Persoonia 25, 2010: 50 – 60
www.persoonia.org
OPINION ARTICLE
doi:10.3767/003158510X548668
A case for re-inventory of Australia’s plant pathogens
K.D. Hyde1,5, P. Chomnunti1, P.W. Crous2,6, J.Z. Groenewald2, U. Damm2,
T.W. Ko Ko1, R.G. Shivas3, B.A. Summerell4, Y.P. Tan3
Key words
disease associated fungi
disease threats
molecular phylogeny
quarantine
taxonomy
Abstract Australia has efficient and visible plant quarantine measures, which through various border controls and
survey activities attempt to prevent the entry of unwanted pests and diseases. The ability to successfully perform
this task relies heavily on determining what pathogens are present and established in Australia as well as those
pathogens that are exotic and threatening. There are detailed checklists and databases of fungal plant pathogens
in Australia, compiled, in part, from surveys over many years sponsored by Federal and State programmes. These
checklists and databases are mostly specimen-based, which enables validation of records with reference herbarium
specimens and sometimes associated cultures. Most of the identifications have been based on morphological
examination. The use of molecular methods, particularly the analysis of DNA sequence data, has recently shown
that several well-known and important plant pathogenic species are actually complexes of cryptic species. We
provide examples of this in the important plant pathogenic genera Botryosphaeria and its anamorphs, Colletotri­
chum, Fusarium, Phomopsis / Diaporthe and Mycosphaerella and its anamorphs. The discovery of these cryptic
species indicates that many of the fungal names in checklists need scrutiny. It is difficult, and often impossible, to
extract DNA for sequence analysis from herbarium specimens in order to validate identifications that may now be
considered suspect. This validation can only be done if specimens are recollected, re-isolated and subjected to DNA
analysis. Where possible, herbarium specimens as well as living cultures are needed to support records. Accurate
knowledge of the plant pathogens within Australia’s borders is an essential prerequisite for the effective discharge
of plant quarantine activities that will prevent or delay the arrival of unwanted plant pathogens.
Article info Received: 1 November 2010; Accepted: 14 November 2010; Published: 1 December 2010.
Introduction
Most records of plant pathogenic fungi in Australia are derived
from, and substantiated by, dried herbarium specimens and
relatively few are based on living cultures. There are several
reasons for this including, i) many groups of pathogens are
obligate and cannot be cultured; ii) many pathogens can be
identified with confidence in situ based on morphology and
thus cultures are not necessary for diagnosis; iii) living cultures
are often difficult to preserve, especially over time and may
loose their ability to sporulate or retain pathogenicity or other
physiological properties; iv) maintaining living cultures is relatively costly; and v) isolation of a presumptive causal organism
does not demonstrate pathogenicity unless Koch’s postulates
are fulfilled. As an example, consider that most plant disease
surveys in northern Australia (Hyde & Alcorn 1993, Shivas
1995, Shivas & Alcorn 1996), and neighbouring countries of
Papua New Guinea (Hyde & Philemon 1994) and Irian Jaya
(Shivas et al. 1996), often as part of the Northern Australian
School of Science, Mae Fah Luang University, 333 M. 1. T. Tasud Muang
District, Chiang Rai 57100, Thailand;
corresponding author e-mail: [email protected].
2
CBS-KNAW Fungal Biodiversity Centre, Uppsalalaan 8, 3584 CT Utrecht,
The Netherlands.
3
Plant Pathology Herbarium, Agri-Science Queensland, Ecosciences Precinct, Dutton Park, Queensland 4012, Australia.
4
Royal Botanic Gardens and Domain Trust, Mrs Macquaries Rd, Sydney,
NSW 2000, Australia.
5
King Saud University, College of Science, Botany and Microbiology Department, P.O. Box 2455, Riyadh 1145, Saudi Arabia.
6
Microbiology, Department of Biology, Utrecht University, Padualaan 8, 3584
CH Utrecht, and Wageningen University and Research Centre (WUR),
Laboratory of Phytopathology, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands.
1
Quarantine Strategy (NAQS), were based almost entirely on
herbarium specimens. The NAQS surveys often focused on
remote parts of these regions, looking for early signs of pest
and disease incursions. The remoteness of many locations
meant that facilities were not available to obtain and look after
cultures. Furthermore, the scientists themselves were often
not allowed to move specimens that might harbour living and
exotic pathogens, particularly if the specimens were collected
offshore.
The importance of maintaining accurate records of pathogens
in Australia is their value in determining those pathogens that
are not present (exotic) and potentially a threat if introduced,
through a process known as pest risk assessment (Plant
Health Australia 2010). The aim of quarantine in Australia is to
prevent entry of exotic pests, diseases and weeds that could
have serious environmental and economic consequences if
introduced. For example, the cost of introducing some exotic
plant diseases, e.g. Karnal bunt of wheat, into Australia could
cost billions of dollars (http://www.dfat.gov.au/facts/quarantine.
html). Several island countries, including Australia, New Zealand, and the Philippines, through their isolation have avoided
the introduction of many important exotic threats.
Specimen-based records of most of the plant pathogens that
occur in Australia can be accessed through the Australian Plant
Disease Database and the Australian Plant Pest Database
(Shivas et al. 2006). Both of these important databases are
username and password protected which limits their availability. These databases, together with the three large Australian
herbaria of plant pathogens that underpin them, are important
resources for resolving quarantine issues and facilitating the
pest risk assessment process.
