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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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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