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REVIEW
Biodiversity and taxonomy of the pleomorphic genus Alternaria
Daniel P. Lawrence
1
&Francesca Rotondo
2
&Philipp B. Gannibal
3
Received: 24 May 2015 /Revised: 8 November 2015 /Accepted: 13 November 2015
#German Mycological Society and Springer-Verlag Berlin Heidelberg 2015
Abstract The genus Alternaria, alternarioid hyphomycetes,
comprise a biologically, ecologically, and morphologically
rich group of fungi that has suffered from taxonomic flux for
many years. The taxonomy of these fungi has been predomi-
nately based on conidial characters, which includes shape,
color, septation, and patterns of secondary sporulation, and
to lesser extent on host association, biochemistry, and metab-
olites. Recent phylogenetic studies have made significant
changes to the systematic taxonomy, the accurate identifica-
tion of a taxon or group of taxa, within Alternaria by elevating
26 clades to the subgeneric taxonomic status of section. This
paper aims to serve as an overview of the historical and con-
temporary taxonomic status of the alternarioid hyphomycetes
with special reference to biology, morphology, and phyloge-
netic biodiversity. Additionally, we propose to synonymize
the genus Pseudoalternaria with Alternaria and elevate this
well-supported clade to the taxonomic rank of section,
Pseudoalternaria sect. nov., bringing the total number of sec-
tions to 27 in order to produce a stable and accepted taxonomy
for this diverse genus.
Keywords Fungi .Systematics .Alternarioid
hyphomycetes .Plant pathogens .Tax ono mic se cti on
Introduction
Alternarioid hyphomycetes have been classified into no less
than 14 genera which typically produce phaeodictyospores or
phaeophragmospores. The taxonomy of these genera has been
debated for many years, and several cycles of classification
and subsequent revisions have occurred. Before the advent of
molecular technologies, these genera were classified based
upon their morphological characteristics (Simmons 1954,
1971,1983,1990a,1992; Joly 1964). The morphological
classification of alternarioid hyphomycetes reached its pinna-
cle with the work of E.G. Simmons (Simmons 1967,1971,
1989,1992,2007) in which he defined the alternarioid mor-
pho-species, and defined the distinctive traits for each of the
species described. In recent years, phylogenetic investigations
(Lawrence et al. 2013,2014; Pryor and Bigelow 2003; Runa
et al. 2009; Woudenberg et al. 2013) have supported the main
morphological groups identified by Simmons.
Alternarioid hyphomycetes occupy diverse ecological
modes ranging from saprobes, to endophytes, to pathogens.
Most of the alternarioid species are considered to be cosmopol-
itan saprobes that are ubiquitous through natural and man-made
environments. As plant pathogens, Altenaria spp. are well
known for their ability to produce a wide spectrum of second-
ary metabolites (Andersen et al. 1995,2001,2002,2005;
Andersen and Thrane 1996; Christensen et al. 2005;Frisvad
et al. 2008; Serdani et al. 2002; Walton and Panaccione 1993).
These metabolites include various plant pathogenesis related
toxins, both host and non-host specific (Fujiwara et al. 1988;
Markham and Hille 2001; Meronuck et al. 1972;Nishimura
and Kohmoto 1983;Otanietal.1995; Robeson and Strobel
Section Editor: Roland Kirschner
*Philipp B. Gannibal
phbgannibal@yandex.ru
1
Department of Plant Pathology, University of California,
Davis, CA 95616, USA
2
Department of Plant Pathology, The Ohio State University, Ohio
Agricultural Research and Development Center, Wooster, OH 44691,
USA
3
Laboratory of Mycology and Phytopathology, All-Russian Institute
of Plant Protection, Shosse Podbelskogo 3, Saint Petersburg 196608,
Russia
Mycol Progress (2016) 15:3
DOI 10.1007/s11557-015-1144-x
1981; Thuleau et al. 1988; Wolpert et al. 2002) and mycotoxins
that can contaminate food products (Alexander et al. 2011;
Fernández-Cruz et al. 2010; Lau et al. 2003; Logrieco et al.
1990,2003;Ostry2008). Small-spored Alternaria spp. (e.g.,
A. alternata) also have a prominent role in inducing allergenic
symptoms and cause severe asthma pathologies (Bush and
Portnoy 2001;Eschetal.2001;Saloetal.2006). Here, we
present a detailed description of the main characteristics defin-
ing the alternarioid hyphomycetes, including a thorough treat-
ment of their taxonomic and natural history, ecology, and im-
pact on human activity. Throughout this review, we hope to
highlight the necessity to recognize the complexity and biolog-
ical diversity of this important group of fungi.
Taxonomic history and confusion between Alternaria
and allied genera
The genus Alternaria comprises a group of fungi in the family
Pleosporaceae (Pleosporales, Dothideomycetes,
Ascomycota). Alternaria was established by Nees in 1816
and since then its taxonomy has been disputed. Taxonomy
of Alternaria and related genera has gone through five stages.
Here, we give brief characteristics of each stage.
The first stage (1816–1850s): assessing alternarioid hypho-
mycete biodiversity During that time, four genera, Alternaria
Nees 1816, Brachycladium Corda 1838, Macrosporium Fr.
1832, and Ulocladium Preuss 1851 that have direct relation-
ships to alternarioid hyphomycetes, were described. An allied
genus, Stemphylium Wallr. 1833, was also described at this
time. In the beginning, the genera Alternaria,
Macrosporium,andStemphylium were confused, while
Brachycladium and Ulocladium were consigned to oblivion.
Only a few species were described during the first stage of
Alternaria taxonomic assessment. The type species of
Alternaria was A. tenuis Nees 1816, but the first validly pub-
lished species name was Torula alternata Fr., 1832.
The second stage (1850s–1930s): description of new spe-
cies Almost 400 specific epithets appeared during this pe-
riod. Approximately 300 species names were described
under the generic name Macrosporium.Bytheendofthe
period, the first attempt to revise the taxonomy and
nomenclature of Alternaria and Macrosporium was
published by Elliott (1917) in which he classified them into
morphological groups based on conidial characteristics and
proposed six morphological Alternaria groups with a rep-
resentative species typifying each group. This produced
the first signs of the increasing nomenclatural problems
within the alternarioid hyphomycetes.
The third stage (1930s–1960s): revisions of Alternaria and
Macrosporium Several attempts were made to delimit these
genera and Stemphylium to determine their taxonomic status.
Every attempt to define the genus Alternaria has encountered
the problem of treating numerous taxa which superficially re-
semble the type species of Alternaria,Macrosporium,or
Stemphylium. Wiltshire’s(1933) main conclusion was that
Macrosporium should be suppressed as a nomen ambiguum in
favor of Alternaria. However, this conclusion was not
immediately and unconditionally accepted. Neergaard (1945)
proposed three morphological Alternaria groups, calling them
sections, based upon conidial catenation: section Longicatenatae
typified by A. tenuis (= A. alternata) with 10 or more catenulate
conidia; section Brevicatenatae typified by A. tenuissima with
short chains of 3–5 conidia; and section Noncatenatae typified
by A. brassicae with conidia borne singly or rarely producing a
secondary conidium. Joly (1964) classified species of Alternaria
into three sections based primarily on conidial color, rigidity, or
lateral symmetry: section Claroseminae with light to translucent
yellowish colors; section Brunneoseminae with brown to
reddish-brown darkly pigmented conidia; and section Rigidae
with conidia that have a rigid appearance with a dearth of lon-
gitudinal septa. The above-mentioned classification schemes did
not follow the rules of nomenclature, were not widely adopted,
and are not used today.
The fourth stage (1960s–2000s): Emory Guy Simmons
(1920–2013) Simmons undertook a complete reappraisal
and revision of all names and taxa related to the genus
Alternaria. Simmons studied very thoroughly and carefully
probably all published descriptions, all type herbarium sam-
ples and living strains. At the same time, other mycologists
described a number of new species (approx. 150 legitimate
names), but the number of Simmons’s taxonomic novelties
(approx. 200) is the largest in the history of Alternaria.
At this time, the genus Alternaria and other morphologi-
cally similar genera that produce pigmented or dark-colored
muriform spores were called “phaeodictyosporic hyphomy-
cetes”. Until the 1970s, all phaeodictyosporic hyphomycetes
were divided into three large genera: Alternaria,
Macrosporium,andStemphylium. The generic boundaries
were formidably confusing. A fourth genus, Ulocladium,
was disregarded by taxonomists for a period of more than
100 years. This stage resulted in substantial revision of those
genera and resulted in abolition of Macrosporium in 1969
because the type species of the genus, M. cheiranthi, was
considered to be an Alternaria species (Simmons 1992). The
genera Alternaria,Stemphylium,andUlocladium were typi-
fied by Simmons in 1967. The type specimen of To r u l a
alternata Fr. 1832 was identified by Simmons as synonymous
with Nees 1816 description of A. tenuis; therefore, he declared
A. alternata as the type for the genus (Simmons 1967). Later,
3 Page 2 of 22 Mycol Progress (2016) 15:3
several new genera were segregated from Alternaria:
Alternariaster E.G. Simmons 2007, Chalastospora E.G.
Simmons 2007, Embellisia E.G. Simmons 1971, Nimbya
E.G. Simmons 1989, and Teretispora E.G. Simmons 2007.
The genus Prathoda Subram. 1956 was resurrected by
Simmons in 2007 (by transferring Alternaria longissimi to
Prathoda), and approximately 280 Alternaria species were
considered as legitimate and recognizable. Simmons began
to promote a practice of utilizing Alternaria representative
strains for taxonomy and identification.
Differentiation of the aforementioned taxa was based on a
number of exclusive morphological traits, particularly conid-
ial shape (Simmons 1967,1992,2007). Previous work re-
vealed that various culturing conditions could greatly influ-
ence conidial morphology (Leach and Aragaki 1970;Zitter
and Hsu 1990). For this reason, Simmons and Roberts
(1993) delineated optimal standardized growing conditions
to produce consistent and reproducible sporulation patterns
of alternarioid hyphomycetes. Furthermore, some novel traits
were utilized, e.g., three-dimensional sporulation pattern,
shape of juvenile conidia, width of septa, etc. Several morpho-
logical Alternaria species-groups (complexes) were described
by Simmons (1992) and typified by a representative species.
Simmons defined a species-group as a group of taxa that pro-
duce similar patterns of sporulation and share a high degree of
conidial morphological characters only and have no relation-
ship to phylogeny or nomenclatural rules. Examples include
the A. alternata species-group with taxa that produce small
catenate conidia such as A. alternata, and the A. porri species-
group with taxa that produce large, long tapering apical beak,
and typically non-catenate conidia such as A. porri.Simmons
and Roberts (1993) further subdivided the small-spored
catenulate species of Alternaria into six morphological
groups. Group 1 was characterized as producing a modest
spore size with moderate to short conidial chains of 5–10;
Group 2 with A. gaisen as the representative producing a larg-
er and more robust spore with moderate to short conidial cat-
enation (5–10); Group 3 taxa produced short (50–70 μm) to
very long (100–150 μm) conidiophores that produced copious
amounts of secondary sporulation by the elongation of
subconidium conidiophores; Group 4 produced short bushy
clumped conidiophores with extensive secondary sporulation,
represented by A. alternata; Group 5 produced moderately
long to long chains of conidia, 10–15(20), with rare to no
secondary braches; and Group 6 with A. infectoria as the rep-
resentative, producing clumps of secondary and tertiary
branching chains with a complex three-dimensional structure.
