Phytopathology® • 2021 • 111:437-454 • https://doi.org/10.

1094/PHYTO-06-20-0211-IA

The History of Botrytis Taxonomy, the Rise of Phylogenetics, and

Implications for Species Recognition
Andrea R. Garfinkel†

Oregon CBD, Independence, OR 97351

Accepted for publication 23 September 2020.

ABSTRACT
Botrytis is one of the oldest, most well studied, and most economically important fungal taxa. Nonetheless, many species in this genus have
remained obscured for nearly 300 years because of the difficulty in distinguishing these species by conventional mycological methods. Aided by the
use of phylogenetic tools, the genus is currently undergoing a taxonomic revolution. The number of putative species in the genus has nearly doubled
over the last 10 years and more species are likely to be discovered in the future. The implementation of phylogenetic species recognition concepts in
Botrytis is providing for more resolution on the relatedness among species than ever before, and this has helped to overcome issues in historical
species recognition using morphology, sexual crosses, and pathogenicity tests. Meanwhile, the use of genetic tools is helping to reveal surprising
insight into this archetypal necrotroph’s behavior, making these approaches increasingly important in species recognition and identification. As
Botrytis taxonomy continues to evolve at a rapid pace, researchers should be encouraged to continue to employ the powerful tool of phylogenetics
while considering how it fits into a larger framework of classical Botrytis species recognition. Starting points for discussion on how to move forward
with Botrytis species recognition are included herein, with an emphasis on the implications and utility of new species descriptions.

Keywords: genetic analysis, gray mold, morphology, mycology, naming species, new species, nomenclature, species concepts, systematics

BOTRYTIS—THE FUNGUS, THE PATHOGEN,
THE REVOLUTION
Nearly 300 years after its inception as a taxon, research into the
genus Botrytis is currently revolutionizing our knowledge of this
group of economically significant and globally distributed plant
pathogens. The pathogen Spotlight Issue of Phytopathology focused
solely on Botrytis, in which this review is published, is itself indicative
of the importance of Botrytis research for the field of plant pathology
as a whole. B. cinerea, the type species of this genus, was voted by
researchers and the scientific community to be the second most
important plant pathogen in molecular plant pathology (Dean et al.
2012). This species has been used as an important model organism for
understanding the development of fungicide resistance (Hahn 2014),
plant–pathogen interactions such as the evolution of necrotrophy
(Amselem et al. 2011) and host specificity (Valero-Jiménez et al.
2019; Staats et al. 2005), and, more surprisingly, the ability of
pathogens to occur as endophytes while maintaining virulence
(Grant-Downton et al. 2014; Shaw et al. 2016; Sowley et al. 2010; van
†
Corresponding author: A. R. Garfinkel; andrea@jackhempicine.com
The author(s) declare no conflict of interest.
© 2021 The American Phytopathological Society
Kan et al. 2014). In perhaps one of the most groundbreaking articles
in molecular plant pathology of the decade, Botrytis cinerea was
shown to secrete small RNAs that behave as effectors to suppress the
plant immune response (Weiberg et al. 2013).
Amid the revolutionary insights brought on by this new age of
Botrytis research, the genus has been undergoing taxonomic
restructuring at an overwhelming pace. As I write this review, the
present number of formally recognized Botrytis species sits at 38.
Nonetheless, since I have reviewed manuscripts describing new
Botrytis species, this number will almost certainly increase prior to
the publication of this article, which serves as a demonstration of
just how rapidly the genus is changing. This review will discuss the
history of Botrytis taxonomy, describe its currently changing status
and criteria for species descriptions, and consider the rise of
phylogenetics in the recognition of new species and its implications
for the future of the genus.
A comprehensive and still quite relevant review of Botrytis
species diversity was published by Walker (2016). However,
because of the rapid pace of change in the genus, an update on
Botrytis taxonomy is warranted (likewise, an update will likely be
justified in a few years following the publication of this review).
Furthermore, since this review editorializes certain elements of
Botrytis taxonomy and since it will not discuss intraspecies
variation and several other topics addressed by Walker (2016), it
can be considered a complement to, rather than a replacement, of

Vol. 111, No. 3, 2021 437

Walker’s review. Indeed, the title of this section is a play on words of
the extremely valuable book in which Walker’s review is published,
to which interested parties are encouraged to direct their attention
for additional information on Botrytis (Fillinger and Elad 2016).
THE IMPORTANCE OF BOTRYTIS SPECIES
IN AGRICULTURE
Botrytis species are some of the most widespread plant pathogens
on the planet and have been found infecting their host species in all
climactic zones from tropical islands to the arctic tundra and from
the rainforest to the desert (Elad et al. 2007). Botrytis species cause
disease and significant yield losses in the field and in greenhouses;
they also represent important postharvest pathogens affecting a wide
range of crops from small fruit, to cut flowers, to bulbous crops such
as onion and garlic and can even be found infecting seeds (Elad et al.
2016). Reports suggest that diseases caused by Botrytis spp. are
responsible for $10 to $100 billion USD in annual losses worldwide
(Boddy 2015) and have an estimated average cost of control of €40/
hectare (approximately $18 USD/acre). The cost of management
varies depending on the importance of Botrytis diseases for any given
crop and the value of the crop, up to €130/hectare (approximately
$57 USD/acre) (Steiger 2007).
Botrytis has historically been characterized by several host-
specific and one generalist species. The generalist B. cinerea has
been reported on >1,400 plant species spanning nearly 600 genera;
however, the actual number of hosts is likely to be much greater and
is expected to grow as additional reports are generated (Elad et al.
2007). The remainder of the genus has traditionally been composed
of species that are considered to have narrow host ranges and that
are often highly virulent on, or attack a specific plant part of, their
preferred host (e.g., B. tulipae on genus Tulipa or B. aclada on genus
Allium). Although some plant hosts have a corresponding host-specific
Botrytis species, the same hosts are also commonly susceptible to
infection by B. cinerea. In some cases, coinfection on the same host or
plant tissue by multiple Botrytis species can occur (Garfinkel et al. 2019;
Giraud et al. 1997).
The symptoms caused by different species of Botrytis are often
difficult to distinguish by sight alone. Symptoms caused by Botrytis
pathogens range from floral decay to leaf spots to bulb rots; however,
the latter is often restricted to host-specific species. The issue of host
specificity will be discussed in more detail later in this review.
Given that the symptoms caused by various species of Botrytis
can resemble one another, visual diagnostics is not usually sufficient to
determine the cause of disease in most pathosystems. Once isolated into
culture, Botrytis species can sometimes be easily distinguished by
morphological characteristics; however, this too can be complicated, and
molecular methods are frequently the most reliable for identifying species.
Identification to the species level is only sometimes important in
determining subsequent management strategies, as the biology and
epidemiology of several Botrytis species are similar. Nonetheless,
species identification is important for some species. For example,
B. narcissicola, a host-specific pathogen of genus Narcissus, has a
unique epidemiology insofar as its only primary inoculum source is
the sexual ascospores, which are only able to infect flowers.
Another example is with B. pseudocinerea, which is naturally
resistant to the fungicide fenhexamid (Fournier et al. 2005; Walker
et al. 2011). Furthermore, the species may indicate and help identify
likely sources of inoculum (Holz et al. 2007). As the number of
Botrytis species grows, additional research will be warranted to help
understand their management in agricultural systems.
THE RISE AND FALL OF BOTRYTIS SPECIES
Figure 1 shows a history of the progression of the number of
species ascribed to Botrytis since its erection by Pier Antonio
Micheli in 1729 as introduced in his book Nova Plantarum Genera,
438 PHYTOPATHOLOGY ®
one of the original and fundamental pieces of literature in modern
mycological studies. Upon validation of the genus by Persoon in
1801, Botrytis was considered to contain just five species
(Persoon 1801, as reported by Hennebert 1973). The genus was
then revised in 1886 by Saccardo to contain 128 species
(Saccardo 1886, as reported by Hennebert 1973) and then
eventually came to contain up to 380 species (Hennebert 1973),
most of which are published in separate, difficult to access
articles (Hyde et al. 2014) written in various languages. These
numbers represented a gross overestimate of the number of
species and were a result of generous morphological boundaries
to define the genus, the lack of consensus of the true lectotype
specimen, and subsequent concurrent mycological research being
conducted on varying type-material (Groves and Loveland 1953;
Jarvis 1980).
The lack of reliable connection between the two distinct
morphological states observed in several species of Botrytis further
complicated early Botrytis taxonomy. Some species of Botrytis have
two distinct morphological states: the asexual morph (also known as
the anamorph, imperfect, or conidial stage), and the sexual morph
(also known as the teleomorph, perfect, or apothecial stage). These
two states vary in their morphology. As such, historically the asexual
morph was given the Botrytis name and the sexual morph the name
Botryotinia (although less commonly referenced, in some taxonomic
descriptions of the genus, up to four states have been defined,
including a “sclerotial” state named Sclerotinia and a “micro-
conidial” state named Myrioconium) (Jarvis 1980).
Botrytis species are also morphologically similar to other non-
Botrytis fungi in the family Sclerotiniaceae. The sexual stage of
Botrytis species closely resembles that of Sclerotinia species and
the asexual and sexual stages resemble those seen in the species
of plant pathogenic genera Amphobotrys and Streptobotrys. In
addition to the morphological similarities among these genera, the
disease symptoms caused by each one of these groups are also quite
similar.
The combination of liberal interpretations of genus boundaries,
the complications of pleomorphism and confusing taxonomy, and
the resemblance of Botrytis to other genera of fungi in Sclerotinia-
ceae led to many species in this family being wrongly ascribed to
Botrytis (Groves and Loveland 1953; Hennebert 1973; Jarvis 1977).
Indeed, genera Amphobotrys and Streptobotrys were included as
Botrytis species in Saccardo’s 1886 treatment of the genus. Finally,
among a series of articles arguing for the removal of species from
Botrytis (Buchwald 1949; Hughes 1958) and culminating in
Hennebert’s reevaluation of the genus in 1973, 22 species
eventually remained and provide for the foundation of modern
Botrytis taxonomy (Hennebert 1973). These studies, like many at
the time (Crous et al. 2015), were performed exclusively on
morphology, primarily with the help of light microscopy.
For the next few decades following Hennebert’s revisions,
Botrytis taxonomy entered a period of relative calm. With the
exception of the descriptions of B. fritillarii-pallidoflori (first
described as Botryotinia fritillarii-pallidoflori) and B. acladiopsis,
both of which are not widely recognized species reported from
China in 1987 and 1996, respectively (Johnston et al. 2014b; Wang
et al. 1996), no new species of Botrytis were described for the
remainder of the twentieth century and into the first decade of the
twenty-first century.
(PHYLO)GENETICS AND THE ASCENT TO POWER
In the late 1990s and early 2000s, genetic methods of understanding
fungi began to reveal critical insights into species diversity not
previously captured by classical mycological studies. In their now
widely cited article, Taylor et al. (2000) introduced the concept of
genealogical concordance phylogenetic species recognition (GCPSR)
(this article will also refer to the concept more simply as phylogenetic
species recognition [PSR]). The GCPSR concept rests on the idea
that species can be delineated by considering multiple gene
genealogies and observed sequence variations among them
(Taylor et al. 2000). In phylogenetics, models of evolutionary
history are used to consider nucleotide substitutions and their
prevalence among certain individuals to estimate divergence time
and relatedness. In their article, the authors describe how the
GCPSR is helpful for delineating fungal species and give
examples of instances where fungal species boundaries were
inaccurately laid owing to failures of classical mycological
taxonomy based on morphology (referred to as morphological
species recognition [MSR]) and the ability of fungi to interbreed
(referred to as biological species recognition [BSR]) (Taylor et al.
2000).
Taylor et al. (2000) cite a study from Giraud et al. (1997) that
represents the first use of genetic tools for species delineation in
Botrytis. Although this particular study did not use phylogenetics
but restriction fragment length polymorphism (RFLP) markers of
the intergenic spacer (IGS) rDNA region, the work of Giraud et al.
(1997) is significant in being the beginning of species recognition
based on genetic markers in Botrytis. The article by Giraud et al.
(1997), and later work describing a B. cinerea complex using
additional genetic data (Fournier et al. 2005), provided the
foundation for a novel species that was not formally described
until 2011 along with genus-wide phylogenetic comparisons
(Walker et al. 2011) (this topic will be discussed later in more
detail).
The earliest examples of using phylogenetics in Botrytis are from
Hoist-Jensen et al. (1998) who sequenced the internal transcribed
spacer (ITS) region of rDNA to look at the relatedness among
members of Sclerotiniaceae. Although the ITS region was unable to
adequately resolve Botrytis at the species level because of the lack
of informative loci, this study was able to confirm the monophyletic
nature of Botrytis and corroborate the genetic relationship between
the Botryotinia sexual stage and Botrytis asexual stage (Hoist-
Jensen et al. 1998), the latter of which was the subject of ongoing
debate through much of the twentieth century (Groves and
Loveland 1953; Jarvis 1977). Other early efforts to examine
Botrytis using phylogenetics also were met with some success.
For example, the ITS region was used in tandem with DNA

FIGURE 1
The evolution of Botrytis taxonomy. A, The number of species ascribed to Botrytis over time, including the current revolution of the discovery of new
Botrytis species aided by phylogenetics. B, Important dates in the use of genetic species identification in fungi, in general, and Botrytis specifically.
RFLP 5 restriction fragment length polymorphism and NEP 5 necrosis and ethylene-inducing protein. The asterisk indicates that this is an ap-
proximate and not exact species count.

