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Genetic Variation Bias toward Noncoding Regions and Secreted Proteins in the Rice Blast Fungus Magnaporthe oryzae
The genomes of plant pathogens are highly variable and plastic. Pathogen gene repertoires change quickly with the plant environment, which results in a rapid loss of plant resistance shortly after the pathogen emerges in the field. Extensive studies have evaluated natural pathogen populations to und...
Autores principales: | , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society for Microbiology
2020
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7329325/ https://www.ncbi.nlm.nih.gov/pubmed/32606028 http://dx.doi.org/10.1128/mSystems.00346-20 |
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author | Zhong, Zhenhui Chen, Meilian Lin, Lianyu Chen, Ruiqi Liu, Dan Norvienyeku, Justice Zheng, Huakun Wang, Zonghua |
author_facet | Zhong, Zhenhui Chen, Meilian Lin, Lianyu Chen, Ruiqi Liu, Dan Norvienyeku, Justice Zheng, Huakun Wang, Zonghua |
author_sort | Zhong, Zhenhui |
collection | PubMed |
description | The genomes of plant pathogens are highly variable and plastic. Pathogen gene repertoires change quickly with the plant environment, which results in a rapid loss of plant resistance shortly after the pathogen emerges in the field. Extensive studies have evaluated natural pathogen populations to understand their evolutionary effects; however, the number of studies that have examined the dynamic processes of the mutation and adaptation of plant pathogens to host plants remains limited. Here, we applied experimental evolution and high-throughput pool sequencing to Magnaporthe oryzae, a fungal pathogen that causes massive losses in rice production, to observe the evolution of genome variation. We found that mutations, including single-nucleotide variants (SNVs), insertions and deletions (indels), and transposable element (TE) insertions, accumulated very rapidly throughout the genome of M. oryzae during sequential plant inoculation and preferentially in noncoding regions, while such mutations were not frequently found in coding regions. However, we also observed that new TE insertions accumulated with time and preferentially accumulated at the proximal region of secreted protein (SP) coding genes in M. oryzae populations. Taken together, these results revealed a bias in genetic variation toward noncoding regions and SP genes in M. oryzae and may contribute to the rapid adaptive evolution of the blast fungal effectors under host selection. IMPORTANCE Plants “lose” resistance toward pathogens shortly after their widespread emergence in the field because plant pathogens mutate and adapt rapidly under resistance selection. Thus, the rapid evolution of pathogens is a serious threat to plant health. Extensive studies have evaluated natural pathogen populations to understand their evolutionary effects; however, the study of the dynamic processes of the mutation and adaptation of plant pathogens to host plants remains limited. Here, by performing an experimental evolution study, we found a bias in genetic variation toward noncoding regions and SPs in the rice blast fungus Magnaporthe oryzae, which explains the ability of the rice blast fungus to maintain high virulence variation to overcome rice resistance in the field. |
format | Online Article Text |
id | pubmed-7329325 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
spelling | pubmed-73293252020-07-10 Genetic Variation Bias toward Noncoding Regions and Secreted Proteins in the Rice Blast Fungus Magnaporthe oryzae Zhong, Zhenhui Chen, Meilian Lin, Lianyu Chen, Ruiqi Liu, Dan Norvienyeku, Justice Zheng, Huakun Wang, Zonghua mSystems Research Article The genomes of plant pathogens are highly variable and plastic. Pathogen gene repertoires change quickly with the plant environment, which results in a rapid loss of plant resistance shortly after the pathogen emerges in the field. Extensive studies have evaluated natural pathogen populations to understand their evolutionary effects; however, the number of studies that have examined the dynamic processes of the mutation and adaptation of plant pathogens to host plants remains limited. Here, we applied experimental evolution and high-throughput pool sequencing to Magnaporthe oryzae, a fungal pathogen that causes massive losses in rice production, to observe the evolution of genome variation. We found that mutations, including single-nucleotide variants (SNVs), insertions and deletions (indels), and transposable element (TE) insertions, accumulated very rapidly throughout the genome of M. oryzae during sequential plant inoculation and preferentially in noncoding regions, while such mutations were not frequently found in coding regions. However, we also observed that new TE insertions accumulated with time and preferentially accumulated at the proximal region of secreted protein (SP) coding genes in M. oryzae populations. Taken together, these results revealed a bias in genetic variation toward noncoding regions and SP genes in M. oryzae and may contribute to the rapid adaptive evolution of the blast fungal effectors under host selection. IMPORTANCE Plants “lose” resistance toward pathogens shortly after their widespread emergence in the field because plant pathogens mutate and adapt rapidly under resistance selection. Thus, the rapid evolution of pathogens is a serious threat to plant health. Extensive studies have evaluated natural pathogen populations to understand their evolutionary effects; however, the study of the dynamic processes of the mutation and adaptation of plant pathogens to host plants remains limited. Here, by performing an experimental evolution study, we found a bias in genetic variation toward noncoding regions and SPs in the rice blast fungus Magnaporthe oryzae, which explains the ability of the rice blast fungus to maintain high virulence variation to overcome rice resistance in the field. American Society for Microbiology 2020-06-30 /pmc/articles/PMC7329325/ /pubmed/32606028 http://dx.doi.org/10.1128/mSystems.00346-20 Text en Copyright © 2020 Zhong et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Research Article Zhong, Zhenhui Chen, Meilian Lin, Lianyu Chen, Ruiqi Liu, Dan Norvienyeku, Justice Zheng, Huakun Wang, Zonghua Genetic Variation Bias toward Noncoding Regions and Secreted Proteins in the Rice Blast Fungus Magnaporthe oryzae |
title | Genetic Variation Bias toward Noncoding Regions and Secreted Proteins in the Rice Blast Fungus Magnaporthe oryzae |
title_full | Genetic Variation Bias toward Noncoding Regions and Secreted Proteins in the Rice Blast Fungus Magnaporthe oryzae |
title_fullStr | Genetic Variation Bias toward Noncoding Regions and Secreted Proteins in the Rice Blast Fungus Magnaporthe oryzae |
title_full_unstemmed | Genetic Variation Bias toward Noncoding Regions and Secreted Proteins in the Rice Blast Fungus Magnaporthe oryzae |
title_short | Genetic Variation Bias toward Noncoding Regions and Secreted Proteins in the Rice Blast Fungus Magnaporthe oryzae |
title_sort | genetic variation bias toward noncoding regions and secreted proteins in the rice blast fungus magnaporthe oryzae |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7329325/ https://www.ncbi.nlm.nih.gov/pubmed/32606028 http://dx.doi.org/10.1128/mSystems.00346-20 |
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