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MOLECULAR PLANT PATHOLOGY (2012) 13(4), 414–430 DOI: 10.1111/J.1364-3703.2011.00783.X

Review
The Top 10 fungal pathogens in molecular plant pathology

RALPH DEAN 1 , JAN A. L. VAN KAN 2 , ZACHARIAS A. PRETORIUS 3 , KIM E. HAMMOND-KOSACK 4 ,

ANTONIO DI PIETRO 5 , PIETRO D. SPANU 6 , JASON J. RUDD 4 , MARTY DICKMAN 7 ,
REGINE KAHMANN 8 , JEFF ELLIS 9 AND GARY D. FOSTER 10, *
1
Department of Plant Pathology, Fungal Genomics Laboratory, North Carolina State University, PO Box 7251, Raleigh, NC 27695, USA
2
Wageningen University, Laboratory of Phytopathology, Droevendaalsesteeg 1, 6708 PB Wageningen, the Netherlands
3
Department of Plant Sciences, University of the Free State, Bloemfontein 9300, South Africa
4
Department of Plant Pathology and Microbiology, Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, UK
5
Departamento de Genética, Universidad de Córdoba, Campus de Rabanales, Edificio Gregor Mendel C5, 14071 Córdoba, Spain
6
Department of Life Sciences, Imperial College London, South Kensington Campus, London, SW7 2AZ, UK
7
Institute for Plant Genomics and Biotechnology, Department of Plant Pathology and Microbiology, Texas A&M University, College Station, TX 77843, USA
8
Max-Planck-Institut für terrestrische Mikrobiologie, Karl-von-Frisch-Straße 10, D-35043 Marburg, Germany
9
CSIRO-Plant Industry, GPO Box 1600, Canberra, ACT 2601, Australia
10
School of Biological Sciences, University of Bristol, Bristol, BS8 1UG, UK

applications claim that a particular plant virus is of huge impor-

SUMMARY
tance, and this is probably rightly so.
The aim of this review was to survey all fungal pathologists with As a result of the interest generated in this exercise for plant
an association with the journal Molecular Plant Pathology and ask viruses, a similar survey was instigated for plant-pathogenic fungi,
them to nominate which fungal pathogens they would place in a and with a similar mechanism to the virus review. All authors,
‘Top 10’ based on scientific/economic importance. The survey gen- reviewers, editorial board members and senior editors of the
erated 495 votes from the international community, and resulted journal Molecular Plant Pathology, with an interest in fungi, were
in the generation of a Top 10 fungal plant pathogen list for contacted and asked to nominate three plant-pathogenic fungi
Molecular Plant Pathology. The Top 10 list includes, in rank order, they would expect to see in a list of the most scientifically/
(1) Magnaporthe oryzae; (2) Botrytis cinerea; (3) Puccinia spp.; (4) economically important fungal pathogens. The review, by its very
Fusarium graminearum; (5) Fusarium oxysporum; (6) Blumeria nature, is similar in format and layout to the Top 10 virus review
graminis; (7) Mycosphaerella graminicola; (8) Colletotrichum spp.; (Scholthof et al., 2011).
(9) Ustilago maydis; (10) Melampsora lini, with honourable men- The survey generated 495 votes from the international commu-
tions for fungi just missing out on the Top 10, including Phakop- nity, and allowed the generation of a Top 10 fungal plant pathogen
sora pachyrhizi and Rhizoctonia solani. This article presents a short list for the journal Molecular Plant Pathology (see Table 1).
resumé of each fungus in the Top 10 list and its importance, with The fungus making the strongest appearance in the voting
the intent of initiating discussion and debate amongst the plant was Magnaporthe oryzae, in first place with almost double the
mycology community, as well as laying down a bench-mark. It will number of votes of Botrytis cinerea, in second place. All voters
be interesting to see in future years how perceptions change and highlighted the economic importance of M. oryzae; with over
what fungi will comprise any future Top 10. one-half of the world’s population relying on rice as the main
source of calories, this pathogen can have devastating effects;
however, many also highlighted how this pathogen has devel-
oped into a model system for the study of plant–pathogen inter-
actions.
INTRODUCTION Botrytis cinerea, in second place, clearly has an impact in many
Recently, the journal Molecular Plant Pathology considered which areas because of the broad host range, causing severe damage,
viruses would appear in a ‘Top 10’ of plant viruses on the basis of both pre- and post-harvest. It may be one of the few entries in the
their perceived importance, scientifically or economically, in terms Top 10 that can claim a potential beneficial use, through its role in
of the views of the contributors to the journal (Scholthof et al., some aspects of wine production, with some benefits also claimed
2011). This was carried out as many papers, reviews and grant for the ninth entry, Ustilago maydis, in infected cobs.
Puccinia spp., with many voters grouping the three wheat-
infesting rust diseases together, are grouped together in third
*Correspondence: Email: [email protected] position. These fungal pathogens were already a serious disease

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414 MOLECULAR PLANT PATHOLOGY © 2012 BSPP AND BLACKWELL PUBLISHING LTD
 Top 10 fungal pathogens 415

Table 1 Top 10 fungal plant pathogens.

Rank Fungal pathogen Author of fungal description

1 Magnaporthe oryzae Ralph Dean

2 Botrytis cinerea Jan A. L. van Kan
3 Puccinia spp. Zacharias A. Pretorius
4 Fusarium graminearum Kim Hammond-Kosack
5 Fusarium oxysporum Antonio Di Pietro
6 Blumeria graminis Pietro Spanu
7 Mycosphaerella graminicola Jason J. Rudd
8 Colletotrichum spp. Marty Dickman
9 Ustilago maydis Regine Kahmann
10 Melampsora lini Jeff Ellis

The table represents the ranked list of fungi as voted for by plant mycologists associated with the journal
Molecular Plant Pathology.

threat, but have increased in impact with the emergence of race it is clearly a disease that has only recently appeared in certain
Ug99, now posing a serious challenge to wheat production. parts of the world and will potentially increase in importance
In fourth and fifth places are two Fusarium species, but with (Goellner et al., 2010).
contrasting host ranges, with F. graminearum causing significant This review contains single-page descriptions of the Top 10
damage predominantly to cereals and a few noncereal species, plant-pathogenic fungi to introduce the reader to each of them,
and F. oxysporum having a wide host range, with severe losses in with illustrative figures and key references for further reading. The
crops as diverse as tomato, cotton and banana. However, patho- intention of this review is to trigger discussion and debate
gens of cereals continue to have a significant presence in the Top amongst the plant mycology community, as well as to lay down a
10 with Blumeria graminis in sixth position and Mycosphaerella bench-mark, as it will be interesting to see how perceptions
graminicola in seventh. change in future years and which fungi enter and leave the list.
Colletotrichum spp., in eighth position, are members of an
important genus of plant pathogens, for which the taxonomy may
be described as being in a state of flux. The proposed number of
species within the genus ranges from 29 to over 700 depending on
taxonomic interpretation. Colletotrichum spp. have long served as
a model system for hemibiotrophic pathogens, with a short bio-
trophic stage, followed by a switch to tissue ramification and
necrotrophic development.
It is interesting that Ustilago maydis and Melampsora lini make
up ninth and tenth positions, respectively, with many voters indi-
cating strong scientific rather than economic reasons for their
inclusion. Both are now developed as model systems, which are
readily tractable, and provide vital insights into the molecular
basis of plant immunity and infection processes.
Although the aim of this review article was to identify the Top
10 most important plant-pathogenic fungi according to the con-
tributors to Molecular Plant Pathology, we are very much aware
that importance and priorities can vary locally across continents
and disciplines. We are also aware that not all fungi can make it
into any Top 10, because of obvious numerical limits, although
such fungi can still be regarded as hugely important. We therefore
felt it appropriate to cite honourable mentions for fungi just
missing out on the Top 10 list, including Phakopsora pachyrhizi
(Goellner et al., 2010) and Rhizoctonia solani (Gonzalez et al.,
2011; Vilgalys and Cubeta, 1994), both clearly important. In future
years, when another survey of the Top 10 is carried out, it will be
interesting to see whether fungi such as Phakopsora pachyrhizi,
the causal agent of Asian soybean rust, makes an appearance, as