Simmons also developed additional morphological species-
groups based solely upon colony and conidium characteris-
tics, including the A. infectoria species-group, the
A. tenuissima species-group, the A. cheiranthi species-group,
and the A. brassicicola species-group (Simmons 1995;
Simmons and Roberts 1993). Again, it should be emphasized
that the informal groups proposed by Simmons and others
were morphological groups that did not follow the rules of
nomenclature and had no relationship to phylogeny. All minor
details of conidial shape were utilized by Simmons for taxo-
nomic purposes. To date, perhaps all available morphological
traits have been inventoried and utilized for alternarioid hy-
phomycete taxonomy. Simmons has made major contribu-
tions in this area and is credited for studying Alternaria and
other phaeodictyosporic hyphomycetes for over 50 years and
publishing many articles and an identification manual
(Simmons 2007). Simmons has to his credit approximately
150 new Alternaria species and 25 new combinations. At this
stage, order was established in the nomenclature of
alternarioid hyphomycetes. Up to the end of the 2000s, the
Alternaria nomenclature system intended to reflect maximum
morphological diversity, to catalog biodiversity, and to allow
for morphological identification (Gannibal 2012).
The fifth stage (2003–2015): molecular phylogenetic tax-
onomy This stage has employed a comprehensive DNA-
based approach for the analysis of alternarioid hyphomycete
biodiversity. Both morphological and molecular data have
been the basis for several taxonomic revisions. The first mo-
lecular phylogenetic analysis of Alternaria and other closely
related phaeodictyosporic hyphomycete genera, Stemphylium
and the former genus Ulocladium, was conducted by Pryor
and Gilbertson (2000). That study provided robust phyloge-
netic support for the sister relationship of Stemphylium and
Alternaria, and also provided strong support for several pre-
viously described morphological species-groups (i.e., the
alternata-, porri-, brassicicola-, and the infectoria species-
groups) as discrete phylogenetic species-groups based on the
analysis of internal transcribed spacer (ITS) and 18S mtSSU
(mitochondrial small subunit) molecular markers. Pryor and
Gilbertson (2000) also described the radicina species-group,
which was supported by morphological and molecular data as
a clade nested amongst the Alternaria lineage.
Subsequent studies, which included morphological and
molecular data, have elucidated additional Alternaria lineages
which included the sonchi species-group (Hong et al. 2005),
the alternantherae species-group (Lawrence et al. 2012) where
three taxa were transferred from the genus Nimbya to
Alternaria, and the panax- and gypsophilae species-groups
(Lawrence et al. 2013). A total of nine Alternaria species-
groups were identified: the alternata-, alternantherae-,
brassicicola-, gypsophilae-, infectoria-, panax-, porri-,
radicina-, and sonchi species-groups. Alternaria species-
groups were defined as a group of taxa that shared a high
degree of conidial morphological characters, and that cluster
as discrete strongly supported monophyletic groups based up-
on molecular phylogenetic approaches utilizing DNA se-
quence data. On the generic level, the alternarioid
Mycol Progress (2016) 15:3 Page 3 of 22 3
hyphomycetes were enlarged by the resurrection of the genus
Brachycladium (Inderbitzin et al. 2006) and typification of
three new genera Undifilum B.M. Pryor, Creamer,
Shoemaker, McLain-Romero & Hambl. (Pryor et al. 2009),
Sinomyces Yong Wang & X.G. Zhang (Wang et al. 2011), and
Pseudoalternaria D.P. Lawr., Gannibal, Dugan & Pryor
(Lawrence et al. 2014). These new genera were erected to
accommodate morphological and phylogenetic novelties.
Continued phylogenetic analyses of Alternaria have utilized
nuclear rDNA (ribosomal DNA) and the intervening ITS
regions, mtSSU, and many protein-coding genes
[glyceraldehyde-3-phosphate dehydrogenase (gpd), endo-
polygalacturonase, Alternaria major allergen Alt a 1, beta-tu-
bulin, translation elongation factor 1-alpha (TEF 1-α), the sec-
ond largest subunit of RNA polymerase II (RPB2), calmodulin,
chitin synthase, Tsr 1 , plasma membrane ATPase, actin, and 1,3,
8–trihydroxynaphthalene (THN)] to produce phylogenetic hy-
potheses at different phylogenetic scales. Most studies have
provided strong support for the above-mentioned phylogenetic
species-groups; however, no studies were able to resolve the
order of divergence of the described species-groups (Andrew
et al. 2009; Hong et al. 2005;Lawrenceetal.2012; Pryor et al.
2009; Pryor and Gilbertson 2000).
Previous evolutionary studies have shown that an increase in
taxon and loci sampling may increase statistical support for key
phylogenetic nodes (Rokas and Carroll 2005). Lawrence et al.
(2013) analyzed 10 nuclear protein-coding loci for the ability to
resolve species-group relationships. In that study, the authors
revealed that two loci, beta-tubulin and TEF 1-α,wereunable
to resolve relationships (polytomous) among Alternaria species-
groups likely due to their slow tempo of molecular evolution,
which is useful for high-level phylogenetic studies (Baldauf and
Palmer 1993; Cheney et al. 2001; Stiller and Hall 1997). In that
same study, the authors revealed a phenomenon that is common-
ly encountered in fungal molecular systematics, substitution sat-
uration of the third codon position of protein-coding genes
(Hansen et al. 2005; Liu et al. 1999; Matheny et al. 2007;
Miller and Huhndorf 2005;Sungetal.2007). They revealed
for the first time that three loci, RPB2,Ts r 1 , and chitin synthase,
possessed statistically significant transition substitution satura-
tion at the third codon position, causing these loci to be phylo-
genetically uninformative for high-level Alternaria phylogenetic
studies (Lawrence et al. 2013). The phylogenetic utility of five
protein-coding loci (gpd, Alt a 1, actin, plasma membrane
ATPase, and calmodulin) from Lawrence et al. (2013) provided
the first strongly supported phylogenetic hypothesis among
Alternaria lineages. Lawrence et al. (2013) elevated eight phy-
logenetic Alternaria species-groups to the taxonomic status of
section each with a type specimen. Similarly, 18 additional phy-
logenetic groups have been elevated to the status of section
within Alternaria, and we propose an additional section, section
Pseudoalternaria D.P. Lawr., Rotondo & Gannibal sect.
nov. (based on the study by Lawrence et al. 2014), bringing
the total number of sections to 27 by synonymizing the genera
Allewia E.G. Simmons 1990, Brachycladium,Chalastospora,
Chmelia Svob.-Pol. 1966, Crivellia Shoemaker & Inderb. 2006,
Embellisia,Lewia M.E. Barr & E.G. Simmons 1986, Nimbya,
Pseudoalternaria,Sinomyces,Teretispora,Ulocladium,
Undifilum,andYbotromyces Rulamort 1986 with Alternaria
(Woudenberg et al. 2013,2014). Figure 1depicts a consensus
cladogram of Alternaria sections based upon seven nuclear loci
from Lawrence et al. (2013,2014), Woudenberg et al. (2013),
and Grum-Grzhimaylo et al. (2015).
Given the overlap of morphological features among
Alternaria species/sections and the morphological plasticity
of some species, phylogenetic species recognition is now be-
coming standard within the genus. Several loci have been
shown to be more informative than others for species delimi-
tation (Lawrence et al. 2013). Within Alternaria, the utility of
ITS for species identification, which is the universal barcoding
gene for Fungi (Nilsson et al. 2014), has been hotly debated
because several morphological species (e.g., A. alternata and
A. tenuissima) are either 100 % identical or nearly so.
Statistical tests of phylogenetic informativeness performed
by Lawrence et al. (2013) revealed that the plasma membrane
ATPase, calmodulin, and Alt a 1 loci were the most
Fig. 1 Phylogeny, taxonomy, and mating system of alternarioid
hyphomycetes. Cladification derived from manual combination of four
phylogenetic trees based on analysis of sequences of seven nuclear genes
(Lawrence et al. 2013,2014; Woudenberg et al. 2013; Grum-Grzhimaylo
et al. 2015). Type of mating system: 1heterothallism, only one of two
idiomorph of MAT1 locus present in a genome; 2homothallism, both
idiomorphs of MAT1 locus present in a genome; ns not studied (data for
sect. Infectoriae obtained from Andersen et al. 2009;dataforsect.
Nimbya obtained from Johnson et al. 2002; data for sect. Crivellia
obtained from Inderbitzin et al. 2006; data for Stemphylium obtained
from Inderbitzin et al. 2005; other data obtained from Gannibal and
Kazartsev 2013 and Gannibal, unpublished)
3 Page 4 of 22 Mycol Progress (2016) 15:3
informative. The Alt a 1 locus unreliably amplifies some spe-
cies within sect. Infectoriae, therefore we suggest that the
most suitable genetic markers for molecular identification of
species within the genus Alternaria are the plasma membrane
ATPase and calmodulin loci (Lawrence et al. 2013).
Morphology and molecular phylogeny of Alternaria
sections
Alternaria species are characterized as alternarioid hyphomy-
cetes that produce darkly pigmented multi-celled conidia that
are typically dictyosporous, some phragmosporous,
catenulate, some borne singly (Fig. 2) (Inderbitzin et al.
2006;Lawrenceetal.2014; Preuss 1851; Pryor et al. 2009;
Simmons 1971,1989,2007; van Zinderen 1940). The genus
Alternariaster is not included in this review because a recent
study revealed that this genus resides in the Leptosphaeriaceae
and not the Pleosporaceae (Alves et al. 2013). The genus
Paradendryphiella Woudenberg et al. 2013 was recently
erected to accommodate the former species Embellisia
annulata which has been shown to consistently cluster outside
of Alternaria and sister to Pleospora Rabenh. ex Ces. & De
Not. 1863, therefore Paradendryphiella is not discussed.
Below is an updated description of the genus Alternaria
which also includes a brief review of the morphology and
phylogenetic position of each section that comprises the
alternarioid hyphomycetes.
Colonies effuse, usually gray, greenish, dark olivaceous,
dark blackish-brown or black. Mycelium immersed and usu-
ally surface; hyphae colorless, olivaceous-brown or brown.
Stroma rarely formed. Setae and hyphopodia absent.
Conidiophores macronematous, mononematous, simple or ir-
regularly and loosely branched, pale brown or brown, solitary
or in fascicles. Conidiogenous cells integrated, terminal be-
coming intercalary, polytretic, sympodial, or sometimes
monotretic, cicatrized. Conidia solitary or in chains, dry, ba-
sically ovoid, obovoid, cylindrical, narrowly ellipsoid or
obclavate, beaked or non-beaked, pale or medium
olivaceous-brown to brown, smooth or verrucose, with trans-
verse and with or without oblique or longitudinal septa. Septa
can be thick, dark and rigid and an internal cell-like structure
can be formed. Species with meristematic growth are known.
Ascomata small, solitary to clustered, erumpent to (nearly)
Fig. 2 Conidia of aAlternaria alternantherae EGS 52–039 (sect.
Alternantherae), bA. arborescens EGS 39–128 (sect. Alternaria), c
A. brassicicola BMP 0325 (sect. Brassicicola), dA. abundans BMP
1928 (sect. Chalastospora), eA. cheiranthi EGS 41–188 (sect.
Cheiranthus), fA. embellisia EGS 38–073 (sect. Embellisia), g
A. proteae EGS 39–031 (sect. Embellisioides), hA. limicola BMP 2239
(sect. Euphorbiicola), iA. eureka EGS 36–103 (sect. Eureka), j
A. infectoria EGS 27–193 (sect. Infectoriae), kA. japonica BMP 0332
(sect. Japonicae), lA. scirpicola EGS 19–016 (sect. Nimbya), m
A. calycipyricola EGS 52–072 (sect. Panax), nA. mouchaccae EGS
31–061 (sect. Phragmosporae), oA. linariae CBS 109156 (sect. Porri),
pA. arrhenatheri BMP 1942 (sect. Pseudoalternaria), qA. chartarum
BMP 0359 (sect. Pseudoulocladium), rA. selini EGS 35–178 (sect.
