Dynamics of Verticillium dahliae race 1 population under managed agricultural ecosystems

Abstract Background 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 wi...

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Main Authors: Jie-Yin Chen, Dan-Dan Zhang, Jin-Qun Huang, Ran Li, Dan Wang, Jian Song, Krishna D. Puri, Lin Yang, Zhi-Qiang Kong, Bang-Zhuo Tong, Jun-Jiao Li, Yu-Shan Huang, Ivan Simko, Steven J. Klosterman, Xiao-Feng Dai, Krishna V. Subbarao
Format: Article
Language:English
Published: BMC 2021-06-01
Series:BMC Biology
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Online Access:https://doi.org/10.1186/s12915-021-01061-w
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spelling doaj-02cab439fff54e1497d17d59a358c15d2021-06-27T11:29:04ZengBMCBMC Biology1741-70072021-06-0119112110.1186/s12915-021-01061-wDynamics of Verticillium dahliae race 1 population under managed agricultural ecosystemsJie-Yin Chen0Dan-Dan Zhang1Jin-Qun Huang2Ran Li3Dan Wang4Jian Song5Krishna D. Puri6Lin Yang7Zhi-Qiang Kong8Bang-Zhuo Tong9Jun-Jiao Li10Yu-Shan Huang11Ivan Simko12Steven J. Klosterman13Xiao-Feng Dai14Krishna V. Subbarao15State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesBGI-ShenzhenState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesDepartment of Plant Pathology, University of California, DavisBGI-ShenzhenState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesBGI-ShenzhenState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesBGI-ShenzhenUnited States Department of Agriculture, Agricultural Research Service, Crop Improvement and Protection Research UnitUnited States Department of Agriculture, Agricultural Research Service, Crop Improvement and Protection Research UnitState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesDepartment of Plant Pathology, University of California, DavisAbstract Background 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. Results 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. Conclusions 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.https://doi.org/10.1186/s12915-021-01061-wVerticillium dahliaeManaged agricultural ecosystemsLocal adaptationGenetic selectionTransposon enrichmentSignal transduction
collection DOAJ
language English
format Article
sources DOAJ
author Jie-Yin Chen
Dan-Dan Zhang
Jin-Qun Huang
Ran Li
Dan Wang
Jian Song
Krishna D. Puri
Lin Yang
Zhi-Qiang Kong
Bang-Zhuo Tong
Jun-Jiao Li
Yu-Shan Huang
Ivan Simko
Steven J. Klosterman
Xiao-Feng Dai
Krishna V. Subbarao
spellingShingle Jie-Yin Chen
Dan-Dan Zhang
Jin-Qun Huang
Ran Li
Dan Wang
Jian Song
Krishna D. Puri
Lin Yang
Zhi-Qiang Kong
Bang-Zhuo Tong
Jun-Jiao Li
Yu-Shan Huang
Ivan Simko
Steven J. Klosterman
Xiao-Feng Dai
Krishna V. Subbarao
Dynamics of Verticillium dahliae race 1 population under managed agricultural ecosystems
BMC Biology
Verticillium dahliae
Managed agricultural ecosystems
Local adaptation
Genetic selection
Transposon enrichment
Signal transduction
author_facet Jie-Yin Chen
Dan-Dan Zhang
Jin-Qun Huang
Ran Li
Dan Wang
Jian Song
Krishna D. Puri
Lin Yang
Zhi-Qiang Kong
Bang-Zhuo Tong
Jun-Jiao Li
Yu-Shan Huang
Ivan Simko
Steven J. Klosterman
Xiao-Feng Dai
Krishna V. Subbarao
author_sort Jie-Yin Chen
title Dynamics of Verticillium dahliae race 1 population under managed agricultural ecosystems
title_short Dynamics of Verticillium dahliae race 1 population under managed agricultural ecosystems
title_full Dynamics of Verticillium dahliae race 1 population under managed agricultural ecosystems
title_fullStr Dynamics of Verticillium dahliae race 1 population under managed agricultural ecosystems
title_full_unstemmed Dynamics of Verticillium dahliae race 1 population under managed agricultural ecosystems
title_sort dynamics of verticillium dahliae race 1 population under managed agricultural ecosystems
publisher BMC
series BMC Biology
issn 1741-7007
publishDate 2021-06-01
description Abstract Background 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. Results 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. Conclusions 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.
topic Verticillium dahliae
Managed agricultural ecosystems
Local adaptation
Genetic selection
Transposon enrichment
Signal transduction
url https://doi.org/10.1186/s12915-021-01061-w
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