© 2010 Nationaal Herbarium Nederland & Centraalbureau voor Schimmelcultures
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51
K.D. Hyde et al.: Plant pathogens in Australia
Prior to the availability of DNA sequence data, the identification
of plant pathogenic fungi was primarily based on morphology,
with herbarium specimens serving as proof of identity for future
reference. The relatively recent application of molecular phylogenetic analysis to species identification has revealed that many
traditionally accepted species actually represent complexes
of species. This is especially true for many important plant
pathogenic genera such as anamorphic Mycosphaerellaceae
(including Cladosporium), Botryosphaeria and its anamorphs,
Colletotrichum, Fusarium, Guignardia with its Phyllosticta
anamorphs, and Diaporthe with its Phomopsis anamorphs
(Crous et al. 2006, 2009a – c, Damm et al. 2007, Alves et al.
2008, Cai et al. 2009, Hyde et al. 2009a, b, Kvas et al. 2009,
Phillips et al. 2008, Shivas & Tan 2009, Wulandari et al. 2009,
Zhang et al. 2009, Schoch et al. 2009, Phoulivong et al. 2010,
Summerell et al. 2010, Walsh et al. 2010). As a result of these
recent advances many of the taxa listed in the aforementioned
Australian checklists and databases of fungi associated with
plant diseases are now outdated. There is a pressing need to
address this problem. The purpose of this paper is to provide
selected examples where there is a need to carry out a re-inventory of the fungal pathogens of plants in Australia so that the
checklist and databases are both accurate and up to date.
MaterialS and methods
Selected sequences from five plant pathogenic fungal genera
were downloaded from GenBank and aligned using either Clustal X or the online MAFFT server (http://mafft.cbrc.jp/alignment/
server/index.html). The alignments were optimised manually
to allow maximum alignment and maximum sequence similarity. Gaps were treated as missing data or fifth character states
(Mycosphaerella and Phomopsis alignments). Phylogenetic
analyses were carried out based on the aligned dataset using
PAUP v4.0b10 (Swofford 2003). Ambiguously aligned regions
were excluded from all analyses, where present. Trees were
inferred using the heuristic search option with TBR branch
swapping and 100 –1 000 random sequence additions. Maxtrees were unlimited, branches of zero length were collapsed,
and all multiple parsimonious trees were saved. Trees were
drawn in TreeView (Page 1996).
RESULTS AND DISCUSSION
Botryosphaeriaceae and its anamorphs
Several Botryosphaeria species and their anamorphs, such
as Lasiodiplodia theobromae, were identified during NAQS
quarantine surveys of plant disease associated fungi of northern
Australia (Hyde & Alcorn 1993, Shivas 1995, Shivas & Alcorn
1996). However, several recent studies have shown that species of Botryosphaeria such as B. dothidea and anamorph
taxa such as Lasiodiplodia theobromae are species complexes
(Alves et al. 2008, Phillips et al. 2008, Abdollahzadeh et al.
2010). Botryosphaeria dothidea was epitypified by Slippers et
al. (2004) with a specimen from Prunus sp. collected on the
Italy-Switzerland border. The taxon has proved to be a complex
comprising several species (Smith et al. 2001, Denman et al.
2003, Slippers et al. 2004). Several other Botryosphaeria species and related anamorphs have also been epitypified (see Fig.
1 in black bold) and this has led to advances in understanding
the genus (Crous et al. 2006, Alves et al. 2008, Phillips et al.
2008). By epitypifying these taxa with living cultures it is now
possible to compare recent collections with that of the type to
establish whether they are the same species. This is necessary
for all diseases for which Botryosphaeria and its anamorphs
are linked to establish accurate disease records.
In Fig. 1 we present a phylogramme comprising 59 ITS sequences downloaded from GenBank including 17 named as
Botryosphaeria dothidea with its epitype sequence highlighted
in red. Sequences from ex-type strains of Neofusicoccum aus­
trale (= B. australis; Crous et al. 2006), N. luteum (= B. lutea),
Diplodia seriata (= B. obtusa; Phillips et al. 2007), N. parvum
(= B. parva), N. ribis (= B. ribis), D. mutila (= B. stevensii), ‘Bot­
ryosphaeria’ tsugae, Lasiodiplodia crassispora, L. gonubensis
and Phaeobotryosphaeria porosa (= Diplodia porosa; Phillips
et al. 2008) are also included. Although the majority of Botryo­
sphaeria dothidea strains cluster around the type sequence
in the upper part of the tree, there are five disparate strains
scatted in the lower part of the tree. This suggests that there
are likely to be many sequences for B. dothidea in GenBank
with wrongly applied names. We do not show the data here
but there are similar situations for Botryosphaeria rhodina and
Lasiodiplodia theobromae. These taxa have not been epitypified
and at present we do not know which strain in GenBank (if any)
represents B. rhodina or L. theobromae, although this situation
is likely to be solved in a future publication (A.J.L. Phillips pers.
comm.). Besides the problem with wrongly applied names in
GenBank, very few of the GenBank sequences are based on
Australian specimens and therefore they need to be recollected,
sequenced and checked against verified or typified names.
Specific examples of erroneous names concern the species of
Botryosphaeria that cause disease of palms. Recent studies in
Thailand have shown some species belong to Neodeightonia,
a genus that is quite similar to Botryosphaeria (Phillips et al.
2008, Liu et al. in press). Therefore it is essential that every
Botryosphaeria-like species associated with disease of palms
should be re-assessed and this should also be the case with
other hosts.
