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 2

Department of Plant Pathology, Fungal Genomics Laboratory, North Carolina State University, PO Box 7251, Raleigh, NC 27695, USA 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

SUMMARY
The aim of this review was to survey all fungal pathologists with an association with the journal Molecular Plant Pathology and ask them to nominate which fungal pathogens they would place in a ‘Top 10’ based on scientific/economic importance. The survey generated 495 votes from the international community, and resulted in the generation of a Top 10 fungal plant pathogen list for Molecular Plant Pathology. The Top 10 list includes, in rank order, (1) Magnaporthe oryzae; (2) Botrytis cinerea; (3) Puccinia spp.; (4) Fusarium graminearum; (5) Fusarium oxysporum; (6) Blumeria graminis; (7) Mycosphaerella graminicola; (8) Colletotrichum spp.; (9) Ustilago maydis; (10) Melampsora lini, with honourable mentions for fungi just missing out on the Top 10, including Phakopsora pachyrhizi and Rhizoctonia solani. This article presents a short resumé of each fungus in the Top 10 list and its importance, with the intent of initiating discussion and debate amongst the plant mycology community, as well as laying down a bench-mark. It will be interesting to see in future years how perceptions change and what fungi will comprise any future Top 10.

INTRODUCTION
Recently, the journal Molecular Plant Pathology considered which viruses would appear in a ‘Top 10’ of plant viruses on the basis of their perceived importance, scientifically or economically, in terms of the views of the contributors to the journal (Scholthof et al., 2011). This was carried out as many papers, reviews and grant

*Correspondence: Email: gary.foster@bristol.ac.uk

applications claim that a particular plant virus is of huge importance, and this is probably rightly so. As a result of the interest generated in this exercise for plant viruses, a similar survey was instigated for plant-pathogenic fungi, and with a similar mechanism to the virus review. All authors, reviewers, editorial board members and senior editors of the journal Molecular Plant Pathology, with an interest in fungi, were contacted and asked to nominate three plant-pathogenic fungi they would expect to see in a list of the most scientifically/ economically important fungal pathogens. The review, by its very nature, is similar in format and layout to the Top 10 virus review (Scholthof et al., 2011). The survey generated 495 votes from the international community, and allowed the generation of a Top 10 fungal plant pathogen list for the journal Molecular Plant Pathology (see Table 1). The fungus making the strongest appearance in the voting was Magnaporthe oryzae, in first place with almost double the number of votes of Botrytis cinerea, in second place. All voters highlighted the economic importance of M. oryzae; with over 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 developed into a model system for the study of plant–pathogen interactions. Botrytis cinerea, in second place, clearly has an impact in many areas because of the broad host range, causing severe damage, both pre- and post-harvest. It may be one of the few entries in the Top 10 that can claim a potential beneficial use, through its role in some aspects of wine production, with some benefits also claimed for the ninth entry, Ustilago maydis, in infected cobs. Puccinia spp., with many voters grouping the three wheatinfesting rust diseases together, are grouped together in third position. These fungal pathogens were already a serious disease

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In fourth and fifth places are two Fusarium species.. The proposed number of species within the genus ranges from 29 to over 700 depending on taxonomic interpretation.. because of obvious numerical limits. but have increased in impact with the emergence of race Ug99. pathogens of cereals continue to have a significant presence in the Top 10 with Blumeria graminis in sixth position and Mycosphaerella graminicola in seventh. it will be interesting to see whether fungi such as Phakopsora pachyrhizi. This review contains single-page descriptions of the Top 10 plant-pathogenic fungi to introduce the reader to each of them. Ustilago maydis Melampsora lini Author of fungal description Ralph Dean Jan A. 1994). respectively. including Phakopsora pachyrhizi (Goellner et al. Fusarium graminearum Fusarium oxysporum Blumeria graminis Mycosphaerella graminicola Colletotrichum spp. both clearly important. graminearum causing significant damage predominantly to cereals and a few noncereal species. as it will be interesting to see how perceptions change in future years and which fungi enter and leave the list. Rudd Marty Dickman Regine Kahmann Jeff Ellis The table represents the ranked list of fungi as voted for by plant mycologists associated with the journal Molecular Plant Pathology. when another survey of the Top 10 is carried out. In future years. 2011. and provide vital insights into the molecular basis of plant immunity and infection processes. The intention of this review is to trigger discussion and debate amongst the plant mycology community. Colletotrichum spp. are members of an important genus of plant pathogens. cotton and banana. Pretorius Kim Hammond-Kosack Antonio Di Pietro Pietro Spanu Jason J. followed by a switch to tissue ramification and necrotrophic development. 414–430 .Top 10 fungal pathogens 415 Table 1 Top 10 fungal plant pathogens. 2010). as well as to lay down a bench-mark. oxysporum having a wide host range.. in eighth position. L. with F. © 2012 THE AUTHORS MOLECULAR PLANT PATHOLOGY © 2012 BSPP AND BLACKWELL PUBLISHING LTD MOLECULAR PLANT PATHOLOGY (2012) 13(4). 2010) and Rhizoctonia solani (Gonzalez et al.. We are also aware that not all fungi can make it into any Top 10. Both are now developed as model systems. However. now posing a serious challenge to wheat production. we are very much aware that importance and priorities can vary locally across continents and disciplines. with illustrative figures and key references for further reading. but with contrasting host ranges. Vilgalys and Cubeta. for which the taxonomy may be described as being in a state of flux. threat. although such fungi can still be regarded as hugely important. and F. We therefore felt it appropriate to cite honourable mentions for fungi just missing out on the Top 10 list. have long served as a model system for hemibiotrophic pathogens. as it is clearly a disease that has only recently appeared in certain parts of the world and will potentially increase in importance (Goellner et al. with many voters indicating strong scientific rather than economic reasons for their inclusion. with severe losses in crops as diverse as tomato. makes an appearance. the causal agent of Asian soybean rust. van Kan Zacharias A. It is interesting that Ustilago maydis and Melampsora lini make up ninth and tenth positions. with a short biotrophic stage. Colletotrichum spp. Although the aim of this review article was to identify the Top 10 most important plant-pathogenic fungi according to the contributors to Molecular Plant Pathology. Rank 1 2 3 4 5 6 7 8 9 10 Fungal pathogen Magnaporthe oryzae Botrytis cinerea Puccinia spp. which are readily tractable.

