Functional genomics and comparative lineage-specific region analyses reveal novel insights into race divergence in Verticillium dahliae

Authors: WANG, DAN - Chinese Academy Of Agricultural Sciences; ZHANG, DAN-DAN - Chinese Academy Of Agricultural Sciences; USAMI, TOSHIYUKI - Chiba University; LIU, LEI - Chinese Academy Of Agricultural Sciences; YANG, LIN - Chinese Academy Of Agricultural Sciences; HUANG, JIN-QUN - Chinese Academy Of Agricultural Sciences; SONG, JIAN - Chinese Academy Of Agricultural Sciences; LI, RAN - Chinese Academy Of Agricultural Sciences; KONG, ZHI-QIANG - Chinese Academy Of Agricultural Sciences; LI, JUN-JIAO - Chinese Academy Of Agricultural Sciences; WANG, JUN - Chinese Academy Of Agricultural Sciences; Klosterman, Steven; SUBBARAO, KRISHNA - University Of California; DAI, XIAO-FENG - Chinese Academy Of Agricultural Sciences; CHEN, JIE-YIN - Chinese Academy Of Agricultural Sciences

Submitted to: Microbiology Spectrum
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/5/2021
Publication Date: 12/22/2021
Citation: Wang, D., Zhang, D., Usami, T., Liu, L., Yang, L., Huang, J., Song, J., Li, R., Kong, Z., Li, J., Wang, J., Klosterman, S.J., Subbarao, K.V., Dai, X., Chen, J. 2021. Functional genomics and comparative lineage-specific region analyses reveal novel insights into race divergence in Verticillium dahliae. Microbiology Spectrum. 9(3). Article e01118-21. https://doi.org/10.1128/Spectrum.01118-21.
DOI: https://doi.org/10.1128/Spectrum.01118-21

Interpretive Summary: The soilborne fungus Verticillium dahliae causes Verticillium wilt diseases on many plant species, worldwide, including many crop plants. In plant-pathogen interactions, certain key genes within the fungus produce protein products that interact with the plant to overcome resistance and cause disease, and certain products that are recognized by the plant which allows the plant to mount a quick defense response to ward off the pathogen. The pathogenic variants of V. dahliae that cause disease on one set of cultivars but are unable to cause disease on another set of cultivars owing to plant resistance are referred to as specific races. In this study, the genomic DNA sequences of three races of V. dahliae were examined, yielding insights into which genes confer specificity in the interaction of races 2 and 3 with the tomato host cultivars. These insights are useful in plant breeding programs to track individual races for disease resistance screening and pathogen diagnostics.

Technical Abstract: Verticillium dahliae is a widespread soilborne fungus that causes Verticillium wilt on numerous economically important plant species. In tomato, until now, three races have been characterized based on the response of differential cultivars to V. dahliae, but the genetic basis of race divergence in V. dahliae remains undetermined. To investigate the genetic basis of race divergence, we sequenced the genomes of two race 2 strains and four race 3 strains for comparative analyses with two known race 1 genomes. The genetic basis of race divergence was described by the pathogenicity-related genes among the three races, orthologue analyses, and genomic structural variations. Global comparative genomics showed that chromosomal rearrangements are not the only source of race divergence and that race 3 should be split into two genotypes based on orthologue clustering. Lineage-specific regions (LSRs), frequently observed between genomes of the three races, encode several predicted secreted proteins that potentially function as suppressors of immunity triggered by known effectors. These likely contribute to the virulence of the three races. Two genes in particular that can act as markers for race 2 and race 3 (VdR2e and VdR3e, respectively) contribute to virulence on tomato, and the latter acts as an avirulence factor of race 3. We elucidated the genetic basis of race divergence through global comparative genomics and identified secreted proteins in LSRs that could potentially play critical roles in the differential virulence among the races in V. dahliae.