Vol. 111, No. 3, 2021 439

 TABLE 1
List of current, widely recognized Botrytis speciesa

Mating
Botrytis sp. (anamorph)b Botryotinia sp. (teleomorph)c Apotheciad system Major host Reference

B. aclada Fresen.* Farr et al. (1989),

Hennebert (1973); Jarvis
(1980); Yohalem et al.
– – – Allium (2003)
B. allii Munn – – – Allium Farr et al. (1989); Jarvis
(1980); Yohalem et al.
(2003)
B. byssoidea Walker* Farr et al. (1989); Jarvis
–e – – Trifolium (1980); Noble (1948)
B. californica – – – Vitis, Noble (1948)
Vaccinium
B. calthae Hennebert* Botryotinia calthae Yes – Caltha Farr et al. (1989);
Hennebert & Elliott Hennebert (1973);
Hennebert and Groves
(1963); Jarvis (1980); Kohn
(1979); Plesken et al.
(2015)
B. caroliniana – – – Rubus, Fernández-Ortuño et al.
Fragariaf (2012); Li et al. (2012)
B. cinerea Pers:Fr* Botryotinia fuckeliana (de Yes Heterothallicg Polyphagoush Farr et al. (1989);
Bary) Whetzel Hennebert (1973); Jarvis
(1980); Kohn (1979)
B. convoluta Whetzel & Botryotinia convoluta Yes – Iris Farr et al. (1989);
Drayton* (Drayton) Whetzel Hennebert (1973); Jarvis
(1980); Kohn (1979)
B. croci Cooke & Massee* Hennebert (1973); Jarvis
– – – Crocus (1980); Moore (1959)
B. deweyae – – Heterothallici Hemerocallis Grant-Downton et al.
(2014)
B. elliptica (Berk.) Cooke* –j Yes Heterothallic Lilium Farr et al. (1989),
Hennebert (1973); Jarvis
(1980); Terhem et al.
(2015), van den Ende and
Pennock-Vos (1997)
B. eucalypti k – – – Eucalyptus Liu et al. (2016)
(Continued on next page)
a
This table is modified from Beever and Weeds (2004) and Walker (2016). Dashes indicate that there is no teleomorph name, that apothecia have
not been observed, or that the mating system is unknown.
b
This table reports species that have been corroborated by molecular phylogenetics and/or been validated by morphological studies. Additional
species may include B. acladiopsis, B. anthophila, B. arachidis, B. convallariae, B. fritillarii-pallidoflori, and the Botrytis state of Botryotinia
spermophila (Beever and Weeds 2004; Jarvis 1980; Johnston et al. 2014b; Walker 2016; Wang et al. 1996). Species that contain an asterisk
represent the 22 Botrytis species that remained after Hennebert’s (1973) taxonomic revision of the genus. Authorities are not given to species
described since 2010.
c
Botryotinia teleomorph names have been given for reference; however, the name Botrytis has been given preference to the genus over
Botryotinia (Johnston et al. 2014b) and should therefore be used in any studies. Following this decision in 2013, new species described since that
time have not been given a Botryotinia name.
d
Species in which apothecia have been observed either in nature or produced in laboratory conditions. Some species are believed to be incapable
of apothecia production/sexual reproduction (Staats et al. 2007b).
e
There is some debate regarding the teleomorph of B. byssoidea, as some consider it to be Botryotinia allii. See Walker (2016) for further details.
f
Species has also been shown to infect additional unrelated host species in laboratory trials.
g
Although B. cinerea has been observed to have a predominantly heterothallic mating system, some isolates have been shown to be self-fertile
and are sexually compatible with both mating types (Faretra et al. 1988).
h
Species has also been putatively isolated as an endophyte (Shaw et al. 2016; Shipunov et al. 2008).
i
Mating system is inferred by presence of only one mating type idiomorph (allele) per thallus; however, sexual crosses have not been successfully
performed.
j
No name has been given to the B. elliptica teleomorph, although apothecia have been observed in the field (van den Ende and Pennock-Vos 1997)
and have been cultured in the laboratory (Terhem et al. 2015).
k
Although B. eucalypti is among the recent species to be described, B. eucalypti does not differ significantly by phylogenetic analysis from B.
cinerea (Liu et al. 2016).
l
B. euroamericana is likely a polyphagous species.
m
The status of B. pelargonii is currently in question owing to phylogenetic evidence presented that shows this species may be conspecific with B.
cinerea (Staats et al. 2005). There is no known living type specimen of this species to determine its taxonomic validity.
n
Røed (1949) reported that apothecia were formed from a single “pure” culture of B. pelargonii.
o
Crosses indicated that one of 38 single-ascospore isolates behaved as homothallic; however, the rest behaved in a heterothallic fashion.

440 PHYTOPATHOLOGY ®
 TABLE 1
(Continued from previous page)
Mating
Botrytis sp. (anamorph)b Botryotinia sp. (teleomorph)c Apotheciad system Major host Reference

B. euroamericana Garfinkel et al. (2017);

Lorenzini and Zapparoli
Vitis, Paeonia, (2014); Moparthi et al.
– – – Cicerf,l (2020)
B. fabae Sardiña* Botryotinia fabae Lu & Wu Yes – Fabaceae Hennebert (1973); Jarvis
(1980); Wu and Lu
(1991)
B. fabiopsis – – – Vicia Zhang et al. (2010a)
B. ficariarum Hennebert* Botryotinia ficariarum Yes – Ficaria Hennebert (1973);
Hennebert Hennebert and Groves
(1963); Jarvis (1980); Kohn
(1979)
B. fragariae – – – Fragariaf Dowling et al. (2017);
Rupp et al. (2017)
B. galanthina (Berk. & – – – Galanthus Farr et al. (1989);
Broome) Sacc.* Hennebert (1973); Jarvis
(1980)
B. gladiolorum Timmerm.* Botryotinia draytonii Yes – Gladiolus Farr et al. (1989);
(Buddin & Wakef.) Seaver Hennebert (1973); Jarvis
(1980); Kohn (1979)
B. globosa Raabe* Botryotinia globosa Buchw. Yes Homothallic Allium Buchwald (1953);
Hennebert (1973); Jarvis
(1980); Kohn (1979)
B. hyacinthi Westerd. & – – – Hyacinthus Farr et al. (1989);
Beyma* Hennebert (1973); Jarvis
(1980)
B. mali Ruehle – – – Malus, Cosseboom et al. (2018);
Fragariah Dowling and Schnabel
(2017); O’Gorman et al.
(2008)
B. medusae – – – Vitis Harper et al. (2019)
B. narcissicola Kleb. Ex Botryotinia narcissicola Yes – Narcissus Farr et al. (1989);
Westerd. & Beyma* (Greg) Buchw. Hennebert (1973); Jarvis
(1980); Kohn (1979)
B. paeoniae Oudem.* – – Heterothallicj Paeonia Coats et al. (2018); Farr
et al. (1989); Hennebert
(1973); Jarvis (1980); Kohn
(1979)
B. pelargonii Røed*m Botryotinia pelargonii Røed Yes Homothallic?n Pelargonium Hennebert (1973);
Hennebert and Groves
(1963); Jarvis (1980); Kohn
(1979); Røed (1949)
B. polyblastis Dowson* Botryotinia polyblastis Yes Heterothallico Narcissus Chastagner (1986); Farr
(Greg.) Buchw. et al. (1989); Hennebert
(1973); Jarvis (1980); Kohn
(1979)
B. polyphyllae – – – Parisf Zhong et al. (2019)
B. porri Buchw.* Botryotinia porri (Beyma) Yes Homothallic Allium Elliott (1964); Hennebert
Whetzel (1973); Jarvis (1980); Kohn
(1979)
B. prunorum – – – Polyphagoush Elfar et al. (2017); Esterio
et al. (2020); Ferrada et al.
(2016, 2020)
B. pseudocinerea Botryotinia Yes Heterothallic Polyphagoush Walker et al. (2011)
pseudofuckeliana
B. pyriformis – – – Saprotroph Zhang et al. (2016)
B. ranunculi Hennebert* Botryotinia ricini (Godfrey) Yes Heterothallic Ranunculus Farr et al. (1989);
Whetzel Hennebert (1973);
Hennebert and Groves
(Continued on next page)

Vol. 111, No. 3, 2021 441

 TABLE 1
(Continued from previous page)
Mating
Botrytis sp. (anamorph)b Botryotinia sp. (teleomorph)c Apotheciad system Major host Reference

(1963); Jarvis (1980); Kohn

B. sinoallii
B. sinoviticola
B. sphaerosperma Buchw.*
B. squamosa Walker*
B. tulipae Lind*
– –
– –
Botryotinia sphaerosperma Yes
(Greg.) Buchw.
Botryotinia squamosa Yes
Vienn.-Bourg.
– –
– Allium
– Vitis
– Allium
Heterothallic Allium
– Tulipa, Allium,
Lilium
(1979)
Zhang et al. (2010b)
Zhou et al. (2014)
Farr et al. (1989); Jarvis
(1980); Kohn (1979)
Bergquist and Lorbeer
(1972); Farr et al. (1989);
Hennebert (1973); Jarvis
(1980); Kohn (1979)
Farr et al. (1989);
Hennebert (1973); Jarvis
(1980); Kohn (1979);
Staats et al. (2007b)

fingerprinting to delineate among five different onion-infecting
Botrytis species (B. cinerea, B. squamosa, B. byssoidea, and what
was then presumed to be two distinct groups of B. aclada) (Nielsen
et al. 2001), and eventually led to the recognition and restoration of
the hybrid species B. allii (Nielsen and Yohalem 2001; Nielsen et al.
2001; Yohalem et al. 2003). However, while for other fungal species
the ITS region is useful for species delineation, its value was proven
to be limited for species recognition in Botrytis as it fails to
adequately resolve the placement of species (Hyde et al. 2014;
Walker 2016).
A turning point in Botrytis taxonomy came with the discovery
and validation of the phylogenetically informative housekeeping
genes, glyceraldehyde-3-phosate dehydrogenase (G3PDH), heat-
shock protein 60 (HSP60), and DNA-dependent RNA polymerase
subunit II (RPB2) (Staats et al. 2005). Staats et al. (2005) built
molecular phylogenies using these protein-encoding genes and
largely corroborated the taxonomic placement of Hennebert’s
(1973) 22 species, with the exception of B. pelargonii, which may
be conspecific with B. cinerea, and confirmed the placement of the
hybrid species B. allii (Staats et al. 2005). This study placed all
Botrytis species into two main clades, clades 1 and 2. In their
analysis, clade 1 contained the polyphagous species B. cinerea as
well as three other putatively host-specific pathogens of eudicot
plants (Staats et al. 2005). Clade 2 contained host-specific species
from plants of both eudicot and monocot plants, yet there was no
clustering among pathogens that infect these groups (Staats et al.
2005). Furthermore, there was no clustering of Botrytis species that
were pathogenic on host plants from the same taxonomic group; this
was especially evident for plants in Ranunculaceae, of which one
Botrytis species (B. calthae) was grouped into clade 1, whereas the
other two species pathogenic on Ranunculaceae hosts (B. ficariarum
and B. ranunculi) grouped into clade 2 (Staats et al. 2005). These
phylogenetic analyses also indicated that the ability for sexual
reproduction has likely been lost many times independently within
the genus (Staats et al. 2005).
In 2007, Staats et al. (2007a) followed up with the publication
and validation of the necrosis and ethylene-inducing proteins 1
and 2 (NEP1 and NEP2) as phylogenetically informative markers.
Caution has been raised at using these genes in phylogenetic
analyses because they were shown to be undergoing positive
selection (Staats et al. 2007a), yet gene tree topologies built with
NEP1 and NEP2 were shown to be of higher resolution and largely
congruent of those built with the housekeeping genes (Hyde et al.
2014; Staats et al. 2007a). Additional studies suggested that these
genes are not involved in virulence and therefore are potentially
considered neutral for phylogenetic tree construction (Hyde et al.
2014).
Following the validation of these genes for species recognition,
phylogenetic analysis of the G3PDH and b-tubulin genes also helped
lead to the revival of a long-lost species, B. mali (O’Gorman et al.
2008), and HSP60 was used to tentatively place six morphologically
uncharacterized endophytic isolates of Botrytis as new species
(Shipunov et al. 2008). Andrew et al. (2012) used a combination of
the G3PDH, HSP60, and calmodulin genes to further understand
taxonomic relationships within the family Sclerotiniaceae, and Khan
et al. (2013) utilized a combination of ITS, IGS, and G3PDH in the
identification of Botrytis species infecting onion. Yet during this time,
no novel species were described.
Then, in 2010, the formal description of two new species of
Botrytis from China, B. fabiopsis (Zhang et al. 2010a) and
B. sinoallii (Zhang et al. 2010b) from broad bean (Vicia faba) and
Allium crops, respectively, kicked off a new decade of taxonomic
transformation. These studies utilized the G3PDH, HSP60, RPB2
(B. sinoallii), and NEP1 and NEP2 (B. fabiopsis) genes and showed
compelling phylogenetic evidence to delineate these species from
their most closely related neighbor species. Since 2010, 12
additional species have been officially described (Ferrada et al.
2016; Garfinkel et al. 2017; Grant-Downton et al. 2014; Harper
et al. 2019; Li et al. 2012; Liu et al. 2016; Rupp et al. 2017; Saito
et al. 2016; Walker et al. 2011; Zhang et al. 2016; Zhong et al. 2019;
Zhou et al. 2014), all of which contain phylogenetic analyses of
some or all of the phylogenetically informative genes from Staats
et al. (2005, 2007a). A list of the currently recognized species is
provided in Table 1 and their phylogenetic relationships are shown
in Figure 2. Clade 1 of Botrytis now contains 10 species (up from
four published in Staats et al. 2005), clade 2 now contains 26
species (up from 18 reported by Staats et al. 2005), and a new
species, B. pyriformis, appears to make up a novel third clade in
Botrytis (the hybrid B. allii cannot be placed definitively into a
clade) (Fig. 2). Also during this time, phylogenetic evidence for an
additional 11 novel species has been reported (Garfinkel et al.
2019; Shaw et al. 2016); however, none have thus far been formally
described. Taken together, these data represent a near doubling of
the number of putative species within Botrytis in only a decade’s
time.
When Staats et al. (2007a) published their second article on the
molecular phylogenetics of Botrytis in 2007, PSR in the genus was
still considered to be “in its infancy” (Beever and Weeds 2004, pg.
32). However, by 2016, this approach was considered as “un-
doubtedly the most widely used concept in Botrytis taxonomy”