1... 1989. MOLECULAR PLANT PATHOLOGY (2012) 13(4). 2009). although the fungus can cause disease on all foliar tissues. M. 2005). is the causal agent of rice blast disease. block host penetration (Woloshuk et al. 2010) which regulate and orchestrate the development of this specialized cell (Fig. Early examination of these data revealed dramatic differences in gene content and organization of repetitive elements. Conidia produced from lesions are splashed onto new plants where they attach firmly and germinate within a few hours. oryzae are poised to grow significantly in the very near future. under appropriate conditions. 1993). Oh et al.. a specialized infection cell (Howard and Valent. 2006). 1). 1980). The ability to perform genetic analyses led to the cloning and characterization of several genes for host and cultivar specificity (Bryan et al. oryzae has emerged as a seminal model in the study of host–fungal pathogen interactions (Dean et al. The development of genetic markers. oryzae elaborates an appressorium... DEAN et al .. oryzae and related species have grown dramatically and presently include more than 30 genomes from strains around the globe. Oh et al. 2008) and emerging proteome datasets. MGR583 and MGR586. Knowledge of the biology.. Nguyen et al. The early stages of infection have been studied in great depth in M. 1991). the appressorium.. 1988. 2002. 2000. MAGNAPORTHE ORYZAE Magnaporthe oryzae. cell signalling pathways (Lee and Dean. 1994). turgor pressure increases within the appressorium. the most destructive disease of rice worldwide (Ou. several effective fungicides. Magnaporthe oryzae is part of a species complex that can cause disease on a variety of grasses and related species. more than 20 years ago stimulated a surge in scientific interest in the rice blast pathogen (Leung et al. 1980.. forms a highly melanized dome-shaped structure. Skamnioti and Gurr.. Today. 1997. as a result of its agronomic significance and tractability. 2000. oryzae. 2007. A B Fig. following the publication of the genome sequence for strain 7-15 (a derivative of Guy11) (Dean et al.. 2 Infection cycle of the rice blast fungus.. 2006.. by 12 h. which inhibit melanization of the appressorium. the germ tube ceases polar growth. Orbach et al. the tip swells and. as well as various transcriptome datasets [expressed sequence tags (ESTs) and small RNAs] (Gowda et al.... Nunes et al. 1991). 1994). Losses of 10%–30% are typical. Silué and Notteghem. however. Appropriate development of this cell is required for infection. oryzae. wheat and millet (Couch et al. Subsequently.. much effort is focused on cloning and characterizing the many avirulence and corresponding rice resistance genes that have been genetically identified (Chao and Ellingboe.. The discovery of Guy11. Talbot. 2005). 2). Consequently. 1996). 2008.. conidiophores emerge bearing conidia to re-initiate the infection cycle. 1992). the fungus is highly amenable to genetic and molecular genetic manipulation (Jeon et al. Over the last 6 years.... 1990. Zeigler et al..416 R. such as tricyclazole. starvation responses (Donofrio et al.. 1991. although regional epidemics can be devastating. a fertile Mat1-2 strain from French Guiana. Valent and Chumley. from which. 2006) and cell cycle checkpoints (Saunders et al. 2009). turgor pressure generation (deJong et al. 1996). 1 Disease resulting from the infection of rice and wheat with Magnaporthe oryzae. Xu and Hamer. providing deep insight into the evolution of phytopathogenesis. indeed. and cultivars typically become ineffective within 2–3 years (Ou. Valent et al.. infection of the panicle can lead to complete loss of grain. 1983). 2003. (A) Classical symptoms of panicle blast on rice. Although host resistance is the most economically viable and environmentally sound practice to manage this disease. genetic diversity and adaptability of this pathogen is key for the development of novel and durable strategies to manage this and related devastating fungal diseases (Fig. 2011. M. Skamnioti and Gurr. 2005). forcing a penetration peg into the underlying tissues. 2008). Typically within 24 h. (B) Head blast on wheat. The ability to induce appressoria ex planta and to perform functional analyses of genes by targeted gene knockout has provided powerful access to many of the underlying molecular processes (Leung et al. 2000. New wheat strains have emerged in South America. 1993. the fungus overcomes blast resistance quickly. such as MAGGY. 414–430 © 2012 THE AUTHORS MOLECULAR PLANT PATHOLOGY © 2012 BSPP AND BLACKWELL PUBLISHING LTD . 1997). All foliar tissues are subject to infection. Fig. The symptoms on wheat are typically restricted to the head and can be mistaken for wheat scab caused by Fusarium graminearum. Eye-shaped necrotic lesions do not appear until several days after infection. genomic resources for M. population biology studies and phylogenomic analyses of M. With the emergence of new sequencing technologies. elevating concerns that the fungus poses a serious threat to global wheat production (Urashima et al. 2005). Jia et al. but also the molecular tools to assess population diversity and the evolution of lineages. recycling cellular contents (autophagy) (Veneault-Fourrey et al. 1996.. valuable knowledge for the breeding and timely release of resistant cultivars (Farman et al. Nguyen et al. from repetitive elements has provided the means to not only create valuable genetic maps for M. Nitta et al. Like many fungal plant pathogens. Its importance is underscored by the fact that approximately one-half of the world’s population relies on rice for its primary caloric intake (Khush. a filamentous ascomycete fungus. 2008). including crops such as barley. Considerable knowledge has been acquired regarding the perception of environmental cues (Lee and Dean.. In addition. Other studies have revealed fundamental insights into host defence and gene silencing mechanisms (Ikeda et al. Hamer et al.