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416 R. DEAN et al.

induce appressoria ex planta and to perform functional analyses of genes by

1. MAGNAPORTHE ORYZAE targeted gene knockout has provided powerful access to many of the under-
lying molecular processes (Leung et al., 1990; Oh et al., 2008). Considerable
Magnaporthe oryzae, a filamentous ascomycete fungus, is the causal agent knowledge has been acquired regarding the perception of environmental
of rice blast disease, the most destructive disease of rice worldwide (Ou, cues (Lee and Dean, 1994), starvation responses (Donofrio et al., 2006), cell
1980). Its importance is underscored by the fact that approximately one-half signalling pathways (Lee and Dean, 1993; Nguyen et al., 2008; Xu and
of the world’s population relies on rice for its primary caloric intake (Khush, Hamer, 1996), turgor pressure generation (deJong et al., 1997), recycling
2005). All foliar tissues are subject to infection; however, infection of the cellular contents (autophagy) (Veneault-Fourrey et al., 2006) and cell cycle
panicle can lead to complete loss of grain. Losses of 10%–30% are typical, checkpoints (Saunders et al., 2010) which regulate and orchestrate the
although regional epidemics can be devastating. In addition, the fungus is development of this specialized cell (Fig. 2).
highly amenable to genetic and molecular genetic manipulation (Jeon et al., Over the last 6 years, following the publication of the genome sequence for
2007; Talbot, 2003; Valent and Chumley, 1991). Consequently, as a result of strain 7-15 (a derivative of Guy11) (Dean et al., 2005), genomic resources for
its agronomic significance and tractability, M. oryzae has emerged as a M. oryzae and related species have grown dramatically and presently include
seminal model in the study of host–fungal pathogen interactions (Dean more than 30 genomes from strains around the globe, as well as various
et al., 2005). Although host resistance is the most economically viable and transcriptome datasets [expressed sequence tags (ESTs) and small RNAs]
environmentally sound practice to manage this disease, the fungus over- (Gowda et al., 2006; Nunes et al., 2011; Oh et al., 2008) and emerging
comes blast resistance quickly, and cultivars typically become ineffective proteome datasets. Early examination of these data revealed dramatic differ-
within 2–3 years (Ou, 1980; Zeigler et al., 1994). Magnaporthe oryzae is part ences in gene content and organization of repetitive elements. Other studies
of a species complex that can cause disease on a variety of grasses and have revealed fundamental insights into host defence and gene silencing
related species, including crops such as barley, wheat and millet (Couch mechanisms (Ikeda et al., 2002; Nguyen et al., 2008). With the emergence of
et al., 2005). New wheat strains have emerged in South America, elevating new sequencing technologies, population biology studies and phylogenomic
concerns that the fungus poses a serious threat to global wheat production analyses of M. oryzae are poised to grow significantly in the very near future,
(Urashima et al., 1993). Knowledge of the biology, genetic diversity and providing deep insight into the evolution of phytopathogenesis.
adaptability of this pathogen is key for the development of novel and durable
strategies to manage this and related devastating fungal diseases (Fig. 1).
The discovery of Guy11, a fertile Mat1-2 strain from French Guiana, more
than 20 years ago stimulated a surge in scientific interest in the rice blast A B
pathogen (Leung et al., 1988; Silué and Notteghem, 1992). The ability to
perform genetic analyses led to the cloning and characterization of several
genes for host and cultivar specificity (Bryan et al., 2000; Jia et al., 2000;
Orbach et al., 2000; Valent et al., 1991). Today, much effort is focused on
cloning and characterizing the many avirulence and corresponding rice
resistance genes that have been genetically identified (Chao and Ellingboe,
1991; Skamnioti and Gurr, 2009). The development of genetic markers, such
as MAGGY, MGR583 and MGR586, from repetitive elements has provided
the means to not only create valuable genetic maps for M. oryzae, but also
the molecular tools to assess population diversity and the evolution of
lineages, valuable knowledge for the breeding and timely release of resistant
cultivars (Farman et al., 1996; Hamer et al., 1989; Nitta et al., 1997; Skam-
nioti and Gurr, 2009).
The early stages of infection have been studied in great depth in Fig. 1 Disease resulting from the infection of rice and wheat with
M. oryzae. Like many fungal plant pathogens, M. oryzae elaborates an Magnaporthe oryzae. (A) Classical symptoms of panicle blast on rice,
appressorium, a specialized infection cell (Howard and Valent, 1996). Appro-
priate development of this cell is required for infection; indeed, several although the fungus can cause disease on all foliar tissues. (B) Head blast on
effective fungicides, such as tricyclazole, which inhibit melanization of the wheat. The symptoms on wheat are typically restricted to the head and can
appressorium, block host penetration (Woloshuk et al., 1983). The ability to be mistaken for wheat scab caused by Fusarium graminearum.

Fig. 2 Infection cycle of the rice blast fungus.

Conidia produced from lesions are splashed
onto new plants where they attach firmly and
germinate within a few hours. Subsequently,
the germ tube ceases polar growth, the tip
swells and, by 12 h, forms a highly melanized
dome-shaped structure, the appressorium.
Typically within 24 h, turgor pressure increases
within the appressorium, forcing a penetration
peg into the underlying tissues. Eye-shaped
necrotic lesions do not appear until several
days after infection, from which, under
appropriate conditions, conidiophores emerge
bearing conidia to re-initiate the infection
cycle. (Scanning electron microscope image in
bottom right courtesy of Nicholas Talbot and
Michael Kershaw, University of Exeter, UK).
[Correction added on 5 July 2012, after online
publication: The bottom right image has been
amended and acknowledgement has been
included in the legend].

