Colletotrichum Genome Project

Project Information

The Colletotrichum genome database provides access to the sequenced genomes of Colletotrichum graminicola and Colletotrichum higginsianum. The C. graminicola genome project is part of the Broad Fungal Genome Initiative, and was funded by the National Institute of Food and Agriculture (NIFA) through the NSF/USDA Microbial Genome Sequencing Program. C. higginsianum was sequenced under the direction of Dr. Richard J. O'Connell, with funding from the Max Planck Institute for Plant Breeding Research, Cologne, Germany.

Introduction

Colletotrichum is one of the most common and important genera of plant-pathogenic fungi. Virtually every crop grown throughout the world is susceptible to one or more species of Colletotrichum. Colletotrichum fungi cause post-harvest rots, and anthracnose spots and blights of aerial plant parts. Members of this genus cause major economic losses, especially of fruits, vegetables, and ornamentals. Colletotrichum is very damaging to important food crops, including bananas, cassava, sorghum, and pulses, grown by subsistence farmers in developing countries throughout the tropics and subtropics. In addition to their considerable economic importance, the Colletotrichum fungi are highly significant as experimental models in studies of many aspects of fungal development, infection processes, host resistance, signal transduction, and the molecular biology of plant-pathogen interactions. Dozens of laboratories around the world are studying the biology and pathology of various species of Colletotrichum.

Intracellular hemibiotrophy is a distinctive aspect of Colletotrichum pathology. Following penetration of the host epidermis, most Colletotrichum species initially colonize living plant cells, breaching the cell wall but without penetrating the host cell plasma membrane or causing widespread cell death. After a variable period of time (the length of which depends on the specific pathosystem) the growth habit switches to necrotrophy, and massive cell death and tissue destruction ensues. This switch in lifestyle is associated with dramatic and well-characterized morphological, genetic, and physiological changes in the hyphae. Biotroph-like and necrotroph-like infection structures of Colletotrichum can be distinguished cytologically and mutants are available that produce only one type, facilitating functional genomic studies. Colletotrichum genes have been cloned that are differentially expressed during the two phases. Many Colletotrichum species have the capacity to produce asymptomatic latent (quiescent) infections on various plant tissues, including unripe fruits, placing them among the most important postharvest pathogens. Many Colletotrichum fungi are also endophytic on their host plants. Thus, Colletotrichum presents a unique opportunity for comparative genomic analyses of common plant-associated lifestyles (biotrophy vs. necrotrophy vs. endophytic vs. latency) within a single genus, and even within a single species.

Colletotrichum graminicola

Colletotrichum graminicola Ces. Wils. causes anthracnose stalk rot and leaf blight of maize. Maize is the dominant crop in the United States, with a value of more than 21 billion dollars in 2005, and a broad range of uses, from animal feed to sweeteners and fuel. C. graminicola is a major cause of stalk rot disease, one of the most economically important diseases of maize. Industry estimates are that stalk rots causes maize yield losses in the range of 6% annually. C. graminicola is likely to become an even more serious problem in the future, because it seems to cause a larger proportion of the stalk rots on maize engineered with the Bt transgene. C. graminicola also causes a leaf blight that is becoming increasingly important, particularly in the tropics and subtropics. C. graminicola is among the best characterized and most tractable of the Colletotrichum fungi. It is one of very few in which sexual crosses can be made (the teleomorph is Glomerella graminicola); it is easily cultured and stored; transformation and gene disruption are routine; and pathogenicity assays are straightforward. Maize, its host, is a classical genetic model as well as an important crop plant. Sequencing of the entire maize genome began in 2005 and should be completed soon.

In 2006, the USDA/National Science Foundation Microbial Genome Sequencing Project National Research Initiative funded a project to sequence the genome of C. graminicola. C. graminicola strain M1.001 (also known as M2) is the first member of the Colletotrichum genus to be fully sequenced. C. graminicola strain M5.001 was sequenced to about 1X coverage by a research team at DuPont Nemours Inc. The sequence data were generously donated to the public by DuPont in 2008.

Colletotrichum higginsianum

Colletotrichum higginsianum causes anthracnose leaf spot disease on many cultivated forms of Brassica and Raphanus, but can also infect the model plant Arabidopsis thaliana. This provides an attractive pathosystem for dissecting fungal pathogenicity and plant resistance, in which both partners can be genetically manipulated. The pathogen employs a hemibiotrophic infection strategy to invade host plants, involving differentiation of a series of specialised cell types (infection structures). After initial penetration of host epidermal cells by appressoria, the fungus grows biotrophically inside living epidermal cells, producing bulbous primary hyphae that invaginate the host plasma membrane, before later switching to a destructive necrotrophic phase associated with filamentous secondary hyphae. The fungus completes its asexual cycle by producing sporulating structures called acervuli on the surface of the dead tissue. Phylogenetic analysis based on sequencing the ITS regions of rDNA indicates that C. higginsianum forms part of a group of closely-related taxa that also includes C. destructivum (tobacco and legume pathogen) and C. linicola (flax pathogen). A characteristic feature of all three species is that the initial biotrophic phase of infection is restricted to a single host epidermal cell, in contrast to other hemibiotrophic Colletotrichum species, including C. graminicola, which establish biotrophy in many host cells.

Including both C. higginsianum and C. graminicola on this single website will facilitate the comparison of the genomes of these two sister species which have contrasting hemibiotrophic lifestyles and also differ in their host specificity. It will also enable the identification of genes undergoing rapid evolution (diversifying selection), which are likely to be involved in interactions with the host plant, e.g. those encoding effector proteins. Overall, we envisage that C. graminicola will provide a model for anthracnose diseases on monocot hosts, while C. higginsianum will become the model of choice for studying Colletotrichum infection of dicot plants.

Main collaborators

Lisa Vaillancourt (PI), The University of Kentucky
Lijun Ma, The Broad Institute
Martin Dickman, Texas A&M University
Michael Thon, The University of Salamanca in Spain
Richard J. O'Connell (PI), Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research

Photo Credits and Captions

The images on the home page are, from left to right:
Perithecia and asci of G. graminicola. Vaillancourt and Hanau, 1991
Primary infection hyphae in a maize leaf. The dark areas (white arrow) are where the hyphae have passed through a very narrow opening from one cell to the next. By C. Venard.
Thick, irregularly shaped primary infection hyphae (white arrow) with narrower secondary hyphae arising from them (orange arrows) in maize stalk cells. From Venard and Vaillancourt, 2007
Acervulus of C. graminicola with falcate spores and setae. By R. Nicholson
Appressoria of C. graminicola (arrows) formed from a spore incubated on a plastic coverslip. By Richard O'Connell from Max Planck Institute for Plant Breeding Research, Cologne, Germany.

 

Data Use and Citation

The genome assembly and annotation of the C. graminicola genome is available in Genbank.  The genomes are also available at the JGI Mycocosm site and at Ensembl using the following links:

http://genome.jgi.doe.gov/Colgr1/Colgr1.home.html
http://genome.jgi.doe.gov/Colhi1/Colhi1.home.html

http://fungi.ensembl.org/Colletotrichum_graminicola/Info/Index
http://fungi.ensembl.org/Colletotrichum_higginsianum/Info/Index

Data files formerly available on this website can be accessed on our fungal ftp site.

For use of this data, please cite: O'Connell et al "Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses." Nature Genetics. 2012 Sep;44(9):1060-5. doi: 10.1038/ng.2372. Epub 2012 Aug 12.