Effector diversification within compartments of the Leptosphaeria maculans genome affected by repeat induced point mutations

Authors: ROUXEL, T - Institut National De La Recherche Agronomique (INRA); GRANDAUBERT, JONATHAN - Institut National De La Recherche Agronomique (INRA); HANE, JAMES - Murdoch University; HOEDE, CLAIRE - Institut National De La Recherche Agronomique (INRA); VAN DE WOUW, ANGELA - University Of Melbourne; COULOUX, ARNAUD - Genoscope; DOMINGUEZ, VICTORIA - Institut National De La Recherche Agronomique (INRA); ANTHOUARD, VERONIQUE - Genoscope; BALLY, PASCAL - Institut National De La Recherche Agronomique (INRA); BOURRAS, SALIM - Institut National De La Recherche Agronomique (INRA); COZIJNSEN, ANTON - University Of Melbourne; CIUFFETTI, LYNDA - Oregon State University; DEGRAVE, ALEXANDRE - Institut National De La Recherche Agronomique (INRA); DILMAGHANI, AZITA - Institut National De La Recherche Agronomique (INRA); DURET, LAURENT - University Of Lyon; FUDAL, ISABELLE - Institut National De La Recherche Agronomique (INRA); Goodwin, Stephen - Steve; GOUT, LILIAN - Institut National De La Recherche Agronomique (INRA); GLASER, NICOLAS - Institut National De La Recherche Agronomique (INRA); LINGLIN, JULIETTE - Institut National De La Recherche Agronomique (INRA); KEMA, GERT H. - University Of Wageningen; LAPALU, NICOLAS - Institut National De La Recherche Agronomique (INRA); LAWRENCE, CHRISTOPHER - Virginia Polytechnic Institution & State University; MAY, KIM - University Of Melbourne; MEYER, MICHEL - Institut National De La Recherche Agronomique (INRA); OLLIVIER, BENEDICTE - Institut National De La Recherche Agronomique (INRA); POULAIN, JULIE - Genoscope; SIMON, ADELINE - Institut National De La Recherche Agronomique (INRA); STACHOWIAK, ANNA - Institute Of Plant Genetics; TURGEON, GILLIAN - Cornell University; TYLER, BRETT - Virginia Polytechnic Institution & State University; VINCENT, DELPHINE - Institut National De La Recherche Agronomique (INRA); WEISSENBACH, JEAN - Institut National De La Recherche Agronomique (INRA); AMSELEM, JOELLE - Institut National De La Recherche Agronomique (INRA); BALESDENT, MARIE-HELENE - Institut National De La Recherche Agronomique (INRA); HOWLETT, BARBARJ - University Of Melbourne; OLIVER, RICHARD - Murdoch University; QUESNEVILLE, HADI - Institut National De La Recherche Agronomique (INRA); WINCKER, PATRICK - Genoscope

Submitted to: Nature Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/11/2011
Publication Date: 2/15/2011
Citation: Rouxel, T., Grandaubert, J., Hane, J.K., Hoede, C., Van De Wouw, A. ., Couloux, A., Dominguez, V., Anthouard, V., Bally, P., Bourras, S., Cozijnsen, A.J., Ciuffetti, L.M., Degrave, A., Dilmaghani, A., Duret, L., Fudal, I., Goodwin, S.B., Gout, L., Glaser, N., Linglin, J., Kema, G.G., Lapalu, N., Lawrence, C.B., May, K., Meyer, M., Ollivier, B., Poulain, J., Simon, A., Stachowiak, A., Turgeon, G.B., Tyler, B.M., Vincent, D., Weissenbach, J., Amselem, J., Balesdent, M., Howlett, B., Oliver, R.P., Quesneville, H., Wincker, P. 2011. Effector diversification within compartments of the Leptosphaeria maculans genome affected by repeat induced point mutations. Nature Communications. 2:202.

Interpretive Summary: The plant-pathogenic fungus Leptosphaeria maculans causes blackleg of canola and other mustard (Brassica) relatives. This disease can cause economically important damage of canola crops grown for food or for biofuels. Control of the disease has been hampered by a limited understanding of the genetic and biochemical bases of pathogenicity. To address this problem, the genome of the fungus was sequenced through an international collaboration lead by GENOSCOPE in France. A unique feature of the fungal genome was its bipartite structure, divided between distinct regions (isochores) containing high or low frequencies of specific DNA building blocks. One group of isochores, comprising two-thirds of the genome and with a high frequency of G and C building blocks was gene rich, whereas the remaining one third of the genome had a low frequency of G and C and contained very few genes. A large number of movable DNA elements occurred in the gene-poor regions. A complete repertoire of putative pathogenicity effector proteins was identified, most of which occurred as small islands of coding sequence in the gene-poor regions. These genes mostly encoded small proteins that are secreted by the fungus and could interact with host genes to cause disease. Understanding the function of these genes should allow more durable resistance to be developed in the future. This information will be useful to fungal geneticists and evolutionary biologists to better understand the genetics and evolution of L. maculans. Plant pathologists may be able to use this information to design better strategies for disease management, particularly once the biochemical bases for the genetic interactions between host and pathogen are better understood.

Technical Abstract: The genome sequence of the phytopathogenic fungus Leptosphaeria maculans has been determined. It has a unique bipartite structure, divided between distinct GC-equilibrated and AT-rich regions (isochores), reminiscent of some plants and animals but not previously observed in fungi. The GC-equilibrated isochores (with 51% GC) are gene-rich whereas AT-rich isochores (34% GC, one third of the genome) are gene-poor. The 45 Mb assembly has families of transposable elements (TEs) that are clustered, truncated and affected by Repeat-Induced Point (RIP) mutation, a process that has also severely affected some of the tandemly repeated ribosomal DNA units. A complete repertoire of putative pathogenicity effectors has been established. A fifth (122) of the genes in AT-rich isochores, encode small, cysteine-rich, secreted proteins (SSPs), with plant cell translocation signals. The genes have a low GC content and distinct codon usage bias, are extremely diverse with no recognizable multigene families and few homologues in databases, and are generally expressed at high levels in planta. Some of these effectors are affected by RIP, which generates diversification as a consequence of their location within RIP-affected isochores.