Radicina), sA. cinerariae EGS 33–169 (sect. Sonchi), tA. leucanthemi
EGS 17–063 (sect. Teretispora), uA. atra BMP 0353 (sect.
Ulocladioides), vA. alternariae BMP 0352 (sect. Ulocladium), w
Alternaria sp. BMP 0951 (sect. Undifilum)
Mycol Progress (2016) 15:3 Page 5 of 22 3
superficial at maturity, globose to ovoid, dark brown, smooth
or setose, apically papillate, ostiolate. Papilla short, blunt.
Peridium thin. Hamathecium of cellular pseudoparaphyses.
Asci few to many per ascoma, (4–6–)8-spored, basal, bitunicate,
fissitunicate, cylindrical to cylindro-clavate, straight or some-
what curved, with a short, furcate pedicel. Ascospores muriform,
ellipsoid to fusoid, slightly constricted at septa, yellow-brown,
without guttules, smooth, 3–7transversesepta,1–2seriesof
longitudinal septa through the two original central segments,
end cells without septa, or with one longitudinal or oblique sep-
tum, or with a Y-shaped pair of septa.
Type :Alternaria alternata Nees (1816).
Taxonomic position: Eukarya: Fungi: Ascomycota:
Pezizomycotina: Dothideomycetes: Pleosporomycetidae:
Pleosporales: Pleosporaceae: Alternaria
Section Alternantherae D.P. Lawr., Gannibal, Peever &
B.M. Pryor 2013
Type species:Alternaria alternantherae (Holcomb &
Antonop.)
Section Alternantherae is comprised of four species
(A. alternantherae,A. celosiicola,A. gomphrenae,and
A. perpunctulata) that were separated from the former genus
Nimbya based on morphological and phylogenetic data.
Primary conidiophores are short to moderately long (70–125×
4–5μm) and possess one to a few conidiogenous loci, the
conidiogenous tip may be slightly enlarged. Conidia are solitary
or rarely paired, narrowly ellipsoid, sometimes subcylindrical,
rarer narrow ellipsoidal, or near obclavate, distoseptate (a thin
septum lacking a septal plate and perforated by cytoplasmic junc-
tions) and euseptate (septum formed from a septal plate). Conidia
are large (80–112 × 18–20 μm) and transversely septate with no
or 1–2 longitudinal or oblique septa, sometimes slightly constrict-
ed at some transverse septa (Fig. 2a). Lumina of transverse sec-
tions are octagonal to rounded. The conidial beak is unbranched,
long filiform (100–470×2–4μm), septate or aseptate, sometimes
with terminal swelling. Section Alternantherae is strongly sup-
ported as the sister group to sect. Alternaria.
Section Alternaria D.P. Lawr., Gannibal, Peever & B.M.
Pryor 2013
Type species:Alternaria alternata (Fr.) Keissl.
This section was named by Lawrence et al. (2013), since it
includes the type for the genus. This version is correct according
to ICBN Arts 22.1 and 22.2. Woudenberg et al. (2013) generated
an orthographic variant ‘Alternata’, which is contradictory to the
ICBN rules and should not be in use because the name of the
subdivision that contains the type species must repeat the generic
name unaltered. Section Alternaria consists of approximately 60
species that are commonly referred to in the literature as small--
spored Alternaria (e.g., A. alternata,A. arborescens,A. gaisen,
and A. tenuissima). Primary conidiophores are curved or straight,
short to very long, simple or branched with one to several termi-
nal conidiogenous loci. Conidia are borne in moderately long to
long chains that are simple or branched. Conidia are small or
moderate in size, 20–35(60)× 8–12 μm, obclavate, long ellipsoid
or ellipsoid, transversely septate 3–7(11), with slight constriction
at some septa, and 1–2 longitudinal septa in one or a few
Fig. 2 (continued)
3 Page 6 of 22 Mycol Progress (2016) 15:3
transverse divisions. Most conidia gradually narrow into a ta-
pered apical beak or secondary conidiophore (Fig. 2b). Apical
beak (5–10 μm sometimes up to 35 μm) is generally shorter than
the conidial body. Secondary conidiophores may be formed api-
cally or laterally and are short to moderately long, with one or a
few conidiogenous loci. Ascomata of A. alternata are typically
small (170–200× 190–240 μm) solitary or clustered, erumpent,
globose to ovoid, smooth, dark brown, apically papillate,
ostiolate. Asci are relatively straight (170–190× 23–30 μm),
(4–6–) 8-spored, bitunicate, fissitunicate, cylindrical to
cylindro-clavate in shape. Ascospores are 37–43× 13–14 μm,
ellipsoid to fusoid with slight constriction at some septa, 3–7
transverse septa, 1–2 longitudinal septa in central segments,
end cells with no septa or one longitudinal or oblique septum
or Y-shaped pair of septa, brown, eguttulate, smooth
(Ariyawansa et al. 2015). Section Alternaria shares a close evo-
lutionary relationship with sections Alternantherae,
Euphorbiicola,andPorri.
Section Brassisicola D.P. Lawr., Gannibal, Peever &
B.M. Pryor 2013
Type species:Alternaria brassicicola (Schwein.) Wiltshire
Section Brassicicola consists of five described species
(A. brassicicola,A. conoidea,A. mimicula,A. septorioides,
and A. solidaccana). Primary conidiophores are short to mod-
erately long (15–150× 5–6μm), simple or branched with one
or several apical conidiogenous loci. Chains of conidia are
long to moderately long, simple or branched. Conidia are el-
lipsoid, ovoid or somewhat obclavate, small to moderate
(20–95×7–22 μm) in size, typically with solitary apical and
sometimes with solitary lateral secondary conidiophores that
are shorter than the conidium body and have only one
conidiogenous locus (Fig. 2c). Conidia are septate with slight
to strong constrictions at transverse septa and no or a few or
many longitudinal septa. The apical cell of a terminal co-
nidium is wide and rounded. Chlamydospores may ap-
pear. Based on a five protein-coding gene analysis sect.
Brassicicola is most closely related to sections Panax,
Gypsophilae,Sonchi,Radicina,Porri,Euphorbiicola,
Alternaria,andAlternanatherae (Lawrence et al. 2013).
Section Chalastospora (E.G. Simmons) Woudenb. &
Crous 2013
Type species:Alternaria cetera E.G. Simmons
The genus Chalastospora wasconceivedbySimmons
(2007) by which he re-classified Alternaria cetera,origi-
nally isolated from Elymus scrabus,asChalastospora
cetera because the conidia “have alternarioid qualities only
in the most tenuous sense”(Simmons 2007).
Section Chalastospora currently consists of six species,
A. abundans,A. armoraciae,A. breviramosa,A. cetera,
A. malorum,andA. obclavata. Primary conidiophores are
solitary, smooth, and brown in color, short to long (10–
30×3–5μm), commonly flask-shaped arising from surface
hyphae or from lateral branches of rope-like aerial hyphae
with one to several conidiogenous loci (Crous et al. 2009).
Conidia are ovoid, narrowly ellipsoid to ellipsoid with no
apical beak, no to multiple (1–3) transverse septa with no
or rare longitudinal septa. Conidia are small (18–22(35)×
3–4(6)μm), rarely solitary, generally in long chains up to
15 units. Secondary conidiophores are usually absent, but
may be formed apically or laterally with one to a few
conidiogenous loci. Molecular phylogenetic studies
strongly suggest that sect. Chalastospora is sister to sec-
tions Infectoriae and Pseudoalternaria (Crous et al. 2009;
Hong et al. 2005;Lawrenceetal.2012,2013,2014.
Interestingly, two species A. abundans (Fig. 2d)and
A. armoraciae (see Woudenberg et al. 2013), do not resem-
ble other species in this clade, but rather species formerly
described as Embellisia sensu lato, with the production of
mostly phragmoconidia that are typically short and not
elongated as in other species in this clade.
Section Cheiranthus Woudenb. & Crous 2013
Type species:Alternaria cheiranthi (Lib.) P.C. Bolle
Section Cheiranthus consists of two species (A. cheiranthi
and A. indefessa) which are characterized as producing short to
moderately long primary conidiophores that may be simple or
branched with one or multiple conidiogenous loci. Conidia are
dictyosporous, ovoid to broadly ellipsoid with slight to strong
constrictions at some transverse septa, catenate in short to long
chains that are simple or branched (Fig. 2e). Secondary conidi-
ophores may be formed apically or laterally with one
conidiogenous locus. Previous phylogenetic studies have placed
these species sister to the ovoid catenate sect. Pseudoulocladium
and to the obovoid noncatenate sect. Ulocladioides (Runa et al.
2009;Lawrenceetal.2012,2013; Woudenberg et al. 2013).
Section Crivellia (Shoemaker & Inderb.) Woudenb. &
Crous 2013
Type species:Alternaria penicillata (Corda) Woudenb. &
Crous
Section Crivellia is comprised of two species
(A. papavericola and A penicillata), both are important patho-
gens of opium poppy (Czyzewska and Zarzycka 1960;
Milatovic 1952). Alternaria papavericola is characterized by
unbranched primary conidiophores (20–30×4–5μm) with de-
velopment of conidiogenous loci (2–4) at the apex. Conidia are
small, cylindrical (17–70× 4–8μm) with tapered apices, solitary
or rarely short-catenate from the apical pore, characterized by
transverse septa (3–6) and absence of longitudinal septa.
Production of microsclerotia has not been observed in culture.
Alternaria penicillata is characterized by the formation of
macro- and microconidiophores. Macroconidiophores (400–
600×20–35 μm) are generally straight, branched at the terminal
region and arise from a globose cell (20–30 μmindiameter)or
Mycol Progress (2016) 15:3 Page 7 of 22 3
from a basal group of cells that resemble a microsclerotium.
Microconidiophores (30–40× 4–6μm) are simple, branched to-
ward the apex and arise from an undifferentiated mycelium.
Conidia are cylindrical (17–30×5–7μm) with transverse septa.
Microsclerotia (20–100× 25–75 μm) are produced in artificial
media and on natural substrates. Alternaria penicillata forms
ascocarps (320–400× 220–300 μm) that are solitary or clustered,
globose to depressed globose, interdispersed with dark
microsclerotia and macroconidiophores. Asci are numerous with
ellipsoidal uniseriate or biseriate ascospores (20–25× 6–9μm).
The phylogenetic position of sect. Crivellia within the genus
Alternaria is not certain.
Section Dianthicola Woudenb. & Crous 2013
Type species:Alternaria dianthicola Neerg.
Section Dianthicola is comprised of three species
(A. dianthicola,A. elegans,andA. simsimi)thatproducesimple
or branched primary conidiophores which may or may not pro-
duce apical proliferations. Conidial shapes vary from narrowly
ovoid to narrowly ellipsoid with multiple transverse septa and
few longitudinal septa with a filiform beak or apical secondary
conidiophores that are solitary or in short chains. Based on a
three protein-coding gene analysis, sect. Dianthicola is sister to
sect. Ulocladioides (Woudenberg et al. 2013).
Section Embellisia (E.G. Simmons) Woudenb. & Crous
2013
Type species:Alternaria embellisia Woudenb. & Crous
The genus Embellisia wasestablishedtoseparatean
atypical species of Helminthosporium Link 1809, H. allii
Campan., originally isolated from garlic, based solely on
conidial and conidiophore morphology (Simmons 1971).