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 Top 10 fungal pathogens 417

Botrytis cinerea is an exceptional pathogen, as it may occasionally be

2. BOTRYTIS CINEREA beneficial! Under specific climatic conditions, B. cinerea may cause noble rot
in grape berries, which are used to produce sweet wines (Sauternes, Tokaj).
Botrytis cinerea Persoon: Fries [teleomorph Botryotinia fuckeliana (de Bary) The most prestigious Botrytis wines are sold for prices up to €500/bottle.
Whetzel; Fig. 3], known as grey mould, can infect more than 200 plant Nevertheless, the overall impact of B. cinerea is negative, even in the wine
species. The fungus is considered as a typical necrotroph, which co-opts industry.
programmed cell death pathways in the host to achieve infection (van Altogether, global expenses of Botrytis control (cultural measures, botry-
Baarlen et al., 2007). The genome sequences of two B. cinerea strains failed ticides, broad-spectrum fungicides, biocontrol) easily surmount €1 billion/
to identify ‘silver bullets’, unique features which distinguish it from other annum. The impacts of product loss occurring despite disease control, and
pathogenic and nonpathogenic fungi (Amselem et al., 2011). The availability the quality loss during the retail chain, are likely to be far higher.
of the genome sequence and a variety of molecular tools [ease of transfor-
mation to obtain knockout mutants (van Kan et al., 1997) or to achieve gene
silencing (Patel et al., 2008, 2010)], together with its economic relevance,
have contributed to B. cinerea being the most extensively studied necro-
trophic fungal pathogen. These studies have considerably advanced our
understanding of the infection strategies of B. cinerea, yet only very few
absolutely essential virulence determinants have been identified by candi-
date gene approaches (Tudzynski and Kokkelink, 2009).
Botrytis cinerea is most destructive on mature or senescent tissues of
dicotyledonous hosts. This fungus sometimes remains quiescent for a con-
siderable time before rotting tissues when the host physiology changes and
the environment is conducive (Williamson et al., 2007). Infestation can occur
all the way from the seedling stage until product ripening. Serious damage
can occur following the harvest of seemingly healthy crops. Harvested com-
modities can be spoiled in the retail chain, during storage, transport to
distant markets or during display at the retailer (Fig. 4).
The costs of Botrytis damage are very difficult to estimate because of the
broad host range. Costs are diffuse as Botrytis damage occurs in different
stages of the production and retail chain. No reliable figures are available for
Botrytis damage during crop cultivation, yet it must be huge. In spite of the
increasingly effective application of biocontrol in some crops (Moser et al.,
2008), fungicide application remains the common method to control Botry-
tis. The average cost for chemical Botrytis control (all crops, all countries) is
Fig. 3 Sexual fruiting bodies (apothecia) of the teleomorph Botryotinia
about €40/ha (Steiger, 2007). Fungicides specifically targeted against Bot-
rytis (‘botryticides’) cost €540 million (2001), representing 10% of the world fuckeliana (de Bary) Whetzel.
fungicide market (UIPP, 2002). The wine and table grapes segment represents
50% of the value of the total market for botryticides, with solanaceous
vegetables, cucurbits, strawberries and ornamentals each making up
5%–9% (Steiger, 2007). The costs of broad-spectrum fungicides also effec-
tive against B. cinerea are unknown. Fungicide resistance is an increasingly
problematic issue, with significant proportions of the fungal population
being resistant to fungicides (Leroch et al., 2011). Multidrug resistance has
been reported and is mostly caused by the increased expression of ABC
transporter genes (Kretschmer et al., 2009).
In wine and table grapes, expenses for the control of Botrytis bunch rot
are a major cause of reduction in profit in Australia (AUS $52 million/year;
Scholefield and Morison, 2010), Chile (US$ 22.4 million/year; Esterio et al.,
2009) and South Africa (SA Rand 25 million/year). Estimates for other coun-
tries could not be obtained. These expenses predominantly include the
chemicals, but do not cover the losses experienced by the lack of treatment
(organic farming, low-input farming), failed treatment (fungicide resistance)
or quality loss (fungicide levels exceeding export requirements; grape quality
insufficient for high-quality wines).
In 2002, about 15%–20% of rose and gerbera bunches traded through
Dutch flower auctions contained detectable Botrytis infection, leading to
vase life reduction of such bunches by 3 days. The loss in revenue for rose Fig. 4 Botrytis cinerea on raspberry fruits (from Williamson et al., 2007).
growers alone was estimated at €1.3 million (Vrind, 2005). Such figures do
not include flowers that were infected before harvest and did not make it
to the auction, or flowers that were spoiled during transport to retailers
and became unsellable. Reduction of the shelf life (fruit) or vase life
(flowers) is a serious quality issue. Consumers experience economic loss
when berries rot before they are eaten, or when roses do not last for a
satisfactory period. From an economic perspective, the loss experienced by
consumers is often disregarded because producers and retailers have
obtained income. However, dissatisfied customers may refrain from pur-
chasing the product again for several weeks, an effect difficult to incorpo-
rate into estimates of economic losses. Official figures of the costs of grey
mould in soft fruit and ornamentals must therefore be considered as
underestimates.

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MOLECULAR PLANT PATHOLOGY © 2012 BSPP AND BLACKWELL PUBLISHING LTD MOLECULAR PLANT PATHOLOGY (2012) 13(4), 414–430
418 R. DEAN et al.

3. PUCCINIA SPP.
Three rust diseases occur on wheat, namely stem (black) rust (caused by
Puccinia graminis f. sp. tritici) (Pgt) (Fig. 5), stripe (yellow) rust (P. striiformis f.
sp. tritici) (Pst) (Fig. 6) and leaf (brown) rust (P. triticina) (Pt). Prolific sporu-
lation, efficient dissemination, pathogenic variability and the widespread
cultivation of wheat, often in conducive environments, all contribute to the
destructive potential of these rusts. Historically, stem rust has been most
notorious for damaging wheat crops.The disease was feared in ancient Rome
where rituals (‘Robigalia’) were performed to save crops from rust (Zadoks,
1985).
Pgt, Pst and Pt are obligate, biotrophic basidiomycete fungi with macro-
cyclic, heteroecious life cycles (Bolton et al., 2008; Jin et al., 2010; Leonard
and Szabo, 2005). Obligate biotrophs differentiate specialized infection
structures, efficiently suppress host defence responses and obtain nutrients
through the formation of specialized feeding structures, called haustoria,
which are situated inside plant cells (Voegele and Mendgen, 2011).
Stem rust is frequently perpetuated by repeating uredinial stages on
common and durum wheat, barley and triticale. However, basidiospores can
infect alternative hosts, such as Berberis vulgaris, furnishing primary inocu-
lum for wheat and new virulence combinations as a result of sexual Fig. 5 Stem rust-infected wheat showing uredinial and telial spore stages.
re-assortment of genes (Jin, 2011). The barberry eradication programme in
the USA between 1918 and 1980 (Roelfs, 1982) and in the UK, which also
started in 1918 and continues today, must be viewed as one of the major
achievements in plant pathology, in both scope and disease management.
Significant and repeated crop failures caused by rusts occurred in North
America between 1904 and 1962 (Hodson, 2011; Roelfs, 1985). Serious
epidemics also occurred in Europe and China (Leonard and Szabo, 2005),
with less frequent outbreaks in Eastern Europe, India, Australia, Mexico,
Chile, Ethiopia and South Africa (Hodson, 2011; Pretorius et al., 2007). In
many instances, exotic incursions of wind-borne spores have occurred, estab-
lishing new race lineages (Park, 2007; Singh et al., 2011). Recently, severe
and widespread stripe rust epidemics have been ascribed to new and more
aggressive races adapted to warmer environments (Hovmøller et al., 2011).
The elucidation of the complete Pst life cycle (Jin et al., 2010) and the
genome sequence of this pathogen (Cantu et al., 2011) are significant steps
towards a better understanding of virulence, and thus breeding for durable
resistance.
Early stem rust epidemics initiated studies on pathogenic variability, epi-
demiology and host–pathogen genetics in Pgt (reviewed by Loegering, 1984
and Roelfs, 1985). The specialization of Pgt in different races has impacted
strongly on wheat breeding and production. Numerous cultivars protected by
single genes have become susceptible to stem rust, often with devastating Fig. 6 Wheat flag leaf infected with stripe rust caused by Puccinia striiformis
‘boom-and-bust’ effects (e.g. Jin, 2011; Kolmer et al., 2007; Martens and f. sp. tritici.
Dyck, 1989; Park, 2007; Pretorius et al., 2007).
The occurrence of race Ug99 of Pgt in East Africa with virulence for Sr31
(Pretorius et al., 2000), a commonly used resistance gene, has renewed stem
rust research (Singh et al., 2011). Seven variants within the Ug99 lineage have
been reported, varying in virulence for Sr21, Sr24, Sr31 and Sr36 (Singh et al.,
2011). As a result of its adaptive capacity, fitness and virulence attributes
(90% of the world’s wheat is susceptible), the Ug99 race group has been
recognized as a major threat to food security (Flood, 2010; McIntosh and
Pretorius, 2011; Singh et al., 2011; Vurro et al., 2010).
Together with progress in the detection, genetic mapping and manage-
ment of genes and quantitative trait loci (QTL) conferring resistance to Ug99
(Durable Rust Resistance in Wheat Project, http://www.globalrust.org), sig-
nificant advances are being made in understanding the molecular basis of
pathogenicity in Pgt (Duplessis et al., 2011). Continued research on surveil-
lance and race analysis, coupled with pathogen genomics, will enable the
discovery, characterization and utilization of sustainable management strat-
egies for resistance. The release and adoption of widely adapted resistant
cultivars are essential for future and effective rust control globally (Lowe
et al., 2011; McIntosh and Pretorius, 2011).