Colletotrichum
The anamorphic ascomycete genus Colletotrichum contains
many well-known plant pathogens that cause a range of diseases worldwide (Crouch & Beirn 2009, Crouch et al. 2009, Damm
et al. 2009, Hyde et al. 2009a, b). MycoBank currently contains
676 records of Colletotrichum (www.mycobank.org), while only
66 species names are in current use (Hyde et al. 2009a). Cai
et al. (2009) outlined a polyphasic approach for studying Col­
letotrichum and provided a backbone tree comprising 42 ex-type
ITS sequences. Many ubiquitous Colletotrichum species have
now been shown to be species complexes containing numerous cryptic species. For example, Colletotrichum acutatum
s.lat. has been shown to contain discrete morphological and
molecular groups that represent discrete species as found in
some Australian isolates (Shivas & Tan 2009).
Perhaps the most commonly known species in the genus is
Colletotrichum gloeosporioides (teleomorph Glomerella cin­
gulata), which is represented in Australian collections by more
than 5 000 specimens from several hundred host plant species
in about 100 different plant families. Very little is known about
whether these fungal records represent saprobes, weak or opportunistic pathogens, or genuine pathogens. It is possible that
many of these records are misidentified as the morphological
characteristics that define C. gloeosporioides are unreliable or
even misleading, i.e. having cylindrical conidia with rounded
ends, and less than 4.5 µm wide according to the widely used
key by Sutton (1980). Cannon et al. (2008) epitypified C. gloeosporioides; conidia of the ex-epitype strain are on average
wider, measuring 14.4 × 5.6 µm. The species had been synonymised by von Arx (1957) with about 600 names, some of
which might represent discrete species.
Because of the morphological similarities between C. gloeospo­
rioides and other Colletotrichum species, the close relationship
between species within the C. gloeosporioides species complex
52
Persoonia – Volume 25, 2010
FJ824768 Guignardia philoprina
AY639595 Lasiodiplodia gonubiensis
64
91 HM346877 Lasiodiplodia theobromae
HM346880 Lasiodiplodia theobromae
DQ103550 Lasiodiplodia crassispora
EU673338 Neodeightonia phoenicum
98
EU673339 Neodeightonia phoenicum
67
EU673340 Neodeightonia phoenicum
AY259108 Botryosphaeria corticola
AY343379 Diplodia porosum
DQ458889 Botryosphaeria obtusa
96
AY259094 Botryosphaeria obtusa
FJ171717 Botryosphaeria obtusa
97 DQ458888 Botryosphaeria tsugae
53
AF243405 Botryosphaeria tsugae
AY236955 Botryosphaeria stevensii
54
AY259093 Botryosphaeria stevensii
84
EU919693 Diplodia mutila
61
EU919690 Diplodia mutila
100
AF246930 Botryosphaeria mamane
EU520213 Botryosphaeria berengeriana
AF027750 Botryosphaeria dothidea
AY343415 Botryosphaeria dothidea
77
AY236949 Botryosphaeria dothidea
GQ355867 Botryosphaeria dothidea
AF027749 Botryosphaeria dothidea
73 AY786322 Botryosphaeria dothidea
FJ755237 Neofusicoccum mediterraneum
GQ865693 Botryosphaeria dothidea
AB454278 Botryosphaeria dothidea
EU520184 Botryosphaeria ribis
67
FJ755201 Botryosphaeria dothidea
FJ755210 Diplodia pinea
AY744378 Botryosphaeria dothidea
GU944810 Botryosphaeria dothidea
96 AY573213 Botryosphaeria iberica
AY573212 Botryosphaeria sarmentorum
AY573202 Botryosphaeria iberica
79
84 AY339262 Botryosphaeria australis
AY236946 Botryosphaeria lutea
67 AY259091 Botryosphaeria lutea
AY662403 Botryosphaeria dothidea
90
AF452701 Botryosphaeria dothidea
AF452705 Botryosphaeria dothidea
AY343381 Fusicoccum viticlavatum
AY343383 Fusicoccum vitifusiforme
AF027743 Botryosphaeria ribis
AY236935 Botryosphaeria ribis
AF027741 Botryosphaeria dothidea
77 AF241177 Botryosphaeria ribis
1 change
AY236936 Botryosphaeria ribis
AF027742 Botryosphaeria dothidea
AF243395 Botryosphaeria parva
AY236939 Botryosphaeria parva
Fig. 1 Phylogramme generated from maximum parsimony analysis based on ITS
AY236937 Botryosphaeria parva
sequences, showing the phylogenetic relationships of B. dothidea with other species of
AY236942 Botryosphaeria parva
Botryosphaeria, those in yellow highlight are wrongly applied names. Values above the
branches are parsimony bootstrap (> 50 %). Ex-type strains are shown in bold.
K.D. Hyde et al.: Plant pathogens in Australia
53
AF017651 Phaeoacremonium aleophilum
GU227800 C. lindemuthianum
EU400138 C. gloeosporioides
EU400137 C. gloeosporioides
EU697200 C. gloeosporioides
GU222380 C. gloeosporioides
GQ924908 C. gloeosporioides
AJ301979 C.
C gloeosporioides
FJ172237 G. cingulata
GQ495615 C. gloeosporioides
100
AJ311878 C. gloeosporioides
HM241948 C. gloeosporioides
87 AY841136 C. gloeosporioides
FJ172225 C. gloeosporioides
AJ301980 C. gloeosporioides
79
EF608055 C.
C gloeosporioides
96 DQ286132 C. acutatum
EU520250 C. gloeosporioides
88
EU520113 C. gloeosporioides
80
96 AB470867 C. gloeosporioides
88
AJ301972 C. gloeosporioides
EU520089 C. gloeosporioides
GU227862 C. truncatum
100
AY266371 C.