Simmons noted that H. allii produced conidiophores as
successive sympodial proliferations which were inconsis-
tent with the erect growth of Helminthosporium conidio-
phores and were more similar to conidiophores produced
by Curvularia Boedijn 1933, Bipolaris Shoemaker 1959,
Drechslera S. Ito 1930, Alternaria,andUlocladium
(Alcorn 1988,1991; Shoemaker 1959,1962; Simmons
1967). Section Embellisia consists of three species,
A. chlamydosporigena,A. embellisia,andA. tellustris,
which produce large populations of phragmoconidia with
a very low percentage of dictyoconidia as opposed to the
strict production of phragmoconidia produced by
Curvularia,Bipolaris,andDrechslera. Additionally, the
conidia of sect. Embellisia possess distinctly dark, rigid
and thickened transverse septa as compared to the external
wall (Fig. 2f). Conidia are variously swollen, usually
straight elliptical or oblong elliptical with a small popula-
tion that may be smoothly curved or sigmoid and typical-
ly borne singly. Conidiogenous sites at conidiophore
geniculations are umbilicate, hyphal coils and intra-
hyphal proliferating chlamydospores are produced in
culture (Simmons 1971,1983). Phylogenetic studies sug-
gest that sect. Embellisia is most closely related to
sections Phragmosporae,Soda,Chalastospora,
Pseudoalternaria,andInfectoriae.
Section Embellisioides Woudenb. & Crous 2013
Type species:Alternaria hyacinthi (de Hoog & P.J. Mull.
Bis) Woudenb. & Crous
Section Embellisioides consists of six species
(A. botryospora,A. hyacinthi,A. lolii,A. planifunda,
A. proteae,andA. tumida) obtained from plants or rhizo-
sphere. Conidiophores simple, short or moderately long,
straight or often with multiple, geniculate, sympodial pro-
liferations. Conidia are solitary or in short chains, obovoid
to ellipsoid, rarely short subcylindrical (Fig. 2g). Apical
and basal cells are wide rounded or short conical.
Conidia have several transverse and longitudinal septa;
transverse septa can be thick, dark and rigid in contrast to
the external wall. Some mature conidia can have no longi-
tudinal or oblique septa. Apical or lateral, short secondary
conidiophores may occur. Chlamydospores and a sexual
morph may occur. Pseudothecia, if present, are ovoid to
spheroid, dark, thin-walled, papillate towards the apex as
asci mature, markedly setose. Asci are subellipsoid to
subcylindrical, straight to somewhat inequilateral,
bitunicate, usually 8-spored. Immature ascospores are
subellipsoid and slightly inequilateral; mature ascospores
are ellipsoid to subclavate, with multiple transverse septa,
discontinuous series of longitudinal septa through major
central spore compartments, and with or without a longi-
tudinal septum in terminal cells. Phylogenetic data support
the sister relationship with sect. Eureka.
Section Euphorbiicola Woudenb. & Crous 2014
Type species:Alternaria euphorbiicola E.G. Simmons &
Engelhard
Section Euphorbiicola consists of two species,
A. limicola and A. euphorbiicola. Conidia are character-
ized as ovoid to obclavate, medium to large, disto- and
euseptate, catenulate in short to moderately long chains,
terminal conidia have no or a simple long apical beak
(Fig. 2h). Conidia possess multiple transverse septa (some
constriction at some transverse septa) and some longitu-
dinal septa. Secondary conidiophores may be produced
apically or laterally. Section Euphorbiicola is sister to
sect. Porri (Woudenberg et al. 2014).
Section Eureka Woudenb. & Crous 2013
Type species:Alternaria eureka E.G. Simmons
Section Eureka consists of six species (A. anigozanthi,
A. cumini,A. eureka,A. geniostomatis,A. leptinellae,and
A. triglochinicola) that were isolated from plants or rhi-
zosphere. Primary conidiophores simple or branched,
3 Page 8 of 22 Mycol Progress (2016) 15:3
short to long, straight or geniculate, with one or several
conidiogenous pores. Conidia are solitary or in short
chains. Juvenile conidia are subspheroid, ovoid to
subcylindrical (Fig. 2i). Mature conidia are obovoid,
ellipsoid, narrowly ellipsoid, cylindrical, obclavate, or
carrot-like. Apical cell is hemispherical to conical.
Conidia have several transverse and no or many longitu-
dinal septa; transverse septa can be thick, dark and rigid
in contrast to the external wall. Conidia may have con-
strictions near several central septa. Sometimes conidia
produce solitary apical or lateral secondary conidiophores
that are usually not longer than the length of the body and
have one to a few conidiogenous loci. Conidium color is
yellowish or dilute brown to medium brown and oliva-
ceous brown. The outer wall is smooth; punctulate orna-
mentation is rarely visible. Chlamydospores are abundant
on vegetative hyphae or absent. They are intercalary or
terminal, swollen, thick-walled. Ascomata, if present, are
spheroid to ovoid, thin-walled, dark, apically papillate by
the time asci begin to mature, conspicuously setose. Asci
are subcylindrical to subellipsoid, straight to somewhat
inequilateral, bitunicate, usually 8-spored. Juvenile asco-
spores are subellipsoid and slightly inequilateral; mature
ascospores are subclavate to ellipsoid, with transverse
septa, discontinuous series of longitudinal septa through
major central spore segments, and with or lacking a lon-
gitudinal septum in terminal cells. Molecular data support
the sister relationship with the morphologically similar
sect. Embellisioides.
Section Gypsophilae D.P. Lawr., Gannibal, Peever &
B.M. Pryor 2013
Type species:Alternaria gypsophilae Neerg.
Section Gypsophilae consists of eight species
(A. axiaeriisporifera,A. ellipsoidea,A. gypsophilae,
A. juxtiseptata,A. nobilis,A. saponariae,A. vaccariae,
and A. vaccariicola) that have only been isolated from
plants in the Caryophyllaceae. Primary conidiophores
are short or long (up to 250 × 5–6μm), simple or occa-
sionally branched, with one or a few conidiogenous
loci. Conidia are formed in simple chains or in
branching chains of 3–7 units. Conidia are ellipsoid or
globose, broadly or narrowly ovoid with the basal co-
nidium usually obclavate. Conidia are small or large
(40–70 to 125–176× 15–30 μm) with many transverse
(10–15(19)) and longitudinal septa, conspicuous con-
striction at some transverse septa. Apex of conidium
may be rounded, cylindrical, conical, or produce a sec-
ondary conidiophore. Apical secondary conidiophores
may be short or longer than conidial body with 1–2(4)
conidiogenous loci. Conidia may produce a single short
lateral secondary conidiophore with a single
conidiogenous locus. Section Gypsophilae is sister to
sections Alternaria,Alternantherae,Euphorbiicola,and
Porri (Lawrence et al. 2013; Woudenberg et al. 2014).
Section Infectoriae Woudenb. & Crous 2013
Type species:Alternaria infectoria E.G. Simmons
Section Infectoriae currently consists of approximately 25
species (e.g., A. ethzedia,A. graminicola,A. infectoria,and
A. metachromatica) with 11 taxa known to produce a sexual
morph previously known as Lewia. Primary conidiophores are
simple or branched, short to long (20–150×3–4μm) with (1)2–6
apical conidiogenous loci. Conidia are obclavate, long-ellipsoid
sometimes subcylindrical, small (12–30× 1–10 μm) to moderate
in size (30–60× 6–15 μm) (Fig. 2j). Conidial body has (1)4–
7(10) transverse and 1–2(3) longitudinal septa in 1–4 transverse
sections with slight constriction near some transverse septa.
Conidial chains are moderately long to long and branched due
to secondary sporulation and polytretic conidiogenous cells.
Apical secondary conidiophores are long (10–60 μm), genicu-
late with multiple (2–3(8)) conidiogenous loci. Lateral secondary
conidiophores are rare. Ascomata, if present, smooth walled, asci
subcylindrical or subellipsoid with 5(−7) transverse septa and 1–
2 longitudinal septa in series in central segments, one or no
longitudinal or oblique septum in terminal cells. Based on
multi-locus analyses sect. Infectoriae is strongly supported as
the sister group to sect. Pseudoalternaria (Lawrence et al. 2014).
Section Japonicae Woudenb. & Crous 2013
Type species:Alternaria japonica Yos hii
Section Japonicae consists of two species (A. japonica and
A. nepalensis) isolated from the Brassicaceae. Primary conid-
iophores are short to long, simple or sometimes branched con-
taining a single conidiogenous locus. Conidia are short to
long-ovoid with transverse and longitudinal septa, constric-
tions at most transverse septa, in short chains (Fig. 2k). An
apical conidiogenous locus may give rise to a secondary co-
nidiophore. The precise phylogenetic position of sect.
Japonicae within Alternaria is not certain; however, it clusters
more closely with taxa that were previously classified as
Alternaria and Ulocladium than to other lineages (Lawrence
et al. 2013; Woudenberg et al. 2013).
Section Nimbya (E.G. Simmons) Woudenb. & Crous
2013
Type species:Alternaria scirpicola (Fuckel) Sivan.
The genus Nimbya was conceived by Simmons (1989)
to segregate the atypical species of Sporidesmium
scirpicola Fuckel, a pathogen of river bulrush. The taxon-
omy of Sporidesmium Link 1809 has historically been
problematic as the type, S. scirpicola, has been previously
classified as Clasterosporium scirpicola (Fuckel) Sacc.,
Cercospora scirpicola (Fuckel) Zind.-Bakker, and
Alternaria scirpicola (Fuckel) Sivanesan (Fuckel 1863;
Saccardo 1886; Sivanesan 1984; van Zinderen 1940).
Mycol Progress (2016) 15:3 Page 9 of 22 3
Currently, section Nimbya consists of four species
(A caricis,A. scirpicola,A. scirpinfestans,and
A. scirpivora). Alternaria scirpicola typically produces
multi-celled apically tapering conidia that may be solitary
or in short chains of 2–8 units. Conidia are distoseptate
which become partially or fully euseptate at maturity and
possess multiple transverse septa (6–13) with conspicuous
constriction near some transverse septa, and extremely
rare longitudinal septa which are key characters that clear-
ly separate sect. Nimbya from other closely related sec-
tions of Alternaria (Fig. 2l). Section Nimbya conidia are
extended obclavate or subcylindrical, moderate in size
30–130×6–22 μm with an extended cone-shaped apical
beak (20–100 μm). Primary conidiophores are generally
simple, 20–150 μm, with 1–4 conidiogenous loci with
close geniculations. The sexual state has long been recog-
nized as Macrospora Fuckel 1870 and is morphologically
similar but distinct as compared to the former teleomorphs
Lewia (sect. Infectoriae), Allewia (sections Embellisioides
and Eureka)(Simmons1986,1990a; Vieira and Barreto
2005), and the teleomorph of Stemphylium spp.,
Pleospora (Crivelli 1983). Section Nimbya is most closely
related to sections Embellisia,Phragmosporae,Soda,
Chalastospora,Pseudoalternaria,andInfectoriae.
Section Panax D.P. Lawr., Gannibal, Peever & B.M.
Pryor 2013
Type species:Alternaria panacis (= A. panax)Whetzel
Section Panax currently consists of seven species pri-
marily isolated from the Araliaceae (A. araliae,
A. avenicola,A. calcipyricola,A. dendropanacis,
A. eryngii,A. panacis,andA. photistica) (Deng et al.
2015). Primary conidiophores are short to moderately
long (100–200×6–8μm) with one to a few conidiogenous
loci. Conidia are arranged in short to moderately long
simple or branched chains. Conidia are obclavate, long
obclavate or ellipsoid to ovoid, medium-sized (65–
80 μm) and conspicuously constricted near several trans-
verse septa and have several or many longitudinal septa
(Fig. 2m). Apex of conidium is rounded conical or cylin-
drical and may produce a short or long secondary conid-
iophore with one to several conidiogenous loci. Some
conidia may produce one to several lateral secondary co-
nidiophores with a single conidiogenous locus.