The genome sequences of two B. failed treatment (fungicide resistance) or quality loss (fungicide levels exceeding export requirements. Serious damage can occur following the harvest of seemingly healthy crops. cinerea may cause noble rot in grape berries. 2007). Fig. Botrytis cinerea is most destructive on mature or senescent tissues of dicotyledonous hosts. The costs of broad-spectrum fungicides also effective against B. 2009) and South Africa (SA Rand 25 million/year). strawberries and ornamentals each making up 5%–9% (Steiger. 2010)]. 2008. 2009). 2011). an effect difficult to incorporate into estimates of economic losses. No reliable figures are available for Botrytis damage during crop cultivation. In spite of the increasingly effective application of biocontrol in some crops (Moser et al.3 million (Vrind. Consumers experience economic loss when berries rot before they are eaten. 2007). cinerea are unknown. 2007). yet only very few absolutely essential virulence determinants have been identified by candidate gene approaches (Tudzynski and Kokkelink. cucurbits. Infestation can occur all the way from the seedling stage until product ripening. 2009).. Chile (US$ 22. Reduction of the shelf life (fruit) or vase life (flowers) is a serious quality issue. 2007). Esterio et al. biocontrol) easily surmount €1 billion/ annum. Official figures of the costs of grey mould in soft fruit and ornamentals must therefore be considered as underestimates. cinerea strains failed to identify ‘silver bullets’. Estimates for other countries could not be obtained. These studies have considerably advanced our understanding of the infection strategies of B. broad-spectrum fungicides. In 2002. The most prestigious Botrytis wines are sold for prices up to €500/bottle. 2002). about 15%–20% of rose and gerbera bunches traded through Dutch flower auctions contained detectable Botrytis infection. botryticides. and the quality loss during the retail chain. 4).. From an economic perspective. cinerea.. Fungicides specifically targeted against Botrytis (‘botryticides’) cost €540 million (2001). expenses for the control of Botrytis bunch rot are a major cause of reduction in profit in Australia (AUS $52 million/year. The wine and table grapes segment represents 50% of the value of the total market for botryticides. yet it must be huge. all countries) is about €40/ha (Steiger. Fig. as it may occasionally be beneficial! Under specific climatic conditions.Top 10 fungal pathogens 417 2. The fungus is considered as a typical necrotroph. The loss in revenue for rose growers alone was estimated at €1. Multidrug resistance has been reported and is mostly caused by the increased expression of ABC transporter genes (Kretschmer et al. This fungus sometimes remains quiescent for a considerable time before rotting tissues when the host physiology changes and the environment is conducive (Williamson et al. cinerea is negative.. 4 Botrytis cinerea on raspberry fruits (from Williamson et al. Scholefield and Morison. cinerea being the most extensively studied necrotrophic fungal pathogen. transport to distant markets or during display at the retailer (Fig. B. 414–430 . or when roses do not last for a satisfactory period. Costs are diffuse as Botrytis damage occurs in different stages of the production and retail chain.. fungicide application remains the common method to control Botrytis. can infect more than 200 plant species. known as grey mould.4 million/year. during storage. 1997) or to achieve gene silencing (Patel et al. even in the wine industry. have contributed to B. Altogether. global expenses of Botrytis control (cultural measures. The average cost for chemical Botrytis control (all crops. Such figures do not include flowers that were infected before harvest and did not make it to the auction. together with its economic relevance. BOTRYTIS CINEREA Botrytis cinerea Persoon: Fries [teleomorph Botryotinia fuckeliana (de Bary) Whetzel. Botrytis cinerea is an exceptional pathogen. The availability of the genome sequence and a variety of molecular tools [ease of transformation to obtain knockout mutants (van Kan et al. unique features which distinguish it from other pathogenic and nonpathogenic fungi (Amselem et al. low-input farming). 3].. the loss experienced by consumers is often disregarded because producers and retailers have obtained income. are likely to be far higher. which co-opts programmed cell death pathways in the host to achieve infection (van Baarlen et al. Fungicide resistance is an increasingly problematic issue.. The costs of Botrytis damage are very difficult to estimate because of the broad host range. grape quality insufficient for high-quality wines). the overall impact of B. In wine and table grapes. leading to vase life reduction of such bunches by 3 days. © 2012 THE AUTHORS MOLECULAR PLANT PATHOLOGY © 2012 BSPP AND BLACKWELL PUBLISHING LTD MOLECULAR PLANT PATHOLOGY (2012) 13(4).. which are used to produce sweet wines (Sauternes.. 2010). with solanaceous vegetables. dissatisfied customers may refrain from purchasing the product again for several weeks. representing 10% of the world fungicide market (UIPP. Tokaj). 2005). 2008).. 2011). The impacts of product loss occurring despite disease control. or flowers that were spoiled during transport to retailers and became unsellable. Nevertheless. Harvested commodities can be spoiled in the retail chain. with significant proportions of the fungal population being resistant to fungicides (Leroch et al. However. but do not cover the losses experienced by the lack of treatment (organic farming. 2007). Fig. These expenses predominantly include the chemicals. 3 Sexual fruiting bodies (apothecia) of the teleomorph Botryotinia fuckeliana (de Bary) Whetzel.

Three rust diseases occur on wheat. Singh et al.. 1984 and Roelfs..globalrust. 2011). sp. McIntosh and Pretorius. tritici) (Pgt) (Fig. Numerous cultivars protected by single genes have become susceptible to stem rust. stripe (yellow) rust (P. Sr31 and Sr36 (Singh et al. The specialization of Pgt in different races has impacted strongly on wheat breeding and production. 2011).. Prolific sporulation. DEAN et al . 2008.. triticina) (Pt).. 2007. 1982) and in the UK. 2011). 2011). Australia. pathogenic variability and the widespread cultivation of wheat. all contribute to the destructive potential of these rusts. Jin. striiformis f. 2007. Stem rust is frequently perpetuated by repeating uredinial stages on common and durum wheat. Chile. Park. 2000). coupled with pathogen genomics.org). 1985).. 2005). The elucidation of the complete Pst life cycle (Jin et al. 2011) are significant steps towards a better understanding of virulence. Serious epidemics also occurred in Europe and China (Leonard and Szabo. efficient dissemination. 1989. Leonard and Szabo. such as Berberis vulgaris. Fig. In many instances. often with devastating ‘boom-and-bust’ effects (e. varying in virulence for Sr21. India. 2007. Seven variants within the Ug99 lineage have been reported. exotic incursions of wind-borne spores have occurred. heteroecious life cycles (Bolton et al. 2011). Together with progress in the detection. will enable the discovery. 2007). sp. Pst and Pt are obligate. Vurro et al. 2011. called haustoria.. furnishing primary inoculum for wheat and new virulence combinations as a result of sexual re-assortment of genes (Jin. with less frequent outbreaks in Eastern Europe. 1985). epidemiology and host–pathogen genetics in Pgt (reviewed by Loegering. 2011). However..g. 6 Wheat flag leaf infected with stripe rust caused by Puccinia striiformis f. tritici) (Pst) (Fig. characterization and utilization of sustainable management strategies for resistance. 2011)..418 R. Recently. Pretorius et al. Early stem rust epidemics initiated studies on pathogenic variability. barley and triticale. Continued research on surveillance and race analysis. 2011). Martens and Dyck. 2010) and the genome sequence of this pathogen (Cantu et al.. http://www. Mexico. basidiospores can infect alternative hosts. tritici.. establishing new race lineages (Park. Ethiopia and South Africa (Hodson. has renewed stem rust research (Singh et al. 2010. 2007). 2011. 5 Stem rust-infected wheat showing uredinial and telial spore stages. As a result of its adaptive capacity. in both scope and disease management. and thus breeding for durable resistance.. 2011. 5). The occurrence of race Ug99 of Pgt in East Africa with virulence for Sr31 (Pretorius et al. which are situated inside plant cells (Voegele and Mendgen. sp. PUCCINIA SPP. Sr24. 2011. genetic mapping and management of genes and quantitative trait loci (QTL) conferring resistance to Ug99 (Durable Rust Resistance in Wheat Project. often in conducive environments. must be viewed as one of the major achievements in plant pathology. 6) and leaf (brown) rust (P. which also started in 1918 and continues today. 2011. the Ug99 race group has been recognized as a major threat to food security (Flood. Jin et al. namely stem (black) rust (caused by Puccinia graminis f. biotrophic basidiomycete fungi with macrocyclic. Significant and repeated crop failures caused by rusts occurred in North America between 1904 and 1962 (Hodson. a commonly used resistance gene. Singh et al. severe and widespread stripe rust epidemics have been ascribed to new and more aggressive races adapted to warmer environments (Hovmøller et al. 414–430 © 2012 THE AUTHORS MOLECULAR PLANT PATHOLOGY © 2012 BSPP AND BLACKWELL PUBLISHING LTD . 3. Pretorius et al.. Kolmer et al. 2005). 2010.. Historically. Obligate biotrophs differentiate specialized infection structures. Pgt. Roelfs. 1985). fitness and virulence attributes (90% of the world’s wheat is susceptible). MOLECULAR PLANT PATHOLOGY (2012) 13(4).The disease was feared in ancient Rome where rituals (‘Robigalia’) were performed to save crops from rust (Zadoks... McIntosh and Pretorius. Fig. 2011. The barberry eradication programme in the USA between 1918 and 1980 (Roelfs. significant advances are being made in understanding the molecular basis of pathogenicity in Pgt (Duplessis et al. 2010). The release and adoption of widely adapted resistant cultivars are essential for future and effective rust control globally (Lowe et al. stem rust has been most notorious for damaging wheat crops. efficiently suppress host defence responses and obtain nutrients through the formation of specialized feeding structures.