C gloeosporioides
l
i id
EF025966 C. gloeosporioides
79 AB051400 C. boninense
HM052822 C. gloeosporioides
92
HM222947 C. gloeosporioides
AY841135 C. gloeosporioides
76
FJ481122 C. gloeosporioides
94
HM467830 C. gloeosporioides
C gloeosporioides
l
i id
98 AY266404 C.
HM852073 C. gloeosporioides
HM997128 C. gloeosporioides
AY266402
C. gloeosporioides
98
AY177330 C. gloeosporioides
AJ536229 C. gloeosporioides
EU371022 C. gloeosporioides
GU223175 G. cingulata
g
GU223180 G. cingulata
DQ991736 G. cingulata
EU358946 G. cingulata
5 changes
AY266389 C. gloeosporioides
GU222379 C. gloeosporioides
FJ972603 C. fructicola
EU008845 C. gloeosporioides
Colletotrichum
GQ120492
Q
C. g
gloeosporioides
p
AY177329 C. gloeosporioides
gloeosporioides
AY902476 C. gloeosporioides
species complex
AY714052 C. gloeosporioides
HM13151 C. jasmini-sambac
GQ485600 C. hymenocallidis
AF451905 C. gloeosporioides
GQ329690 C. horii
92
GU174550 C. kahawae
Fig. 2 The first of 8 900 equally most parsimonious trees obtained
DQ991734 G. cingulata
from a heuristic search with 100 random taxon additions of an
GU174551 C. xanthorrhoeae
ITS alignment for Colletotrichum (PAUP v4.0b10). Bootstrap supDQ991735 G. cingulata
port values > 69 % are shown at the nodes and strict consensus
EU697014 G. cingulata
branches are thickened and type sequences are in bold. GenBank
EU697201 C. gloeosporioides
accessions of C. gloeosporioides and Glomerella cingulata are
EF025938 C. gloeosporioides
indicated in blue colours. Tree length = 431, CI = 0.719, RI = 0.903
GU233807 C. gloeosporioides
and RC = 0.649.
92
and the only recent epitypification, most of the sequences
lodged in GenBank as C. gloeosporioides are doubtful and
belong to many different species. As demonstrated in Fig. 2,
ITS sequences lodged in GenBank as C. gloeosporioides and
G. cingulata are found throughout the C. gloeosporioides species complex and outside the C. gloeosporioides complex, the
latter applies to more than 100 of the about 750 ITS sequences
of C. gloeosporioides in GenBank. Furthermore, Fig. 2 shows
the difficulty of species recognition within the C. gloeosporio­
ides species complex using ITS sequences only. Only a few
of these GenBank sequences were derived from specimens
from Australia.
The C. gloeosporioides aggregate is currently the subject of
intensive phylogenetic analysis and Hyde et al. (2009a) noted
54
Persoonia – Volume 25, 2010
Togninia novae-zealandiae AY179946
AY485771
97 FJ790866
EU851107
86
EU851108
EU851109
AF230751
AY485762
FJ790863
AY662404
AY485768
AY485763
AY485785
Phomopsis viticola
Diaporthe perjuncta
100 AJ312352 Diaporthe helianthi
10 changes
AF046906 Diaporthe ambigua
FJ228187 Diaporthe helianthi
88 AF230744
Diaporthe
AJ458386 Diaporthe perjuncta
australafricana
AJ458385 Diaporthe perjuncta
100 AY485750
HQ166424
FN386282
Diaporthe viticola
99 GQ250200
GQ250199
AY485751
99 AJ312361 Diaporthe meridionalis
DQ286275 Diaporthe aspalathi
AJ312360 Diaporthe phaseolus var. caulivora
FJ441612 Diaporthe helianthi
FJ009524 Phomopsis theicola
FJ441631 Phomopsis theicola
FJ904853 Phomopsis theicola
FJ009526 Phomopsis theicola
AB470863 Phomopsis viticola
DQ286287 Phomopsis theicola
DQ286288 Phomopsis theicola
DQ286286
Phomopsis theicola
71 CBS 187.27
GQ281809
HM575422
Diaporthe neotheicola
GQ250192
EU814480
AF358435
100
AY705840
AY705842
Diaporthe helianthi
72 AJ312364
AY705844
95
AY705843
AF230749 Phomopsis vitimegaspora
AJ312351 Diaporthe helianthi
AY745993 Diaporthe helianthi
100 AY746005 Diaporthe helianthi
AJ312348 Diaporthe helianthi
90
AY485749 Diaporthe helianthi
AY339322
Phomopsis cuppatea
100 DQ286283
EU888929 Diaporthe helianthi
FJ441611 Diaporthe helianthi
100 AJ312356 Diaporthe helianthi
EU878427 Diaporthe helianthi
AY705839 Diaporthe helianthi
AJ312357 Diaporthe helianthi
99 AJ312359 Diaporthe phaseolus var. soyae
AF230767
AJ312349 D. helianthi
DQ286270
Diaporthe
100 DQ286268
ambigua
EU814479
HM575420
HM575419
EU814478
AJ312353 D. helianthi
Fig. 3 The first of 319 equally most parsimonious trees obtained from a heuristic search with 100 random taxon additions of an ITS alignment for Phomopsis
(PAUP v4.0b10). Bootstrap support values > 69 % are shown at the nodes and strict consensus branches are thickened and type sequences are in bold.