Phylogenetic analyses suggest that sect. Panax is sister
to a monotypic lineage (A. thalictrigena)andsect.
Teretispora (Woudenberg et al. 2013).
Section Phragmosporae Woudenb. & Crous 2013
Type species:Alternaria phragmospora Emden
Section Phragmosporae consists of six species
(A. chlamydospora,A. didymospora,A. limaciformis,
A. molesta,A. mouchaccae,andA. phragmospora).
Primary conidiophores are relatively short or moderately
long, usually simple, sometimes geniculate bearing one
or a few conidiogenous loci. Conidia are solitary or in
short or moderately long chains usually simple or some-
times with short branches (Fig. 2n). Juvenile conidia are
subspherical, ellipsoid, ovoid or cylindrical with rounded
base and apex. Mature conidia are ellipsoid, ovoid or
somewhat cylindrical, straight or curved, or limaciform,
septate, sometimes with solitary apical and seldom with
solitary lateral secondary conidiophores that usually are
not longer than the length of the body and have one to a
few conidiogenous loci. Some transverse septa are dark-
ened and induce slight to conspicuous constriction. Some
conidia remain with no longitudinal or oblique septa but
other part of conidia has 1–2(4) longisepta in some or
many transverse segments. Some conidia produce an
oblique septum in the basal segment. Conidium color is
yellowish or dilute brown to medium brown. The outer
wall is smooth. Chlamydospores are abundant or absent.
They are intercalary or terminal, solitary, swollen, thick-
walled. One to all cells on conidia can also become
chlamydosporic (enlarged, swollen, thick-walled) making
conidia asymmetrical. Thus, each species is able to pro-
duce swollen cells, on hyphae, on conidia or on both,
hyphae and conidia (at least some conidial cells become
rounded with relatively deep constriction). All strains of
all species in this section are known from soil, seawater,
or seawater plants and animals. Only one isolate,
A. didymospora, was collected from another substrate,
equine nasal mucosa. No species or strains were evident-
ly associated with living land plants. Phylogenetic anal-
yses suggest that sect. Phragmosporae is sister to sec-
tions Soda,Chalastospora,Pseudoalternaria,and
Infectoriae (Lawrence et al. 2013).
Section Porri D.P. Lawr., Gannibal, Peever & B.M.
Pryor 2013
Type species:Alternaria porri (Ellis) Cif.
Section Porri consists of 63 species (e.g., A. dauci,
A. macrospora,A. porri,andA. solani) (Woudenberg
et al. 2014). Primary conidiophores are short to rarely
long(upto250μm), simple or branched with one or a
few conidiogenous loci. Conidia are generally solitary or
in short to moderately long chains. Conidia are moderate-
ly large (40–110 × 10 –25(30)μm), broad ovoid ellipsoid,
obclavate, subcylindrical or obovoid, disto- and euseptate
with longitudinal septa and slight constriction near some
transverse septa (5–9to8–13). Most mature conidia pro-
duce a long (80–300(400)μm) filamentous apical beak
that is simple or branched and septate or aseptate
(Gannibal 2015)(Fig.2o). The apical beak may develop
into secondary conidiophores. Conidia may produce api-
cal or lateral secondary conidiophores with no filiform
3 Page 10 of 22 Mycol Progress (2016) 15:3
beak. Lateral secondary conidiophores may arise from the
beak or conidial body. Section Porri consistently clusters
sister to sections Euphorbiicola,Alternaria,and
Alternantherae (Woudenberg et al. 2014;Lawrenceetal.
2013).
Section Pseudoalternaria D.P. Lawr., Rotondo &
Gannibal, sect. nov. MycoBank no. MB812913
=Pseudoalternaria D.P. Lawr., Gannibal, F.M. Dugan &
B.M. Pryor, Mycological Progress 13:272. (2013) 2014, nom.
inval.
Type species:Alternaria arrhenatheri D.P. Lawr., Rotondo
& Gannibal, sp. nov.
=Pseudoalternaria arrhenatheri (as “arrhenatheria”)D.P.
Lawr., Gannibal, F.M. Dugan & B.M. Pryor, Mycological
Progress 13:272. (2013) 2014, nom. inval.
Section Pseudoalternaria consists of two species
(A. arrhenatheri and A. rosae) that produce primary
conidiophores that are simple or branched,
multigeniculate, short to long (9–75(150+) μm) and
may produce several lateral branches. Secondary conid-
iophores short to long, simple to multiple geniculations
and conidiogenous loci that may form apically or lat-
erally. Conidia are ovoid or elliptical, relatively small
(10–33×5–10 μm), catenulate, medium brown to gold-
en brown with 3–5 transverse septa and at most one to
two longitudinal septa in 1–2 transverse segments,
smooth to conspicuously granulate (Fig. 2p). Sexual
state is unknown. Section Pseudoalternaria is strongly
supported as the sister group to sect. Infectoriae
(Lawrence et al. 2014).
Alternaria arrhenatheri D.P. Lawr., Rotondo & Gannibal,
sp. nov. MycoBank no. MB813314
Etym.: arrhenatheria (Latin) referring to host of isola-
tion (Arrhenatherum elatius). Holotype specimen (LEP
140372), dried WPDA culture of the strain 564692-
12FD, is kept in the Mycological herbarium of VIZR,
Saint Petersburg, Russia.
Colony diameter 63 mm in 7 days at 25 °C on
WPDA, tan to light brown, rapidly growing.
Sporulation aggregated appearing granular to the naked
eye. Mycelium subhyaline to light brown, hyphae
smooth, branched, septate, 3.75–5μm wide. Primary
conidiophores aggregated on agar surface or arising
from arachnoid vegetative aerial hyphae, simple or
branched, medium brown, septate, smooth, 8.75–
37.5×3.75–5μm(M=18.05×4.8 μm, n=30), simple
with single apical pore. Secondary conidiophore short
to long, simple to multiple geniculations with one to
several conidiogenous loci. Conidia 17.5–32.5×7.5–
10 μm(M=20.8×8.55 μm, n=50), mainly catenulate,
ellipsoid to obclavate, medium brown to golden
brown, 3–4 transverse septa, 1–2 longitudinal septa,
smooth, may produce a false beak (secondary conid-
iophore).
Section Pseudoulocladium Woudenb. & Crous 2013
Type species:Alternaria chartarum Preuss
Section Pseudoulocladium is comprised of four species
(A. aspera,A. chartarum,A. concatenata,andA. septospora)
that are characterized as producing simple or branched prima-
ry conidiophores with short, geniculate, sympodial prolifera-
tions with multiple conidiogenous loci. Conidia are predomi-
nately ovoid or obovoid, non-beaked, in simple or branched
chains (Fig. 2q). Apical secondary conidiophores produce
multiple conidiogenous loci while lateral secondary conidio-
phores typically only form one conidiogenous locus.
Phylogenetic analyses support the sister relationship with sect.
Ulocladioides.
Section Radicina D.P. Lawr., Gannibal, Peever & B.M.
Pryor 2013
Type species:Alternaria radicina Meier, Drechsler & E.D.
Eddy
Section Radicina consists of five species
(A. carotiincultae,A. petroselini,A. radicina,A. selini,
and A. smyrnii) isolated from the Apiaceae. Primary co-
nidiophores are straight, simple or branched, short or
long, with multiple geniculations, with 1–4aggregated
conidiogenous loci at the apex. The sporulation pattern
resembles clusters or clumps of conidia. Conidia are sol-
itary or in short chains of 2–3. Conidia are wide ovoid or
short ellipsoid, subcylindrical or rarely subspheroid,
moderate in size (30–80(96)× 15–38 μm), with several
transverse septa (3–12) and a few longitudinal septa
(1–3) (Fig. 2r). The apical cell of the conidium is round-
ed, hemispherical, or conical. Some conidia produce a
solitary short apical secondary conidiophore.
Phylogenetic analyses suggest that sect. Radicina and
sect. Gypsophilae share a close evolutionary relationship
(Lawrence et al. 2013).
Section Soda Bilanenko, Georgieva & A.A. Grum-
Grzhim. 2015
Type species:Alternaria kulundii Bilanenko, Georgieva &
A.A. Grum-Grzhim.
Section Soda consists of three species (A. kulundii,
A. petuchovskii,andA. shukurtzii) isolated from highly
alkaline soda lake soils in Kulunda Steppe in Western
Siberia Russia. Primary conidiophores are branched,
short to moderately long with a single conidiogenous
locus. Secondary conidiophores may be lateral or apical
with a single conidiogenous locus, conidiogenous apex
may be enlarged. Conidia borne singly or in short to
long chains that are simple or branched, narrowly ellip-
soid to long-ovoid somewhat obclavate, moderate to
Mycol Progress (2016) 15:3 Page 11 of 22 3
large (60–120× 7–30 μm) with many transverse
(7–11(−18)) and no to several longitudinal septa with
conspicuous constrictions at some basal transverse septa.
Chlamydospores and microsclerotia may develop in
culture. The analysis by Grum-Grzhimaylo et al. (2015)
suggests that sect. Soda is sister to sections
Chalastospora,Pseudoalternaria,andInfectoriae.
Section Sonchi D.P. Lawr., Gannibal, Peever & B.M.
Pryor 2013
Type species:Alternaria sonchi J.J. Davis
Section Sonchi is comprised of two species (A. cinerariae
and A. sonchi) from multiple hosts in the Asteraceae. Primary
conidiophores are moderately long (less than 100 μm) to long
(up to 250 μm), simple or branched, with 1–3 conidiogenous
loci. Conidia are solitary or in short chains, subcylindrical,
broadly ovoid, broadly ellipsoid or obclavate, moderately
large to large (70–150×15–30 μm), with 3–7to8–12 trans-
verse septa which may be slightly or sufficiently constricted
and 1–3 longitudinal septa in (1–4(7)) transverse sections
(Fig. 2s). The apex of the conidium is blunt and consists of a
broadly tapering apical cell or short strong beak or secondary
conidiophore. The secondary conidiophore is short one-celled
or may be as long as or longer than the conidium body. The
analysis by Woudenberg et al. (2013)placedsect.Sonchi as
the sister group to two monotypic lineages, A. brassicae and
A. helianthiinficiens,respectively.
Section Ter e ti spora (E.G. Simmons) Woudenb. & Crous
2013
Type species:Alternaria leucanthemi Nelen
This section is comprised of only one species, A. leucanthemi,
isolated from Leucanthemum maximum, Asteraceae (Gannibal
2012; Simmons 2007). Primary conidiophores are simple and
bear few conidiogenous loci (1–3). Cylindrical conidia (80–
130(160)×17–23(30) μm) are generally solitary, and character-
ized by the presence of both transverse septa (7–14(17)), and
longitudinal septa (3–7) (Fig. 2t). According to the phylogenetic
study by Woudenberg et al. (2013)Teretispora clustered with
Alternaria and Ulocladium species and was re-circumscribed as
a section within the genus Alternaria.
Section Ulocladioides Woudenb. & Crous 2013
Type specimen:Alternaria cucurbitae Letendre & Roum.
