pistacia atlantica HM639742
Pucciniastrum fagi on Fagus crenata AB221374 AB221420
Cronartium ribicola DQ533975 AF522166
Milesina sp. on Abies sp. MG907234
Coleosporium euphrasiae on Rhinanthus alectorolophus KY810469
Pucciniastrum hikosanense on Acer rufinerve AB221389 AB221440
Cronartium flaccidum on Paeonia lactiflora HMAS89231
Pucciniastrum actinidiae on Actinidia arguta AB221403 AB221446
Pucciniastrum fagi on Fagus crenata AB221377 AB221423
Pucciniastrum hydrangeae on Hydrangea petiolaris AB221385 AB22143939
Pucciniastrum fagi on Fagus crenata AB221378 AB221425
Endocronartium harknessii on Pinus sp. DQ206982 AY700193
Cronartium comandrae on Comandra umbeilata MICH253364
Quasipucciniastrum agrimoniae on Agrimonia pilosa MG907236
Coleosporium ipomoeae on Pomoea sp. MF769639 MF769624
Pucciniastrum hikosanense on Acer rufinerve AB221388 AB221441
Quasipucciniastrum agrimoniae on Agrimonia pilosa HMAS172173
Quasipucciniastrum agrimoniae on Agrimonia pilosa HMAS77430
Pucciniastrum kusanoi on Clethra barbinervis AB221400 AB221429
Quasipucciniastrum agrimoniae on Agrimonia pilosa HMAS134791
Quasipucciniastrum agrimoniae on Agrimonia pilosa HMAS172175
Pucciniastrum miyabeanum on Viburnum furcatum AB221394 AB221442
Melampsoridium betulinum on Betula nana KF031549 KF031562
Melampsoridium hiratsukanum on Alnus incana KF031541 KF031554
Milesina vogesiaca on Polystichum aculeatum MG907235
Cronartium strobilinum on Pinus taeda FLAS-F-53222
Quasipucciniastrum agrimoniae on Agrimonia pilosa HMAS67306
Quasipucciniastrum agrimoniae on Agrimonia pilosa HMAS248092
Pucciniastrum kusanoi on Clethra barbinervis AB221399 AB221427
Pucciniastrum tiliae on Tilia mandshurica AB221412 AB221455
Chrysomyxa chiogenis on Gaultheria hispidula GU049452 GU049532
Chrysomyxa arctostaphyli on Arctostaphylos sp. DQ200930 AY700192
Coleosporium senecionis on Jacobaea alpina KY810472
Pucciniastrum yoshinagai on Stewartia monadelpha AB221411 AB221434
Quasipucciniastrum agrimoniae on Agrimonia pilosa HMAS248093
100 1.00
96 1. 00
99 1. 00
91 1. 00
100 -
100 1.00
100 1.00
100 0.95
93 0. 98
100 1.00
80 1. 00
99 1. 00
81 1. 00
100 1.00
99 0. 99
96 1. 00
75 1. 00
100 1.00
92 0. 99
87 1. 00
83 1. 00
95 1. 00
100 1.00
100 1.00
100 1.00
85 1. 00
98 0. 85
87 1. 00
98 0. 98
89 1. 00
100 1.00
99 1. 00
94 1. 00
88 -
100 1.00
100 1.00
100 1.00
100 1.00
79 1. 00
100 0.99
97 0.91
93 1. 00
- 0.90
- 0.9 9
- 0.80
- 0.97
- 0.81
- 0.9 6
- 0.93
- 0.89
- 0.81
- 0.9 8
- 0.9 8
Quasipucciniastrum gen. nov
Figure 1. Bayesian 50% majority-rule consensus tree based on concatenated data of rDNA ITS and LSU sequences. Pileolaria
terebinthi was used as outgroup. Values on the branches indicate maximum likelihood bootstrap values and Bayesian posterior
probabilities. Hyphen indicates that bootstrap values were less than 75% and Bayesian posterior probabilities less than 0.80.
6X.-H. QI ET AL.
A. pilosa, 1 September 2000, J.Y. Zhuang
(HMAS172173); CHINA. SICHUAN: Liangshan Yi
Autonomous Prefecture, Meigu, II, III on A. pilosa,
8 October 1989, J.Y. Zhuang (HMAS63892); CHINA.
SICHUAN: Liangshan Yi Autonomous Prefecture,
Yanyuan, II, III on A. pilosa, 11 September 2010, J.Y.
Zhuang (HMAS243033); CHINA. SICHUAN: Tibetan
Qiang Autonomous Prefecture of Ngawa, Wolong, II,
III on A. pilosa, 23 September 1989, J.Y. Zhuang & S.X.
Wei (HMAS63888); CHINA. SICHUAN: Yi Bin, Xingwen, II,
III on A. pilosa, 21 June 2016, P. Zhao (HMAS248093);
CHINA. TIBET: Rikaze, Yadong, II, III on A. pilosa,
20 August 2011, J.Y. Zhuang & T.Z. Wei
(HMAS244481); CHINA. YUNNAN: Hong He, Binbian, II,
III on A. pilosa, 19 September 2007, J.Y. Zhuang
(HMAS199430); CHINA. YUNNAN: Hong He, Mengzi, II,
Figure 2. Morphological characters of Quasipucciniastrum agrimoniae. A: Uredinia (white arrow) on the hypophyllous leaf surface. B:
No uredinia and telia on eiphyllous leaf surface. C: Uredinium with echinulate ostiolar cells (white arrow) observed by SEM. D:
Urediniospores with echinulate spines observed by SEM. E: Uredinium with well-developed ostiolar cells (black arrow) observed by
LM. F: Uredinium with peridium cell (black arrow). G: Urediniospores observed by LM. H: Vertical section of hypophyllous telia. I:
Subepidermal teliospores with apparently thickened apical wall. J: Subglobose teliospores with vertical or oblique septa. Bars: A,
B = 0.6 mm; C, E, G, H, I, J = 20µm; D, F = 10µm.
