Comparative Genomics Reveals Mobile Pathogenicity Chromosomes in Fusarium

Authors: MA, LI-JUN - Broad Institute Of Mit/harvard; BORKOVICH, KATHERINE - University Of California; COLEMAN, JEFFREY - University Of Arizona; DABOUSSI, MARIE-JOSEE - University Of Paris; PIETRO, ANTONIO - University Of Spain; DUFRESNE, MARIE - University Of Paris; FREITAG, MICHAEL - Oregon State University; GRABHERR, MANFRED - Broad Institute Of Mit/harvard; HENRISSAT, BERNARD - National Council For Scientific Research-Cnrs; KANG, SEOGCHAN - Pennsylvania State University; PARK, JONGSUN - Seoul National University; REP, MARTIJN - University Of Amsterdam; SHIM, WON-BO - Texas A&M University; WOLOSHUK, CHARLES - Purdue University; XIE, XIAOHUI - University Of California; XU, JIN-RONG - Purdue University; ANTONIW, JOHN - Rothamsted Centre For Sustainable Pest And Disease Management; BAKER, SCOTT - Pacific Northwest National Laboratory; BLUHM, BURTON - Purdue University; BREAKSPEAR, ANDREW - University Of Minnesota; Brown, Daren; Butchko, Robert; CHAPMAN, SINEAD - Broad Institute Of Mit/harvard; COULSON, RICHARD - European Bioinformatics Institute; COUTINHO, PEDRO - National Council For Scientific Research-Cnrs; DANCHIN, ETIENNE G.J. - National Council For Scientific Research-Cnrs; DIENER, ANDREW - University Of California; GALE, LIANE - University Of California; GARDINER, DONALD - Commonwealth Scientific And Industrial Research Organisation (CSIRO); GOFF, STEPHEN - University Of Arizona; HAMMOND-KOSACK, KIM - Rothamsted Centre For Sustainable Pest And Disease Management; HILBURN, KAREN - University Of Minnesota; HUA-VAN, AURELIE - University Of Paris; JONKERS, WILFRIED - University Of Amsterdam; KAZAN, KEMAL - Commonwealth Scientific And Industrial Research Organisation (CSIRO); KODIRA, CHINNAPPA - Broad Institute Of Mit/harvard; KOEHRSEN, MICHAEL - Broad Institute Of Mit/harvard; KUMAR, LOKESH - Broad Institute Of Mit/harvard; LEE, YONG-HWAN - Seoul National University; LI, LIANDE - University Of California; MANNERS, JOHN - Commonwealth Scientific And Industrial Research Organisation (CSIRO); MIRANDA-SAAVEDRA, DIEGO - Cambridge Institute Of Medical Research; MUKHERJEE, MALA - Texas A&M University; PARK, GYUNGSOON - University Of California; PARK, JONGSUN - Seoul National University; PARK, SOOK-YOUNG - Seoul National University; Proctor, Robert; REGEV, AVIV - Broad Institute Of Mit/harvard; RUIZ-ROLDAN, M. CARMEN - University Of Spain; SAIN, DIVYA - University Of California; SAKTHIKUMAR, SHARADHA - Broad Institute Of Mit/harvard; SYKES, SEAN - Broad Institute Of Mit/harvard; SCHWARTZ, DAVID - University Of Wisconsin; TURGEON, GILLIAN - Cornell University; WAPINSKI, ILAN - Broad Institute Of Mit/harvard; YODER, OLEN - Retired Non ARS Employee; YOUNG, SARAH - Broad Institute Of Mit/harvard; ZENG, QIANDONG - Broad Institute Of Mit/harvard; ZHOU, SIGUO - University Of Wisconsin; GALAGAN, JAMES - Broad Institute Of Mit/harvard; CUOMO, CHRISTINA - Broad Institute Of Mit/harvard; Kistler, Harold

Submitted to: Nature
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/20/2010
Publication Date: 3/18/2010
Citation: Ma, L., Borkovich, K.A., Coleman, J.J., Daboussi, M., Pietro, A.D., Dufresne, M., Freitag, M., Grabherr, M., Henrissat, B., Kang, S., Park, J., Rep, M., Shim, W., Woloshuk, C., Xie, X., Xu, J., Antoniw, J., Baker, S.E., Bluhm, B.H., Breakspear, A., Brown, D.W., Butchko, R.A., Chapman, S., Coulson, R., Coutinho, P.M., Danchin, E., Diener, A., Gale, L., Gardiner, D., Goff, S., Hammond-Kosack, K.E., Hilburn, K., Hua-Van, A., Jonkers, W., Kazan, K., Kodira, C.D., Koehrsen, M., Kumar, L., Lee, Y., Li, L., Manners, J., Miranda-Saavedra, D., Mukherjee, M., Park, G., Park, J., Park, S., Proctor, R., Regev, A., Ruiz-Roldan, M., Sain, D., Sakthikumar, S., Sykes, S., Schwartz, D.C., Turgeon, G., Wapinski, I., Yoder, O., Young, S., Zeng, Q., Zhou, S., Galagan, J., Cuomo, C.A., Kistler, H.C. 2010. Comparative Genomics Reveals Mobile Pathogenicity Chromosomes in Fusarium. Nature. 464(7287):367-373.

Interpretive Summary: The results of this research demonstrate differences in genome sequences that affect toxin production and ability to cause plant disease in the fungus Fusarium. Species of this fungus are among the most economically important fungal pathogens of crop plants because they occur worldwide and on many crops, they can reduce crop yield and quality, and they can produce toxins (mycotoxins) that are hazards to human and animal health. Here, the whole genome sequence was determined for two Fusarium species, one that causes disease on tomato and a second that causes disease on corn. The sequences were compared with a previously determined whole genome sequence of a third species that causes disease on wheat, corn, and barley. The results demonstrate that the genome sequences are highly similar in the three species, but that important differences exist. Some of the genes that differ among the three species are required for production of different toxic metabolites, whereas others are important for ability to cause disease on crop hosts. These findings provide information that plant breeders and plant biotechnologists can use to improve the resistance of crops to diseases caused by Fusarium and to reduce mycotoxin contamination of crops.

Technical Abstract: Fusarium species are among the most important phytopathogenic and toxigenic fungi, having significant impact on crop production and animal health. Distinctively, strains of F. oxysporum exhibit wide host range and are pathogenic to both plant and animal species, reflecting remarkable genetic adaptability. To understand the mechanism underlying such genetic plasticity and rapid pathogenic development, we compared the genomes of three economically important and phylogenetically related, yet phenotypically distinct phytopathogenic species, F. graminearum, F. verticillioides and F. oxysporum f. sp. lycopersici. Comparative analysis revealed diverse and actively transcribed secondary metabolite biosynthetic clusters in F. graminearum and F. verticillioides as well as greatly expanded lineage-specific (LS) genomic regions in F. oxysporum that include four entire chromosomes and account for more than one-quarter of the genome. LS regions are rich in transposons and genes involved in host-pathogen interactions, including known effectors, enzymes targeting plant substrates or processes, and genes involved in lipid signalling and gene silencing. We found evidence for the acquisition of the LS chromosomes through horizontal transfer, which may explain the polyphyletic origin of host specificity in F. oxysporum and the rapid emergence of new pathogenic lineages in distinct genetic backgrounds.