Section Ulocladioides currently consists of ten species
(e.g., A. atra,A. cucurbitae,multiformis,andA. obovoidea)
that were previously classified as Ulocladium species. Here,
briefly summarized, are the characteristic morphological traits
observed by Simmons and Roberts (1993) and reassessed by
Gannibal (2012). Section Ulocladioides 3-dimensional spor-
ulation pattern is usually characterized by simple or branched
conidiophores (5–200× 3–5μm). Secondary conidiophores,
when present, are short and characterized by several
conidiogenous loci. Conidia are obovoid or sub-spherical
(14–40×7–21 μm) with no beak and transverse (1–7) and
longitudinal (1–3) septa (Fig. 2u). Conidia arise in clusters
when conidiophore development is closely geniculate.
Phylogenetic studies suggest that sect. Ulocladioides is sister
to sections Pseudoulocladium,Dianthicola,andCheiranthus.
Section Ulocladium (Preuss) Woudenb. & Crous 2013
Type species:Alternaria botrytis (Preuss) Woudenb. &
Crous
The epitype of the former genus Ulocladium is Alternaria
botrytis CBS 197.67. Additionally, two former Ulocladium
species, U. alternariae (originally isolated from Daucus
carota)andU. oudemansii (unknown source), have consis-
tently clustered outside of the core Ulocladium group (sect.
Ulocladioides) in previous phylogenetic studies (Hong et al.
2005;PryorandBigelow2003; Pryor and Gilbertson 2000;
Runa et al. 2009). Morphological examination of
U. alternariae and two new isolates of Ulocladium-like taxa
from China revealed divergent conidiophore and conidial
morphologies as compared to the core Ulocladium group
(sect. Ulocladioides) (Wang et al. 2011). The Chinese group
detailed distinct morphological features (production of simple
conidiophores with a single apical pore or one or two short,
uniperforate, geniculate sympodial proliferations) that sepa-
rated U. alternariae and the two novel taxa from the core
Ulocladium group (conidiophore geniculations often
multiperforate and closely to widely spaced) and erected the
genus Sinomyces (Wang et al. 2011). Woudenberg et al.
(2013) synonymized Sinomyces with Alternaria and placed
these species in sect. Ulocladium.SectionUlocladium con-
sists of four species (A. alternariae,A. botrytis,A. capsici-
annui,andA. oudemansii) and is characterized as producing
simple or branched septate primary conidiophores that are
short to moderate (10–60× 3–5μm) with a single apical pore
occasionally with 1–2 uniperforate geniculations. Conidia are
obclavate to fusoid, obovoid to ellipsoid, or obovoid to broad-
ly ellipsoid with 2–6 transverse and 1–3 longitudinal septa,
and moderate in size (18–39× 11–17 μm) (Fig. 2v). Section
Ulocladium clusters sister to A. argyranthemi and A. thlaspis
(two monotypic lineages) that together are sister to sections
Crivellia,Undifilum,Nimbya,Embellisia,Soda,
Chalastospora,Pseudoalternaria,andInfectoriae (Lawrence
et al. 2013).
Section Undifilum (B.M. Pryor, Creamer, Shoemaker,
McLain-Romero & Hambl.) Woudenb. & Crous 2013
Type species:Alternaria bornmuelleri (Magnus) Woudenb.
&Crous
The genus Undifilum was erected to differentiate two spe-
cies, Embellisia oxytropis and Helminthosporium
bornmuelleri (originally isolated from the Fabaceous plants
Oxytropis kansuensis and Securigera varia,respectively),as
3 Page 12 of 22 Mycol Progress (2016) 15:3
morphologically and phylogenetically distinct from other
alternarioid hyphomycetes (Pryor et al. 2009). Section
Undifilum consists of four species (A. bornmuelleri,
A. cinerea,A. fulva,andA. oxytropis) that are extremely slow
growing on culture media, often requiring more than 30 days
to attain a colony diameter of 5 mm. Primary conidiophores of
A. bornmuelleri are produced in clustered groups, rarely sol-
itary, moderate in length and wider at the base (10)20–50×
10–12 μm (basally) 6–8μm (apically). Conidia are ovate to
obclavate to long ellipsoidal to cylindrical, generally widest at
the second cell from the base, longer conidia are slightly
narrowed at the apex, broadly rounded at both ends, thin
walled, transverse segments divided by (2)3–4(5) dark brown
transverse septa, small to moderate in size (29)39–50(55)×
10–12(15)μm, catenate but in short chains (Fig. 2w). Upon
conidial germination the germ tube is wavy and unbranched
for three to four spore lengths. Section Undifilum is more
closely related to sections Ulocladium,Crivellia,Nimbya,
Embellisia,Soda,Chalastospora,Pseudoalternaria,and
Infectoriae than to other Alternaria sections based on a five-
gene combined dataset (Lawrence et al. 2013).
Monotypic lineages
Multi-locus phylogenetic analyses have identified eight spe-
cies (listed below) that do not cluster with strong support
among the 27 described sections of Alternaria, thus additional
sections may be described in future studies as more/new
Alternaria species/isolates are molecularly characterized.
Alternaria argyranthemi E.G. Simmons & C.F. Hill,
Mycotaxon 65:32. 1997.
Alternaria brassicae (Berk.) Sacc., Michelia 2 (no.6): 129.
1880.
Alternaria dennisii M.B. Ellis, Mycol. Pap. 125: 27. 1971.
Alternaria helianthiinficiens E.G. Simmons, Walcz & R.G.
Roberts, Mycotaxon 25: 204. 1986.
Alternaria peucedani S.H. Yu, Mycobiology 42:1. 2014.
Alternaria soliardae E.G. Simmons, CBS Biodiversity Ser.
(Utrecht) 6: 374. 2007.
Alternaria thalictrigena K. Schub. & Crous, Fungal Planet
No. 12: 2. 2007.
Alternaria thlaspis (E.G. Simmons & J.C. David) D.P.
Lawr., Rotondo & Gannibal comb. nov. MycoBank
MB812914.
Basionym: Embellisia thlaspis E.G. Simmons & J.C. David,
Mycoscience 41: 533. 2000.
Asexual–sexual connections
Taxonomic achievements and current nomenclature rules
have abolished the form phylum Deuteromycota. The place-
ment of all mitosporic (imperfect) fungal “species”should be
defined in a phylogenetically supported framework. Clear
phylogenetic concordance between anamorph and teleomorph
genera has been established and unites both classifications
into one natural system based on the principle “one fungus –
one name”(Taylor 2011). As we previously mentioned, phy-
logenetic analyses have shown that the sexual morphs of the
alternarioid hyphomycetes, and currently all asexual
alternarioid hyphomycetes, should be placed in the
Pleosporaceae (Inderbitzin et al. 2006; Pryor and Bigelow
2003; Woudenberg et al. 2013; Zhang et al. 2012).
Considerable molecular phylogenetic studies, together with
the connection between teleomorphic genera and alternarioid
hyphomycetes, have allowed the true placement of the latter
within the modern systematics of fungi. Pleosporaceae is the
largest family in the Pleosporales (Dothideomycetes,
Ascomycota) and is comprised of 36 teleomorphic genera
and approximately 770 species (Kirk et al. 2008).
During the taxonomic history of Alternaria, several ascomy-
cetous genera were considered to be its sexual state. Those con-
troversial taxonomies have caused several misidentifications.
The genera Clathrospora Rabenh. 1857, Comoclathris Clem.
1909, Leptosphaeria Ces. & De Not. 1863, and Pleospora were
described as having Alternaria asexual morphs (Domsch et al.
1980; Ellis 1971; Ellis and Ellis 1985; Simmons 1954;
Whitehead and Dickson 1952; von Arx and Muller 1950)and
among these Pleospora was often mentioned as the sexual state
of Alternaria. Furthermore, the name Pleospora was ambigu-
ouslyusedwhenDendryphion Wallr. 1833, Diplodia Fr. 1834,
Phoma Fr. 1821, and Stemphylium-like asexual morphs were
described (Sivanesan 1984). Simmons (1986) established that
the name Pleospora should be used for the sexual state of
Stemphylium. The genus Lewia was described to morphologi-
cally group Alternaria-related teleomorphs. Later, the connec-
tion with Lewia was repeatedly well-established (Kwaśna and
Kosiak 2003; Simmons 1986,2007). The type species of Lewia,
L. scrophulariae, previously was mentioned as belonging to the
genera Sphaeria Haller 1768, Leptosphaeria,andPleospora.At
least one Lewia species was identified by Whitehead and
Dickson (1952) as a species of Pyrenophora Fr. 1849
(Kwaśna and Kosiak 2003). For Ulocladium, Bonar (1928)
and Farr et al. (1989) mistakenly proposed its sexual state as
Lasiobotrys Kunze 1823 (Venturiaceae). However, molecular
phylogenetic studies have clearly shown that these fungi belong
in the Pleosporaceae (Inderbitzin et al. 2006; Pryor et al. 2009;
Pryor and Bigelow 2003;Runaetal.2009;Wangetal.2011).
Allewia,Crivellia,Lewia,andMacrospora were consid-
ered teleomorphs of some alternarioid hyphomycetes.
Simmons (1986,1990b) elucidated that Lewia and Allewia
were the sexual morphs of Alternaria and Embellisia,respec-
tively. Macrospora was connected with the former anamor-
phic genus Nimbya (Simmons 1989). Similarly, the genus
Crivellia was shown to be the sexual morph of
Brachycladium (Inderbitzin et al. 2006). Currently, one sect.
Mycol Progress (2016) 15:3 Page 13 of 22 3
Alternaria, ten sect. Infectoriae, two sect. Panax, one sect.
Embellisioides, one sect. Eureka,foursect.Nimbya and one
sect. Crivellia sexual species have been described. However,
the names of the conidial state for Lewia chlamidosporiformans
and L. sauropodis were not defined and the descriptions of
conidia were not provided (Vieira and Barreto 2005;Zhang
and David 1996).
The genus Pleospora and sections Alternaria,
Embellisioides,Eureka,Infectoriae,andNimbya share some
morphologically similar features but each also possesses dis-
tinct ascomata and ascospore characters. Section Infectoriae
species are characterized by small ascomata and ascospores,
when compared with those produced by Pleospora (Simmons
1986). The morphological characteristics described by
Simmons (1990b) for the former genus Allewia (sections
Embellisioides and Eureka) fall into ranges of variability of
sect. Infectoriae (Simmons 1986). The ability to form differ-
ent conidial states was fundamental to distinguish these genera
(Simmons 1990b). However, ascostromata of both A. proteae
(sect. Embellisioides)andA. eureka (sect. Eureka) are con-
spicuously setose, while those of sections Alternaria and
Infectoriae are smooth.
Unfortunately, E.G. Simmons did not perform his own de-
scription of Macrospora (sect. Nimbya), which was originally
described by Fuckel in 1870. However, Fuckel observed that
the type species, M. scirpicola, was characterized by larger
ascomata and ascospores, with asci broadly obovate-saccate
compared to the subcylindrical or subellipsoid asci produced
by sect. Infectoriae and sections Embellisioides and Eureka
(Simmons 1989).
Section Crivellia differs from other sexual morphs of the
alternarioid hyphomycetes by producing ascospores with few-
er numbers of transverse septa. Mature sect. Infectoriae,sec-
tions Embellisioides and Eureka, and sect. Nimbya ascospores
have 5(−7) transverse septa (up to 9 in sections Embellisioides
and Eureka)and1–2 series of longitudinal septa through the
central spore segments, terminal cells without septa, or with
one longitudinal or oblique septum. Mature sect. Crivellia
ascospores only produce three transverse septa, with one lon-
gitudinal septum in either or both central cells, but not in
terminal cells.