. verticillioides and F. a ‘two-speed’ genome is recognized.. sp. Later. Minimizing consecutive cereal crops and ploughing under any infected residues remain the best methods to reduce disease pressure locally. 2005). e. strong host defence responses are activated in the rachis and hyphal colonization is restricted to the florets (Jansen et al. At the advancing hyphal front.. Fig.scabusa. 2010. LESION CENTRE numerous dead hyphae lacking cellular contents Wheat rachis cell VISIBLE DISEASE extracellular and intracellular hyphae Wheat rachis cell SYMPTOMLESS ADVANCING FRONT extracellular hyphae Wheat rachis cell DON DON Fg hyphae Most host cells dead. if infected cereal grain is stored or transported at too high a moisture content. 7 The floral tissues of hexaploid wheat severely infected with Fusarium graminearum. 2011). An additional 160 pathogenicity/ virulence factors are now recognized to contribute to cereal floral infection. 2010). Urban and Hammond-Kosack.org. but spray coverage and the timing of applications remain difficult. Excellent genetic. within the lesion centre (>10 days). Ma et al. which greatly suppresses the burst of plant defence responses (depicted in blue). Host cells only die on intracellular hyphal invasion. with discrete regions of high recombination and high single nucleotide polymorphisms (SNPs) located near telomeres and in the middle of the four large chromosomes. 2012). post-harvest growth of the fungus occurs and mycotoxin levels increase (Magan et al.The genome lacks repetitive sequences and contains a low level of duplicated genes.net). 2011). the most important of which are deoxynivalenol (DON). Once hyphae enter the plant cells. animal feed or malting purposes. oxysporum f. rather than lowering grain yield.scabusa. Fusarium ear blight (FEB) or head scab. onset of host cell death Fg hyphae High DON production suppresses plant defences © 2012 THE AUTHORS MOLECULAR PLANT PATHOLOGY © 2012 BSPP AND BLACKWELL PUBLISHING LTD MOLECULAR PLANT PATHOLOGY (2012) 13(4). High TRI gene expression is detected at the advancing front and diminishes thereafter (Brown et al. In the absence of DON.. but a high level of polymorphism exists between strains. When aligned to a genetic map.g. The production of DON mycotoxin contributes to disease formation on wheat floral tissue (Proctor et al. DON binds to the peptidyl transferase protein in the ribosome and inhibits protein translation. 8). http://www. A recent re-investigation of the biology of the wheat floral infection process has revealed that a considerable phase of symptomless infection exists in which hyphae advance extracellularly between the living host cells. is a highly destructive pathogen of all cereal species (http://www. biochemical. the resistance sources identified are only partially effective and are major QTL based (Buerstmayr et al.plexdb. DON synthesis is tightly regulated by at least three transcription factors: TRI6. graminearum genome were the result of ancestral chromosome fusion events (Cuomo et al.org). 2007.Top 10 fungal pathogens 419 4. http://www. with the majority functioning post-penetration (http://www. the presence of the released proteins and sugars and the high density of fungal hyphae lead to a strong activation of plant defence responses. 2003). Mycotoxin-contaminated grain is often unsafe for human consumption.. graminearum co-exists and co-infects with other Fusarium species. The greatest economic losses occur when the floral tissues become infected (Fig. strict upper limits on specific mycotoxin levels in grain and foods have been imposed [Commission Regulation (EC) 1881/2006. Different natural isolates (termed chemotypes) produce different mycotoxin types (Alexander et al. http://www. F. TRI10 and TRI15. the cellular contents of fungal cells residing deep within the dead cortical tissue are relocated to the hyphae just below the rachis epidermis and asexual sporulation then occurs. FUSARIUM GRAMINEARUM The ascomycete Fusarium graminearum (teleomorph Gibberella zeae). Direct replacement of a gene of interest with a selectable marker via homologous recombination is now relatively straightforward.org. genomic.. This disease mainly reduces grain quality.fgsc. In Europe. nivalenol and the phytoestrogen zearalenone. This disease is frequently referred to as Fusarium head blight (FHB). Worldwide. transcriptomic and isolate collection resources now exist for F. molecular genetic. 7). 1995). Fusarium graminearum produces several trichothecene mycotoxins. These findings indicate that F.phi-base.. extensive degradation of plant cell walls Fg hyphae Plant defences activated. Locally. 2009). graminearum (http:// www. and results in mycotoxincontaminated grain. 8 A simplified three-phase model of the Fusarium graminearum (Fg) infection process through wheat rachis tissue. which resides in the order Hypocreales. 2010).org]. Comparisons with the sequenced genomes of F. and extensive degradation of plant cell walls is a relatively late process. the USA and other regions. in soybean and sugar beet. Some azole fungicides are moderately effective. deoxynivalenol (DON) mycotoxin inhibits protein translation. all the major cereal-growing regions have reported a re-emergence of Fusarium epidemics (Leonard and Bushnell. During the post-harvest period. graminearum uses a stealth approach to facilitate successful floral infections (Fig. Control of Fusarium floral infections remains problematic. 414–430 . acetylated DON derivatives. In most cereal species.. lycopersici suggest that the high-diversity sites in the F. Fig.org. Fusarium graminearum infection of noncereal species in the crop rotation is increasingly being reported.scabusa.