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 Top 10 fungal pathogens 419

(Proctor et al., 1995). In the absence of DON, strong host defence responses
4. FUSARIUM GRAMINEARUM are activated in the rachis and hyphal colonization is restricted to the florets
(Jansen et al., 2005). DON synthesis is tightly regulated by at least three
The ascomycete Fusarium graminearum (teleomorph Gibberella zeae), which transcription factors: TRI6, TRI10 and TRI15. An additional 160 pathogenicity/
resides in the order Hypocreales, is a highly destructive pathogen of all cereal virulence factors are now recognized to contribute to cereal floral infection,
species (http://www.scabusa.org). Locally, F. graminearum co-exists and with the majority functioning post-penetration (http://www.phi-base.org;
co-infects with other Fusarium species. The greatest economic losses occur Urban and Hammond-Kosack, 2012).
when the floral tissues become infected (Fig. 7). This disease mainly reduces A recent re-investigation of the biology of the wheat floral infection
grain quality, rather than lowering grain yield, and results in mycotoxin- process has revealed that a considerable phase of symptomless infection
contaminated grain. Worldwide, all the major cereal-growing regions have exists in which hyphae advance extracellularly between the living host cells.
reported a re-emergence of Fusarium epidemics (Leonard and Bushnell, High TRI gene expression is detected at the advancing front and diminishes
2003). During the post-harvest period, if infected cereal grain is stored or thereafter (Brown et al., 2010, 2011). Host cells only die on intracellular
transported at too high a moisture content, post-harvest growth of the hyphal invasion, and extensive degradation of plant cell walls is a relatively
fungus occurs and mycotoxin levels increase (Magan et al., 2010). late process. These findings indicate that F. graminearum uses a stealth
Mycotoxin-contaminated grain is often unsafe for human consumption, approach to facilitate successful floral infections (Fig. 8).
animal feed or malting purposes. In Europe, the USA and other regions, strict
upper limits on specific mycotoxin levels in grain and foods have been
imposed [Commission Regulation (EC) 1881/2006; http://www.scabusa.org].
Fusarium graminearum produces several trichothecene mycotoxins, the most
important of which are deoxynivalenol (DON), acetylated DON derivatives,
nivalenol and the phytoestrogen zearalenone. DON binds to the peptidyl
transferase protein in the ribosome and inhibits protein translation. Different
natural isolates (termed chemotypes) produce different mycotoxin types
(Alexander et al., 2011).
Control of Fusarium floral infections remains problematic. In most cereal
species, the resistance sources identified are only partially effective and are
major QTL based (Buerstmayr et al., 2009). Some azole fungicides are mod-
erately effective, but spray coverage and the timing of applications remain
difficult. Minimizing consecutive cereal crops and ploughing under any
infected residues remain the best methods to reduce disease pressure locally.
Fusarium graminearum infection of noncereal species in the crop rotation is
increasingly being reported, e.g. in soybean and sugar beet.
Excellent genetic, biochemical, molecular genetic, genomic, transcriptomic
and isolate collection resources now exist for F. graminearum (http://
www.scabusa.org, http://www.plexdb.org, http://www.fgsc.net).The genome
lacks repetitive sequences and contains a low level of duplicated genes, but a
high level of polymorphism exists between strains. When aligned to a genetic
map, a ‘two-speed’ genome is recognized, with discrete regions of high
recombination and high single nucleotide polymorphisms (SNPs) located near
telomeres and in the middle of the four large chromosomes. Comparisons with
the sequenced genomes of F. verticillioides and F. oxysporum f. sp. lycopersici
suggest that the high-diversity sites in the F. graminearum genome were the
result of ancestral chromosome fusion events (Cuomo et al., 2007; Ma et al.,
2010).
Direct replacement of a gene of interest with a selectable marker via Fig. 7 The floral tissues of hexaploid wheat severely infected with Fusarium
homologous recombination is now relatively straightforward. The production graminearum. This disease is frequently referred to as Fusarium head blight
of DON mycotoxin contributes to disease formation on wheat floral tissue (FHB), Fusarium ear blight (FEB) or head scab.

LESION CENTRE VISIBLE DISEASE SYMPTOMLESS

Fig. 8 A simplified three-phase model of the numerous dead hyphae extracellular and ADVANCING FRONT
Fusarium graminearum (Fg) infection process lacking cellular contents intracellular hyphae extracellular hyphae
through wheat rachis tissue. At the advancing
hyphal front, deoxynivalenol (DON) mycotoxin
inhibits protein translation, which greatly Wheat rachis cell Wheat rachis cell Wheat rachis cell
suppresses the burst of plant defence responses
(depicted in blue). Once hyphae enter the plant
cells, the presence of the released proteins and
sugars and the high density of fungal hyphae DON DON
lead to a strong activation of plant defence
Fg hyphae Fg hyphae Fg hyphae
responses. Later, within the lesion centre (>10
days), the cellular contents of fungal cells
residing deep within the dead cortical tissue are Most host cells dead, Plant defences activated, High DON production
relocated to the hyphae just below the rachis extensive degradation onset of host cell death suppresses
epidermis and asexual sporulation then occurs. of plant cell walls plant defences

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420 R. DEAN et al.