442 PHYTOPATHOLOGY ®
(Walker 2016, pg. 97). Although PSR is the trend of numerous plant short timeframe. In order to contextualize this rise to dominance, this
pathogenic genera (and perhaps microorganisms in general), it is review will consider the ways in which species have historically been
potentially valuable to consider why and how Botrytis taxonomy described and delineated in Botrytis, challenges of these methods,
specifically came to this point of phylogenetic dominance within this advancements in the knowledge of Botrytis biology that have

FIGURE 2
Phylogenetic tree describing the relationship between Botrytis species. Clades are designated as per Staats et al. (2005) with the addition of the new
species B. pyriformis that represents a third clade. Species preceded by a black diamond have been described since 2010. The tree was constructed
using a concatenated dataset of the glyceraldehyde-3-phosate dehydrogenase (G3PDH), heat-shock protein 60 (HSP60), and DNA-dependent RNA
polymerase subunit II (RPB2) genes using the maximum likelihood method with Sclerotinia sclerotiorum as an outgroup. Numbers on branches
represent bootstrap support (n 5 1,000). Species B. mali and B. allii are not included because of the absence of sufficient sequence data and hybrid
status, respectively. B. mali would group closely related to B. paeoniae. B. allii is a hybrid species between B. byssoidea and B. aclada.

Vol. 111, No. 3, 2021 443

 TABLE 2
Data related to sexual and asexual morphology and mating systems in new species of Botrytis described since 2010

Isolates Closely related Colony Macroconidia Conidiophore Sclerotia

Botrytis sp. (n) speciesa morphology measurements (n)b measurements (n) measurements (n)

B. californica 6 –d + 100 50 50
B. caroliniana 6 – + 50 10 +
B. deweyae 6 – + + + +
B. eucalypti 4 – + 25–50 25–50 25–50
B. euroamericana 3 + + 50 10 +
B. fabiopsis 3 + + 50 20 50
B. fragariae 4 – + 100 + +
B. medusae 1 – + 100 50 30
B. polyphyllae 3 – + + + 30
B. prunorum 7f – + 40 10 +
B. pseudocinerea 13 + + 100 + –
B. pyriformis 3 –d + 50 20 30
B. sinoallii 3 –d + 50 + 50
B. sinoviticola 3 g
– + 50 20 30
(Continued on next page)
a
This column delineates whether or not the authors obtained a culture of the most closely related Botrytis species to the new species in question
and used it in side-by-side assessments. This does not indicate whether comparisons were made to published data. Dashes indicate that the
stated criterion was not used in the new species description, and plus signs indicate that these data were included in the new species
description.
b
The macroconidia, conidiophore, and sclerotia columns indicate the number of replicates used in measurements, if reported. Plus signs indicate
that these measurements were taken, but the authors did not report how many replicates were assessed.
c
Mating system was either inferred by performing crosses or sequencing the mating type (MAT) loci.
d
The most closely related Botrytis species was not assessed; however, these studies directly compared the new species with either sympatric
Botrytis species or B. cinerea. For B. pyriformis, which makes up its own phylogenetic clade, B. cinerea was assessed.
e
Although unsuccessful, the authors of the species B. deweyae attempted crosses to induce apothecia production.
f
Seven species were collected, but it is unclear for how many species morphological data were assessed.
g
Trials for B. sinoviticola were conducted using a subset of three isolates, but 12 were collected total.

occurred in the last few decades, and how phylogenetics is helping
resolve both old and new issues in Botrytis taxonomy.
CRYPTIC SPECIES, INTRASPECIES VARIATION, AND
THE PLASTICITY PROBLEM
Classical mycology is an art and science deeply rooted in detailed
descriptions, careful observations, and ornate drawings of the
morphology of fungal structures, and Botrytis taxonomy is no
exception. Traditionally, Botrytis species have been largely recog-
nized by the use of morphological features and the implementation of
the BSR concept; the characteristic “botryose,” or grape cluster-like
structure of the conidiophores, has served as the unifying character-
istic within the genus. In a field of study referred to by Jarvis (1977,
1980) as “numerical taxonomy,” the differences in length and
width of conidiophores, the size and shape of macroconidia, and
the size, shape, and production of sclerotia in culture (among other
features) have historically been important quantitative ways of
distinguishing among species. These traits remain important
elements of modern Botrytis species descriptions and usually
accompany varying levels of descriptions of colony morphology,
sclerotial morphology, macroconidia production and germination
rates, microconidia production and morphology, radial growth
rates, and temperature sensitivity (Ferrada et al. 2016; Garfinkel
et al. 2017; Grant-Downton et al. 2014; Harper et al. 2019; Li et al.
2012; Liu et al. 2016; Rupp et al. 2017; Saito et al. 2016; Walker
et al. 2011; Zhang et al. 2010a, b, 2016; Zhong et al. 2019; Zhou
et al. 2014) (Tables 2, 3, and 4). Nonetheless, in addition to
the difficulties noted previously regarding the distinct states of
Botrytis species, these species display unique morphological
characteristics that complicate MSR.
High levels of morphological variation among individuals within
a species, known as intraspecies variation, is common in Botrytis
and makes characterizing a standard phenotype a challenge. This
peculiarity has been well documented in the literature of Botrytis
cinerea from early studies of the fungus. Studies as early as 1929
identified morphological variations in terms of the number, size,
and arrangement of conidiophores and sclerotia among several
B. cinerea isolates (Paul 1929). Some cultures of B. cinerea failed
entirely to produce conidia and/or sclerotia and remained strictly
vegetative, producing only mycelium (Paul 1929). Other authors
have noted such major differences in conidial sizes among
B. cinerea isolates from a single host that these isolates were
divided into different races of the pathogen (as reported in Jarvis
1980). Similarly, some B. cinerea isolates were shown to produce
characteristic red pigments or varying levels of citric acids, leading
some early mycologists to designate these isolates as distinct forms
(as reported in Jarvis 1980). A more comprehensive review of the
literature on the variation in morphotypes of Botrytis species is given
by Jarvis (1980); much of the literature cited in Jarvis’s review is not
published in English, so the review may be more useful than the
primary literature for some readers. Although these early studies
can be somewhat suspect given the taxonomic changes that have
occurred since their publication (i.e., it is not possible to
corroborate that all of the isolates used in these studies were
B. cinerea sensu stricto), modern studies have confirmed the
intraspecies variation seen in B. cinerea (e.g., Fernández et al.
2014). Some newly reported species appear to have similar

444 PHYTOPATHOLOGY ®
 TABLE 2
(Continued from previous page)

Sclerotia cell Denticle Ampullae Infection Mating

Botrytis sp. description measurements measurements cushions Microconidia Apothecia systemc

B. californica – – – – – – –
B. caroliniana – – – – – – –
B. deweyae – – – – – –e
+
B. eucalypti – – – – – – –
B. euroamericana + + + – + – –
B. fabiopsis – – – – – – –
B. fragariae – – – – + – –
B. medusae – – – – – – –
B. polyphyllae – – – – – – –
B. prunorum – – – – – – –
B. pseudocinerea – – – – + + +
B. pyriformis – – – + – – –
B. sinoallii – – – – – – –
B. sinoviticola – – – – – – –

tendencies for intraspecies morphological variations. Figure 3
clearly shows variation in colony morphology observed among
three isolates of the newly characterized species B. euroamericana
(Garfinkel et al. 2017). In Figure 3, sclerotia are shown for only
one isolate, as the other two isolates of this species did not produce
sclerotia during any trials (Garfinkel et al. 2017).
In addition to the variation seen within individuals of the same
species, high levels of morphological plasticity within individual
isolates are also common in many Botrytis species. Colony, spore,
and sclerotium morphologies have been shown to differ signifi-
cantly with variations in substrate, temperature, pH, C:N ratios,
relative humidity, and light regimes (reviewed in Jarvis 1980).
Figure 4 shows the differences in colony morphology of B. cinerea
and new species B. prunorum grown on various culture media
(Ferrada et al. 2016). Furthermore, significant differences in
morphology among cultures initiated from conidia from the same
thallus, or ascospores from the same ascus, have also been observed;
variations in pathogenicity among the resultant cultures were often
observed as well (Lorenz 1983). Studies also found that these
phenotypes were not always stable following repeated subculture
(Lorenz 1983) or following passage through a host (as reported in
Jarvis 1980). The differences in intra-isolate morphology led some
authors to question the validity of morphological descriptions
of cultured isolates entirely and others to conclude that unless
drastic, stable morphological differences existed among isolates,
new species descriptions were not warranted (various citations, see
Jarvis 1980).
Another morphological oddity of Botrytis involves the pro-
duction, or lack thereof, of macroconidia. Conidial measurements
have historically been an important factor in distinguishing among
species; however, like some isolates of B. cinerea, several new
species appear reticent to produce conidia on culture media and/or
only sporulate under very specific cultural conditions. Such is the
case for the new species B. deweyae, which only reliably produces
macroconidia following 7 days of exposure to near-ultraviolet light
in the absence of other light sources (the authors allude to several
other attempts at inducing sporulation) (Grant-Downton et al.
2014). Despite sporulation occurring under these conditions for
most isolates of B. deweyae, still one isolate of B. deweyae failed to
sporulate during trials (Grant-Downton et al. 2014). The new
species B. caroliniana does not produce conidia on potato dextrose
agar (PDA) medium, a standard growth medium for Botrytis;
conidia and conidiophore measurements were therefore reported
from artificially inoculated blackberries (Li et al. 2012). This
feature of B. caroliniana made it impossible to directly compare its
conidia and conidiophores to the most closely related species,
B. galanthina, as the latter is not pathogenic on blackberry (Li et al.
2012). Similar comparisons were not possible for B. fabiopsis and
the most closely related species B. galanthina, as the latter did not
sporulate in the same cultural conditions as the former (Zhang et al.
2010a). Sporulation is also rare or absent on PDA for the new
species B. polyphyllae (Zhong et al. 2019), B. euroamericana
(Garfinkel et al. 2017), B. sinoallii (Zhang et al. 2010b), and
B. prunorum (reports from acidified PDA) (Ferrada et al. 2016).
Several putative species collected and reported from peony in
2019 have not been observed to sporulate despite several attempts
to induce sporulation (Garfinkel et al. 2019), a fact that has
complicated their official descriptions as new species. Cohrs et al.
(2016) reported that so-called “blind” strains, or those that fail to
produce conidia, are prevalent in the field and that numerous
photoreceptive pathways are likely responsible for this phenom-
enon. Even if macroconidia are readily formed, sizes within
species often span a wide range, and conidia from different species
frequently overlap in size, making definitive separation based on
this trait quite difficult.
Lastly, the term “cryptic species” has now become common
vernacular in the world of Botrytis taxonomy since the discovery of
the new species B. pseudocinerea in 2011 (Fournier et al. 2005;
Walker et al. 2011). This species, morphologically indistinguish-
able from B. cinerea on the basis of spore size, germination rate, or
mycelial growth, was first discovered in France on grape (Vitis
vinifera) and blackberry (Rubus fruticosus) using RFLP data and
through the detection of the presence or absence of transposable
elements (Fournier et al. 2005; Giraud et al. 1997). B. pseudoci-
nerea was eventually formally recognized as distinct from B.
cinerea after the implementation of a combination of GCPSR, us-
ing G3PDH and HSP60, and BSR, as the authors were unable to
successfully perform sexual crosses between the two species
(Fournier et al. 2005; Giraud et al. 1997; Walker et al. 2011).
B. pseudocinerea has subsequently been found in at least six