Names of paraphyletic species are indicated in different colours and clades containing the type sequences of these paraphyletic species are indicated with a
coloured bar corresponding to the colour of the species name. Tree length = 568, CI = 0.583, RI = 0.876 and RC = 0.511.
K.D. Hyde et al.: Plant pathogens in Australia
that it was likely a series of well-supported monophyletic (though
not host-specific) clades may be identified. This research has
resulted in several publications revealing, describing or typifying
species within the C. gloeosporioides species complex (Shivas
& Tan 2009, Yang et al. 2009, Phoulivong et al. 2010, Rojas
et al. 2010, Weir & Johnston 2010). The taxon was previously
considered as a pathogen of many tropical fruits, causing
anthracnose (Holliday 1980). Phoulivong et al. (2010) isolated
Colletotrichum species from anthracnose symptoms of eight
tropical fruits in Laos and Thailand and none of these isolates
was C. gloeosporioides. This illustrates the need to re-investigate the Colletotrichum species in Australia using molecular
data to establish which species occur in this country.
Diaporthe/Phomopsis
The anamorphic ascomycete genus Phomopsis contains about
1 000 species names (Uecker 1988) with teleomorphic connections in Diaporthe for about 180 species (van der Aa & Vanev
2002). Phomopsis spp. are widespread and occur on a diversity
of host plants as pathogens, endophytes and saprobes (Uecker
1988). Plant pathogenic species cause serious diseases of
many cultivated plants worldwide, including grapevines (van
Niekerk et al. 2005), sunflower (Gulya et al. 1997), strawberry
(Maas 1998), and soybean (Li et al. 2010). Interest in Phomop­
sis has also focused on the secondary metabolites produced
by some endophytic and saprobic forms. Two examples are
given. Firstly, Diaporthe toxica is known to produce toxic meta­
bolites, phomopsins, on infected Lupinus stubble or seed,
which can result in the death of grazing animals (Peterson et
al. 1987, Cowley et al. 2010). Secondly, strains of endophytic
Phomopsis from healthy plants have been shown to produce
taxol, which has strong cytoxicity towards human cancer cells
(Kumaran & Hur 2009).
Species delimitation in Phomopsis has been traditionally based
on host association as morphological characters are few and
not reliable, for example, most species do not produce β-conidia
or the teleomorph in culture (Rehner & Uecker 1994). Increasingly molecular phylogenies, especially those derived from the
sequences of the internal transcribed spacer (ITS) region of the
ribosomal DNA have been used to identify species (Mostert et
al. 2001, van Niekerk et al. 2005, van Rensburg et al. 2006,
Santos & Phillips 2009, Ash et al. 2010). Fig. 3 shows an ITS
phylogeny consisting of 72 sequences (including the outgroup
sequence) obtained from NCBIs GenBank nucleotide database.
A total of 489 characters were used in the analysis, of which
134 characters were parsimony informative, 267 were constant
and 88 variable characters were parsimony uninformative. The
tree clearly illustrates the confusion around the application of
species names such as Diaporthe ambigua and D. helianthi.
In Australia, specimens of Phomopsis deposited in the major
plant pathology herbaria are mostly not identified to species
level. The reason for this is that the species concept in Pho­
mopsis needs modernisation, particularly in light of additional
biological, biochemical and molecular data (van der Aa & Vanev
2002). Discarding the host-based species concept is the first
step in the development of a useful and reliable classification for
Phomopsis. This needs to be followed by a major international
collaborative effort, as is happening in Botryosphaeria, Colleto­
trichum and Fusarium, to develop a reliable taxonomy.
Fusarium
Fusarium contains some of the most damaging plant pathogenic
fungi as well as species that are important toxin producers and
human pathogens (Desjardin 2006, Leslie & Summerell 2006).
It is also one of the most actively researched groups of fungi
and consequently the taxonomic concepts of many of the key
55
plant pathogens have changed dramatically over the past two
decades (Leslie & Summerell 2006). Added to this there have
been many new species of Fusarium described from a diversity
of environments and host substrates, including a number from
Australia, e.g. F. aywerte and F. nurragi (Benyon et al. 2000),
F. babinda (Summerell et al. 1995), F. beomiforme (Nelson et
al. 1987), F. gaditjirri (Phan et al. 2004), F. lyarnte and F. wer­
rikimbe (Walsh et al. 2010). Like the other genera described
above, Fusarium has been shown to be rich in cryptic species,
and while some may argue that cryptic speciation is of interest
only to taxonomists and evolutionary biologists in Fusarium
these species have clearly been demonstrated to have critical
importance to plant pathologists, plant breeders and quarantine
officials.
Several species provide good examples of the problems in
Fusarium. Stalk rot of maize is caused by F. verticillioides but
much of the literature and most of the specimens in Australian
collections will use the name F. moniliforme. This latter name we
now know refers to at least three species currently described,
namely F. verticillioides, F. thapsinum and F. andiyazi (Seifert et
al. 2003, Leslie et al. 2005) with a number of undescribed taxa
known; all are morphologically identical but differ biologically,
ecologically and phylogenetically. We now know that F. verticil­
lioides causes stalk rot of maize and produces the mycotoxin
fumonisin, F. thapsinum causes stalk rot of sorghum and does
not produce fumonisin, but does produce other less important
toxins and F. andiyazi causes some disease in sorghum (Les­
lie et al. 2005). Clearly in this case accurate identification is
critical because of the implications to crop and human health.
