Genetic Variation Bias toward Noncoding Regions and Secreted Proteins in the Rice Blast Fungus <named-content content-type="genus-species">Magnaporthe oryzae</named-content>

ABSTRACT 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 populatio...

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Autores principales:	Zhenhui Zhong, Meilian Chen, Lianyu Lin, Ruiqi Chen, Dan Liu, Justice Norvienyeku, Huakun Zheng, Zonghua Wang
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Magnaporthe experimental evolution genetic variant Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/c4b8df1ac4e940af988668cf5998cc71
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spelling	oai:doaj.org-article:c4b8df1ac4e940af988668cf5998cc712021-12-02T19:47:39ZGenetic Variation Bias toward Noncoding Regions and Secreted Proteins in the Rice Blast Fungus <named-content content-type="genus-species">Magnaporthe oryzae</named-content>10.1128/mSystems.00346-202379-5077https://doaj.org/article/c4b8df1ac4e940af988668cf5998cc712020-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00346-20https://doaj.org/toc/2379-5077ABSTRACT 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.Zhenhui ZhongMeilian ChenLianyu LinRuiqi ChenDan LiuJustice NorvienyekuHuakun ZhengZonghua WangAmerican Society for MicrobiologyarticleMagnaportheexperimental evolutiongenetic variantMicrobiologyQR1-502ENmSystems, Vol 5, Iss 3 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Magnaporthe experimental evolution genetic variant Microbiology QR1-502
spellingShingle	Magnaporthe experimental evolution genetic variant Microbiology QR1-502 Zhenhui Zhong Meilian Chen Lianyu Lin Ruiqi Chen Dan Liu Justice Norvienyeku Huakun Zheng Zonghua Wang Genetic Variation Bias toward Noncoding Regions and Secreted Proteins in the Rice Blast Fungus <named-content content-type="genus-species">Magnaporthe oryzae</named-content>
description	ABSTRACT 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	article
author	Zhenhui Zhong Meilian Chen Lianyu Lin Ruiqi Chen Dan Liu Justice Norvienyeku Huakun Zheng Zonghua Wang
author_facet	Zhenhui Zhong Meilian Chen Lianyu Lin Ruiqi Chen Dan Liu Justice Norvienyeku Huakun Zheng Zonghua Wang
author_sort	Zhenhui Zhong
title	Genetic Variation Bias toward Noncoding Regions and Secreted Proteins in the Rice Blast Fungus <named-content content-type="genus-species">Magnaporthe oryzae</named-content>
title_short	Genetic Variation Bias toward Noncoding Regions and Secreted Proteins in the Rice Blast Fungus <named-content content-type="genus-species">Magnaporthe oryzae</named-content>
title_full	Genetic Variation Bias toward Noncoding Regions and Secreted Proteins in the Rice Blast Fungus <named-content content-type="genus-species">Magnaporthe oryzae</named-content>
title_fullStr	Genetic Variation Bias toward Noncoding Regions and Secreted Proteins in the Rice Blast Fungus <named-content content-type="genus-species">Magnaporthe oryzae</named-content>
title_full_unstemmed	Genetic Variation Bias toward Noncoding Regions and Secreted Proteins in the Rice Blast Fungus <named-content content-type="genus-species">Magnaporthe oryzae</named-content>
title_sort	genetic variation bias toward noncoding regions and secreted proteins in the rice blast fungus <named-content content-type="genus-species">magnaporthe oryzae</named-content>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/c4b8df1ac4e940af988668cf5998cc71
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Genetic Variation Bias toward Noncoding Regions and Secreted Proteins in the Rice Blast Fungus <named-content content-type="genus-species">Magnaporthe oryzae</named-content>

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