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Gapless Genome Assembly of Puccinia triticina Provides Insights into Chromosome Evolution in Pucciniales

Chromosome evolution drives species evolution, speciation, and adaptive radiation. Accurate genome assembly is crucial to understanding chromosome evolution of species, such as dikaryotic fungi. Rust fungi (Pucciniales) in dikaryons represent the largest group of plant pathogens, but the evolutionar...

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Autores principales: Li, Chuang, Qiao, Liuhui, Lu, Yanan, Xing, Guozhen, Wang, Xiaodong, Zhang, Gengyun, Qian, Huimin, Shen, Yilin, Zhang, Yibo, Yao, Wen, Cheng, Kun, Ma, Zhenling, Liu, Na, Wang, Daowen, Zheng, Wenming
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9927501/
https://www.ncbi.nlm.nih.gov/pubmed/36688678
http://dx.doi.org/10.1128/spectrum.02828-22
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author Li, Chuang
Qiao, Liuhui
Lu, Yanan
Xing, Guozhen
Wang, Xiaodong
Zhang, Gengyun
Qian, Huimin
Shen, Yilin
Zhang, Yibo
Yao, Wen
Cheng, Kun
Ma, Zhenling
Liu, Na
Wang, Daowen
Zheng, Wenming
author_facet Li, Chuang
Qiao, