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Extensive chromosomal rearrangements and rapid evolution of novel effector superfamilies contribute to host adaptation and speciation in the basal ascomycetous fungi

The basal ascomycetes in genus Taphrina have strict host specificity and coevolution with their host plants, making them appealing models for studying the genomic basis of ecological divergence and host adaption. We therefore performed genome sequencing and comparative genomics of different Taphrina...

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Autores principales: Wang, Qinhu, Sun, Manli, Zhang, Yimei, Song, Zhenzhen, Zhang, Shijie, Zhang, Qiang, Xu, Jin‐Rong, Liu, Huiquan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7036362/
https://www.ncbi.nlm.nih.gov/pubmed/31916390
http://dx.doi.org/10.1111/mpp.12899
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author Wang, Qinhu
Sun, Manli
Zhang, Yimei
Song, Zhenzhen
Zhang, Shijie
Zhang, Qiang
Xu, Jin‐Rong
Liu, Huiquan
author_facet Wang, Qinhu
Sun, Manli
Zhang, Yimei
Song, Zhenzhen
Zhang, Shijie
Zhang, Qiang
Xu, Jin‐Rong
Liu, Huiquan
author_sort Wang, Qinhu
collection PubMed
description The basal ascomycetes in genus Taphrina have strict host specificity and coevolution with their host plants, making them appealing models for studying the genomic basis of ecological divergence and host adaption. We therefore performed genome sequencing and comparative genomics of different Taphrina species with distinct host ranges to reveal their evolution. We identified frequent chromosomal rearrangements and highly dynamic lineage‐specific (LS) genomic regions in Taphrina genomes. The LS regions occur at the flanking regions of chromosomal breakpoints, and are greatly enriched for DNA repeats, non‐core genes, and in planta up‐regulated genes. Furthermore, we identified hundreds of candidate secreted effector proteins (CSEPs) that are commonly organized in gene clusters that form distinct AT‐rich isochore‐like regions. Nearly half of the CSEPs constitute two novel superfamilies with modular structures unique to Taphrina. These CSEPs are commonly up‐regulated during infection, enriched in the LS regions, evolved faster, and underwent extensive gene gain and loss in different species. In addition to displaying signatures of positive selection, functional characterization of selected CSEP genes confirmed their roles in suppression of plant defence responses. Overall, our results showed that extensive chromosomal rearrangements and rapidly evolving CSEP superfamilies play important roles in speciation and host adaptation in the early‐branching ascomycetous fungi.
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spelling pubmed-70363622020-02-26 Extensive chromosomal rearrangements and rapid evolution of novel effector superfamilies contribute to host adaptation and speciation in the basal ascomycetous fungi Wang, Qinhu Sun, Manli Zhang, Yimei Song, Zhenzhen Zhang, Shijie Zhang, Qiang Xu, Jin‐Rong Liu, Huiquan Mol Plant Pathol Original Articles The basal ascomycetes in genus Taphrina have strict host specificity and coevolution with their host plants, making them appealing models for studying the genomic basis of ecological divergence and host adaption. We therefore performed genome sequencing and comparative genomics of different Taphrina species with distinct host ranges to reveal their evolution. We identified frequent chromosomal rearrangements and highly dynamic lineage‐specific (LS) genomic regions in Taphrina genomes. The LS regions occur at the flanking regions of chromosomal breakpoints, and are greatly enriched for DNA repeats, non‐core genes, and in planta up‐regulated genes. Furthermore, we identified hundreds of candidate secreted effector proteins (CSEPs) that are commonly organized in gene clusters that form distinct AT‐rich isochore‐like regions. Nearly half of the CSEPs constitute two novel superfamilies with modular structures unique to Taphrina. These CSEPs are commonly up‐regulated during infection, enriched in the LS regions, evolved faster, and underwent extensive gene gain and loss in different species. In addition to displaying signatures of positive selection, functional characterization of selected CSEP genes confirmed their roles in suppression of plant defence responses. Overall, our results showed that extensive chromosomal rearrangements and rapidly evolving CSEP superfamilies play important roles in speciation and host adaptation in the early‐branching ascomycetous fungi. John Wiley and Sons Inc. 2020-01-08 /pmc/articles/PMC7036362/ /pubmed/31916390 http://dx.doi.org/10.1111/mpp.12899 Text en © 2020 The Authors. Molecular Plant Pathology published by British Society for Plant Pathology and John Wiley & Sons Ltd This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Articles
Wang, Qinhu
Sun, Manli
Zhang, Yimei
Song, Zhenzhen
Zhang, Shijie
Zhang, Qiang
Xu, Jin‐Rong
Liu, Huiquan
Extensive chromosomal rearrangements and rapid evolution of novel effector superfamilies contribute to host adaptation and speciation in the basal ascomycetous fungi
title Extensive chromosomal rearrangements and rapid evolution of novel effector superfamilies contribute to host adaptation and speciation in the basal ascomycetous fungi
title_full Extensive chromosomal rearrangements and rapid evolution of novel effector superfamilies contribute to host adaptation and speciation in the basal ascomycetous fungi
title_fullStr Extensive chromosomal rearrangements and rapid evolution of novel effector superfamilies contribute to host adaptation and speciation in the basal ascomycetous fungi
title_full_unstemmed Extensive chromosomal rearrangements and rapid evolution of novel effector superfamilies contribute to host adaptation and speciation in the basal ascomycetous fungi
title_short Extensive chromosomal rearrangements and rapid evolution of novel effector superfamilies contribute to host adaptation and speciation in the basal ascomycetous fungi
title_sort extensive chromosomal rearrangements and rapid evolution of novel effector superfamilies contribute to host adaptation and speciation in the basal ascomycetous fungi
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7036362/
https://www.ncbi.nlm.nih.gov/pubmed/31916390
http://dx.doi.org/10.1111/mpp.12899
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