Population genomics demystifies the defoliation phenotype in the plant pathogen Verticillium dahliae

Authors: ZHANG, DAN-DAN - Chinese Academy Of Agricultural Sciences; WANG, JIE - Chinese Academy Of Agricultural Sciences; WANG, DAN - Chinese Academy Of Agricultural Sciences; KONG, ZHI-QIANG - Chinese Academy Of Agricultural Sciences; ZHOU, LEI - Chinese Academy Of Agricultural Sciences; ZHANG, GENG-YUN - Chinese Academy Of Agricultural Sciences; GUI, YUE-JING - Chinese Academy Of Agricultural Sciences; LI, JUN-JIAO - Chinese Academy Of Agricultural Sciences; HUANG, JIN-QUN - Bgi Shenzhen; WANG, BAO-LI - Chinese Academy Of Agricultural Sciences; LIU, CHUN - Bgi Shenzhen; YIN, CHUN-MEI - Chinese Academy Of Agricultural Sciences; LI, RUI-XING - Chinese Academy Of Agricultural Sciences; LI, TING-GANG - Chinese Academy Of Agricultural Sciences; WANG, JIN-LONG - Chinese Academy Of Agricultural Sciences; SHORT, DYLAN - University Of California; Klosterman, Steven; BOSTOCK, RICHARD - University Of California; SUBBARAO, KRISHNA - University Of California; CHEN, JIE-YIN - Chinese Academy Of Agricultural Sciences; DAI, XIAO-FENG - Chinese Academy Of Agricultural Sciences

Submitted to: New Phytologist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/18/2018
Publication Date: 1/4/2019
Citation: Zhang, D., Wang, J., Wang, D., Kong, Z., Zhou, L., Zhang, G., Gui, Y., Li, J., Huang, J., Wang, B., Liu, C., Yin, C., Li, R., Li, T., Wang, J., Short, D.P., Klosterman, S.J., Bostock, R.M., Subbarao, K.V., Chen, J., Dai, X. 2019. Population genomics demystifies the defoliation phenotype in the plant pathogen Verticillium dahliae. New Phytologist. 222(2):1012-1029. https://doi.org/10.1111/nph.15672.
DOI: https://doi.org/10.1111/nph.15672

Interpretive Summary: Verticillium dahliae is a pathogenic fungus that causes vascular wilt diseases in over 200 plant species worldwide, including economically important crops. Historically, Verticillium dahliae isolates from several hosts such as cotton have been categorized as defoliating and nondefoliating, with defoliating isolates recognized as being more aggressive on their host plants. This research investigated the genetic basis for the defoliation characteristic by comparisons of DNA sequences of defoliating isolates with nondefoliating isolates, and identification and testing of the differences of between them. This research revealed a cluster of seven genes, and two in particularly, that are required for Verticillium dahliae to cause defoliation of its host. One of these genes in the cluster identified shares homology to genes involved in the production of a secondary metabolite, which on its own, is able to cause defoliation. Identification of genes important for the more highly virulent pathotypes in Verticillium dahliae is critical to the development of control measures that target the pathogen directly or help us develop disease resistant plants.

Technical Abstract: Verticillium dahliae is a broad host-range pathogen that causes stunting, wilting, and vascular discoloration in plants. Interactions between some hosts and V. dahliae genotypes result in severe defoliation, although the underlying mechanisms for defoliation are unresolved. Population genomics revealed that a lineage-specific genomic region, G-LSR2, was horizontally transferred from Fusarium oxysporum f. sp. vasinfectum to V. dahliae. G-LSR2 determines host adaptation and is found exclusively in the genomes of defoliating strains. Deletion mutants involving seven genes within G-LSR2 (VdDfs) displayed a non-defoliating phenotype on cotton, olive, and okra. Genes VdDf5 and VdDf6 were associated with defoliation. Several genes in G-LSR2 share homology with genes involved in biosynthesis of N-lauroylethanolamine (NAE), which induces defoliation. Evidence is presented herein that illustrates defoliation and the highly virulent phenotype of the D pathotype strains may be due to secondary metabolite NAE 12:0, the biosynthesis of which is controlled by genes in the lineage specific region G-LSR2.