Vol. 111, No. 3, 2021 445

additional countries (Farr and Rossman 2020), from China (Li et al. corymbosum) (Saito et al. 2016), strawberry (Fragaria × ananassa)
2015; Xue et al. 2019) to New Zealand (Johnston et al. 2014a), to the (Rupp et al. 2017), marsh marigold (Caltha palustris) (Plesken et al.
United States (Garfinkel 2020; Saito et al. 2016) and on various, 2015), and hemp (Cannabis sativa) (Garfinkel 2020) and has even
taxonomically unrelated species including blueberry (Vaccinium been isolated from symptomless dandelion (Taraxacum officinale)

TABLE 3
Additional biological and pathogenicity data included in Botrytis species descriptions since 2010a

Additional
Conidia Conidia Sclerotia Pathogenicity hosts
production germination production Temperature Fungicide on original tested
Botrytis sp. rate rate/temp rate RGRb trialsc sensitivity host (n)d

B. californica – + + + + + + 0
B. caroliniana – – – + – – + 1
B. deweyae – – + – – – + 3
B. eucalypti – – + + + – + 0
B. euroamericana – – + + + – + 2e
B. fabiopsis – – + + + – + 0
B. fragariae – + – + – + + 4
B. medusae – – + + + + + 0
B. polyphyllae – – – + + – + 5
B. prunorum + – – + + – + 2
B. pseudocinerea + + + + + + + 2
B. pyriformis – + + + + – + 29
B. sinoallii – – + + – – + 0
B. sinoviticola – + + + + + + 0

a Dashes indicate the criterion was not used in the new species description, and plus signs indicate that the data were included in the new species
description.
b RGR 5 radial growth rate.
c Temperature trials indicate that RGR was assessed at more than one temperature.
d The number of additional hosts tested indicates on how many taxonomically unrelated hosts pathogenicity trials were executed other than the
host from which the species was isolated.
e Additional host species were tested in a previous article reporting this Botrytis species (Lorenzini and Zapparoli 2014).

TABLE 4
Molecular data included in new Botrytis species descriptions since 2010a

Botrytis sp. ITS G3PDH/HSP60/RPB2 NEP1/NEP2 Additional molecular datab

B. californica +c + – +
B. caroliniana +c + + –
B. deweyae +c
+ + –
B. eucalypti + + + –
B. euroamericana – + + –
B. fabiopsis +c + + –
B. fragariae – + + +
B. medusae – + + +
B. polyphyllae + + – –
B. prunorum + + + +
B. pseudocinerea – + – +
B. pyriformis + + – –
B. sinoallii + + – –
B. sinoviticola + + – +

a ITS 5 internal transcribed spacer, G3PDH 5 glyceraldehyde-3-phosate dehydrogenase, HSP60 5 heat-shock protein 60, RPB2 5 DNA-
dependent RNA polymerase subunit II, and NEP 5 necrosis and ethylene-inducing protein. Dashes indicate the criterion was not used in the new
species description, and plus signs indicate that the data were included in the new species description.
b Additional molecular data includes restriction fragment length polymorphism, transposon, and/or microsatellite data.
c Data were reported, but phylogenetic analyses were not performed.

446 PHYTOPATHOLOGY ®
in what is referred to as a “cryptic infection” (Shaw et al. 2016). The
apparent widespread presence of this species and the fact that it
went so long undetected using the morphological methods is
indicative of a shortcoming of MSR in Botrytis taxonomic studies.
In what is likely the most comprehensive review of morpholog-
ical studies of Botrytis (up to the date it was published), Jarvis
(1980) emphasizes the need for “a standardized, chemically-
defined culture medium and standardized environmental condi-
tions… for use in all laboratories where critical taxonomic and
morphologic studies are undertaken on Botrytis…” Nonetheless, in
light of the presence of intraspecies morphological variations, the
morphological plasticity of individual isolates, and the inability to

FIGURE 3
An example of intraspecies variation in Botrytis euroamericana. A, B,
and C, Three different isolates of B. euroamericana grown on the same
growth medium under the same temperature and light regime. D, E,
and F, The same three isolates grown on a second medium. G, H, and
I, Sclerotia from a single isolate. Only one isolate formed sclerotia
during trials. Figure originally published in Garfinkel et al. (2017).

FIGURE 4
An example of the morphological plasticity of a single isolate of Botrytis
cinerea and B. prunorum grown on three different culture media:
acidified potato dextrose agar (APDA), King’s medium B (KMB), and
pea agar medium (PAM). Reproduced by permission from
Ferrada et al. (2016).