2001). but not in plants (Caracuel et al. Fusarium oxysporum is also an emerging pathogen of humans that can cause invasive infections in immunocompromised patients (Nucci and Anaissie.. Because F. 1981... O’Donnell et al. 9). is a ubiquitous soil-borne pathogen that causes vascular wilt on a wide range of plants. including four entire chromosomes that are absent from other Fusarium species. 414–430 © 2012 THE AUTHORS MOLECULAR PLANT PATHOLOGY © 2012 BSPP AND BLACKWELL PUBLISHING LTD . tomato. Ortoneda et al. 1998). 9 (A) Fusarium oxysporum microconidium (C) germinating on the surface of a tomato root. progressive wilting. analysis of the complete genome sequence of the tomato pathogenic form F. 5. This dichotomy has both fascinated and puzzled generations of plant pathologists. 2011). are required for virulence in the mouse model. oxysporum include genome-wide insertional mutagenesis screens (López-Berges et al. The interaction between tomato and Fol was used to study the molecular basis of disease resistance and susceptibility (Houterman et al. 2001. infecting the same host plant. individual isolates of F. Transfer of two LS chromosomes from Fol to a nonpathogenic isolate enabled it to cause disease on tomato plants.. 2009). Adding to the intrigue. the mechanism through which these new pathogenic lineages emerged in otherwise distinct genetic backgrounds has long remained elusive. sp.. 2010). Recently. MOLECULAR PLANT PATHOLOGY (2012) 13(4). Fig. oxysporum lacks a known sexual cycle...420 R. 2004). 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 trans-kingdom pathogenicity in fungi (Ortoneda et al. Michielse et al. leaf epinasty. cotton and banana. 2009a) leading. which collectively infect more than 100 different hosts. FUSARIUM OXYSPORUM Fusarium oxysporum Schlecht.. 2005). phylogenetic studies suggest that different isolates of a given forma specialis. to the discovery of a master regulator of pathogenic development (Michielse et al. such as a mitogen-activated protein kinase (MAPK) or a small G-protein. graminearum and F.. Gordon and Martyn.. 1997). have originated independently during evolution (O’Donnell et al. 2004). Dominant plant resistance (R) genes against different races of F. among others (Michielse and Rep. 2009. oxysporum have been identified in several crops (Simons et al. The F. 2010) and the characterization of a novel mucin-type transmembrane sensor (Pérez-Nadales and Di Pietro. This suggests that horizontal transfer of small chromosomes could account for the emergence of new pathogenic lineages (Ma et al... 2008. These results indicate that F.. 2004). Characteristic disease symptoms include vascular browning. such as the cereal pathogens F. Future studies in the F. 2009b).. Others.). Ortoneda et al. 2010). oxysporum species complex comprises different formae speciales (f. Penetration occurs by directed growth of the infectious hypha (IH) towards a natural opening between epidermal root cells (penetration site indicated by an arrow). 2007. verticillioides (Ma et al. stunting. some of which can function as both elicitors and suppressors of R gene-based plant immunity (reviewed in Takken and Rep. 2003. Martinez-Rocha et al. sp.. 2009. In contrast with the remarkably broad host range at the species level. 2004). oxysporum cause disease only on one or a few plant species (Armstrong and Armstrong. 2008. oxysporum system will continue to provide new insights into the molecular mechanisms of fungal pathogenicity (Fig. are dispensable for virulence in mice (Di Pietro et al. Genetic analysis using targeted mutants has revealed that signalling components which are essential for the infection of tomato plants. oxysporum f. Recent advances towards an understanding of the genetic basis of pathogenicity in F. DEAN et al . 2010). defoliation and plant death (Agrios. 1998). oxysporum employs fundamentally distinct infection strategies on plants and mammals. lycopersici (Fol) has revealed the presence of lineage-specific (LS) genomic regions. the identification of a conserved nitrogen response pathway regulating invasive growth functions (López-Berges et al. such as the pH response transcription factor PacC.. Genome sequences from additional F. oxysporum isolates will provide invaluable tools to further explore this hypothesis. provoking severe losses in crops such as melon. These studies led to the identification of a classical gene-forgene system with at least three fungal avirulence genes. (B) Fusarium oxysporum hypha growing in a xylem vessel of a tomato root (from Di Pietro et al. Further studies are addressing the presence of common virulence mechanisms that are required on both types of host. Rep et al.. 2004).. among others.