MYCOLOGY 7
III on A. pilosa, 14 June 2016, P. Zhao (HMAS248092);
CHINA. YUNNAN: Kun Ming, II, III on A. pilosa,
17 June 2016, P. Zhao (HMAS248097).
Hosts of uredinial and telial stages and geogra-
phical distribution: Agrimonia pilosa –China:
Beijing, Gansu, Guangxi, Guizhou, Heilongjiang,
Inner Mongolia, Ningxia, Sichuan, Tibet, Yunnan.
Discussion
In this study, we recognised a new genus
Quasipucciniastrum on Agrimonia pilosa, and described
a new species Q. agrimoniae based on morphological
and molecular evidences. Hitherto, rust species in gen-
era Puccinia Pers., Pucciniastrum, Thekopsora, Uredo
Pers. and Uropyxis J. Schröt. have been recorded on
Agrimonia species, but Quasipucciniastrum clearly dif-
fers from above-mentioned genera by its hypophyllous
telia, subepidermal teliospores with subglobose shape,
and multicellular teliospores with thickened apical wall.
rDNA based phylogenies further supported the inde-
pendence of Quasipucciniastrum from these genera,
especially Pucciniastrum and other genera in
Pucciniastraceae, which have similar uredinial and telial
morphologies. Here we confirmed the close relation-
ship of Quasipucciniastrum and Cronartium (Figure 1).
Quasipucciniastrum is currently best placed in
Cronartiaceae, together with Cronartium, although
this should be better confirmed after the examination
of the morphological characters in spermogonial and
aecial stages of Q. agrimoniae.Morphologically,genus
Cronartium owned Milesia-type uredinia that is similar
to Quasipucciniastrum, but its columnar telia and uni-
cellular teliopsores are embedded in a common matrix
(Cummins and Hiratsuka 2003). Hitherto, we are not
successful to obtain the spermogonial and aecial
stages of Q. agrimoniae. Further investigation on its
life cycles and detailed morphological examination of
spermogonia and aecia are necessary.
The rust fungus on Agrimonia pilosa was pre-
viously frequently recognised as Pucciniastrum agri-
moniae due to its ostiolar cells and subepidermal
teliospores divided by vertical septa (Tai 1979;Guo
1989; Zhang et al. 1997; Cao and Li 1999;Zhuang
and Wei 1999; Cao et al. 2000;Zhuang2001,2005).
P. agrimoniae was first described on A. pilosa from
Western Siberia Borus Mountains, Altai in Russia by
Tranzschel (1895). Based on the original description
of P. agrimoniae from its type specimens and other
Russian materials (Tranzschel 1895;Sydowand
Sydow 1915; Kuprevich and Tranzschel 1957), our
novel species Quasipucciniastrum agrimoniae on
A. pilosa resembles P. agrimoniae in several aspects
but still clearly differs in its 2 to 6 celled and
subglobose teliospores with apparently thickened
apical wall. Similarly P. agrimoniae-like rust on
A. eupatoria was once reported to bear phyloge-
netic affinities to Cronartium flaccidum and
C. ribicola (Cronartiaceae) Maier et al. (2003).
Those specimens used by Maier et al. (2003)have
been shown to be conspecifictoQ. agrimoniae in
our study. As for P. agrimoniae,currentlythereis
no type-derived sequence to confirm its phyloge-
netic affinities.Sincethetypespecimenof
P. agrimoniae was not obtained from all possibly
deposited herbaria, it might have been lost.
Neotypification is thus needed using a new and
suitable specimen from the original host and
locality.
Hitherto, several genera in Pucciniastraceae
have been delimitated based on morphological
characters in teliospores (Cummins and Hiratsuka
2003), even at generic level, the position of telia
and morphology of teliospores have long been
used as important taxonomic criteria (Hiratsuka
1958; Cummins and Hiratsuka 2003; Liang et al.
2005;Yang2015). Although there have been
much debates concerning the generic classifica-
tion based on telial morphologies, recent phylo-
genetic studies and our study supported the
monophyly of all sampled genera in
Pucciniastraceae, thus, supported the effective-
ness of telial morphologies as taxonomic criteria
at generic level. In addition, our morphological
and molecular studies further emphasised the
importance of the uredinial morphology at gen-
eric level because Quasipucciniastrum and
Cronartium with Milesia-type uredinia show
a much closer relationship than those with
Caeoma-type uredinia (e.g.Cronartium,
Chrysomyxa). These overlooked morphological
characters appeared to be very useful in delimit-
ing taxa at generic and suprageneric level. Further
comprehensive studies need to be conducted to
evaluate the effectiveness of these morphological
characters in rust taxonomy.
8X.-H. QI ET AL.
Acknowledgements
We express our gratitude to Dr. Yi-Jian Yao (State Key
Laboratory of Mycology, Institute of Microbiology, CAS,
Beijing, China), Dr. Matthew E. Smith (University of Florida
Herbarium, USA), Dr. Timothy James (University of Michigan
Herbarium, USA), Dr. Barbara M. Thiers (The New York
Botanical Garden, NY, USA) for providing dried specimens
for this study.
Disclosure statement
No potential conflict of interest was reported by the authors.
Funding
This work was financially supported by National Natural
Science Foundation of China [Grant number 31670017],
[China National Funds for Distinguished Young Scholars
[Grant number 31725001];National Key R&D Program of
China [[Grant number 2016YFF0203201].
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