Vol. 111, No. 3, 2021 447

assess certain species in what could be considered “standard”
cultural conditions, Jarvis’s recommendation would be difficult, if
not impossible, to achieve.
In the context of these challenges, it is no wonder that some of the
earliest described Botrytis isolates display relatively consistent or
unique phenotypes or are pathogenic on a specific host (discussed
later). Indeed, while isolates of B. tulipae and B. paeoniae, for
example, were shown to vary morphologically on different media or
under different environmental conditions (as reported in Jarvis
1980), the individuals of these species display a relatively low
amount of intraspecies morphological variation. Other “older”
species display unique phenotypes that helped support their initial
recognition as new species, such as B. convoluta, which produces
extremely large, wrinkled or “convoluted” sclerotia (Drayton
1937), and B. polyblastis, whose large conidia germinate to produce
eight to nine and as many as 13 germ tubes (Dowson 1928; Gregory
1938). With perhaps the exceptions B. californica and its extraordi-
narily long conidiophores (Saito et al. 2016) and B. pyriformis
with its unique villiform appendages present on the macroconidia
(Zhang et al. 2016), very few of the species being described
today have extraordinary morphological characteristics that
would easily and conclusively separate them from another Botrytis
species using MSR.
SEX IN BOTRYTIS—IT’S COMPLICATED
The biological species concept (BSC) as implemented in fungi
relies on performing mating crosses to determine fertility among
individuals. It is assumed, then, that those individuals who
successfully interbreed are of the same species.
This review has already discussed the two morphological states
of Botrytis fungi, the sexual and asexual stages. The sexual stage is
the result of a successful cross that occurs when microconidia
fertilize a mature sclerotium to form an apothecium, within which
sexual ascospores are borne (Jarvis 1980). Depending on the mating
system, either one or two individuals are required for sexual
reproduction, referred to as homothallism and heterothallism,
respectively. Botrytis displays a bipolar mating system that is
governed by two alleles that lack sequence homology (known as
“idiomorphs”), MAT1-1 and MAT1-2 (Amselem et al. 2011).
Individuals in homothallic species contain both idiomorphs and are
self-fertile, whereas individuals in heterothallic species contain
only one of the idiomorphs and successful crosses require two
individuals (or “thalli”) of the opposite mating type. In Botrytis,
both mating systems have been observed (Table 1).
Although some species of Botrytis are known to produce the
sexual stage, a fact that complicated taxonomy as previously
discussed, apothecia have been observed in only 16 of the 38
currently named species (Table 1). Of the 22 remaining species in
which apothecia have not been observed, it is suspected that
some are incapable of sexual reproduction. Such is alleged for
B. paeoniae and B. tulipae, both of which have small sclerotia
thought not to contain sufficient nutrients for apothecia production
(Staats et al. 2007b). Unusually, using molecular sequencing, both
mating types in B. paeoniae have been identified in populations of
sympatric isolates (Coats et al. 2018). However, despite co-
occurrence of both mating types, the analysis of simple sequence
repeat data suggests that sexual reproduction is not likely occurring
in this species (A. R. Garfinkel, unpublished data). Likewise,
genetic data largely support clonal reproduction in B. tulipae;
apothecia of B. tulipae have also never been observed in the field,
nor have repeated attempts at sexual crosses in vitro been successful
(Staats et al. 2007b). B. aclada, B. hyacinthi, B. croci, and
B. galanthina have also been presumed to be strictly asexually
reproducing (Staats et al. 2005). Apothecia for one of the oldest
species in the genus, B. elliptica described in 1901, were only
448 PHYTOPATHOLOGY ®
observed for the first time in 1995 (van den Ende and Pennock-Vos
1997). However, upon observation of the apothecia, no description
of the structures was written. It was not until 2015 (Terhem et al.
2015), when B. elliptica apothecia were generated under laboratory
conditions, that a formal description was made. Previous attempts to
generate mature B. elliptica apothecia in vitro had been made but
were unsuccessful (Chastagner et al. 1992). Prior to the successful
generation of apothecia in vitro, studies using genetic markers
provided strong evidence for the presence of sexual recombination
in B. elliptica (Huang et al. 2001; Staats et al. 2007b).
Given that few species have been confirmed to sexually
reproduce and there is a need for prerequisite knowledge of mating
type and systems required to successfully perform crossing trials,
the BSC for species recognition has not widely been implemented
and has therefore been of limited value in Botrytis. There are two
exceptions: sexual crosses were successful in delineating between
B. squamosa and B. cinerea (Bergquist and Lorbeer 1972), and in
distinguishing the morphologically identical B. pseudocinerea
from B. cinerea (Walker et al. 2011). In both instances, the two
species were unable to produce apothecia when crossed; apothecia
were successfully generated in crosses within species. Besides
B. pseudocinerea, none of the new species descriptions since 2010
have implemented the BSC, nor have they reported apothecia in
their taxonomic treatments (Ferrada et al. 2016; Garfinkel et al.
2017; Grant-Downton et al. 2014; Harper et al. 2019; Li et al. 2012;
Liu et al. 2016; Rupp et al. 2017; Saito et al. 2016; Walker et al.
2011; Zhang et al. 2010a, b, 2016; Zhong et al. 2019; Zhou et al.
2014). The authors of the new species B. deweyae attempted sexual
crosses of separate mating types identified by molecular sequenc-
ing, but attempts were unsuccessful at generating apothecia (Grant-
Downton et al. 2014).
The repeated failures of attempting sexual crosses indicate that
the BSC is unlikely to be a widely valuable strategy for Botrytis
species recognition. Furthermore, the fact that no sexual stage has
ever been reported in several species of Botrytis, some of which may
be incapable of sexual reproduction entirely, makes implementation
of the BSC for the recognition of some species impossible.
Although sexual crosses have been helpful in understanding mating
systems in species that readily produce apothecia (Walker 2016),
genetic evidence has been the most reliable predictor of the
presence of sexual reproduction and the elucidation of mating
systems of Botrytis species.
Prior to moving on from the discussion of sexual reproduction, it
is worth noting that for at least one species, B. polyblastis, the sexual
stage is an important factor in the disease cycle; in this system,
ascospores represent an important source of initial inoculum
(Chastagner 1983; Dowson 1928; Gregory 1938). In this case,
then, apothecia production is important not just in understanding
sexual reproduction but also in terms of understanding epidemiol-
ogy and performing pathogenicity trials, the latter of which is the
subject of the next section.
MONOPHAGY AND PATHOGENICITY: VESTIGES OF
THE PAST?
Another set of criteria for delineating species not explicitly
discussed by Taylor et al. (2000), but one that has historically been
important in Botrytis, is the issue of host specificity. Of the 22
species retained by Hennebert (1973), all but B. cinerea were
considered to be host-specific pathogens, many of which were
named after their host (e.g., B. tulipae is a pathogen of genus Tulipa
and B. narcissicola is a pathogen of genus Narcissus). Even up to the
most recent review by Walker (2016), most Botrytis species (with
the exception of the addition of B. pseudocinerea, which appears
equally as polyphagous as its eponym, B. cinerea) were considered
to be host specific or with narrow host ranges. Indeed, many species
in the genus have been shown to be quite specialized. As such,
pathogenicity trials to determine host range have historically been
an important part of Botrytis species recognition and delineation.
However, the usefulness of this metric is being called into
question. Many of the recently described species appear to be
polyphagous, as evidenced by their pathogenicity on taxonomically
unrelated hosts (Table 1). B. prunorum, a species originally isolated
from plum (Prunus salicina) in Chile (Ferrada et al. 2016), has
subsequently been officially reported as a naturally occurring
pathogen of kiwi (Actinidia deliciosa) (Elfar et al. 2017), grape
(Esterio et al. 2020), and pear (Pyrus communis) (Ferrada et al.
2020) and provisionally on peony (Garfinkel et al. 2019) and
legume (Fabaceae) seeds (S. Moparthi, personal communication).
B. prunorum is therefore likely to be a third truly polyphagous
species in Botrytis. Other newly described species appear to be
polyphagous as well. The new species B. euroamericana has been
found naturally occurring on grape, peony (Paeonia lactiflora), and
chickpea (Cicer arietinum) (Moparthi et al. 2020) and also was able
to also cause lesions during laboratory tests on hosts from 10
additional plant families (Garfinkel et al. 2017; Lorenzini and
Zapparoli 2014). The species B. caroliniana, originally isolated
from blackberry, was pathogenic on broad bean in laboratory trials
(Li et al. 2012) and was also found naturally occurring on
strawberry (Fernández-Ortuño et al. 2012). This species has also
been reported to cause lesions on apple (Malus), pear (Pyrus),
orange (Citrus), lemon (Citrus), grape, and raspberry (Rubus)
(Walker 2016). Isolates of B. polyphyllae, found on the Chinese
flowering plant Paris polyphylla, were also shown to be able to
cause lesions on the fruits of strawberry, tomato (Solanum
lycopersicum), and cherry (Prunus avium), which are all taxonom-
ically unrelated to the host on which they were originally isolated
(Zhong et al. 2019). Although not officially recognized as species,
in a survey of Botrytis pathogens of peony in the United States, some
of the Botrytis isolates collected appear to be genetically identical
to isolates collected from symptomatic hemp (Garfinkel 2020)
and blackberry (L. Jones, personal communication), and they were
found colonizing legume seeds (S. Moparthi, personal communica-
tion). Although it appears that many new species may be polyph-
agous, additional official reports of naturally occurring infections
would be required to confirm this prediction.
Despite shifting paradigms in the genus, even in the most recent
species descriptions, host-range specificity has been helpful in
distinguishing new Botrytis species, especially from closely related
host-specific species. For example, B. euroamericana, a species
closely related to the onion pathogen B. aclada, was only able to
cause small, primary lesions on onion bulbs as compared with the
virulent host-specific pathogen (Garfinkel et al. 2017). B. fabiopsis
was shown to be pathogenic on broad bean, while leaves inoculated
with the most closely related species, B. galanthina, a host-specific
pathogen of genus Galanthus, remained uninfected (Zhang et al.
2010a). Although these tests were successful in discriminating
species, phylogenetic analyses were used to determine the most
closely related species to the novel isolates in question.
In addition to the emerging questions regarding the prevalence of
host specificity, research has begun to question whether pathoge-
nicity is even a “hard-and-fast” rule within the genus. In a cleverly
titled article, van Kan et al. (2014) posit the question of whether
Botrytis species are indeed “relentless necrotrophic thugs” or
potentially “endophytes gone rogue.” Included in their review is
mounting evidence of a surprising and cryptic lifestyle of
pathogenic Botrytis species as endophytes. The authors specifically
discuss a Botrytis species first described in 2014, B. deweyae,
which appears to live primarily as an endophyte with facultative
pathogenic behavior (Grant-Downton et al. 2014; van Kan et al.
2014). In 2005, attempts to isolate endophytes from the invasive
plant species Centaurea stoebe recovered Botrytis isolates
representing six distinct, putatively novel species (Shipunov et al.
2008). A survey of Botrytis species revealed that many of the
species found on symptomatic peony plants shared phylogenetic
similarity to those species isolated from Centaurea stoebe
(Garfinkel et al. 2019). Studies of endophytic Botrytis species on
dandelion revealed that both B. cinerea and B. pseudocinerea have
the ability to behave as endophytes, as does an isolate that appears
genetically identical to B. mali and one other that appears novel
based on phylogenetic analysis (Shaw et al. 2016). Further calling
into question the dogma of Botrytis as a pathogen, the Botrytis
species B. pyriformis was described as a “likely saprophytic species
of Botrytis” and may not be a pathogen at all, as it was unable to
reinfect the host from which it was first isolated, nor was it able to
infect 29 additional plant species on which it was tested (Zhang et al.
2016). Phylogenetic data indicated that this species clustered into a
third, seemingly ancestral clade of Botrytis species (Fig. 2). Several
additional species isolated from peony showed similarly low
virulence on the host on which they were initially recovered
(Garfinkel et al. 2019). While it may be too early to make final
conclusions about the true ecological role(s) of Botrytis species, these
new insights nonetheless challenge historical species recognition
concepts.
Prior to ending the discussion on pathogenicity of Botrytis
species, additional oddities of this genus are important as related to
virulence. Investigations on B. cinerea have shown that this fungus
exhibits a light-regulated “circadian rhythm” wherein virulence is
affected by the time of day infection occurs (Hevia et al. 2015). It is
unknown how many other species of Botrytis show similar
tendencies; nonetheless, these data suggest that pathogenicity tests
may be highly influenced by light, further complicating the
implementation of pathogenicity as a way to delineate species.
PHYLOGENETICS TO THE RESCUE
Although the genus was once dominated by readily distinguish-
able species based on morphology, symptoms, or host range,
researchers now have the tools to see with more resolution what
other species recognition concepts were unable to provide in
Botrytis. Using phylogenetics tools, researchers have overcome the
difficulties associated with traditional species recognition methods
and uncovered an unexpected and fascinating amount of diversity
within the genus that challenges centuries-long dogmas relating
to Botrytis taxonomy, biology, and ecology. Not only has the
implementation of the phylogenetic species concept (PSC) in
Botrytis been able to rectify potentially erroneously delineated
species (e.g., B. pelargonii), but it has also helped revive old species
(B. mali and B. allii) and find new ones at an extraordinary pace. It