similar to those of the cereal mildews (Glawe. and because it is a model to study other mildews and other obligate biotrophic pathogens. Mildew infections of cereals reduce grain yield and must be kept in check to ensure an economically viable product. 10 Barley leaves infected with Blumeria graminis f. After a few hours. updated and developed because of the emergence of fungicide resistance. 10). 11). sp. 414–430 . produces first a short primary germ tube dedicated to surface sensing (Wright et al. graminis.. The genomes of barley and other powdery mildews are >120 Mb. Other Erysiphales cause mildews which affect many other high-value fruit and vegetables. Fig. where the ‘formae speciales’ tritici and hordei can infect only wheat or barley. graminis is thus a result of its persistent and central role as the causal agent of disease of prominent cereal crops (Murray and Brennan. including wheat and barley. 10 mm. 2008). 2004). but has very different biochemical properties (Micali et al. In common with other obligate biotrophic pathogens. which also act as resting structures to survive adverse conditions. These control measures need to be continually revised. which are amongst the top agricultural crops world-wide (FaoStat. including tomato. 2006. 11) (Hückelhoven and Panstruga. The typical powdery ‘pustules’ produced by the mildew colonies which grow on the outer surface of the host plant consist of hundreds of thousands of highly infectious asexual conidia blown by air currents to propagate the disease. and the more conventional small secreted proteins which are further characterized as highly lineage specific (Spanu et al. © 2012 THE AUTHORS MOLECULAR PLANT PATHOLOGY © 2012 BSPP AND BLACKWELL PUBLISHING LTD MOLECULAR PLANT PATHOLOGY (2012) 13(4). In common with other mildews. At the end of the host growth season. a secondary germ tube emerges from the conidium. Within 3 days from inoculation. 2006). In mildews... grapes and strawberries. aetiology and pathology are. by a partial loss of genes involved in secondary metabolism. All powdery mildews are strictly obligate biotrophic pathogens: they are absolutely dependent on a live host plant. hooked appressorium from which a peg penetrates through the host cuticle and epidermal cell wall. Epidemics are caused by a rapid succession of asexual cycles which begin with the landing of airborne conidia on a host surface. 2011). It causes powdery mildews of grasses (Fig. compatible strains mate and produce chasmothecia (Braun et al. the haustorium is devoted to the feeding and control of host immunity and metabolism (Panstruga and Dodds. the perihaustorial membrane is thought to be the gateway for nutrients and effectors. 2010). 2011). unlike other mildews.. 2002).. conidiophores develop from specialized foot cells and produce masses of conidia: the eponymous ‘powder’ of these mildews. septates and differentiates an elongated. Blumeria. 2000. 11 Blumeria graminis f. BLUMERIA GRAMINIS Blumeria graminis is an ascomycete belonging to the Erysiphales (Takamatsu. respectively (Wyand and Brown. The epiphytic colonies are fed by intracellular haustoria which develop inside the epidermal cells (see Fig. it was stained with a lectin (wheatgerm agglutinin) bound to Alexa-288. Fig. 2011). This is caused by an extraordinary proliferation of retrotransposons.e. 2010).. on the one hand. Two classes of effector are currently recognized: the ‘EKA’ effectors paralogous to the Avrk1 and Avra10 genes closely associated with retrotransposons (Ridout et al. Genome expansion is accompanied. the conidia germinate. sp hordei. Their biology. Plant-derived nutrients are transported to hyphae growing on the plant surface. 1990) to the extremely narrow host ranges of B. The Erysiphales exhibit a wide range of host specificity. The importance of B. ranging from broad polyphagy observed in many of the dicot mildews (Ing. i. on the other. 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. hordei haustorium.Top 10 fungal pathogens 421 6. Bar. Sacristán et al.. this specialized membrane is continuous with the host plasma membrane. Within a few minutes.Yamaoka et al. The multidigitate structure is surrounded by the perihaustorial membrane of host origin. 2009). 2010). 2003). 2009). much larger than those of related Ascomycota (Spanu et al.. The peg develops a complex multidigitate haustorium surrounded by a perihaustorial matrix and a specialized host membrane (Fig. carbohydrate degradation and nitrate uptake and. changing regulatory constraints and the evolution of mildew strains capable of overcoming host resistance. cucumbers. by massive proliferation of genes predicted to encode protein effectors. Control of Blumeria is achieved by the deployment of fungicides and disease-resistant plant varieties. overall.

. leaf cell death and the loss of membrane permeability occur. 2002. 2011). MYCOSPHAERELLA GRAMINICOLA The ascomycete Mycosphaerella graminicola (anamorph Septoria tritici) is in the order Dothideales and causes Septoria tritici blotch (STB) disease of wheat (Fig.. This latter phase involves a switch to necrotrophic nutrition (Fig. 13). 1996. allowing nutrient release into the apoplast. 12). Fig.422 R. 2011.. particularly in temperate growth regions (Orton et al. Keon et al. A lengthy period of symptomless intercellular colonization (>7 days) then follows.. Stukenbrock et al. The genome sequences of a model isolate. Extensive hyphal growth and asexual sporulation (pycnidia and pycnidiospore formation) are now supported within leaf lesions.. 2011). 7.. This represents the largest number of dispensable chromosomes so far reported in fungi (Wittenberg et al. DPI) involves the release of plant defence-suppressing apoplastic effectors (red and blue triangles) from slow-growing intercellular hyphae. This initial evasion of plant defences reflects a mechanism more typical of obligate biotrophs. followed by subsequent ‘hijack’ of plant defence signalling (Deller et al. what follows is an acute activation of plant defences involving host cell death as the fungus transitions to necrotrophic colonization (Keon et al. These studies have highlighted the existence of 21 chromosomes. graminicola arises indirectly from its rapid evolution in response to selective pressures. 2011).. 2005). which culminates in the formation of necrotic leaf lesions within which My.. 2005). DEAN et al . 2011). 2007).. Stukenbrock et al. involving initial ‘subterfuge’. Subsequent post-penetration stealth pathogenesis is supported through a reduced gene set for cell wall-degrading enzymes (Goodwin et al. 2002). This level of genetic diversity arises from the heterothallic sexual reproductive system and the formation of ascospores that initiate epidemics each season (Chen and McDonald. 2011. Functional genomics analysis of the plant infection process has identified a number of genes important for signalling transitions to hyphal growth and stomatal penetration (Orton et al. Examples of this include the speed with which My. 2011) and high-level expression of secreted effector proteins which suppress the activation of plant defences (Marshall et al. 2011.. Long-term datasets (from 1843 to 2003) have demonstrated that STB is influenced by climatic changes. 2009). Early symptomless colonization (<7 days post-leaf inoculation. and the rapid evolution of the CYP51 target protein in response to the widespread use of particular azole fungicides (Cools et al. Wittenberg et al. 2003). This constitutes an intriguing mechanism for future analysis (Fig. which comprises the largest number of plant-pathogenic fungi. Waalwijk et al. 2008). However. 12 Septoria tritici blotch (STB) disease of wheat caused by Mycosphaerella graminicola.. the eight smallest of which are all dispensable for plant infection and vary in number and structure between isolates (Goodwin et al.. together with relatives collected from wild grasses. © 2012 THE AUTHORS MOLECULAR PLANT PATHOLOGY © 2012 BSPP AND BLACKWELL PUBLISHING LTD MOLECULAR PLANT PATHOLOGY (2012) 13(4). 13). 1996.. 2007. including those associated with the industrial revolution (Bearchell et al. 13). Defence-suppressing effectors are ‘switched off’. 2011). Fig. which may be shared by other members of the genus Mycosphaerella. Mycosphaerella graminicola infection of wheat begins with hyphal extension on the leaf surface and penetration through stomata without differentiation of an appressorium (Fig. Much of the economic cost incurred by My.. Mycosphaerella graminicola has also been the subject of intense genetics and genomics analyses.. Rudd et al... have been published recently (Goodwin et al.. 2011). Mycosphaerella graminicola is a well-established model organism for the study of pathogen population dynamics and evolution. graminicola sporulates asexually (Kema et al. graminicola field populations evolved and propagated a genetic mutation providing resistance to the strobilurin class of fungicides (Fraaije et al.. although other potentially toxic effectors (blue diamonds) may be produced. 2009). Linde et al. 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. including disease-resistant wheat cultivars and the sustained use of fungicides.. This is a major economic constraint on wheat productivity. After 7 days.. 414–430 . 13 A model for wheat leaf infection by Mycosphaerella graminicola.