5. FUSARIUM OXYSPORUM
Fusarium oxysporum Schlecht. is a ubiquitous soil-borne pathogen that
causes vascular wilt on a wide range of plants. Characteristic disease symp-
toms include vascular browning, leaf epinasty, stunting, progressive wilting,
defoliation and plant death (Agrios, 2005). The F. oxysporum species
complex comprises different formae speciales (f. sp.), which collectively
infect more than 100 different hosts, provoking severe losses in crops such as
melon, tomato, cotton and banana, among others (Michielse and Rep, 2009).
Fusarium oxysporum is also an emerging pathogen of humans that can
cause invasive infections in immunocompromised patients (Nucci and Anais-
sie, 2007; O’Donnell et al., 2004).
In contrast with the remarkably broad host range at the species level,
individual isolates of F. oxysporum cause disease only on one or a few plant
species (Armstrong and Armstrong, 1981; Gordon and Martyn, 1997). This
dichotomy has both fascinated and puzzled generations of plant patholo-
gists. Adding to the intrigue, phylogenetic studies suggest that different
isolates of a given forma specialis, infecting the same host plant, have
originated independently during evolution (O’Donnell et al., 1998). Because
F. oxysporum lacks a known sexual cycle, the mechanism through which
these new pathogenic lineages emerged in otherwise distinct genetic back-
grounds has long remained elusive. Recently, analysis of the complete
genome sequence of the tomato pathogenic form F. oxysporum f. sp. lyco-
persici (Fol) has revealed the presence of lineage-specific (LS) genomic
regions, including four entire chromosomes that are absent from other
Fusarium species, such as the cereal pathogens F. graminearum and F. ver-
ticillioides (Ma et al., 2010). Transfer of two LS chromosomes from Fol to a
nonpathogenic isolate enabled it to cause disease on tomato plants. This
suggests that horizontal transfer of small chromosomes could account for
the emergence of new pathogenic lineages (Ma et al., 2010). Genome
sequences from additional F. oxysporum isolates will provide invaluable
tools to further explore this hypothesis.
Dominant plant resistance (R) genes against different races of F. oxyspo-
rum have been identified in several crops (Simons et al., 1998). The interac-
tion between tomato and Fol was used to study the molecular basis of
disease resistance and susceptibility (Houterman et al., 2008, 2009; Rep
et al., 2004). These studies led to the identification of a classical gene-for- Fig. 9 (A) Fusarium oxysporum microconidium (C) germinating on the
gene system with at least three fungal avirulence genes, some of which can surface of a tomato root. Penetration occurs by directed growth of the
function as both elicitors and suppressors of R gene-based plant immunity infectious hypha (IH) towards a natural opening between epidermal root cells
(reviewed in Takken and Rep, 2010).
(penetration site indicated by an arrow). (B) Fusarium oxysporum hypha
The unusual ability of a single Fol isolate to cause disease on both tomato
plants and in immunodepressed mice provides a unique model to study growing in a xylem vessel of a tomato root (from Di Pietro et al., 2001).
trans-kingdom pathogenicity in fungi (Ortoneda et al., 2004). Genetic analy-
sis using targeted mutants has revealed that signalling components which
are essential for the infection of tomato plants, such as a mitogen-activated
protein kinase (MAPK) or a small G-protein, are dispensable for virulence in
mice (Di Pietro et al., 2001; Martinez-Rocha et al., 2008; Ortoneda et al.,
2004). Others, such as the pH response transcription factor PacC, are
required for virulence in the mouse model, but not in plants (Caracuel et al.,
2003; Ortoneda et al., 2004). These results indicate that F. oxysporum
employs fundamentally distinct infection strategies on plants and mammals.
Further studies are addressing the presence of common virulence mecha-
nisms that are required on both types of host.
Recent advances towards an understanding of the genetic basis of
pathogenicity in F. oxysporum include genome-wide insertional mutagen-
esis screens (López-Berges et al., 2009; Michielse et al., 2009a) leading,
among others, to the discovery of a master regulator of pathogenic devel-
opment (Michielse et al., 2009b), the identification of a conserved nitrogen
response pathway regulating invasive growth functions (López-Berges
et al., 2010) and the characterization of a novel mucin-type transmem-
brane sensor (Pérez-Nadales and Di Pietro, 2011). Future studies in the
F. oxysporum system will continue to provide new insights into the
molecular mechanisms of fungal pathogenicity (Fig. 9).

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 Top 10 fungal pathogens 421

perihaustorial matrix and a specialized host membrane (Fig. 11) (Hückelhoven

6. BLUMERIA GRAMINIS and Panstruga, 2011). In common with other obligate biotrophic pathogens,
the haustorium is devoted to the feeding and control of host immunity and
Blumeria graminis is an ascomycete belonging to the Erysiphales (Takamatsu, metabolism (Panstruga and Dodds, 2009). Plant-derived nutrients are trans-
2004). It causes powdery mildews of grasses (Fig. 10), including wheat and ported to hyphae growing on the plant surface. Within 3 days from inocula-
barley, which are amongst the top agricultural crops world-wide (FaoStat, tion, conidiophores develop from specialized foot cells and produce masses of
2011). Mildew infections of cereals reduce grain yield and must be kept in conidia: the eponymous ‘powder’ of these mildews. At the end of the host
check to ensure an economically viable product. Control of Blumeria is growth season, compatible strains mate and produce chasmothecia (Braun
achieved by the deployment of fungicides and disease-resistant plant varie- et al., 2002), which also act as resting structures to survive adverse conditions.
ties. These control measures need to be continually revised, updated and The genomes of barley and other powdery mildews are >120 Mb, i.e.
developed because of the emergence of fungicide resistance, changing regu- much larger than those of related Ascomycota (Spanu et al., 2010). This is
latory constraints and the evolution of mildew strains capable of overcoming caused by an extraordinary proliferation of retrotransposons. Genome
host resistance. expansion is accompanied, on the one hand, by a partial loss of genes
The Erysiphales exhibit a wide range of host specificity, ranging from broad involved in secondary metabolism, carbohydrate degradation and nitrate
polyphagy observed in many of the dicot mildews (Ing, 1990) to the extremely uptake and, on the other, by massive proliferation of genes predicted to
narrow host ranges of B. graminis, where the ‘formae speciales’ tritici and encode protein effectors. Two classes of effector are currently recognized: the
hordei can infect only wheat or barley, respectively (Wyand and Brown, 2003). ‘EKA’ effectors paralogous to the Avrk1 and Avra10 genes closely associated
Other Erysiphales cause mildews which affect many other high-value fruit and with retrotransposons (Ridout et al., 2006; Sacristán et al., 2009); and the
vegetables, including tomato, cucumbers, grapes and strawberries. Their more conventional small secreted proteins which are further characterized as
biology, aetiology and pathology are, overall, similar to those of the cereal highly lineage specific (Spanu et al., 2010).
mildews (Glawe, 2008). All powdery mildews are strictly obligate biotrophic The importance of B. graminis is thus a result of its persistent and
pathogens: they are absolutely dependent on a live host plant. central role as the causal agent of disease of prominent cereal crops
Epidemics are caused by a rapid succession of asexual cycles which begin (Murray and Brennan, 2010), and because it is a model to study other
with the landing of airborne conidia on a host surface. Within a few minutes, mildews and other obligate biotrophic pathogens.
the conidia germinate. Blumeria, unlike other mildews, produces first a short
primary germ tube dedicated to surface sensing (Wright et al., 2000;Yamaoka
et al., 2006). After a few hours, a secondary germ tube emerges from the
conidium, septates and differentiates an elongated, hooked appressorium
from which a peg penetrates through the host cuticle and epidermal cell wall.
The peg develops a complex multidigitate haustorium surrounded by a