has helped to uncover cryptic species as well as cryptic lifestyles
and challenged current notions of what constitutes a plant pathogen.
Considering all of the difficulties of applying traditional
morphological species recognition concepts, the impracticality of
implementing sexual crosses, and shifting paradigms of pathoge-
nicity within the genus, it is no wonder that the quantitative, easily
interpreted PSR concept has come (and is likely to continue) to
dominate Botrytis taxonomy. Given the relative ease of genetic
sequencing, it is likely that researchers are recognizing new species,
perhaps even those with exceptional morphological features, first
by using phylogenetic methods and only later undertaking the
arduous, time-consuming tasks of morphological analysis, patho-
genicity tests, or sexual crosses.
When reading many of the new Botrytis species descriptions, it
does in fact seem that morphology or other biological character-
istics are often an afterthought, an attempt to corroborate or find
biological significance in the genetic data or simply to do due justice
to classical mycological methods. In many cases, authors will note
that (phylo)genetic data were initially generated and then all or a
subset of isolates were subject to additional morphological or
pathogenicity testing to “check off the boxes” for a more complete
Vol. 111, No. 3, 2021 449
taxonomic treatment. The question becomes, then: what constitutes
a complete Botrytis species description?
THE HETEROGENEITY OF SPECIES DESCRIPTIONS AND
A CALL FOR MINIMUM STANDARDS
Formal species descriptions of fungi are officially regulated by
the International Code of Botanical Nomenclature (ICBN). This
governing body dictates that any new species description is required
to have an official diagnosis (formerly the diagnosis was required to
be written in Latin; however, English diagnoses are now accepted
and encouraged) and a preserved type specimen that has been
deposited into a public herbarium that will assign the specimen an
accession number and make it widely available for interested parties
for additional scientific studies (Seifert and Rossman 2010). The
new fungus must also be named according to strict nomenclatural
standards.
Past what is required by the ICBN, there are no additional formal
requirements for new species descriptions; however, there are a
number of informal requirements from journals or additional
suggestions that have been published by mycologists. Most journals
require submission of the new species into the online database
Mycobank, and they also require molecular data to accompany
morphological descriptions (Seifert and Rossman 2010). Although
not required by the ICBN, living cultures are considered important
for many fungal species (Seifert and Rossman 2010). Several
publications have outlined guidelines for best practice in describing
new fungal species (Seifert and Rossman 2010; Sigler and
Hawksworth 1989a, b, c, d). In an effort to continue to improve
the nomenclatural standards for certain groups of fungi, the
International Commission on the Taxonomy of Fungi was
established in 1982 (Hawksworth 2010); however, none of the
suggestions are binding, nor have Botrytis systematics been
specifically discussed. Minimum standards to promote uniformity
in species descriptions have been strictly implemented in other
organisms, such as bacteria (Hibbett and Taylor 2013), and have
been suggested in some fungal species, such as Aspergillus (Samson
and Varga 2009). Standards for nomenclature were also suggested
for fungi at the beginning of genetic studies (Yoder et al. 1986), yet
standards remain uncommon in mycology.
In reviewing the current literature, there is no universal answer to
which criteria should accompany a new Botrytis species de-
scription. New species descriptions are quite heterogeneous in
content; the official descriptions especially contain varying levels of
detail. Nonetheless, there are some similarities. Tables 2, 3, and 4
show the Botrytis species described since 2010 and indicate the
criteria used for descriptions included in each.
All of the new species descriptions contain the following at
minimum: descriptions of colony morphology, macroconidia
measurements, conidiophore measurements, and sclerotia mea-
surements (all on some medium, whether it be artificial culture
medium or the host plant, except for B. pseudocinerea for which
measurements are lacking), pathogenicity tests on the original host
plant, and phylogenetic analysis using the G3PDH, HSP60, and
RPB2 genes (Tables 2, 3, and 4). All but one of the new species
descriptions also contain radial growth rate data at either one or
multiple temperatures, all but four contain sclerotia counts, and
more than half also include either genetic data for the ITS
region and/or phylogenetic analysis of the NEP1 and NEP2 genes
(Tables 3 and 4). The rest of the contents of the species de-
scriptions are highly variable.
The number of isolates used in new species descriptions range
from a single individual (B. medusae) to 13 (B. pseudocinerea),
with the majority using between three and six individuals (Table 2).
Of the 14 new species described, just over half (eight) of the
descriptions include pathogenicity tests on a host other than the
species from which the fungus was originally isolated, five assess
450 PHYTOPATHOLOGY ®
conidial germination rate and/or temperature optima, another five
look at fungicide sensitivity, and three include any discussion of
microconidia (Tables 2 and 3). Two consider the mating system or
apothecia (although for only one species were apothecia actually
observed), two reported conidia production rates, one observed the
production of infection cushions (an important question given that
this species, B. pyriformis, showed an inability to cause disease in
all infection trials), and one went as far as to describe the fine
structures of the ampullae, denticles, and sclerotial medullar
structures (Tables 2 and 3).
Although there are currently no official minimum standards for
species descriptions in Botrytis, those features that are consistent in
species descriptions can provide an indication as to what the
community has implicitly deemed important. Since there are many
who are involved in new Botrytis species descriptions around the
world, it would be audacious to propose a concrete set of standards
prior to a discussion with the international community; this is a
discussion I hope will be had at the upcoming, but delayed
BotrySclero 2020 (now 2021) conference in Avignon, France.
Nonetheless, the following is a list of possible recommended
criteria that may provide a starting point for discourse.
A species description should be based on more than one
representative isolate. This is, of course, not to say that a report
cannot or should not be published of a single isolate. In fact, quite
the contrary is true, and there is extreme value in publishing the
discovery of a single novel isolate. An example of the value is
fortunately already present in Botrytis to avoid theoretical
discussion.
In 2014, Lorenzini and Zapparoli published an article describing
a single genetically novel isolate of Botrytis from withered grape in
Italy that was given the name Botrytis sp. B83. Their comprehensive
article described not only phylogenetic data but also morphological
descriptions of the fungus, pathogenicity tests, and RFLP profiles
(Lorenzini and Zapparoli 2014). Upon discovery of the same
genetic species from peony in Alaska, researchers from the two
groups collaborated to officially describe the species as B. euroamericana
just 3 years later in 2017 (Garfinkel et al. 2017). The collaboration
and use of multiple isolates was then able to more adequately
capture the breadth of host and geographical range and the
morphological variation seen among individuals of this species
(Fig. 3).
The idea governing the number of representatives for describing
new species is not completely novel. In their article “How to
Describe a New Fungal Species,” Seifert and Rossman (2010) also
suggest having more than one representative of a fungal species. Yet
the authors leave room for this rule to be broken if “clear taxonomic
novelty” is proven. Perhaps there is value in describing only a single
representative as a new species if it has clear ramifications for
agricultural quarantines as an invasive or particularly virulent
pathogen; however, in the case that a new species of Botrytis is
important in this way, it is likely that more than one isolate will be
recovered.
Given the difficulty and time associated with morphological
and pathogenicity tests to publish a full article like the one
presented on Botrytis sp. B83, perhaps the Botrytis community
can consider a platform where sequence data alone can be
presented in a “note” fashion to expedite the discovery and formal
description of new species and facilitate collaboration among
research groups in the instance that other representatives of a
species are recovered. This strategy is likely to be successful.
Garfinkel et al. (2019) published an article concerning the genetic
diversity of Botrytis species discovered in the United States, and
the authors were subsequently contacted by and are in collabo-
ration with other laboratories to produce formal species descrip-
tions (A. R. Garfinkel, unpublished data). In the case of Garfinkel
et al. (2019), the publication of sequence data alone was warranted
because of the number of genetically novel isolates collected
in their study (nonetheless, even the phylogenetic species for
which there were multiple representatives were not given official
names). However, a platform for reporting a single isolate would
allow scientists without sufficient numbers to publish a full report
to increase their opportunities for identifying enough isolates
to collaborate on an official description. Even in the case where
multiple representative isolates of novel phylogenetic species are
found, such a database would be useful prior to conducting the
additional studies that are required and should be encouraged for
naming species.
New species descriptions should include deposition of
sequence data for the G3PDH, HSP60, RPB2, NEP1, and
NEP2 genes in a public database and phylogenetic trees for at
least the former. It is clear that phylogenetics has played a vital
role in modern Botrytis taxonomy and is likely to continue to
dominate Botrytis species recognition. The genes from Staats et al.
(2005, 2007a) are currently the preferred loci for genetic analysis to
delineate species in Botrytis (Hyde et al. 2014). At this point in this
review, not much discussion is needed to indicate their importance,
since it has been established that these genes have been at the crux of
the revolution of new species recognitions. As such, new species
descriptions should provide publicly available data of these gene
sequences for researchers around the world to utilize in their own
research and to corroborate species status of new isolates. Since
trees built with G3PDH, HSP60, and RPB2 have been shown to be
largely congruent with those built with NEP1 and NEP2 gene
sequences, it perhaps is not critical to perform phylogenetic analysis
using the latter two genes if the analysis from the former is
conclusive. However, given that NEP1 and NEP2 provide for
additional phylogenetic resolution among species of Botrytis (Hyde
et al. 2014; Staats et al. 2007a) and that their generation is not overly
difficult or expensive for laboratories already performing DNA
sequencing, these data should be encouraged to be made readily
available. The deposition of these gene sequences in public
databases would not only help facilitate species recognition but
also later identification of these species for the publication of first
reports that help elucidate host and geographical range.
It should be highly encouraged that the most closely related
Botrytis species be included in all studies of a new species.
Unlike the last criterion, which is relatively easy to achieve for most
laboratories with molecular capabilities, this criterion could prove
to be substantially more difficult. Although cultures of type
specimens can be readily ordered from a culture collection, such
as the Westerdijk Fungal Biodiversity Institute (formerly known as
CBS-KNAW), restrictions on the movement of plant pathogens may
make acquisition difficult. For example, in the United States,
acquisition of fungal cultures from outside of the state in which the
laboratory is located requires inspections and then an issuance of a
permit from the U.S. Department of Agriculture Animal and Plant
Health Inspection Service, a process that demands time, equipment,
and laboratory resources dedicated to maintaining compliance
standards.
Nonetheless, this criterion serves as an important way to serve as
a “check” for the results of phylogenetics analyses. In fact, during
the peer review of this article, one of the reviewers suggested that
this criterion be essential rather than recommended; this is precisely
the discourse I hope these suggested criteria will generate. Yet of the
14 new species reports published in the last 10 years, fewer than half
(six) have included any analysis of the most closely related species
or a species that is not the one being described (Table 2).
Even if the phylogenetic analysis shows separation of the new
species to its closest neighbor, it should be the burden of the
researcher to corroborate the genetic separation, or at least compare
morphological or other biological data whenever possible. Such
was done in the assessment of B. fabiopsis, a new species most
closely related to B. galanthina (Zhang et al. 2010a). Not only did
the authors provide distinction of B. fabiopsis from B. galanthina
using phylogenetic and other genetic data, but they also directly
compared the two species and determined that B. galanthina was
not pathogenic on the host on which B. fabiopsis was isolated
(Zhang et al. 2010a). Furthermore, the authors separated the two
species by observing variations in conidia production on artificial
culture media (Zhang et al. 2010a).
Perhaps in some cases it is also relevant to compare the new
species with species in which it exists in sympatry or with which it
shares a host range. Although the article to describe the new species
B. sinoallii did not include any of the species to which it was most
closely related, the authors did compare this species and its
morphology and pathogenicity to other species found in their survey
of Allium crops and found it had important differences in conidia
and sclerotia size and production and elucidated important
similarities in virulence (Zhang et al. 2010b).
Providing side-by-side comparisons with the most closely
related species is especially important if the phylogenetic evidence
is not unambiguously delineating the species. The new species
B. eucalypti described from eucalyptus in China is phylogenetically
nearly identical to B. cinerea, yet the authors do not report any side-
by-side comparisons with B. cinerea in any of the morphological or
