The Genomics of Colletotrichum 3 Joanne Crouch, Richard O’Connell, Pamela Gan, Ester Buiate, Maria F
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The Genomics of Colletotrichum 3 JoAnne Crouch, Richard O’Connell, Pamela Gan, Ester Buiate, Maria F. Torres, Lisa Beirn, Ken Shirasu, and Lisa Vaillancourt top ten most important fungal phytopathogens 3.1 Introduction (Dean et al. 2012). Economically important diseases caused by The fungal genus Colletotrichum includes more Colletotrichum are widespread, occurring on than 100 species responsible for anthracnose maize, beans, strawberries, coffee, chili peppers, foliar blight and rot diseases of nearly every crop cucurbits, potatoes, and countless other culti- grown for food, fiber, and forage worldwide vated plants (e.g., Bergstrom and Nicholson (Cannon et al. 2012b; Hyde et al. 2009). 1999; Hyde et al. 2009; Lees and Hilton 2003; Because of their ubiquity, substantial capacity Legard 2000; Melotto et al. 2000; Prihastuti for destruction, and scientific importance as et al. 2009; Singh and Schwartz 2010; Than model pathosystems, fungi in the genus Collet- et al. 2008; Ureña-Padilla et al. 2002; Varzea otrichum are collectively ranked by the inter- et al. 2002; Waller 1992; Wasilwa et al. 1993; national plant pathology community among the Xie et al. 2010). Colletotrichum postharvest fruit rots are responsible for major economic losses, with severe infections resulting in up to 100 % J. Crouch Systematic Mycology and Microbiology Lab, loss during storage (Prusky 1996). Colletotri- USDA-ARS 10300 Baltimore Ave. Bldg. chum diseases also produce substantial damage 10A, Room 228, Beltsville, MD, on important subsistence crops including lentil, 20705, USA cowpea, yam, banana, sorghum, and cassava e-mail: [email protected] (Adegbite and Amusa 2008; Chona 1980; R. O’Connell Chongo et al. 2002; Finlay and Brown 1993; UMR1290 BIOGER-CPP, INRA-AgroParisTech, Avenue Lucien Brétignières, 78850, Thiverval-Grignon, France E. Buiate e-mail: [email protected] e-mail: [email protected] P. Gan Á K. Shirasu M. F. Torres Plant Science Center, RIKEN, Yokohama, e-mail: [email protected] Japan e-mail: [email protected] M. F. Torres Functional Genomics Laboratory, Weill Cornell K. Shirasu Medical College, Cornell University, Qatar e-mail: [email protected] Foundation-Education City, Doha, Qatar E. Buiate Á M. F. Torres Á L. Vaillancourt (&) L. Beirn Department of Plant Pathology, University of Department of Plant Biology and Pathology, Kentucky, 201F Plant Science Building, Lexington, Rutgers, The State University of New Jersey, 59 KY 40546, USA Dudley Road, New Brunswick, NJ 08901, USA e-mail: [email protected] e-mail: [email protected] R. A. Dean et al. (eds.), Genomics of Plant-Associated Fungi: Monocot Pathogens, 69 DOI: 10.1007/978-3-662-44053-7_3, Ó Springer-Verlag Berlin Heidelberg 2014 70 J. Crouch et al. Green and Simons 1994; Moses et al. 1996; substantially elucidated using Colletotrichum Moura-Costa et al. 1993). (Kubo and Takano 2013). Key components of Colletotrichum diseases can negatively the cyclic-AMP, MAP kinase, and calcium- impact many of the most important monocots mediated signaling pathways have been cloned targeted as candidate bioenergy crops, including and characterized from Colletotrichum species switchgrass, miscanthus, maize, sorghum, indi- (e.g., Chen and Dickman 2002, 2004; Dickman angrass, and sugarcane (Crouch 2013; Crouch and Yarden 1999; Ha et al. 2003; Kim et al. and Beirn 2009; Crouch et al. 2009a, b; Cortese 2000; Takano et al. 2000; Warwar and Dickman and Bonos 2012; Dahlberg et al. 2011; Hartman 1996; Yang and Dickman 1997, 1999a, b). et al. 2011; King et al. 2011; Waxman and Today, Colletotrichum species continue to serve Bergstrom 2011a, b; Zeiders 1987). Plants in a as important models for studies of the molecular wide variety of uncultivated terrestrial and and cellular basis of pathogenicity (Kubo and aquatic biomes may also be impacted by Col- Takano 2013; O’Connell et al. 2012; O’Connell letotrichum infections, including forests, grass- and Panstruga 2006; Perfect et al. 1999). lands, prairie, shrub land, savannahs, and deserts (Abang et al. 2006; Ammar and El-Naggar 2011; Crouch 2013; Crouch et al. 2009b; Damm et al. 3.2 Systematics of Colletotrichum 2012a; Dingley and Gilmour 1972; Lubbe et al. 2004; Soares et al. 2009). Colletotrichum is an asexual fungus, with the Colletotrichum occupies a noteworthy place sexual state traditionally classified in the Asco- in the history of plant pathology and mycology. mycete genus Glomerella (Sordariomycetes; The first description of physiological races and Hypocreomycetidae; Glomerellaceae; Glome- cultivar specificity involved the causal agent of rellales) (Réblová et al. 2011). With the adoption bean anthracnose, C. lindemuthianum (Barrus of single