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United States Department of Agriculture

Agricultural Research Service

Research Project: MOLECULAR AND GENETIC MECHANISMS OF HESSIAN FLY RESISTANCE IN SOFT WINTER WHEAT Title: The genomes of the fungal plant pathogens Cladosporium fulvum and Dothistroma septosporum reveal adaptation to different hosts and lifestyles but also signatures of common ancestry

Authors
item Dewit, Pierre -
item Van Der Burgt, Ate -
item Okmen, Bilal -
item Datema, Erwin -
item Cox, Murray -
item Ganley, Austen -
item Aerts, Andrea -
item Sun, Hui -
item Goodwin, Stephen

Submitted to: PLoS Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: September 19, 2012
Publication Date: November 29, 2012
Citation: Dewit, P., Van Der Burgt, A., Okmen, B., Datema, E., Cox, M.P., Ganley, A.R., Aerts, A., Sun, H., Goodwin, S.B. 2012. The genomes of the fungal plant pathogens Cladosporium fulvum and Dothistroma septosporum reveal adaptation to different hosts and lifestyles but also signatures of common ancestry. PLoS Genetics. 8(11): e1003088. DOI:10.1371/journal.pgen.1003088.

Interpretive Summary: The plant-pathogenic fungi Cladosporium fulvum and Dothistroma septosporum are very closely related but have very different lifestyles and hosts. The tomato pathogen C. fulvum obtains nutrients from living cells, while D. septosporum kills host cells before extracting nutrients from pine needles. How the two lifestyles evolved and the mechanisms of their pathogenicity are not known. To address these questions, the genomes of both pathogens were sequenced and compared. More than 70% of the genes were similar in both fungi, but the genome size of C. fulvum was almost twice that of D. septosporum, mainly due to a huge amplification of movable genetic elements called transposons in the genome of the tomato pathogen. Repeat-rich areas of the C. fulvum genome were enriched for species-specific genes including those for secreted proteins that might be involved with host interactions. Surprisingly, genes corresponding to those in C. fulvum that are involved in host-pathogen interactions also are present in D. septosporum. Two of those from the pine pathogen were recognized by tomato resistance genes to cause a hypersensitive type of resistance response. Although C. fulvum obtains nutrients from living cells, it has an enzyme catalog that is more similar to those of fungi that kill host cells before extracting nutrients and also contains a gene cluster for a toxin in D. septosporum. This information will be useful to fungal geneticists and evolutionary biologists to better understand the genetics and evolution of host specificity and lifestyle type. Plant pathologists and breeders may be able to use this information to design better strategies for disease management, particularly to explore the idea that tomato resistance genes might be useful in pine.

Technical Abstract: We sequenced and compared the genomes of Dothideomycete fungal plant pathogens Cladosporium fulvum and Dothistroma septosporum that are related phylogenetically, but have different lifestyles and infect different hosts. C. fulvum is a biotroph that infects tomato, while D. septosporum is a hemibiotroph infecting pine. The genomes of these fungi share 70% of their genes but differ significantly in size (C. fulvum, 61.1 Mb; D. septosporum, 31.2 Mb), mainly due to repeat content (47.8% versus 3.2%). Repeat-rich areas, which have expanded in C. fulvum mainly due to LINE retrotransposons and in D. septosporum to helitron-like elements, were enriched for species-specific genes including those encoding secreted proteins. Impressively, homologs of the previously cloned effector genes from C. fulvum are not only present in D. septosporum but two of them (Ecp2 and Avr4) are recognized by tomato Cf-Ecp2 and Cf-4 resistance proteins, respectively, and cause a Cf-mediated hypersensitive response. Although a biotroph, C. fulvum has a carbohydrate-degrading enzyme catalog that is more similar to that of a necrotroph; it has a larger pectinolytic gene arsenal than D. septosporum but many genes are not expressed in planta. Surprisingly, both fungi grow well on different complex carbohydrate substrates including lignin. Strikingly, some gene clusters encoding secondary metabolites (SM) including dothistromin toxin, well studied in D. septosporum, are conserved in C. fulvum. However, overall the two species have different expression profiles of SM genes; whilst EST data show that SM genes of D. septosporum are expressed during needle infection, their expression in planta is low for C. fulvum and some are pseudogenized, which might relate to their present different lifestyles.

Last Modified: 12/18/2014
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