Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens.

Authors: Klosterman, Steven; SUBBARAO, KRISHNA - University Of California; KANG, SEOGCHAN - Pennsylvania State University; VERONESE, PAOLA - North Carolina State University; GOLD, SCOTT - University Of Georgia; THOMMA, BART PHJ - Wageningen University And Research Center; CHEN, ZEHUA - Broad Institute Of Mit/harvard; HENRISSAT, BERNARD - National Council For Scientific Research-Cnrs; LEE, YONG-HAWN - Seoul National University; PARK, JONGSUN - Seoul National University; GARCIA-PEDRAJAS, MARIA - Consejo Superior De Investigaciones Cientificas (CSIC); DEZ, BARBARA - University Of Warwick; Anchieta, Amy; DE JONGE, RONNIE - Wageningen University And Research Center; PARTHASARATHY, SANTHANAM - Wageningen University And Research Center; MARUTHACHALAM, KARUNAKARAN - University Of California; ATALLAH, ZAHI - University Of California; AMYOTTE, STEFAN - Agriculture And Agri-Food Canada; PAZ, ZAHI - University Of Georgia; INDERBITIZIN, PATRIK - University Of California; Hayes, Ryan; HEIMAN, DAVID - Broad Institute Of Mit/harvard; YOUNG, SARAH - Broad Institute Of Mit/harvard; ZENG, QIANDONG - Broad Institute Of Mit/harvard; ENGELS, REINHARD - Broad Institute Of Mit/harvard; GALAGAN, JAMES - Broad Institute Of Mit/harvard; CUOMO, CHRISTINA - Broad Institute Of Mit/harvard; DOBINSON, KATHERINE - Agriculture And Agri-Food Canada; MA, LI-JUN - Broad Institute Of Mit/harvard

Submitted to: PLoS Pathogens
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/13/2011
Publication Date: 7/28/2011
Citation: Klosterman, S.J., Subbarao, K.V., Kang, S., Veronese, P., Gold, S.E., Thomma, B.P.H.J, Chen, Z., Henrissat, B., Lee, Y., Park, J., Garcia-Pedrajas, M.D., Dez, B.J., Anchieta, A.G., De Jonge, R., Parthasarathy, S., Maruthachalam, K., Atallah, Z.K., Amyotte, S., Paz, Z., Inderbitizin, P., Hayes, R.J., Heiman, D.I., Young, S., Zeng, Q., Engels, R., Galagan, J., Cuomo, C., Dobinson, K.F., Ma, L-J. 2011. Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens. PLoS Pathogens. 7(7): e1002137.

Interpretive Summary: Vascular wilts are chronic and very often severe plant diseases that cause billions of dollars in annual crop losses. The characteristic wilt symptom is a result of water blockage caused by the colonization and proliferation of pathogenic microbes in the plant xylem, a water-conducting system. We sequenced genomes of two Verticillium wilt pathogens and compared them to the genome of another wilt fungus, Fusarium oxysporum. The shared genomic features among these three wilt fungi suggest the acquisition of homologs of a bacterial glucosyltransferase, involved in adaptation to osmotic stress, through horizontal transfer. Analyses of glucosyltransferase gene deletion mutants in Verticillium dahliae revealed decreased virulence in the host plant Nicotiana benthamiana. Compared to other fungi, both Verticillium genomes encode more plant cell wall degrading enzymes, including those that are able to degrade cell walls of live plants. Between the two closely related Verticillium genomes, we discovered flexible genomic islands in the primary causal agent of Verticillium wilts, Verticillium dahliae. Coupled with the impressive arsenal of plant cell wall-degrading enzymes, these flexible genomic islands may have contributed to expanding genetic diversity for this organism to invade more plant hosts. In summary, our study reveals insights into the evolution and niche adaptation of fungal wilt pathogens and sheds light on the development of novel disease management strategies for combating the destructive wilt diseases.

Technical Abstract: The vascular wilt fungi Verticillium dahliae and V. albo-atrum infect over 200 plant species, causing billions of dollars in annual crop losses. The characteristic wilt symptoms are a result of colonization and proliferation of the pathogens in the xylem vessels, which undergo fluctuations in osmolarity. To gain insights into the mechanisms that confer the organisms’ pathogenicity and enable them to proliferate in the unique ecological niche of the plant vascular system, we sequenced the genomes of V. dahliae and V. albo-atrum and compared them to each other, and to the genome of Fusarium oxysporum, another fungal wilt pathogen. Our analyses identified a set of proteins that are shared among all three wilt pathogens, and present in few other fungal species. One of these is a homolog of a bacterial glucosyltransferase that synthesizes virulencerelated osmoregulated periplasmic glucans in bacteria. Pathogenicity tests of the corresponding V. dahlia glucosyltransferase gene deletion mutants indicate that the gene is required for full virulence in the Australian tobacco species Nicotiana benthamiana. Compared to other fungi, the two sequenced Verticillium genomes encode more pectindegrading enzymes and other carbohydrate-active enzymes, suggesting an extraordinary capacity to degrade plant pectin barricades. The high level of synteny between the two Verticillium assemblies highlighted four flexible genomic islands in V. dahliae that are enriched for transposable elements, and contain duplicated genes and genes that are important in signaling/transcriptional regulation and iron/lipid metabolism. Coupled with an enhanced capacity to degrade plant materials, these genomic islands may contribute to the expanded genetic diversity and virulence of V. dahliae, the primary causal agent of Verticillium wilts. Significantly, our study reveals insights into the genetic mechanisms of niche adaptation of fungal wilt pathogens, advances our understanding of the evolution and development of their pathogenesis, and sheds light on potential avenues for the development of novel disease management strategies to combat destructive wilt diseases.