name nomenclature for pleomorphic 1911), with that work leading to some of the first fungi established by the 2013 Melbourne Code of resistance breeding efforts using race differen- the International Code of Nomenclature for tials (reviewed in Geffroy et al. 1999). Sub- algae, fungi, and plants (www.iapt-taxon.org/ sequent work with the bean anthracnose nomen/main.php), it is unlikely that the Glome- pathosystem has greatly advanced our under- rella name will continue to be used in the future. standing of the gene-for-gene system (López Although several species in the genus are known et al. 2003; Melotto and Kelly 2001). Work with that produce the teleomorph readily (e.g., the teleomorph of C. gloeosporioides pioneered G. cingulata, G. acutata), Colletotrichum species early investigations of fungal sexual determina- are predominantly observed in the vegetative or tion and development (Lucas et al. 1944, Chilton asexual state, with the sexual morph rarely et al. 1945, Chilton and Wheeler 1949a, b; identified for most species (Vaillancourt et al. Driver and Wheeler 1955; Edgerton et al. 1945; 2000b). Since plant pathologists and mycologists Lucas 1946; Wheeler 1950, 1954; Wheeler et al. working with the fungus typically encounter the 1948; Wheeler and McGahan 1952). In the anamorph, the Colletotrichum name more accu- 1960s and 1970s, Colletotrichum studies were at rately communicates biological information the cutting edge of our understanding of the about the organism. Furthermore, Colletotrichum nature of systemic induced resistance, the is the older of the two genera and has priority chemistry of host defense, and the importance of (1831 vs. 1903; www.mycobank.org). Final res- phytoalexins in the defense response, and they olution of the sole adopted genus name will go enabled purification of elicitor molecules from through the formal channels established by the fungal cell walls for the first time (Kuc 1972; International Subcommission of Colletotrichum Sticher et al. 1997). The development and Taxonomy (www.fungaltaxonomy.org/ subcom- function of melanized appressoria has been missions) to ensure community consensus. In this 3 The Genomics of Colletotrichum 71 chapter we will use Colletotrichum to refer both characterized through multilocus phylogenies to the anamorphic and the teleomorphic phases. (Crouch et al. 2009a; Damm et al. 2009; 2012a, Colletotrichum is the sole member of the b; Weir et al. 2012), yielding a framework for Glomerellaceae, one of three families that col- understanding evolutionary relationships across lectively make up the order Glomerellales in the the genus as a whole (Cannon et al. 2012b). Sordariomycete subclass Hypocreomycetidae (Réblová et al. 2011). Earlier reports suggested Colletotrichum as a sister group to Verticillium 3.3 Colletotrichum Lifestyles (Zhang et al. 2006), but more comprehensive and Modes of Infection research has shown that this inferred relationship reflected insufficient sampling rather than an Fungi in the genus Colletotrichum display a actual close phylogenetic association, as Verti- range of nutritional strategies and lifestyles, cillium is a member of the Plectosphaerellaceae including plant associations that occupy a con- (Cannon et al. 2012a; Réblová et al. 2011; Zare tinuum from necrotrophy to hemibiotrophy and et al. 2000). endophytism. Some species employ a sapro- During the past several years, Colletotrichum trophic lifestyle to obtain nutrients from soil and taxonomy has been the subject of several sub- organic matter. Colletotrichum are also known to stantive revisions. Species concepts are still in a colonize organisms outside the plant kingdom, state of flux, but it is now well-established that including insects and humans. the genus consists of several major monophy- Plant-associated Colletotrichum species typi- letic clades that are referred to as species cally use a melanized appressorium to penetrate aggregates, described by the name and attributes host tissues (Kubo and Takano 2013) (Fig. 3.2). of the most prominent representative species in The melanin is required for appressorial func- the group (O’Connell et al. 2012; Cannon et al. tion, permitting the accumulation of significant 2012b; Fig. 3.1). To date, nine aggregates have turgor pressure that facilitates mechanical pene- been described based on multilocus molecular tration of the host cell wall (Bechinger et al. phylogenetics, namely acutatum, graminicola, 1999; Kubo and Furusawa 1991). The appres- spaethianum, destructivum, dematium, gloeo- sorium also secretes pectinases and cell wall- sporioides, boninense, truncatum, and orbiculare degrading enzymes that are likely to play diverse (Cannon et al. 2012b). Although the Colletotri- roles in preparing the infection court, adhesion, chum aggregates carry no formal taxonomic signaling,