An even more complex situation occurs within a large group of
species previously described as F. subglutinans. Fig. 4 shows a
phylogenetic tree comprised of 72 translation elongation factor
sequences sourced from GenBank of species either named
as F. subglutinans or previously called F. subglutinans and
those species closely related in the Gibberella fujikuroi clade.
This tree highlights the diversity that exists within this species
concept and how names are wrongly applied to data present in
GenBank, and also demonstrates the confusion that surrounds
a number of the species complexes within Fusarium, especially
when using data sourced from databases such as GenBank.
Detailed phylogeny-based investigations of the previously broad
species concept that applied to F. subglutinans have shown
it to include more than 20 species (Steenkamp et al. 2002,
Leslie & Summerell 2006) of some extremely important plant
pathogens including F. sacchari, F. circinatum and F. mangiferei;
the latter two being of high importance to Australia as pathogens of quarantine importance. Several other species such as
F. oxysporum (Wang et al. 2004), F. solani (O’Donnell 2000),
F. dimerum (Schroers et al. 2009) and F. graminearum (O’Don­
nell et al. 2004) have been shown to be quite diverse species
complexes and the impact of these studies on the identity of
cultures in the collections still awaits to be explored.
Unfortunately, none of the major plant pathogen reference
collections or major research collections of Fusarium has
completed a full analysis of their holdings and as such urgently
need review to determine the status of the isolates held. The
preliminary analyses that have been done using DNA based
techniques have shown that there is considerable diversity held
in these collections that are not reflected in the lists of species
present in Australia and as such it is difficult to determine the
quarantine status of many species of Fusarium. A checklist
including plant pathogenic and quarantine status of Fusarium
in Australia has been prepared (Summerell et al. in press) and
this will provide a basis on which to analyse the species found
in collections in Australia.
56
Persoonia – Volume 25, 2010
AF008513 Fusarium sp. NRRL 22903
AF008485 Fusarium oxysporum f.sp. canariensis NRRL 26035
AF160268 Fusarium sp. NRRL 25221
AF160278 Fusarium sacchari NRRL13999
AF160302 Fusarium sp. NRRL 26064
99
AF160274 Fusarium phyllophilum NRRL 13617
56
AF160275 Fusarium udum NRRL 22949
AF160271 Fusarium pseudocircinatum NRRL 22946
AF160270 Gibberella thapsina NRRL 22045
63
97 DQ837698 Fusarium subglutinans
AF160273 Fusarium nygamai NRRL 13488
AF160272 Fusarium lactis NRRL 25200
AF160309 Fusarium sp. NRRL 26793
67
EU091074 Fusarium subglutinans
AF160304 Fusarium sp. NRRL 25615
94
AF160266 Fusarium napiforme NRRL 13604
AF160267 Fusarium ramigenum NRRL 25208
99
AF160263 Fusarium pseudonygamai NRRL 13592
59
100
AF160265 Fusarium brevicatenulatum NRRL 25446
AF160264 Fusarium pseudoanthophilum NRRL 25206
AF160277 Fusarium dlaminii NRRL 13164
100
94 AF160303 Fusarium sp. NRRL 26061
AF160306 Fusarium sp. NRRL 26152
97
AF160281 Fusarium sp. NRRL 25226
50
AF160286 Fusarium sp. NRRL 26427
78
98 AF160283 Fusarium sp. NRRL 25303
AF160282 Fusarium concentricum NRRL 25181
AF160284 Fusarium sp. NRRL 25309
71
AF160287 Fusarium sp. NRRL 26794
AF160288 Fusarium sp. NRRL 28852
88
AF160279 Gibberella fujikuroi NRRL 13566
100
85
AF160285 Fusarium globosum NRRL 26131
AF160280 Fusarium proliferatum NRRL 22944
AF160269 Fusarium denticulatum NRRL 25302
AF160276 Fusarium acutatum NRRL13308
53
AF160296 Fusarium sp. NRRL 25346
82
85 AF160307 Fusarium sp. NRRL 26756
99
AF160308 Fusarium sp. NRRL 26757
AY337444 Fusarium subglutinans
AY337431 Fusarium subglutinans
10 changes
HM067691 Fusarium subglutinans
99 AF160289 Fusarium subglutinans NRRL 22016
HM347131 Fusarium subglutinans
AF160289 Fusarium subglutinans
HM057336 Fusarium subglutinans
AF160290 Fusarium bactridioides NRRL 20476
AF160291 Fusarium succisae NRRL 13613
59
AF160292 Fusarium anthophilum NRRL 13602
AF160294 Fusarium bulbicola NRRL 13618
84 EU574683 Fusarium sp. CML 1021
EU574684 Fusarium sp. CML 1039
58
EU574680 Fusarium sp. CML 383
98
AF160305 Fusarium sp. NRRL 25807
AF160300 Fusarium sp. NRRL 25623
AF160298 Fusarium sp. NRRL 25195
EU574681 Fusarium sp. CML 908
AF160297 Fusarium guttiforme NRRL 22945
AF160299 Fusarium sp. NRRL 25204
AF160293 Fusarium begoniae NRRL 25300
EU574682 Fusarium sp. CML 914
AF160295 Gibberella circinata NRRL 25331
80
85 AF160310 Fusarium sp. NRRL 29123
AF160311 Fusarium sp. NRRL 29124
AY337443 Fusarium subglutinans
HM067690 Fusarium sp. JS-2010
FJ966229 Fusarium subglutinans
100
HM067686 Fusarium sp. JS-2010
HM067689 Fusarium sp. JS-2010
67
HM067687 Fusarium sp. JS-2010
AF160301 Fusarium sp. NRRL 25622
Fig. 4 One of 5 000 most parsimonious trees (CI = 0.656, RI = 0.853, RC = 0.559, HI =
HM067688 Fusarium sp. JS-2010
0.4463) of the Gibberella fujikuroi species complex inferred from the translation elongaHM067684 Fusarium sp. JS-2010
tion factor-1α gene sequence data. Fusarium sp. NRRL22903 was used as outgroup in
the analysis.