grown by subsistence farmers in developing countries throughout the tropics and subtropics. 414–430 . Magnaporthe) have long been of interest to phytopathologists. It is particularly successful as a post-harvest pathogen because latent infections. producing its conidia in acervuli. e. Fig. The recently completed C. Photograph courtesy of Dr Richard O’Connell (Department of Plant Microbe Interactions. biochemical. The fungus later switches to a destructive. gloeosporioides (Table 2). and RAS/small G-protein and calcium-mediated signalling pathways have been cloned. Lexington. Up to 100% of the stored fruit can be lost as a result of Colletotrichum disease (Prusky. boninense C. Max Planck Institute for Plant Breeding Research. the number of species can range from 29 to over 700 (von Arx. factors regulating the transition from biotrophy to necrotrophy await identification. vegetables and ornamentals. These fungi cause anthracnose spots and blights of aerial plant parts and post-harvest rots. University of Kentucky. For example.g. MAPK. C. fragariae C. lindemuthianum Host Papaya/citrus/many other hosts Strawberry/others Tomato Corn Broad host range Alfalfa Pepper/other hosts Legumes/tobacco Several grasses Dryandra Radish/other hosts Coffee Melon/cucumber Sorghum Legumes Banana Strawberry/other hosts Spinach Common bean Lifestyle Hemibiotrophy Necrotrophy Hemibiotrophy Hemibiotrophy Hemibiotrophy Hemibiotrophy Necrotrophy Hemibiotrophy ? Hemibiotrophy Hemibiotrophy Hemibiotrophy Hemibiotrophy Hemibiotrophy Hemibiotrophy Hemibiotrophy Hemibiotrophy Hemibiotrophy Hemibiotrophy *Dependent on host and infected tissue. Many uncertainties exist with regard to the systematics of fungal pathogens from this genus and. 1911). 14)... Chen et al. crassipes C. graminicola sequence (Vaillancourt et al. graminicola C. conidium. 1996). COLLETOTRICHUM SPP. 1957. Most Colletotrichum species initially establish infection through a brief biotrophic phase. Colletotrichum is an asexual genus. acutatum C. orbiculare C. associated with large intracellular primary hyphae. For example. Colletotrichum on bean was the model for many of the early studies on phytoalexins (reviewed by Kuc. Department of Plant Pathology. Key genes of the cyclic adenosine monophosphate (cAMP). With permission). trifolii C. It belongs to the Coelomycetes.g. the phenomenon of pathogenic variation (race/cultivar specificity) was first recognized in C. e. although some species are described as subcuticular. Sutton. 2000). thinner necrophic penetrating hyphae (PH) degrade tissue whilst growing inside the cell. 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. associated with narrower secondary hyphae which ramify throughout the host tissue (Fig. capsici C. dematium C. 594 species of Colletotrichum were reclassified by von Arx as synonyms of C. appressorium. Dickman and Yarden. sublineolum C. particularly during conidial germination and appressorium development. do not become active until after the fruit has been stored or appears on the market shelf. the taxonomy of Colletotrichum remains in a state of flux. depending on criteria. 2004). spinaceae C. extends to important staple food crops. gloeosporioides* C. C. © 2012 THE AUTHORS MOLECULAR PLANT PATHOLOGY © 2012 BSPP AND BLACKWELL PUBLISHING LTD MOLECULAR PLANT PATHOLOGY (2012) 13(4). Colletotrichum species C. lindemuthianum (Barrus. capsici. 1972). its unique intracellular hemibiotrophic lifestyle and the ease with which it can be cultured and manipulated. 14 Transmission electron micrograph showing hemiotrophic growth of Colletotrichum destructivum during cowpea infection. A. 1995. 2004. In particular. including bananas. gloeosporioides. kahawae C. Cologne. musae C. The molecular details that govern the hemibiotrophic lifestyle (also known to occur in other fungal species. which are initiated before harvest. classified within the Fungi imperfecti. physiological and genetic studies. Subsequently. The host cell is still alive and its plasma membrane can be seen surrounding the hypha. 1992).. truncatum C. 2006. Note the thick biotrophic infection vesicle (IV) following appressorium penetration. together with several other Colletotrichum species in the pipeline. Takano et al. Virtually every crop grown throughout the world is susceptible to one or more species of Colletotrichum. Table 2 The major species of Colletotrichum. 1999. One of the most confusing species is C. Despite significant developments. destructivum C. The damage caused by Colletotrichum spp. Dickman et al. caudatum C. The function of these genes. necrotrophic phase. During the 1970s and through the 1990s. Colletotrichum has a long and distinguished history as a model pathogen for fundamental.. Colletotrichum is one of the most common and important genera of plantpathogenic fungi. As a result of its importance as a pathogen. promises to increase our understanding of this important fungal phytopathogen. Kentucky).Top 10 fungal pathogens 423 8. has been characterized in several Colletotrichum species (reviewed by Chen and Dickman. Members of this genus cause major losses to economically important crops. coccodes C. cassava and sorghum. especially fruits.

