Dynamics of Verticillium dahliae race 1 population under managed agricultural ecosystems

Authors: CHEN, JIE-YIN - Chinese Academy Of Agricultural Sciences; ZHANG, DAN-DAN - Chinese Academy Of Agricultural Sciences; HUANG, JIN-QUN - Beijing Genome Institute; LI, RAN - Chinese Academy Of Agricultural Sciences; WANG, DAN - Chinese Academy Of Agricultural Sciences; SONG, JIAN - Chinese Academy Of Agricultural Sciences; PURI, KRISHNA - University Of California; LIN, YANG - Chinese Academy Of Agricultural Sciences; KONG, ZHI-QIANG - Chinese Academy Of Agricultural Sciences; TONG, BANG-ZHUO - Beijing Genome Institute; LI, JUN-JIAO - Chinese Academy Of Agricultural Sciences; HUANG, YU-SHAN - Beijing Genome Institute; Simko, Ivan; Klosterman, Steven; DAI, XIAO-FENG - Chinese Academy Of Agricultural Sciences; SUBBARAO, KRISHNA - University Of California

Submitted to: BMC Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/27/2021
Publication Date: 6/21/2021
Citation: Chen, J., Zhang, D., Huang, J., Li, R., Wang, D., Song, J., Puri, K.D., Lin, Y., Kong, Z., Tong, B., Li, J., Huang, Y., Simko, I., Klosterman, S.J., Dai, X., Subbarao, K.V. 2021. Dynamics of Verticillium dahliae race 1 population under managed agricultural ecosystems. BMC Biology. 19. Article 131. https://doi.org/10.1186/s12915-021-01061-w.
DOI: https://doi.org/10.1186/s12915-021-01061-w

Interpretive Summary: The plant pathogenic fungus Verticillium dahliae causes Verticillium wilt disease on many economically important crops, including strawberry and lettuce. Changes in the genomic DNA sequences in a Verticillium wilt race 1 strain from lettuce were analyzed for changes over a six-year period in a field plot. The field was inoculated with the race 1 strain and was planted with race 1-resistant lettuce. We identified increased genetic variation in certain regions of the race 1 genome, including subsets of genes that have broad regulatory functions. An understanding of how V. dahliae evolves in the field when associated with its plant host may provide insights into the means by which the pathogen adapts over time under selection pressure, i.e., host plant resistance, that may lead to alternative approaches to control the pathogen.

Technical Abstract: Plant pathogens and their hosts undergo adaptive changes in managed agricultural ecosystems, by overcoming host resistance, but the underlying genetic adaptations are difficult to determine in natural settings. Verticillium dahliae is a fungal pathogen that causes Verticillium wilt on many economically important crops including lettuce. We assessed the dynamics of changes in the V. dahliae genome under selection in a long-term field experiment. In this study, a field was fumigated before the Verticillium dahliae race 1 strain (VdLs.16) was introduced. A derivative 145-strain population was collected over a 6-year period from this field in which a seggregating population of lettuce derived from Vr1/vr1 parents were evaluated. We de novo sequenced the parental genome of VdLs.16 strain and resequenced the derivative strains to analyze the genetic variations that accumulate over time in the field cropped with lettuce. Population genomics analyses identified 2769 single-nucleotide polymorphisms (SNPs) and 750 insertion/deletions (In-Dels) in the 145 isolates compared with the parental genome. Sequence divergence was identified in the coding sequence regions of 378 genes and in the putative promoter regions of 604 genes. Five-hundred and nine SNPs/In-Dels were identified as fixed. The SNPs and In-Dels were significantly enriched in the transposon-rich, gene-sparse regions, and in those genes with functional roles in signaling and transcriptional regulation. Under the managed ecosystem continuously cropped to lettuce, the local adaptation of V. dahliae evolves at a whole genome scale to accumulate SNPs/In-Dels nonrandomly in hypervariable regions that encode components of signal transduction and transcriptional regulation.