59 HM067685 Fusarium sp. JS-2010
57
K.D. Hyde et al.: Plant pathogens in Australia
Cladosporium bruhnei EF679337
100 AY260085 Leucadendron sp.
95
74
10 changes
Mycosphaerella konae
GQ852746 Eucalyptus sp.
EF394842 Eucalyptus camaldulensis
AF309589 Eucalyptus sp.
EU851931 Eucalyptus maidenii
DQ302981 Eucalyptus camaldulensis
100 EU301066 Eucalyptus pellita
Mycosphaerella marksii
EU301063 Eucalyptus pellita
DQ302984 Vepris reflexa
DQ302979 Leucadendron tinctum
Ps. epispermogonia DQ267596 Eucalyptus grandis
EU301078 Eucalyptus sp.
100 EU301075 Eucalyptus sp.
Dissoconium dekkeri
EU301076 Eucalyptus sp.
EU301077 Eucalyptus sp.
100
EU301071 Eucalyptus grandis x E. urophylla
EU301074 Eucalyptus sp.
Dissoconium dekkeri
EU301073 Eucalyptus sp.
99
EU042176 Eucalyptus sp.
AY509763 Eucalyptus globulus
AY725539 Protea magnifica
GQ852738 Eucalyptus globulus
91
Dissoconium commune
AY725537 Eucalyptus cladocalyx
AY725541 Eucalyptus globulus
EU514232 Musa acuminata
DQ302975 Eucalyptus sp.
EU255886 Eucalyptus globulus
Dissoconium dekkeri
89 EU301079 Eucalyptus sp.
AF173309 Juniperus chinensis
AF309625 Eucalyptus grandis
EU255901 Eucalyptus globulus
100 AY725572 Eucalyptus globulus
GQ852809 Eucalyptus globulus
Teratosphaeria nubilosa
GQ852818 Eucalyptus coniocalyx
AY725562 Eucalyptus globulus
99
GQ852806 Acacia auriculiformis
100 AF309622 Eucalyptus sp.
Teratosphaeria cryptica
DQ239971 Eucalyptus globulus
(now called T. xenocryptica)
DQ239971 Eucalyptus globulus
95 AF309623 Eucalyptus globulus
DQ302951 Eucalyptus nitens
89 AY509754 Eucalyptus delegatensis
Teratosphaeria cryptica
74 GQ852798 Eucalyptus globulus
EU301085 Eucalyptus camaldulensis
GQ852794 Eucalyptus globulus
EU301086 Eucalyptus pellita
Teratosphaeria parva
GQ852828 Eucalyptus moluccana
100
AY725579 Eucalyptus dunnii
GQ852832 Eucalyptus dunnii
DQ267589 Eucalyptus sp.
Teratosphaeria suberosa
AY626985 Eucalyptus dunnii
AY045504 Eucalyptus sp.
AY045503 Eucalyptus sp.
EU707874 Protea repens
100 EU707877 Protea nitida
Teratosphaeria parva
EU707875 Eucalyptus globulus
81
GQ852820 Eucalyptus globulus
EF394824 Eucalyptus dunnii
100 EF394828 Eucalyptus tereticornis
EU707858 Protea lepidocarpodendron
Teratosphaeria associata
EF394827 Corymbia variegata
EF394826 Corymbia henryii
EU707857 Protea lepidocarpodendron
Fig. 5 The first of four equally most parsimonious trees obtained from a heuristic search with 100 random taxon additions (PAUP v4.0b10). Bootstrap support values > 69 % are shown at the nodes and strict consensus branches are thickened and type sequences are in bold. Names of paraphyletic species
are indicated in different colours. Green blocks represent species with a wide host range or host jumping between different host genera whereas the yellow
blocks represent those with a wide host range or host jumping across host species (i.e. same genus but different species of the genus). Tree length = 555,
CI = 0.674, RI = 0.952 and RC = 0.641.
58
Mycosphaerella and it anamorphs
The genus Mycosphaerella s.lat. is commonly accepted as the
largest genus of Ascomycetes, containing over 10 000 taxa if
anamorph states are included. Recent studies have shown,
however, that Mycosphaerella is para- and polyphyletic (Hunter
et al. 2006, Schoch et al. 2006, Crous et al. 2007a, b, 2009a–c,
Arzanlou et al. 2007, Batzer et al. 2008), and in fact contains
numerous genera, most of which can only be distinguished
based on their unique anamorphs. In most cases anamorph
genera are now used as holomorph names for these different
clades, and new teleomorph names have not been introduced
in an effort to stop the proliferation of dual nomenclature in
this complex.
Most species in Mycosphaerella s.lat. (incl. Teratosphaeria)
have been described on the assumption that they are hostspecific (Chupp 1954, Corlett 1991, Braun 1995, 1998, Crous &
Braun 2003, Aptroot 2006). Although this assumption holds true
for many species, such as M. fijiensis, M. musicola and M. eu­
musae on banana (Arzanlou et al. 2008) and M. graminicola on
wheat (Stukenbrock et al. 2007), some Mycosphaerella species
are able to colonise different and even unrelated hosts (Crous et
al. 2004b, Crous & Groenewald 2005). Furthermore, examples
are also known of host-specific necrotrophic pathogenic species
of Mycosphaerella and Teratosphaeria that appeared to also
exhibit a facultative saprobic behaviour (Crous et al. 2009a, b).