. 15D) and an infection cycle is completed in about 2 weeks. nourseothricine resistance (NatR). 15F) are available (Böhmer et al.gov/geo/). CbxR. USTILAGO MAYDIS Corn smut is not an economically important or devastating disease. Ustilago maydis has not made it into the Top 10 for this reason. 15C). Skibbe et al. in most cases. fungal hyphae are stained with WGA-AF488 (green). reilianum (F) (E) (D) visualization of the actin cytoskeleton tumours on leaves and biotrophic growth whole-genome arrays MOLECULAR PLANT PATHOLOGY (2012) 13(4).helmholtz-muenchen.. and mating and the formation of a dikaryotic filament are absolutely required. (E) Affymetix gene chips allow genome-wide expression studies. 2009. DEAN et al . (H) Phylogenetic tree of U. please note that their permission for using these Figures has been obtained. the fungus is haploid and grows by budding (Fig. maydis disease symptoms in infected maize cob. tools and disease symptoms. Such strains enable forward genetic screens and greatly reduce work in reverse genetics approaches..ncbi. 2004). Basse and Steinberg.. Mendoza-Mendoza et al. which are likely to reveal insights into both genome evolution and host specialization. 2010a. These steps can be reproduced in the laboratory (Fig.de/genre/proj/ustilago). Wahl et al. From genome analysis. do not spread and are hence not associated with severe losses in corn yield..424 R. Quite the contrary. 15G.. 2008). Holloman. centre). 2009. 15A) and forms compact colonies on plates that can be replica plated. This knowledge has allowed the construction of haploid solopathogenic strains that cause disease without need for a mating partner (Bölker et al. Transcriptional profiles (Fig. NatR. 2006. maydis is more closely related to humans than to budding yeast.. (A) Haploid cells display budding growth. (D) Macroscopic U. 15. plant-pathogenic basidiomycetes? Ustilago maydis can be grown in culture in defined media. 2010). b). What are the attractions of this fungus and why has it become a model for biotrophic. 2009. farmers in Mexico infect corn artificially to harvest infected cobs for the preparation of Huitlacoche. Steinberg and Perez-Martin. The genome is ‘lean’ and contains little repetitive DNA. mitosis.. Homologous recombination is amazingly efficient (Kämper. Therefore. 15E) have been established for the most important developmental fungal stages and plant responses (accessible through GeneExpressionOmnibus: http:// www. 2011. Typical for smut fungi is that pathogenic development equals sexual development. both at the Max Planck Institute for Terrestrial Microbiology. maydis disease symptoms on a maize leaf 12 days post-infection (left) and fungal hyphae in tumour tissue 10 days post-infection (right) are visualized by confocal microscopy. Symptoms can develop on all above-ground parts of maize plants in 5–6 days (Fig. Fig. provide insights into fungal nutrition during plant colonization (Eichhorn et al. PhleoR S.. the 20. 2004) and makes use of four dominant selectable markers (Fig. 2008). 2006. and numerous proteins are shared only by U. These were actually some of the reasons for choosing this fungus for seminal early studies on homologous recombination (Holliday. 2006. 15D). a traditional dish popular in pre-Hispanic times. maydis strains expressing cytoplasmic red fluorescent protein (RFP) (red) and green fluorescent protein (GFP) (green) under a constitutive promoter mate and produce a filamentous dikaryon (yellow). 2006). maydis and its closest relatives. infections remain local.. Since 2006. (B) Compatible haploid U. 2009. mating revealed by colour budding growth (A) (B) filamentous growth and appressoria formation (C) homologous recombination (G) Gene of interest phylogeny (H) U. http:// mips. This includes proteins involved in basic principles of longdistance transport. maydis Selection marker HygR.. (C) A solopathogenic strain expressing cytoplasmic RFP from a constitutive promoter and an appressorial marker gene fused to triple GFP efficiently forms appressoria on a hydrophobic surface. Although its symptoms on corn can be quite dramatic (Fig. after stimulation with hydroxy-fatty acids. (G) Highly efficient homologous recombination is used for gene replacement employing hygromycin resistance (HygR). 2011. 15B) up to the formation of appressoria on appropriate hydrophobic surfaces (Fig. 414–430 © 2012 THE AUTHORS MOLECULAR PLANT PATHOLOGY © 2012 BSPP AND BLACKWELL PUBLISHING LTD . Kämper et al. 1995.nih. 9. Ustilago maydis is therefore a perfect host for the study of such processes (Banuett et al. 2010) and serve as the blueprint for comparative approaches (Schirawski et al.. Where is this system heading? It will allow the establishment of the hierarchy of effector action during plant colonization. This has spurred reverse genetics approaches and has allowed the identification of clustered genes encoding secreted effectors that play crucial roles during host colonization. (F) Visualization of F-actin through LifeAct-YFP in budding cells. centre). 2010). 2008. and the determination of which tissue can be infected (Doehlemann et al. Kämper et al.5-Mb manually annotated and curated genome sequence has been available (Kämper et al. as well as a heterodimeric transcription factor formed after cell fusion that triggers a regulatory cascade (Brefort et al. Figures were kindly provided by Patrick Berndt and Rolf Rösser (U. The proteins controlling these events are known: pheromones and pheromone receptors. corn seedlings can be infected. motor-based microtubule organization and homologous recombination. and fluorescent proteins for live cell imaging of gene expression and visualization of subcellular structures (Fig.nlm. Tools include regulated promoters for the study of essential genes and a variety of staining methods to visualize the fungus during biotrophic growth (Fig. it has also become apparent that U. Steinberg and PerezMartin. plant cell walls are stained with propidium iodide (red).. Heimel et al. For host colonization and symptom development.. carboxin resistance (CbxR) or phleomycin resistance (PhleoR) as dominant selectable markers. Also. maydis and Homo sapiens. hordei U. 2004). 15 Developmental stages of Ustilago maydis.

its main impact on food and fibre production came (and comes) from its role as a model system. 2010). nematodes. Classical genetic studies (approximately 1926–1981) Through pioneering genetic studies (Fig. cytoplasmic nucleotide-binding leucine-rich repeat (NB-LRR) proteins.. flax rust is more famous than infamous. 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 corresponding avirulence gene or genetic re-assortment during sexual reproduction of previously ‘hidden’ recessive virulence alleles to produce progeny homozygous for virulence. 1988. 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. Genetic analysis in flax rust depends on the ability to replicate all stages of the life cycle under controlled conditions to produce selfed and outcrossed progeny from flax rust isolates. Although it was initially studied as a pathogen having an impact on the flax and linseed industries. and is complicated by the rust being an obligate biotroph... 16). The same protein group was subsequently identified in animals as part of the innate immune system. The intracellular nature of the flax resistance proteins implied that the Avr (effector) proteins were detected by R proteins within host cells. providing insights into the molecular basis of plant immunity. In practical terms. and duplication and deletion of LRR units by intragenic recombination (Ellis et al.. the foundation for the development of the current knowledge of the basis of plant immunity. H. requiring all manipulations to be undertaken on the living host plant. Lawrence. viruses. 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. MELAMPSORA LINI In contrast with most of the other pathogens on this ‘Top 10’ list. 414–430 . and that the likely origin of new resistance specificities in nature results from point mutations. 2007). 2007). re-assortment of the mutations. bacteria. specific members of which provided host plant resistance against fungi. Fig. 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 transformation system for this obligate biotroph (Lawrence et al. 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. which provided pathologists and plant breeders with a logical foundation to reconcile the process of breeding other crop species for resistance to pathogens. 2007). Molecular studies (1988 to present) The flax rust system was among the first three systems to provide cloned resistance genes and the identification of a new class of immune receptor. 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. 2010) (Fig. 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.. sucking insects and parasitic plants (Ellis et al.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. 16 Life cycle of flax rust. 2007). 16) of the pathogenicity of different physiological races of the pathogen and the resistance and susceptibility to rust in flax. The molecular basis for gene-for-gene recognition was shown to rely on specific and direct interaction between flax R proteins and corresponding Avr proteins. and a resulting recognition event that gives rise to host resistance.. © 2012 THE AUTHORS MOLECULAR PLANT PATHOLOGY © 2012 BSPP AND BLACKWELL PUBLISHING LTD MOLECULAR PLANT PATHOLOGY (2012) 13(4). Melampsora lini. 1956.This became known as the ‘gene-for-gene’ relationship. oomycetes.Top 10 fungal pathogens 425 10.H. Lawrence et al.

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