pathogenicity trials, nor did they perform any attempts to sexually
cross the two species (Liu et al. 2016) (a criterion which would
be valuable in this case, as it was with B. pseudocinerea). Although
the authors report data from publications describing B. cinerea
conidia and conidiophore measurements (Liu et al. 2016), the issues
discussed earlier in this article regarding intraspecies variation and
morphological plasticity in B. cinerea make this approach espe-
cially problematic. Without direct comparison, the phylogenetic data
and the status of B. eucalypti as a separate species remain suspect.
Descriptions should include morphological descriptions of
the colony, macroconidia, conidiophores, sclerotia, and radial
growth rate. These morphological measurements are included in
every or nearly every new species description over the last 10 years
(and surely before then) and can implicitly be assumed to represent
a consensus minimum of the laboratories from around the world that
have thus far reported new Botrytis species. These descriptions
include color, size, and shape and, in the case of sclerotia,
distribution and production rate as well. These traits have been
historically important in species recognition within the genus, with
special consideration of the shape of the conidiophores linking them
to Botrytis. Furthermore, the growth rate of the species (at least one
temperature on one culture medium) should be considered. These
features may or may not be conclusive in species delineation, owing
to reasons discussed above; however, they provide an important
baseline for morphological identification of the new species.
Although other features have been described, such as the ampullae,
denticles, and sclerotial medulla, these features seem to be of
limited value, either currently or historically, in species delineation.
A larger discussion could be had with regard to their value from a
“pure” mycology or completeness-of-morphological-description
standpoint, but they have thus far not been useful in species
delineation.
In some cases, additional morphological data have been helpful
in understanding the biology of the new species. An example is with
B. pyriformis. Zhang et al. (2016) observed and reported the
absence of the production of infection cushions on this putatively
saprophytic, nonpathogenic species, which could potentially
explain its inability to cause disease on the plants in the pathogenicity
tests. Fungicide resistance patterns have also been a helpful
delineator of species, such as with B. pseudocinerea (Fournier
et al. 2005; Walker et al. 2011). When additional morphological or
otherwise biological features of the fungus are relevant to help
explain its behavior or uniqueness in some way, authors should be
encouraged to publish these observations.
New species descriptions should include pathogenicity tests
on the original host and on the host(s) of the most closely
Vol. 111, No. 3, 2021 451
related species, if applicable. This review previously discussed
the expanding host ranges of many Botrytis species and begs the
question not only of the value of host range testing, but how many
hosts need to be tested in order to make a conclusive decision
regarding species delineations. Nonetheless, a minimum standard
of confirming pathogenicity of the new species on the host(s) on
which it was first isolated should be essential. Pathogenicity testing
on the original host plant and confirming pathogenicity by
performing Koch’s postulates is a critical component of the study
of plant pathology as a whole and should be an indisputable element
of new species descriptions of Botrytis isolated from symptomatic
tissue. These tests, even if disease does not develop, may even lead
to interesting features of the pathogen, such as those found in the
putatively nonpathogenic B. pyriformis (Zhang et al. 2016).
Pathogenicity testing on the host(s) of the most closely related
Botrytis species may also be encouraged, especially in cases where
the most closely related species is a host-specific pathogen. An
example of this strategy can be seen for the pathogenicity tests
conducted with B. euroamericana on onion. These tests were
helpful in delineating this species from the most closely related
species, B. aclada, a virulent onion-specific pathogen (Garfinkel
et al. 2017). Lastly, especially in the case that a new Botrytis species
is isolated from an economically unimportant host, authors may be
encouraged to test the pathogenicity of the new Botrytis species on
the most closely related, economically important plant species. That
said, pathogenicity testing may become somewhat complicated if
(and almost inevitably when) additional species are found as
endophytes. Research has indicated that at least some isolates of
Botrytis that have been isolated as endophytes retain their ability to
cause disease (Grant-Downton et al. 2014; Shaw et al. 2016);
nonetheless, shifting criteria regarding pathogenicity tests may be
warranted in the future as more is learned about the biology of
endophytic Botrytis isolates.
Ideally, a set of minimum criteria for Botrytis would provide for a
“checks and balances” system in which no one species recognition
concept dominates. The above criteria emphasize the utility of three
species recognition concepts (morphological species concept, PSC,
and host range) and leave room for additional delineation tools
on a case-by-case basis. Implementing a combination of species
recognition criteria will allow researchers to fully employ powerful
phylogenetic analysis tools while paying due respect to the classical
mycological methods and the nuances of the genus. Hopefully, too,
these criteria can be considered flexible and allow for change as
Botrytis research moves forward.
FINAL THOUGHTS ON SPECIES—WHAT’S IN A NAME?
In their article, Taylor et al. (2000) introduce the following
question: “Isn’t determining the limits of a species inherently
subjective because there is a continuum of genetic differentia-
tion…?” “Yes,” they admit. This is not just an issue with PSR, of
course, as is there a continuum in the evolution of morphological
traits, virulence, sexual divergence, and all of the other traits
historically used to delineate species. Hey (2001) reminds us that
“When we devise taxa, we are not objective…” and warns against
the dangers of failing to “recognize our taxa as inherently subjective.”
Scientists and philosophers alike have debated the definitions and
merits of species and how to recognize their limits; the theoretical
understanding of what constitutes a real species (or if they indeed
exist) is far from resolved.
“So,” one might ask, “why should we even care about species if it
is just a series of lines drawn in the sand?” There are potentially a
number of ways to answer this question; however, since this review is
discussing the Botrytis, it is perhaps prudent to address the question in
that context. For a broader discussion of why fungal systematics is
important, see Rossman and Palm-Hernández (2008).
452 PHYTOPATHOLOGY ®
Although it is a worthwhile and interesting strictly intellectual
pursuit to delineate and define new Botrytis species, it is important
to remember the impact that this group of fungi have on the world’s
agricultural systems and the potential ramifications of discovering
and describing new Botrytis species in terms of movement of
agricultural goods and agricultural quarantines. In the last 10 years,
new species discoveries and descriptions have helped reveal
innately fungicide-resistant species (B. pseudocinerea) (Fournier
et al. 2005; Walker et al. 2011) and species that appear to have
“adapted” to living in the presence of fungicides (B. fragariae)
(Rupp et al. 2017), or they have simply helped provide baseline
understanding of the levels of fungicide resistance in high-value
cropping systems in which Botrytis is an important pathogen
(B. californica and B. sinoviticola) (Saito et al. 2016; Zhou et al.
2014). Studies have also helped elucidate important variations in
virulence among sympatric Botrytis species (B. sinoallii) (Zhang
et al. 2010b), exposed emerging pathogens that might help reveal
mechanisms regarding the evolution of pathogenicity and the
influence of selective breeding (B. deweyae) (Grant-Downton et al.
2014), and uncovered that some Botrytis species may not even be
pathogens at all (B. pyriformis) (Zhang et al. 2016). And among
these new species that are found, additional first reports have helped
expand the geographical range in which they are known to exist
from Europe (Rupp et al. 2017) to the United States (Dowling et al.
2017) (B. fragariae), and from China (Li et al. 2015) to New
Zealand (Johnston et al. 2014a) (B. pseudocinerea). For those
species in which we do not yet understand their impact, new species
descriptions provide the foundation for further investigation into
this fascinating genus. Therefore, perhaps in addition to asking what
is a species and what is a valid description, we could ask the
question: Why are Botrytis species important, and what is a useful
description? And then go from there.
ACKNOWLEDGMENTS
I thank Gary Chastagner for his presubmission revisions and for
many years of thoughtful conversations that led to the conceptu-
alization of the topic for this review; Nick A. Lorenz for his help
with creating Figure 1; and Katherine Otten for her prepublication
grammar edits.
LITERATURE CITED
Amselem, J., Cuomo, C. A., van Kan, J. A., Viaud, M., Benito, E. P., Couloux,
A., Coutinho, P. M., de Vries, R. P., Dyer, P. S., Fillinger, S., Fournier, E.,
Gout, L., Hahn, M., Kohn, L., Lapalu, N., Plummer, K. M., Pradier, J. M.,
Quévillon, E., Sharon, A., Simon, A., ten Have, A., Tudzynski, B.,
Tudzynski, P., Wincker, P., Andrew, M., Anthouard, V., Beever, R. E.,
Beffa, R., Benoit, I., Bouzid, O., Brault, B., Chen, Z., Choquer, M.,
Collémare, J., Cotton, P., Danchin, E. G., Da Silva, C., Gautier, A., Giraud,
C., Giraud, T., Gonzalez, C., Grossetete, S., Güldener, U., Henrissat, B.,
Howlett, B. J., Kodira, C., Kretschmer, M., Lappartient, A., Leroch, M.,
Levis, C., Mauceli, E., Neuvéglise, C., Oeser, B., Pearson, M., Poulain, J.,
Poussereau, N., Quesneville, H., Rascle, C., Schumacher, J., Ségurens, B.,
Sexton, A., Silva, E., Sirven, C., Soanes, D. M., Talbot, N. J., Templeton,
M., Yandava, C., Yarden, O., Zeng, Q., Rollins, J. A., Lebrun, M. H., and
Dickman, M. 2011. Genomic analysis of the necrotrophic fungal pathogens
Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet. 7:e1002230.
Andrew, M., Barua, R., Short, S. M., and Kohn, L. M. 2012. Evidence for a
common toolbox based on necrotrophy in a fungal lineage spanning necrotrophs,
biotrophs, endophytes, host generalists and specialists. PLoS One 7:e29943.
Beever, R. E., and Weeds, P. L. 2004. Taxonomy and genetic variation of
Botrytis and Botryotinia. Pages 29-52 in: Botrytis: Biology, pathology and
control. Y. Elad, B. Williamson, P. Tudzynski, and N. Delen, eds. Springer,
Dordrecht, Netherlands.
Bergquist, R. R., and Lorbeer, J. W. 1972. Apothecial production, compati-
bility and sex in Botryotinia squamosa. Mycologia 64:1270-1281.
Boddy, L. 2015. Pathogens of autotrophs. Pages 245-292 in: The fungi. 3rd ed.
S. C. Watkinson, L. Boddy, and N. P. Money, eds. Elsevier, Waltham, MA.
Buchwald, N. F. 1949. Studies in the Sclerotiniaceae. I. Taxonomy of the Scle-
rotiniaceae. Kongelige Veterinær og Landbohøjskole Aarsskrift. 32:1-116.
Buchwald, N. F. 1953. Botryotinia (Sclerotinia) globosa sp. n. on Allium ursinum,
the perfect stage of Botrytis globosa Raabe. Phytopathol. Z. 20:241-254.
Chastagner, G. A. 1983. Narcissus fire: Prevalence, epidemiology, and control
in western Washington. Plant Dis. 67:1384-1386.
Chastagner, G. A. 1986. In vitro production of Botryotinia polyblastis
apothecia and factors affecting germination of ascospores. Acta Hortic. 177:
461-468.
Chastagner, G. A., Riley, K. L., and Doss, R. P. 1992. An attempt to produce
an apothecial state of Botrytis elliptica in vitro. Acta Hortic. 325:689-694.
Coats, K. P., Garfinkel, A., and Chastagner, G. A. 2018. Novel sequencing
reveals diagnostic assay of MAT1-1 and MAT1-2 mating type idiomorphs
in Botrytis paeoniae (Abstract). Phytopathology 108:S2.43.
Cohrs, K. C., Simon, A., Viaud, M., and Schumacher, J. 2016. Looking
through the eyes of Botrytis: Molecular genetics of photoperception and its
consequences (Abstract). Page 22 in: 17th International Botrytis Sympo-
sium Abstract Book, Santa Cruz, Chile.
Cosseboom, S. D., Ivors, K. L., Schnabel, G., and Holmes, G. 2018. First
report of Botrytis mali causing gray mold on strawberry in California. Plant
Dis. 102:679.
Crous, P. W., Hawksworth, D. L., and Wingfield, M. J. 2015. Identifying and
naming plant-pathogenic fungi: Past, present, and future. Annu. Rev. Phy-
topathol. 53:247-267.
Dean, R., van Kan, J. A. L., Pretorius, Z. A., Hammond-Kosack, K. E.,
Di Pietro, A., Spanu, P. D., Rudd, J. J., Dickman, M., Kahmann, R., Ellis, J.,
and Foster, G. D. 2012. The top 10 fungal pathogens in molecular plant
pathology. Mol. Plant Pathol. 13:414-430.
Dowling, M. E., Hu, M.-J., and Schnabel, G. 2017. Identification and char-
acterization of Botrytis fragariae isolates on strawberry in the United
States. Plant Dis. 101:1769-1773.
Dowling, M. E., and Schnabel, G. 2017. First report of Botrytis mali causing
gray mold on strawberry in the United States. Plant Dis. 101:1034.
Dowson, W. J. 1928. On an extraordinary Botrytis causing a disease of Nar-
cissus leaves. Trans. Br. Mycol. Soc. 13:95-102, IN4.
Drayton, F. L. 1937. The perfect stage of Botrytis convoluta. Mycologia 29:
305-318.
Elad, Y., Pertot, I., Cotes Prado, A. M., and Stewart, A. 2016. Plant hosts of
Botrytis spp. Pages 413-486 in: Botrytis–The Fungus, the Pathogen, and Its
Management in Agricultural Systems. S. Fillinger and Y. Elad, eds.
Springer, Cham, Switzerland.
Elad, Y., Williamson, B., Tudzynski, P., and Delen, N. 2007. Botrytis spp. and
diseases they cause in agricultural systems-an introduction. Pages 1-8 in:
Botrytis: Biology, Pathology, and Control. Y. Elad, B. Williamson, P.
Tudzynski, and N. Delen, eds. Springer, Dordrecht, The Netherlands.
Elfar, K., Riquelme, D., Zoffoli, J. P., and Latorre, B. 2017. First report of
Botrytis prunorum causing fruit rot on kiwifruit in Chile. Plant Dis. 101:
388.
Elliott, M. E. 1964. Self-fertility in Botryotinia porri. Can. J. Bot. 42:
1393-1395.
Esterio, M., Osorio-Navarro, C., Carreras, C., Azócar, M., Copier, C., Estrada,
V., Rubilar, M., and Auger, J. 2020. Botrytis prunorum associated to Vitis
vinifera blossom blight in Chile. Plant Dis. 104:2324-2329.
Faretra, F., Antonacci, E., and Pollastro, S. 1988. Sexual behaviour and mating
system of Botryotinia fuckeliana, teleomorph of Botrytis cinerea. Micro-
biology 134:2543-2550.
Farr, D. F., Bills, G. F., Chamuris, G. P., and Rossman, A. Y. 1989. Fungi on
plants and plant products in the United States. American Phytopathological
Society, St. Paul, MN.
Farr, D. F., and Rossman, A. Y. 2020. Fungal Databases, U.S. National Fungus