It is imperative, therefore, that to identify all species occurring
in a specific lesion, DNA techniques are also employed.
For the purpose of this paper, we chose to focus on the host
genus Eucalyptus, which is indigenous to Australia, but also cultivated as exotics in commercial plantations in many countries
of the world. Specific examples of the Mycosphaerella complex
that occur on eucalypts and have a wider host range include
the following: Dissoconium commune (on Eucalyptus in South
Africa, Spain, New Zealand, Musa in Trinidad, Protea magnifica
in Australia) (Crous et al. 2009c), M. konae (Leucospermum in
Hawaii, Eucalyptus in Thailand) (Crous et al. 2007c), M. marksii
(Eucalyptus, Australia, Bolivia, China, Ecuador, Ethiopia, Papua
New Guinea, New Zealand, South Africa, Spain, Tanzania,
Uruguay, Leucadendron on the Madeira Islands, and Musa in
Mozambique) (Arzanlou et al. 2008), Teratosphaeria associata
(Eucalyptus and Protea in Australia) (Summerell et al. 2006,
Crous et al. 2007c), T. parva (Eucalyptus in Australia, Chile,
Ethiopia, Portugal, South Africa, Spain, and Protea in South
Africa), T. nubilosa (Eucalyptus in Australia, New Zealand,
Europe, South America, and Acacia in Thailand (Crous &
Groenewald 2005, Hunter et al. 2009), and Mycosphaerella
citri (Musa in Florida, Acacia in Thailand, and Eucalyptus in
Vietnam, and Aeglopsis, Citrus, Fortunella, Murraya, and Pon­
cirus in North and South America, as well as Asia (Pretorius
et al. 2003, Crous et al. 2004a, b, Crous & Groenewald 2005,
Burgess et al. 2007) (Fig. 5).
Furthermore, to illustrate the complexity of the problem, several
species occurring on eucalypts were initially described from
exotic plantations outside of their native range. These include
M. heimii from Madagascar (Crous & Swart 1995), M. fori and
M. ellipsoidea from South Africa (Crous & Wingfield 1996, Hunter et al. 2006), Teratosphaeria tasmaniensis from Tasmania
(Crous et al. 1998), T. molleriana from Portugal and California
(Crous & Wingfield 1997), Dissoconium dekkeri from Europe
and Africa (de Hoog et al. 1983, Crous & Wingfield 1996), and
T. mexicana from Mexico (Crous 1998), which were only later
reported from Australia (Maxwell et al. 2003, Whyte et al. 2005,
Jackson et al. 2008). Fig. 5 shows an ITS phylogeny consisting
of 119 sequences (including the outgroup sequence) obtained
from GenBank. A total of 447 characters were used in the
analysis, of which 203 characters were parsimony informative,
Persoonia – Volume 25, 2010
230 were constant and 14 variable characters were parsimony
uninformative. Although the taxonomy of Mycosphaerella / Ter­
atosphaeria has been subjected to a concerted effort by several
research groups to clarify species boundaries, the tree clearly
illustrates the confusion around the application of some species names such as Dissoconium dekkeri and Teratosphaeria
parva. Furthermore, species with wider host ranges or involved
in host jumping are also indicated on the tree.
Conclusions
In this paper we have looked at five fungal groups and have
shown that in each case the present knowledge of plant disease associated fungi in these genera is often based on names
that have now been shown to be species complexes. There
are numerous other plant pathogenic genera where recent
publications have revealed that what we thought were species
now comprise species complexes and the species present
in Australia need reassessing. These include Cladosporium
(Crous et al. 2007b, Schubert et al. 2007, Bensch et al. 2010),
Phoma (Aveskamp et al. 2008, 2010, de Gruyter et al. 2009),
Phyllosticta (Wulanderi et al. 2009), and Mycosphaerella and
its anamorphs (Crous 2009). We predict the situation to be the
same in many other plant pathogenic genera such as Alternaria,
Ascochyta, the helminthosporioid genera (including Bipolaris,
Drechslera, Exserohilum, Curvularia and their teleomorphs)
and Pestalotiopsis.
It is evident based on newly emerging molecular data that
checklists of many plant pathogenic genera in Australia are now
outdated and in need of revision. There is an urgent need for
re-assessment of these plant-associated pathogens in order to
preserve the effectiveness of Australia’s biosecurity measures.
Unfortunately, it is often difficult or impossible to extract DNA
from herbarium specimens in order to validate identifications,
and morphology alone cannot always differentiate taxa in
species complexes. Mycologists and plant pathologists need
to go back to the field and recollect specimens from which
fungal pathogens can be isolated and their DNA extracted and
sequenced for the purpose of validating identifications. Revised
checklists and databases must be supported by herbarium
material, living cultures and DNA libraries. In Australia the Bio­
security Bank provides a reference collection of DNA from a
range of agriculturally important plant pathogens and pests for
molecular analyses, linking DNA specimens to voucher specimens for taxonomic verification (www.biosecuritybank.com). It
is only through the combination of molecular and morphological
approaches that the plant pathogens within Australia’s borders
will be reliably identified. This in turn will preserve the effective
role that quarantine plays in keeping unwanted plant pathogens
out of Australia.
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