Fig. 11 Blumeria graminis f. sp. hordei haustorium. This haustorium was

isolated by manually dissecting the epidermis of an infected barley leaf and
digesting away the host cell wall with a protoplasting cocktail; it was stained
Fig. 10 Barley leaves infected with Blumeria graminis f. sp hordei. The typical with a lectin (wheatgerm agglutinin) bound to Alexa-288. The multidigitate
powdery ‘pustules’ produced by the mildew colonies which grow on the outer structure is surrounded by the perihaustorial membrane of host origin. In
surface of the host plant consist of hundreds of thousands of highly common with other mildews, this specialized membrane is continuous with
infectious asexual conidia blown by air currents to propagate the disease. The the host plasma membrane, but has very different biochemical properties
epiphytic colonies are fed by intracellular haustoria which develop inside the (Micali et al., 2011). In mildews, the perihaustorial membrane is thought to
epidermal cells (see Fig. 11). be the gateway for nutrients and effectors. Bar, 10 mm.

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422 R. DEAN et al.

signalling transitions to hyphal growth and stomatal penetration (Orton et al.,

7. MYCOSPHAERELLA GRAMINICOLA 2011). Subsequent post-penetration stealth pathogenesis is supported
through a reduced gene set for cell wall-degrading enzymes (Goodwin et al.,
The ascomycete Mycosphaerella graminicola (anamorph Septoria tritici) is in 2011) and high-level expression of secreted effector proteins which suppress
the order Dothideales and causes Septoria tritici blotch (STB) disease of wheat the activation of plant defences (Marshall et al., 2011). This initial evasion of
(Fig. 12). This is a major economic constraint on wheat productivity, particu- plant defences reflects a mechanism more typical of obligate biotrophs.
larly in temperate growth regions (Orton et al., 2011). Mycosphaerella However, what follows is an acute activation of plant defences involving host
graminicola infection of wheat begins with hyphal extension on the leaf cell death as the fungus transitions to necrotrophic colonization (Keon et al.,
surface and penetration through stomata without differentiation of an 2007; Rudd et al., 2008). This constitutes an intriguing mechanism for future
appressorium (Fig. 13). A lengthy period of symptomless intercellular coloni- analysis (Fig. 13), involving initial ‘subterfuge’, followed by subsequent
zation (>7 days) then follows, which culminates in the formation of necrotic ‘hijack’ of plant defence signalling (Deller et al., 2011), which may be shared
leaf lesions within which My. graminicola sporulates asexually (Kema et al., by other members of the genus Mycosphaerella, which comprises the largest
1996; Keon et al., 2007). This latter phase involves a switch to necrotrophic number of plant-pathogenic fungi.
nutrition (Fig. 13).
Mycosphaerella graminicola is a well-established model organism for the
study of pathogen population dynamics and evolution. Long-term datasets
(from 1843 to 2003) have demonstrated that STB is influenced by climatic
changes, including those associated with the industrial revolution (Bearchell
et al., 2005). It has also been reported that as much as 90% of the global
genetic variation in this fungus can be present within a single infected wheat
field (Zhan et al., 2003). This level of genetic diversity arises from the heter-
othallic sexual reproductive system and the formation of ascospores that
initiate epidemics each season (Chen and McDonald, 1996; Linde et al., 2002;
Waalwijk et al., 2002). Much of the economic cost incurred by My. gramini-
cola arises indirectly from its rapid evolution in response to selective pres-
sures, including disease-resistant wheat cultivars and the sustained use of
fungicides. Examples of this include the speed with which My. graminicola
field populations evolved and propagated a genetic mutation providing
resistance to the strobilurin class of fungicides (Fraaije et al., 2005), and the
rapid evolution of the CYP51 target protein in response to the widespread use
of particular azole fungicides (Cools et al., 2011).
Mycosphaerella graminicola has also been the subject of intense genetics
and genomics analyses. The genome sequences of a model isolate, together
with relatives collected from wild grasses, have been published recently
(Goodwin et al., 2011; Stukenbrock et al., 2011). These studies have high-
lighted the existence of 21 chromosomes, the eight smallest of which are all
dispensable for plant infection and vary in number and structure between
isolates (Goodwin et al., 2011; Stukenbrock et al., 2011; Wittenberg et al.,
2009). This represents the largest number of dispensable chromosomes so far
reported in fungi (Wittenberg et al., 2009). Functional genomics analysis of
the plant infection process has identified a number of genes important for

Fig. 13 A model for wheat leaf infection by Mycosphaerella graminicola.

Early symptomless colonization (<7 days post-leaf inoculation, DPI) involves
the release of plant defence-suppressing apoplastic effectors (red and blue
triangles) from slow-growing intercellular hyphae. After 7 days, leaf cell death
and the loss of membrane permeability occur, allowing nutrient release into
the apoplast. Defence-suppressing effectors are ‘switched off’, although other
Fig. 12 Septoria tritici blotch (STB) disease of wheat caused by
potentially toxic effectors (blue diamonds) may be produced. Extensive hyphal
Mycosphaerella graminicola.
growth and asexual sporulation (pycnidia and pycnidiospore formation) are
now supported within leaf lesions.
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 Top 10 fungal pathogens 423