Phylogenetic data (Lawrence et al. 2014) revealed that
the types of section Infectoriae and several other sections
including Chalastospora,Embellisia,Phragmosporae,
and Nimbya are closely related. However, two former
Lewia species, A. avenicola and A. photistica, have been
placed in sect. Panax (Woudenberg et al. 2013). These
two groups of former Lewia species are characterized by
similar conidial sizes and shapes, but A. avenicola and
A. photistica connected with sect. Panax are able to pro-
duce ascomata under pure culture conditions, while only
protoascomata with no mature ascospores were found in
cultures of sect. Infectoriae (Andersen et al. 2009).
Anamorph–teleomorph connections for several sections
within the alternarioid hyphomycetes has clearly been demon-
strated by single conidium-to-ascospore and ascospore-to-
conidium studies. The distinct and robust morphological differ-
ences among ascomata and ascospores of sections Crivellia,
Embellisioides,Eureka,Infectoriae,andNimbya support the
demarcation of these taxa as well-defined morphological sec-
tions. Additionally, molecular phylogenetic data support the sep-
aration of these taxa as discrete phylogenetic clades.
Taxonomic c o n c l u s i on s
The field of systematics consists of three broad areas, taxonomy
which includes naming and cataloguing taxa, classification of
organisms in a hierarchical fashion from domain to the species-
level or lower, and evolutionary biology by which phylogenetic
relationships among taxa are deduced. The name of a taxon or
group of taxa is perhaps one of the most important aspects of
systematic biology because thisishowinformationaboutan
organism or group of organisms is communicated and allows
for predictions about the biology of said organisms. Scientific
names of fungi may change over time as increased knowledge
is obtained regarding an organism’s biology which may include
morphological characters, host and geographical associations,
and DNA-based phylogenetic position. As for many fungal
groups, a polyphasic classification scheme, which includes
the above-mentioned biological and molecular characters,
should be utilized when classifying fungal taxa in order to
convey as much biological information as possible.
The taxonomy and classification of alternarioid taxa have
been largely based on morphological characters of conidia and
conidiophores and to a lesser extent on host associations
(Simmons 1989,2007; Zhao and Zhang 2005). DNA-based
molecular phylogenetics have supported as well as over-
turned some of these classification schemes (Alves et al.
2013; Inderbitzin et al. 2006; Lawrence et al. 2012,2013,
2014; Pryor et al. 2009;Runaetal.2009;Wangetal.2011;
Woudenberg et al. 2013). Mycologists as well as other biolog-
ical scientists seek congruence between morphological char-
acters and molecular phylogenetic hypotheses that result in
phylogenetic clades. The resolution of alternarioid hyphomy-
cetes groups is largely supported by morphological characters
albeit that some conidial characters have been shown to over-
lap to some degree between distantly and closely related
groups.
For instance, some members of sect. Alternaria as
circumscribed by Lawrence et al. (2013) share some sim-
ilar conidial characters with some members of sect.
Infectoriae even though they are distantly related
(Lawrence et al. 2013,2014). Significant biological dif-
ferences exist between the two groups such as the pro-
duction of biological compounds including mycotoxins
3 Page 14 of 22 Mycol Progress (2016) 15:3
and other secondary metabolites that are not produced
reciprocally (Andersen et al. 2002;Andersenand
Thrane 1996; Christensen et al. 2005), the presence of
mating-type genes where members of sect. Alternaria
are heterothallic (Arie et al. 2000;Berbeeetal.2003)
and members of sect. Infectoriae arepresumedtobeho-
mothallic based on ascospore-to-conidium and conidium-
to-ascoma studies of some known sexual taxa in this
section (Simmons 1989,2007).
Some authors have suggested collapsing certain genera
based on morphological characters, namely Alternaria and
Ulocladium sensu lato (sections Ulocladioides and
Pseudoulocladium) as a single genus, Alternaria (Joly
1964). Pryor and Gilbertson (2000) also suggested that species
of Ulocladium should be synonymized with Alternaria,based
on molecular phylogenetics of three individual loci. However,
extended phylogenetic analyses have revealed that sections
Ulocladioides and Pseudoulocladium are well-supported sec-
tions distinct from other Alternaria lineages (Lawrence et al.
2013;Runaetal.2009; Woudenberg et al. 2013). Even though
some morphological overlap exists between them (i.e.,
A. septospora and A. chartarum conidia are predominately
ovoid, a character associated with sect. Alternaria). Runa
et al. (2009) hypothesized that this incongruence may be the
result of a loss of the fundamental obovoid shape of sect.
Pseudoulocladium conidia or that these taxa (A. septospora
and A. chartarum) preceded the development of the diagnostic
obovoid conidium shape as evidenced by the strongly sup-
ported bifurcation of the A. septospora and A. chartarum
clade and the core obovoid sect. Ulocladioides.
The efforts of Lawrence et al. (2013)andWoudenberg
et al. (2013) have greatly improved the taxonomic nomen-
clature of the alternarioid hyphomycetes by increasing the
taxonomic resolution of an important and pleomorphic
group of fungi. The improved taxonomy will allow both
specialists and non-specialists to easily identify taxa that
reside in this large and hyperdiverse group of fungi that
are perhaps the most commonly encountered fungi by
mycologists and plant pathologists. Undoubtedly, future
studies will identify and describe additional taxa and sec-
tions as novel alternarioid hyphomycetes are discovered
from natural and man-made environments.
Ecology and life cycle of Alternaria
Ecological features of Alternaria species have been reviewed
several times (Kwaśna 1992; Scheffer 1992; Thomma 2003).
The most scrupulous review was performed by Rotem (1994),
who predominately concentrated on all available information
on overseasoning, effect of temperature and wetting on spor-
ulation and infection processes, and on the effect of weather
on epidemics. Most of Rotem’s conclusions are contemporary
and generally accepted.
Alternaria species demonstrate a variety of ecologicalchar-
acteristics and forms of interactions with hosts, including plant
parasites, saprobes and endophytes. Some cause serious eco-
nomically important crop diseases. Occasionally, Alternaria
spp. are detected as endophytes or human and animal patho-
gens. The diversity of plant and human mycoses induced by
Alternaria and possible pathogenicity factors were briefly
reviewed by Lawrence et al. (2008). The interesting and ob-
scure contemporary question is an origin of such diversity, i.e.,
evolution of parasitic features in alternarioid hyphomycetes.
Pathogenicity in alternarioid hyphomycetes correlates with
their phylogeny. Several large groups contain predominantly
plant pathogens or saprobes. Several relatively small
Alternaria sections (e.g., sect. Nimbya) consist mainly of path-
ogens restricted to plants in one or two families. The pathoge-
nicity and specialization of several groups were poorly studied
or were not studied at all (e.g., sections Chalastospora and
Embellisia). Here, we present a brief description of four eco-
logical groups of the alternarioid hyphomycetes characterized
by different substrate association and pathogenicity.
Plant pathogens Alternaria sect. Porri (large-spored species)
is the largest group of phytopathogens, with approximately 63
species, that infect numerous plants from different families.
The greatest diversity of large-spored species has been found
on the Asteraceae, while a smaller number of species have
been described on the Solanaceae and other plant families
(Simmons 2007). Usually, one phytopathogenic fungal spe-
cies is associated with one host-plant species or a small group
of taxa in a single genus. Phylogenetic analyses suggest that
these specific host-pathogen associations within different
plant families have occurred multiple times throughout the
evolution of this clade.
A number of small Alternaria sections contain patho-
genic species associated with one restricted group of
plants. Both species in sect. Crivellia are pathogens of
poppy. Four species in sect. Nimbya have a connection
with only the Cyperaceae. Similarly, all three species in
sect. Alternantherae are associated with Amaranthaceae,
eight species from sect. Gypsophilae were found only on
Caryophyllaceae, five species from sect. Radicina are
pathogens of Apiaceae, and both species from sect.
Sonchi are pathogens of Asteraceae. Here, we consider
only species for which the phylogenetic position has been
elucidated. It is likely that, when the intrageneric position
of all Alternaria species is delimited, and as additional
species and sections are defined, the fungal section–plant
family connection will likely degenerate. An example of a
small section with no strong plant family association is
sect. Brassicicola. Alternaria brassicicola, the common
noxious pathogen of Brassicaceae, is nested in one section
Mycol Progress (2016) 15:3 Page 15 of 22 3
with four rare species found on plants of the Resedaceae
and Solanaceae, in soil or on latex drying on wounded
trunks of Hevea sp.
Saprobes The most common saprobes among the alternarioid
hyphomycetes are within sections Alternaria,Infectoriae,and
Ulocladioides, totaling more than 120 species. Many of these
alternarioid hyphomycetes can be recovered from predomi-
nantly lifeless substrates of plant origin including dead plants,
paper, and food (Rotem 1994). However, they can also be
isolated from living plants, usually from senescent or dam-
aged tissues, and cause important yield losses. Very often,
saprobic as well as pathogenic species inhabit seeds, especial-
ly seeds formed in dry fruits with no thick pulpy pericarp, e.g.,
seeds of Poaceae, Brassicaceae, Apiaceae, etc. Frequently,
species within sect. Alternaria are isolated from plant organs
primarily infected by other phytopathogens. Usually, such
species are described in the literature as A. alternata or
A. tenuissima. However, artificial inoculations with small-
spored Alternaria species are rarely successful in completing
Koch’s postulates. Yet, a number of cases supporting
A. alternata and A. tenuissima pathogenicity on several plants
have been reported: cucumber, pistachio, hazelnut, noni, blue-
berry, apple, amaranth, and some weeds (Blodgett and Swart
2002; Harteveld et al. 2013;Hongetal.2006; Hubballi et al.
2011; Karunakara Murthy et al. 2003; Pryor and Michailides
2002; Rotondo et al. 2012; Vakalounakis 1990; Milholland
1973). There are a few exceptional cases, when A. alternata-
like strains are narrowly specialized strong pathogens and
produce host-specific toxins due to possessing clusters of con-
ditionally dispensable genes located on supernumerary chro-
mosomes. These cases are described in a subsequent section.
Endophytes There are some cases where Alternaria species
have been isolated from asymptomatic plant tissues. Several
studies have demonstrated the ability of Alternaria species to
live endophytically without inducing pathogenesis inside
leaves of tomato, wheat, maple, tropical epiphytic orchid, am-
aranth, and some other plants (Blodgett et al. 2000;Chenetal.
2011; Larran et al. 2001,2007;Maetal.2010;Qietal.2009).
A study investigating the pathogenicity of A. infectoria-like
strains isolated from apple leaves also indicated a true endo-
phytic lifestyle for some specimens (Serdani et al. 2002). Only
normally saprobic species were revealed as endophytes. Since
this result was found by several studies in different plants, it
cannot be attributed to methodological mistakes. Further in-
vestigations are necessary to better understand the type of
interactions between plant and fungus in this system. Is the
endophytic phase just a sluggish latent period for disease in-
duced by a weak pathogen, and/or is pathogenesis initiated
due to the health state of the host?
Three endophytic species within sect. Undifilum,fromthe
Fabaceae (Astragalus and Oxytropis), A. cinereum,A. fulva,
and A. oxytropis, produce the toxic compound swaisonine
(Baucom et al. 2012), which causes a neurological disease,
locism, of grazing animals, resulting in economic losses in
livestock (James 1989). Probably, sect. Undifilum species as
compared to other Alternaria species have some specific ad-
aptations characteristic for “true”endophytes.
Human pathogens Several Alternaria species mainly attrib-
uted to A. alternata or A. infectoria and a number of
uncharacterized Alternaria isolates have been associated with
infections of the cornea, oral and sinus cavities, respiratory
tract, skin, and nails (Arrese et al. 1996;Barbassoetal.