Collection, ARS, USDA. https://nt.ars-grin.gov/fungaldatabases/
Fernández, J. G., Fernández Baldo, M. A., Sansone, G., Calvente, V., Benuzzi,
D., Salinas, E., Raba, J., and Sanz, M. I. 2014. Effect of temperature on the
morphological characteristics of Botrytis cinerea and its correlated with the
genetic variability. J. Costal Life Med. 2:543-548.
Fernández-Ortuño, D., Li, X. P., Wang, F., and Schnabel, G. 2012. First report
of gray mold of strawberry caused by Botrytis caroliniana in North Caro-
lina. Plant Dis. 96:914.
Ferrada, E. E., Latorre, B. A., Zoffoli, J. P., and Castillo, A. 2016. Identifi-
cation and characterization of Botrytis blossom blight of Japanese plums
caused by Botrytis cinerea and B. prunorum sp. nov. in Chile. Phytopa-
thology 106:155-165.
Ferrada, E. E., Naranjo, P., Briceño, E. X., Lolas, M., and Dı́az, G. A. 2020.
Occurrence of Botrytis prunorum causing calyx-end rot in European pear
fruits during cold storage in Chile. Plant Dis. 104:590.
Fillinger, S., and Elad, Y., eds. 2016. Botrytis–The fungus, the pathogen, and
its management in agricultural systems. Springer, Cham, Switzerland.
Fournier, E., Giraud, T., Albertini, C., and Brygoo, Y. 2005. Partition of the
Botrytis cinerea complex in France using multiple gene genealogies.
Mycologia 97:1251-1267.
Garfinkel, A. 2020. Three Botrytis species found causing gray mold on in-
dustrial hemp (Cannabis sativa) in Oregon. Plant Dis. 104:2026.
Garfinkel, A. R., Coats, K. P., Sherry, D. L., and Chastagner, G. A. 2019.
Genetic analysis reveals unprecedented diversity of a globally-important
plant pathogenic genus. Sci. Rep. 9:6671.
Garfinkel, A. R., Lorenzini, M., Zapparoli, G., and Chastagner, G. A. 2017.
Botrytis euroamericana, a new species from peony and grape in North
America and Europe. Mycologia 109:495-507.
Giraud, T., Fortini, D., Levis, C., Leroux, P., and Brygoo, Y. 1997. RFLP
markers show genetic recombination in Botryotinia fuckeliana (Botrytis
cinerea) and transposable elements reveal two sympatric species. Mol. Biol.
Evol. 14:1177-1185.
Grant-Downton, R. T., Terhem, R. B., Kapralov, M. V., Mehdi, S.,
Rodriguez-Enriquez, M. J., Gurr, S. J., van Kan, J. A. L., and Dewey, F. M.
2014. A novel Botrytis species is associated with a newly emergent foliar
disease in cultivated Hemerocallis. PLoS One 9:e89272.
Gregory, P. H. 1938. Sclerotinia polyblastis n. sp. on Narcissus the perfect
stage of Botrytis polyblastis Dowson. Trans. Br. Mycol. Soc. 22:201-203.
Groves, J. W., and Loveland, C. A. 1953. The connection between Botryotinia
fuckeliana and Botrytis cinerea. Mycologia 45:415-425.
Hahn, M. 2014. The rising threat of fungicide resistance in plant pathogenic
fungi: Botrytis as a case study. J. Chem. Biol. 7:133-141.
Harper, L. A., Derbyshire, M. C., and Lopez-Ruiz, F. J. 2019. Identification
and characterization of Botrytis medusae, a novel cryptic species causing
grey mould on wine grapes in Australia. Plant Pathol. 68:939-953.
Hawksworth, D. L. 2010. A vision for the future of the ICTF. IMA Fungus 1:
20-21.
Hennebert, G. L. 1973. Botrytis and Botrytis-like genera. Persoonia 7:183-204.
Hennebert, G. L., and Groves, J. W. 1963. Three new species of Botryotinia on
Ranunculaceae. Can. J. Bot. 41:341-370.
Hevia, M. A., Canessa, P., Müller-Esparza, H., and Larrondo, L. F. 2015. A
circadian oscillator in the fungus Botrytis cinerea regulates virulence when
infecting Arabidopsis thaliana. Proc. Nat. Acad. Sci. U.S.A. 112:8744-8749.
Hey, J. 2001. The mind of the species problem. Trends Ecol. Evol. 16:326-329.
Hibbett, D. S., and Taylor, J. W. 2013. Fungal systematics: Is a new age of
enlightenment at hand? Nat. Rev. Microbiol. 11:129-133.
Hoist-Jensen, A., Vaage, M., and Schumacher, T. 1998. An approximation to
the phylogeny of Sclerotinia and related genera. Nord. J. Bot. 18:705-719.
Holz, G., Coertze, S., and Williamson, B. 2007. The ecology of Botrytis on
plant surfaces. Pages 9-27 in: Botrytis: Biology, Pathology and Control. Y.
Elad, B. Williamson, P. Tudzynski, and N. Delen, eds. Springer, Dordrecht,
Netherlands.
Huang, J., Hsieh, T.-F., Chastagner, G. A., and Hsiang, T. 2001. Clonal and
sexual propagation in Botrytis elliptica. Mycol. Res. 105:833-842.
Hughes, S. J. 1958. Revisiones hyphomycetum aliquot cum appendice de
nominibus rejiciendis. Can. J. Bot. 36:727-836.
Hyde, K. D., Nilsson, R. H., Alias, S. A., Ariyawansa, H. A., Blair, J. E., Cai,
L., de Cock, A. W. A. M., Dissanayake, A. J., Glockling, S. L.,
Goonasekara, I. D., Gorczak, M., Hahn, M., Jayawardena, R. S., van Kan,
J. A. L., Laurence, M. H., Lévesque, C. A., Li, X., Liu, J.-K.,
Maharachchikumbura, S. S. N., Manamgoda, D. S., Martin, F. N.,
McKenzie, E. H. C, McTaggart, A. R., Mortimer, P. E., Nair, P. V. R.,
Pawlowska, J., Rintoul, T. L., Shivas, R. G., Spies, C. F. J., Summerell,
B. A., Taylor, P. W. J., Terhem, R. B., Udayanga, D., Vaghefi, N., Walther,
G., Wilk, M., Wrzosek, M., Xu, J.-C., Yan, J., and Zhou, N. 2014. One stop
shop: Backbones trees for important phytopathogenic genera: I (2014).
Fungal Divers. 67:21-125.
Jarvis, W. R. 1977. Botryotinia and Botrytis species: Taxonomy, physiology
and pathogenicity. A guide to the literature. Monograph No. 15. Agriculture
Canada, Ottawa, ON, Canada.
Jarvis, W. R. 1980. Taxonomy. Pages 1-18 in: The Biology of Botrytis. J. R.
Coley-Smith, K. Verhoeff, and W. R. Jarvis, eds. Academic Press, San
Diego, CA.
Johnston, P. R., Hoksbergen, K., Park, D., and Beever, R. E. 2014a. Genetic
diversity of Botrytis in New Zealand vineyards and the significance of its
seasonal and regional variation. Plant Pathol. 63:888-898.
Johnston, P. R., Seifert, K. A., Stone, J. K., Rossman, A. Y., and Marvanová, L.
2014b. Recommendations on generic names competing for use in Leotio-
mycetes (Ascomycota). IMA Fungus 5:91-120.
Khan, M. I., Marroni, V., Keenan, S., Scott, I. A. W., Viljanen-Rollinson,
S. L. H., and Bulman, S. 2013. Enhanced molecular identification of Bo-
trytis spp. from New Zealand onions. Eur. J. Plant Pathol. 136:495-507.
Kohn, L. M. 1979. Delimitation of the economically important plant patho-
genic Sclerotinia species. Phytopathology 69:881-886.
Vol. 111, No. 3, 2021 453
Li, N., Zhang, J., Yang, L., Wu, M. D., and Li, G. Q. 2015. First report of
Botrytis pseudocinerea causing gray mold on tomato (Lycopersicon escu-
lentum) in central China. Plant Dis. 99:283.
Li, X., Kerrigan, J., Chai, W., and Schnabel, G. 2012. Botrytis caroliniana, a new
species isolated from blackberry in South Carolina. Mycologia 104:650-658.
Liu, Q., Li, G., Li, J., and Chen, S. 2016. Botrytis eucalypti, a novel species
isolated from diseased Eucalyptus seedlings in South China. Mycol. Prog.
15:1057-1079.
Lorenz, D. 1983. Investigations on the morphological variability and patho-
genicity of Botrytis cinerea Pers. and Botryotinia fuckeliana Whetz. Z.
Pflanzenkr. Pflanzenschutz 90:622-633.
Lorenzini, M., and Zapparoli, G. 2014. An isolate morphologically and phy-
logenetically distinct from Botrytis cinerea obtained from withered grapes
possibly represents a new species of Botrytis. Plant Pathol. 63:1326-1335.
Moore, W. C. 1959. Basic parasitic fungi: A host-parasite index and a guide to
British literature on the fungus diseases of cultivated plants. Cambridge
University Press, Cambridge, UK.
Moparthi, S., Peluola, C., Agnidotan, B., McPhee, K., and Burrows, M. 2020.
First report of gray mold of chickpea caused by Botrytis euroamericana in
the USA. Crop Prot. 137:105297.
Nielsen, K., Justesen, A. F., Jensen, D. F., and Yohalem, D. S. 2001. Uni-
versally primed polymerase chain reaction alleles and internal transcribed
spacer restriction fragment length polymorphisms distinguish two subgroups
in Botrytis aclada distinct from B. byssoidea. Phytopathology 91:527-533.
Nielsen, K., and Yohalem, D. S. 2001. Origin of a polyploid Botrytis pathogen
through interspecific hybridization between Botrytis aclada and
B. byssoidea. Mycologia 93:1064-1071.
Noble, M. 1948. Seed-borne diseases of clover. Trans. Br. Mycol. Soc. 30:
84-91, IN5-IN6.
O’Gorman, D. T., Sholberg, P. L., Stokes, S. C., and Ginns, J. 2008. DNA
sequence analysis of herbarium specimens facilitates the revival of Botrytis
mali, a postharvest pathogen of apple. Mycologia 100:227-235.
Paul, W. R. C. 1929. A comparative morphological and physiological study of
a number of strains of Botrytis cinerea Pers. with special reference to their
virulence. Trans. Br. Mycol. Soc. 14:118-135.
Persoon, C. H. 1801. Synopsis Methodica Fungorum. Dieterich, Gottingen, Germany.
Plesken, C., Westrich, L.-D., and Hahn, M. 2015. Genetic and phenotypic
characterization of Botrytis calthae. Plant Pathol. 64:128-136.
Røed, H. 1949. Botryotinia pelargonii n. sp., det perfekte stadium av en Bo-
trytis av cinerea-typen pa Pelargonium. Blyttia 7:65-79.
Rossman, A. Y., and Palm-Hernández, M. E. 2008. Systematics of plant
pathogenic fungi: Why it matters. Plant Dis. 92:1376-1386.
Rupp, S., Plesken, C., Rumsey, S., Dowling, M., Schnabel, G., Weber, R. W.,
and Hahn, M. 2017. Botrytis fragariae, a new species causing gray mold on
strawberries, shows high frequencies of specific and efflux-based fungicide
resistance. Appl. Environ. Microbiol. 83:e00269-17.
Saccardo, P. A. 1886. Sylloge fungorum omnium hucusque cognitorum, Vol. 4.
Patavii.
Saito, S., Margosan, D., Michailides, T. J., and Xiao, C. L. 2016. Botrytis
californica, a new cryptic species in the B. cinerea species complex causing
gray mold in blueberries and table grapes. Mycologia 108:330-343.
Samson, R. A., and Varga, J. 2009. What is a species in Aspergillus? Med.
Mycol. 47:S13-S20.
Seifert, K. A., and Rossman, A. Y. 2010. How to describe a new fungal
species. IMA Fungus 1:109-111.
Shaw, M. W., Emmanuel, C. J., Emilda, D., Terhem, R. B., Shafia, A.,
Tsamaidi, D., Emblow, M., and van Kan, J. A. L. 2016. Analysis of cryptic,
systemic Botrytis infections in symptomless hosts. Front. Plant Sci. 7:625.
Shipunov, A., Newcombe, G., Raghavendra, A. K., and Anderson, C. L. 2008.
Hidden diversity of endophytic fungi in an invasive plant. Am. J. Bot. 95:
1096-1108.
Sigler, L., and Hawksworth, D. L. 1989a. International Commission on the
Taxonomy of Fungi (ICTF) code of practice for systematic mycologists.
Microbiol. Sci. 4:83-86.
Sigler, L., and Hawksworth, D. L. 1989b. International Commission on the
Taxonomy of Fungi (ICTF) code of practice for systematic mycologists.
Mycopathologia 99:3-7.
Sigler, L., and Hawksworth, D. L. 1989c. International Commission on the
Taxonomy of Fungi (ICTF) code of practice for systematic mycologists.
Mycologist 21:101-105.
454 PHYTOPATHOLOGY ®
Sigler, L., and Hawksworth, D. L. 1989d. International Commission on the
Taxonomy of Fungi (ICTF) code of practice for systematic mycologists.
Acta Mycol. Sin. 8:154-159.
Sowley, E. N. K., Dewey, F. M., and Shaw, M. W. 2010. Persistent, symp-
tomless, systemic, and seed-borne infection of lettuce by Botrytis cinerea.
Eur. J. Plant Pathol. 126:61-71.
Staats, M., van Baarlen, P., Schouten, A., van Kan, J. A. L., and Bakker, F. T.
2007a. Positive selection in phytotoxic protein-encoding genes of Botrytis
species. Fun. Gen. Biol. 44:52-63.
Staats, M., van Baarlen, P., and van Kan, J. A. L. 2005. Molecular phylogeny
of the plant pathogenic genus Botrytis and the evolution of host specificity.
Mol. Biol. Evol. 22:333-346.
Staats, M., van Baarlen, P., and van Kan, J. A. L. 2007b. AFLP analysis of
genetic diversity in populations of Botrytis elliptica and Botrytis tulipae
from the Netherlands. Eur. J. Plant Pathol. 117:219-235.
Steiger, D. 2007. Global economic importance of Botrytis protection (Ab-
stract). Page 7 in: 14th International Botrytis Symposium Abstract Book,
Cape Town, South Africa.
Taylor, J. W., Jacobson, D. J., Kroken, S., Kasuga, T., Geiser, D. M., Hibbett,
D. S., and Fisher, M. C. 2000. Phylogenetic species recognition and species
concepts in fungi. Fun. Gen. Biol. 31:21-32.
Terhem, R. B., Staats, M., and van Kan, J. A. L. 2015. Mating type and sexual
fruiting body of Botrytis elliptica, the causal agent of fire blight in lily. Eur.
J. Plant Pathol. 142:615-624.
Valero-Jiménez, C. A., Veloso, J., Staats, M., and van Kan, J. A. L. 2019.
Comparative genomics of plant pathogenic Botrytis species with distinct
host specificity. BMC Genomics 20:203.
van den Ende, J. E., and Pennock-Vos, M. G. 1997. Primary sources of in-
oculum of Botrytis elliptica in lily. Acta Hortic. 430:591-596.
van Kan, J. A. L., Shaw, M. W., and Grant-Downton, R. T. 2014. Botrytis
species: Relentless necrotrophic thugs or endophytes gone rogue? Mol.
Plant Pathol. 15:957-961.
Walker, A.-S. 2016. Diversity within and between species of Botrytis. Pages
91-125 in: Botrytis–The Fungus, the Pathogen and Its Management in
Agricultural Systems. S. Fillinger and Y. Elad, eds. Springer, Cham, Switzerland
Walker, A.-S., Gautier, A., Confais, J., Martinho, D., Viaud, M., Le Pêcheur,
P., Dupont, J., and Fournier, E. 2011. Botrytis pseudocinerea, a new cryptic
species causing gray mold in French vineyards in sympatry with Botrytis
cinerea. Phytopathology 101:1433-1445.
Wang, X., Zhang, L., and Zhang, Z. 1996. A new species of Botrytis and 5
known Botrytis species in China. Acta Phytopathol. Sin. 26:79-85.
Weiberg, A., Wang, M., Lin, F.-M., Zhao, H., Zhang, Z., Kaloshian, I., Huang,
H.-D., and Jin, H. 2013. Fungal small RNAs suppress plant immunity by
hijacking host RNA interference pathways. Science 342:118-123.
Wu, T., and Lu, J. 1991. A new species of Botryotinia-the teleomorph of
Botrytis fabae Sardina. Acta Mycol. Sin. 10:27-30.
Xue, L. H., Liu, Y., Zhang, L., Huang, X. Q., Zhou, X. Q., Yang, X. X., and
Wu, W. X. 2019. Botrytis pseudocinerea, a new pathogen causing gray
mold on Brassica napus in China. Plant Dis. 103:367.
Yoder, O. C., Valent, B., and Chumley, F. 1986. Genetic nomenclature and
practice for plant pathogenic fungi. Phytopathology 76:383-385.
Yohalem, D. S., Nielsen, K., and Nicolaisen, M. 2003. Taxonomic and no-
menclatural clarification of the onion neck rotting Botrytis species.
Mycotaxon 85:175-182.
Zhang, J., Wu, M.-D., Li, G.-Q., Yang, L., Yu, L., Jiang, D.-H., Huang, H.-C.,
and Zhuang, W.-Y. 2010a. Botrytis fabiopsis, a new species causing choc-
olate spot of broad bean in central China. Mycologia 102:1114-1126.
Zhang, J., Yang, H., Yu, Q. Y., Wu, M. D., Yang, L., Zhuang, W. Y., Chen,
W. D., and Li, G. Q. 2016. Botrytis pyriformis sp. nov., a novel and likely
saprophytic species of Botrytis. Mycologia 108:682-696.
Zhang, J., Zhang, L., Li, G.-Q., Yang, L., Jiang, D.-H., Zhuang, W.-Y., and
Huang, H.-C. 2010b. Botrytis sinoallii: A new species of the grey mould
pathogen on Allium crops in China. Mycoscience 51:421-431.
Zhong, S., Zhang, J., and Zhang, G.-Z. 2019. Botrytis polyphyllae: A new
Botrytis species causing gray mold on Paris polyphylla. Plant Dis. 103:
1721-1727.
Zhou, Y. J., Zhang, J., Wang, X. D., Yang, L., Jiang, D. H., Li, G. Q., Hsiang,
T., and Zhuang, W. Y. 2014. Morphological and phylogenetic identification
of Botrytis sinoviticola, a novel cryptic species causing gray mold disease
of table grapes (Vitis vinifera) in China. Mycologia 106:43-56.