8. COLLETOTRICHUM SPP.
Colletotrichum is one of the most common and important genera of plant-
pathogenic fungi. Virtually every crop grown throughout the world is sus-
ceptible to one or more species of Colletotrichum. These fungi cause
anthracnose spots and blights of aerial plant parts and post-harvest rots.
Members of this genus cause major losses to economically important crops,
especially fruits, vegetables and ornamentals. The damage caused by Colle-
totrichum spp. extends to important staple food crops, including bananas,
cassava and sorghum, grown by subsistence farmers in developing countries
throughout the tropics and subtropics. It is particularly successful as a
post-harvest pathogen because latent infections, which are initiated before
harvest, do not become active until after the fruit has been stored or appears
on the market shelf. Up to 100% of the stored fruit can be lost as a result of
Colletotrichum disease (Prusky, 1996).
Colletotrichum is an asexual genus, classified within the Fungi imperfecti.
It belongs to the Coelomycetes, producing its conidia in acervuli. Despite
significant developments, the taxonomy of Colletotrichum remains in a state
of flux. Many uncertainties exist with regard to the systematics of fungal
pathogens from this genus and, depending on criteria, the number of species
can range from 29 to over 700 (von Arx, 1957; Sutton, 1992). One of the most
confusing species is C. gloeosporioides. For example, 594 species of Colletot-
richum were reclassified by von Arx as synonyms of C. gloeosporioides
(Table 2).
As a result of its importance as a pathogen, its unique intracellular
hemibiotrophic lifestyle and the ease with which it can be cultured and
manipulated, Colletotrichum has a long and distinguished history as a model
pathogen for fundamental, biochemical, physiological and genetic studies.
For example, the phenomenon of pathogenic variation (race/cultivar specifi-
city) was first recognized in C. lindemuthianum (Barrus, 1911). Colletotri-
chum on bean was the model for many of the early studies on phytoalexins
(reviewed by Kuc, 1972). During the 1970s and through the 1990s, much of
the work that established and characterized the phenomenon of systemic
acquired/induced resistance (SAR) was performed using a Colletotrichum–
cucumber model pathosystem (Durrant and Dong, 2004). Key genes of the
cyclic adenosine monophosphate (cAMP), MAPK, and RAS/small G-protein
and calcium-mediated signalling pathways have been cloned. The function of
these genes, particularly during conidial germination and appressorium
development, has been characterized in several Colletotrichum species
(reviewed by Chen and Dickman, 2004; Chen et al., 2006; Dickman and
Yarden, 1999; Dickman et al., 1995; Takano et al., 2000). Fig. 14 Transmission electron micrograph showing hemiotrophic growth of
Most Colletotrichum species initially establish infection through a brief Colletotrichum destructivum during cowpea infection. Note the thick biotrophic
biotrophic phase, associated with large intracellular primary hyphae, infection vesicle (IV) following appressorium penetration. The host cell is still
although some species are described as subcuticular, e.g. C. capsici. The
alive and its plasma membrane can be seen surrounding the hypha. Subse-
fungus later switches to a destructive, necrotrophic phase, associated with
narrower secondary hyphae which ramify throughout the host tissue quently, thinner necrophic penetrating hyphae (PH) degrade tissue whilst
(Fig. 14). The molecular details that govern the hemibiotrophic lifestyle (also growing inside the cell. A, appressorium; C, conidium. Photograph courtesy of
known to occur in other fungal species, e.g. Magnaporthe) have long been of Dr Richard O’Connell (Department of Plant Microbe Interactions, Max Planck
interest to phytopathologists. In particular, factors regulating the transition Institute for Plant Breeding Research, Cologne. With permission).
from biotrophy to necrotrophy await identification. The recently completed
C. graminicola sequence (Vaillancourt et al., Department of Plant Pathology, Table 2 The major species of Colletotrichum.
University of Kentucky, Lexington, Kentucky), together with several other
Colletotrichum species in the pipeline, promises to increase our understand- Colletotrichum species Host Lifestyle
ing of this important fungal phytopathogen.
C. gloeosporioides* Papaya/citrus/many other hosts Hemibiotrophy
C. acutatum Strawberry/others Necrotrophy
C. coccodes Tomato Hemibiotrophy
C. graminicola Corn Hemibiotrophy
C. boninense Broad host range Hemibiotrophy
C. trifolii Alfalfa Hemibiotrophy
C. capsici Pepper/other hosts Necrotrophy
C. destructivum Legumes/tobacco Hemibiotrophy
C. caudatum Several grasses ?
C. crassipes Dryandra Hemibiotrophy
C. dematium Radish/other hosts Hemibiotrophy
C. kahawae Coffee Hemibiotrophy
C. orbiculare Melon/cucumber Hemibiotrophy
C. sublineolum Sorghum Hemibiotrophy
C. truncatum Legumes Hemibiotrophy
C. musae Banana Hemibiotrophy
C. fragariae Strawberry/other hosts Hemibiotrophy
C. spinaceae Spinach Hemibiotrophy
C. lindemuthianum Common bean Hemibiotrophy

*Dependent on host and infected tissue.

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424 R. DEAN et al.

Homologous recombination is amazingly efficient (Kämper, 2004) and makes

9. USTILAGO MAYDIS use of four dominant selectable markers (Fig. 15G; Basse and Steinberg,
2004). Tools include regulated promoters for the study of essential genes and
Corn smut is not an economically important or devastating disease. There- a variety of staining methods to visualize the fungus during biotrophic
fore, Ustilago maydis has not made it into the Top 10 for this reason. growth (Fig. 15D), and fluorescent proteins for live cell imaging of gene
Although its symptoms on corn can be quite dramatic (Fig. 15, centre), in expression and visualization of subcellular structures (Fig. 15F) are available
most cases, infections remain local, do not spread and are hence not asso- (Böhmer et al., 2009; Mendoza-Mendoza et al., 2009; Steinberg and Perez-
ciated with severe losses in corn yield. Quite the contrary, farmers in Mexico Martin, 2008). Since 2006, the 20.5-Mb manually annotated and curated
infect corn artificially to harvest infected cobs for the preparation of Huitla- genome sequence has been available (Kämper et al., 2006; http://
coche, a traditional dish popular in pre-Hispanic times. mips.helmholtz-muenchen.de/genre/proj/ustilago). The genome is ‘lean’ and
What are the attractions of this fungus and why has it become a model for contains little repetitive DNA. Transcriptional profiles (Fig. 15E) have been
biotrophic, plant-pathogenic basidiomycetes? Ustilago maydis can be grown established for the most important developmental fungal stages and
in culture in defined media, the fungus is haploid and grows by budding plant responses (accessible through GeneExpressionOmnibus: http://
(Fig. 15A) and forms compact colonies on plates that can be replica plated. www.ncbi.nlm.nih.gov/geo/). This has spurred reverse genetics approaches
These were actually some of the reasons for choosing this fungus for seminal and has allowed the identification of clustered genes encoding secreted
early studies on homologous recombination (Holliday, 2004). For host colo- effectors that play crucial roles during host colonization, and the determi-
nization and symptom development, corn seedlings can be infected. Symp- nation of which tissue can be infected (Doehlemann et al., 2009, 2011;
toms can develop on all above-ground parts of maize plants in 5–6 days Kämper et al., 2006; Skibbe et al., 2010). From genome analysis, it has also
(Fig. 15D) and an infection cycle is completed in about 2 weeks. Typical for become apparent that U. maydis is more closely related to humans than to
smut fungi is that pathogenic development equals sexual development, and budding yeast, and numerous proteins are shared only by U. maydis and
mating and the formation of a dikaryotic filament are absolutely required. Homo sapiens. This includes proteins involved in basic principles of long-
These steps can be reproduced in the laboratory (Fig. 15B) up to the forma- distance transport, mitosis, motor-based microtubule organization and
tion of appressoria on appropriate hydrophobic surfaces (Fig. 15C). The pro- homologous recombination. Ustilago maydis is therefore a perfect host for
teins controlling these events are known: pheromones and pheromone the study of such processes (Banuett et al., 2008; Holloman, 2011; Steinberg
receptors, as well as a heterodimeric transcription factor formed after cell and Perez-Martin, 2008). Where is this system heading? It will allow the
fusion that triggers a regulatory cascade (Brefort et al., 2009; Heimel et al., establishment of the hierarchy of effector action during plant colonization,
2010a, b). This knowledge has allowed the construction of haploid solo- provide insights into fungal nutrition during plant colonization (Eichhorn
pathogenic strains that cause disease without need for a mating partner et al., 2006; Wahl et al., 2010) and serve as the blueprint for comparative
(Bölker et al., 1995; Kämper et al., 2006). Such strains enable forward approaches (Schirawski et al., 2010), which are likely to reveal insights into
genetic screens and greatly reduce work in reverse genetics approaches. both genome evolution and host specialization.