2005;Barnesetal.2007;Cascioetal.2004;Duboisetal.
2005; Mirkin 1994; Neumeister et al. 1994; Romano et al.
2001). Alternaria species have importance as emerging hu-
man invasive pathogens in immuno-compromised patients
(Morrison and Weisdorf 1993; Vartivarian et al. 1993). The
species Alternaria molesta was described from a skin lesion of
a porpoise, Phocaena phocaena (Simmons 2007). Species
residing in sect. Ulocladioides have also been recorded as
agents of keratitis (Badenoch et al. 2006).
Life cycle The life cycle of Alternaria consists of only an
asexual haploid phase or both sexual and asexual phases
(haplo–diploid cycle). Generally, the asexual haploid phase
with conidial reproduction is dominant. An overwhelming
majority of alternarioid hyphomycetes have presumably lost
the ability to reproduce sexually. Nevertheless, many
alternarioid hyphomycete lineages have retained genetic de-
terminants of the heterothallic mating system—two indepen-
dent idiomorphs (~alleles) of MAT1 locus. Homothallic spe-
cies contain both idiomorphs in a single genome.
Ascomata production in pure culture under laboratory con-
ditions has been documented in seven species: two sect.
Nimbya species (A. scirpinfestans and A. scirpivora), one sect.
Embellioides species (A. proteae)andonesect.Eureka species
(A. eureka), two sect. Panax species (A. avenicola and
A. photistica) and one species in sect. Infectoriae
A. hordeicola (Johnson et al. 2002; Kwaśna and Kosiak
2003;Kwaśna et al. 2006;Simmons1990a,2007).
Alternaria calycipyricola,sect.Panax, can produce
protoascomata on agar media (Roberts 2007).
All species with a known sexual state (excluding the
recently described sexual state of A. alternata)arepre-
sumably homothallic. This is supported by observations
of cultures (Andersen et al. 2009; Johnson et al. 2002)
or by PCR assays of mating-type genes (Gannibal and
Kazartsev 2013;Gasichetal.2013;Inderbitzinetal.
2006). Two species, A. alternata (sect. Alternaria)and
A. penicillata (sect. Crivellia), have preserved the
heterothallic mating system for sexual reproduction.
Interestingly, another species from the same lineage
(sect. Crivellia), A. papavericola,hasbeenshowntobe
3 Page 16 of 22 Mycol Progress (2016) 15:3
homothallic (Inderbitzin et al. 2006). In sect. Panax a
heterothallic species without an identified sexual state as
well as homothallic species producing ascomata has been
found (Gannibal, unpublished).
The ratio of recombination and clonality is a genetic basis
for adaptation of fungi to environmental pressures. This ratio
depends on the ecological niche and ecological strategy of the
organism. Homogenous conditions in agroecosystems (e.g.,
monoculture crops) seem to promote a decrease in the role
of sexual recombination in parasitic host-specialized fungi
(Taylor et al. 1999). At the same time saprobic species live
in more mutable conditions and continually adapt to environ-
mental changes spurred primarily via sexual recombination.
In alternarioid hyphomycetes, almost all species with
a known sexual state are homothallic. On the contrary,
all heterothallic species have no sexual reproduction
with only two exceptions as mentioned above. Thus, it
can be proposed that the evolution of alternarioid hy-
phomycetes reduced recombination and this may have
occurred in two possible ways: (1) conversion from het-
erothallism to homothallism i.e., replacement of out-
breeding with inbreeding, and (2) total lack of the abil-
ity to begin or complete the sexual cycle. In the latter
case, the genetic system of determination of mating was
preserved but does not function properly. The fusion of
MAT1-loci leading to homothallism seems to be an ir-
reversible process. Homothallic species have been found
in several distant lineages. Therefore, we hypothesize
that homothallism has evolved several times indepen-
dently within the alternarioid hyphomycetes. Several
groups of homothallic species with a sexual state have
heterothallic ancestors without a known sexual state. To
our knowledge, no examples of sexual species deriving
from asexual fungi have been documented except for
A. alternata. In fact, the most common plant pathogenic
Alternaria species (sect. Porri) have no known sexual
state, but there are also many saprobic species lacking
the sexual state (e.g., sect. Brassicicola). Do they all
have clonal population structure? Truly, it seems to be
clonal in some species, but it has been revealed that
A. brassicicola and A. alternata have a means for gen-
erating and maintaining significant genotypic variation
providing ecologic plasticity (Bock et al. 2002;Bock
et al. 2005; Stewart et al. 2013). Is it parasexual recom-
bination or by another cryptic means? This is still not
clearly understood.
Alternaria toxins
Traditionally, fungal toxins are classified on the basis of their
host specificity, and assigned to two main classes: non-host-
specific toxins (non-HSTs) and host-specific toxins (HSTs).
The genus Alternaria represents a good model to investigate
and characterize the distribution of these compounds
(Logrieco et al. 1990,2003; Lou et al. 2013; Ostry 2008;
Scott 2001;Thomma2003). In recent years, several studies
have been carried out to evaluate Alternaria mycotoxin prev-
alence and their potential dangers concerning human con-
sumption in food and foodstuffs (Fernández-Cruz et al.
2010;Kocher2007; Lau et al. 2003; Ostry et al. 2004;Scott
et al. 2006;Scott2001; Solfrizzo et al. 2004,2005).
Beyond noting that Alternaria species can produce myco-
toxins and their effects on humans, the Alternaria toxin litera-
ture lays critical groundwork in understanding the ecological
and evolutionary implications of fungal toxins. Of particular
interest are those studies elucidating the role and characteristics
of HSTs (Markham and Hille 2001; Nishimura and Kohmoto
1983;Otanietal.1995; Wolpert et al. 2002) and non-HSTs
(Fujiwara et al. 1988; Meronuck et al. 1972; Robeson and
Strobel 1981; Thuleau et al. 1988) with plants.
Chemotaxonomic studies, based on secondary metabolites pro-
files, have been successfully utilized to discriminate species
within the genus Alternaria (Andersen et al. 1995,2001,
2002,2005; Andersen and Thrane 1996; Christensen et al.
2005; Frisvad et al. 2008; Serdani et al. 2002). Many non-
HSTs have been identified, but only a few of the modes of
action have been elucidated, and they are not directly involved
in the infection process (Lawrence et al. 2008;Thomma2003).
Instead, HSTs are a determinant for the development of a
few destructive diseases, and they generally display severe
effects on a rather narrow host species range (Howlett 2006;
Kohmoto and Otani 1991; Markham and Hille 2001;
Nishimura and Kohmoto 1983; Otani et al. 1995; Scheffer
and Livingston 1984; Walton and Panaccione 1993; Wolpert
et al. 2002). Toxins that are produced by these pathotypes are
chemically diverse, ranging from low molecular weight sec-
ondary metabolites to peptides. Tsuge et al. (2013)presenteda
detailed review of the HST-producers belonging to
A. alternata sensu lato. That work covers all the aspects in-
volved in the different HST pathosystems, describing chemi-
cal structures, role in pathogenesis, mode of action, and their
molecular genetics. In the present review, we summarize the
main steps of the HSTs characterization and how this has been
utilized to investigate evolutionary processes and phylogenet-
ic relationships among Alternaria HST-producers.
The comparison between pathogenic and non-pathogenic
A. alternata species has demonstrated that pathogenicity is
strictly related to the presence of small supernumerary chro-
mosomes, termed conditionally dispensable chromosomes
(CDCs) (Ajiro et al. 2010; Akagi et al. 2009;Akamatsu
et al. 1997,1999; Hatta et al. 2002; Ito et al. 2004; Johnson
et al. 2000; Masunaka et al. 2005; Miyamoto et al. 2009,
2010; Tanaka et al. 1999). Gene clusters responsible for the
synthesis of HSTs have been identified for the pathogenic
variants of A. alternata andarelessthan2Mbinsize.
Mycol Progress (2016) 15:3 Page 17 of 22 3
Moreover, it has been demonstrated that four of the seven
A. alternata pathotypes (Japanese pear, apple, strawberry
and tangerine), multiple copies of the toxin biosynthetic genes
are necessary to initiate pathogenesis (Barnes et al. 2007;
Harimoto et al. 2007; Hatta et al. 2002;Itoetal.2004;
Johnson et al. 2001;Masunakaetal.2000,2005; Ruswandi
et al. 2005;Tanakaetal.1999; Tanaka and Tsuge 2000)
similar to pathosystems in other plant pathogenic
Dothideomycete fungi such as Cochliobolus carbonum,HC-
toxin producer (Ahn and Walton 1996), and Pyrenophora
tritici-repentis, a PtrToxB producer (Lamari et al. 2003).
The AAL toxin biosynthetic genes clustered on CDCs
have also proven to be useful in elucidating the evolution
and differentiation of pathogenesis of A. alternata tomato
pathotype strains (Akagi et al. 2009). CDCs have been
used to demonstrate that horizontal gene transfer (HGT)
occurs in fungal species, both inter- and intra-kingdom
transfers have been documented (Akagi et al. 2009;
Friesen et al. 2006;Huetal.2012;Milanietal.2012;
Richards et al. 2006;RosewichandKistler2000;Schmitt
and Lumbsch 2009; Syvanen 1985). Hu et al. (2012),
utilizing next generation sequencing of the Alternaria
arborescens genome, were able to provide evidence of
HGT and hypothesized a model of how the transfer may
have occured. They demonstrated HGT utilizing phyloge-
netic incongruence between gene trees and species trees,
codon bias, and GC content. Furthermore, the horizontal
gene transfer can explain the discontinuous distribution of
toxin production among and within Alternaria species.
Interestingly, two separate studies (Harteveld et al. 2013;
Rotondo et al. 2012), conducted in two different geo-
graphical locations (Australia and Italy, respectively),
showed that multiple species of Alternaria are responsible
for leaf blotch disease on apple. The comparison with
Alternaria mali strains highlighted that AM-toxin produc-
tion is not species-restricted (Rotondo et al. 2012).
Together, the studies on HST production by A. alternata
variants highlight the necessity to further investigate the
transfer of CDCs to elucidate the speciation process and
evolution within this genus.
Concluding remarks
The recent efforts to further resolve the phylogeny of
Alternaria have led to a much more stable and predictable
taxonomy based upon both morphological and to a greater
extent molecular data. Species identification using morpho-
logical traits is difficult for specialists and non-specialists alike
due to high levels of morphological plasticity amongst and
within several Alternaria sections. The use of DNA-based
species recognition, incorporating sequences from type spec-
imens, has now become the norm for several fungal groups,
especially when morphological overlap exists (Travadon et al.
2015;Lawrenceetal.2015). Simmons advocated using type
and representative strains for accurate morphological species
identification. Many of Simmons’morphological species have
been corroborated using molecular data as unique and/or
emerging species while others have been rejected
(Woudenberg et al. 2014). To date, multiple locus sequencing
is required to clearly delimit species within several Alternaria
sections (e.g., sections Alternaria,Brassicicola,and
Ulocladioides). The use of the universal barcode (ITS) is not
informative for many Alternaria species, therefore we recom-
mend the use of more phylogenetically informative loci, plas-
ma membrane ATPase and calmodulin (Lawrence et al. 2013),
and comparison of type or representative isolates for accurate
species identification within Alternaria. By employing these
strategies, the systematics of Alternaria will be greatly im-
proved by limiting the inadvertent addition of erroneous no-
menclatural data with sequence data in GenBank by providing
accurate and clearly annotated specimen data for all.
Acknowledgments This work was supported in part by the Russian
Science Foundation (grant # 14-26-00067). We thank Barry M. Pryor
for supplying images for Fig. 2.
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