Fig. 15 Developmental stages of Ustilago maydis, mating revealed filamentous growth

tools and disease symptoms. (A) Haploid cells by colour and appressoria
display budding growth. (B) Compatible haploid budding growth formation
(B)
U. maydis strains expressing cytoplasmic red fluo- (A) (C)
rescent protein (RFP) (red) and green fluorescent
protein (GFP) (green) under a constitutive promoter
mate and produce a filamentous dikaryon (yellow).
(C) A solopathogenic strain expressing cytoplasmic
RFP from a constitutive promoter and an appresso-
rial marker gene fused to triple GFP efficiently
homologous recombination phylogeny
forms appressoria on a hydrophobic surface, after
Gene of interest U. hordei
stimulation with hydroxy-fatty acids. (D) Macro- (G) (H)
U. maydis
scopic U. maydis disease symptoms on a maize leaf
12 days post-infection (left) and fungal hyphae in
Selection marker
tumour tissue 10 days post-infection (right) are HygR, NatR, CbxR, PhleoR
S. reilianum
visualized by confocal microscopy; fungal hyphae
are stained with WGA-AF488 (green); plant cell (F) (D)
walls are stained with propidium iodide (red). (E) (E)
Affymetix gene chips allow genome-wide expres-
sion studies. (F) Visualization of F-actin through
LifeAct-YFP in budding cells. (G) Highly efficient
homologous recombination is used for gene
replacement employing hygromycin resistance visualization of tumours on leaves and
(HygR), nourseothricine resistance (NatR), carboxin the actin biotrophic growth
resistance (CbxR) or phleomycin resistance (PhleoR) cytoskeleton whole-genome arrays
as dominant selectable markers. (H) Phylogenetic
tree of U. maydis and its closest relatives. Figures
were kindly provided by Patrick Berndt and Rolf
Rösser (U. maydis disease symptoms in infected
maize cob, centre), both at the Max Planck Institute
for Terrestrial Microbiology. Also, please note that
their permission for using these Figures has been
obtained.

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 Top 10 fungal pathogens 425

10. MELAMPSORA LINI

In contrast with most of the other pathogens on this ‘Top 10’ list, flax rust is
more famous than infamous. Although it was initially studied as a pathogen
having an impact on the flax and linseed industries, its main impact on food
and fibre production came (and comes) from its role as a model system,
providing insights into the molecular basis of plant immunity.

Classical genetic studies (approximately 1926–1981)

Through pioneering genetic studies (Fig. 16) of the pathogenicity of different
physiological races of the pathogen and the resistance and susceptibility to
rust in flax, H.H. Flor observed that there was a specific relationship between
each gene determining pathogenicity in rust [avirulence (Avr) genes] and
corresponding genes [resistance (R) genes] in the host determining resistance
(Flor, 1956; Lawrence, 1988; Lawrence et al., 2007).This became known as the
‘gene-for-gene’ relationship, which provided pathologists and plant breeders
with a logical foundation to reconcile the process of breeding other crop
species for resistance to pathogens. The observations also provided insights
into breeders’ experience that single resistance genes deployed over large
areas frequently ‘break down’ as a result of the mutation of a single corre-
sponding avirulence gene or genetic re-assortment during sexual reproduc-
tion of previously ‘hidden’ recessive virulence alleles to produce progeny
homozygous for virulence. In practical terms, this classical genetics-based
knowledge also underpinned the approach to more durable resistance
through the pyramiding of multiple resistance genes in a single genotype of
crop species.The gene-for-gene hypothesis also gave rise to the postulate that
resistance genes encode receptor proteins that detect the presence of specific
avirulence proteins in the pathogen, and a resulting recognition event that
gives rise to host resistance, the foundation for the development of the current
knowledge of the basis of plant immunity.

Molecular studies (1988 to present)

Fig. 16 Life cycle of flax rust, Melampsora lini. Genetic analysis in flax rust
The flax rust system was among the first three systems to provide cloned depends on the ability to replicate all stages of the life cycle under controlled
resistance genes and the identification of a new class of immune receptor, conditions to produce selfed and outcrossed progeny from flax rust isolates,
cytoplasmic nucleotide-binding leucine-rich repeat (NB-LRR) proteins, spe- and is complicated by the rust being an obligate biotroph, requiring all
cific members of which provided host plant resistance against fungi, oomyc- manipulations to be undertaken on the living host plant.
etes, bacteria, viruses, nematodes, sucking insects and parasitic plants (Ellis
et al., 2007). The same protein group was subsequently identified in animals
as part of the innate immune system.
The examination of alleles from the L resistance locus and chimeric genes
between alleles expressed in transgenic flax provided the first indication that
the specificity of gene-for-gene interactions was determined by sequence
variation of the LRR domain of the receptor proteins, and that the likely
origin of new resistance specificities in nature results from point mutations,
re-assortment of the mutations, and duplication and deletion of LRR units by
intragenic recombination (Ellis et al., 2007).
The intracellular nature of the flax resistance proteins implied that the Avr
(effector) proteins were detected by R proteins within host cells. This was
subsequently confirmed by the cloning of several Avr genes from flax rust
which encode diverse proteins secreted from the rust and were taken into
the plant cell through the mediation of uptake signals located near the
N-terminus of the Avr proteins (Rafiqi et al., 2010). The molecular basis for
gene-for-gene recognition was shown to rely on specific and direct interac-
tion between flax R proteins and corresponding Avr proteins. Only those R
and Avr proteins that interacted in yeast two-hybrid assays induced plant
resistance responses when co-expressed in plants (Wang et al., 2007). The
study of the flax rust fungus and its interaction with its host is now set for
further advances following the development of an Agrobacterium transfor-
mation system for this obligate biotroph (Lawrence et al., 2010) (Fig. 16).

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426 R. DEAN et al.

Brown, N.A., Urban, M., Van de Meene, A.M.L. and Hammond-Kosack, K.E. (2010)
ACKNOWLEDGEMENTS The infection biology of Fusarium graminearum: defining the pathways of spikelet to
spikelet colonisation in wheat ears. Fungal Biol. 114, 535–571.
The authors would like to thank Dr Diane Hird for the distribution of voting Brown, N.A., Bass, C., Baldwin, T.K., Chen, H., Massot, F., Carion, P.W.C., Urban,
information and the collation of voting results. M., van de Meene, A. and Hammond-Kosack, K.E. (2011) Characterisation of the
JALvK acknowledges Marcela Esterio (Universidad de Chile, Santiago, Fusarium graminearum–wheat floral interaction. J. Pathogens e626345, 9 pages.
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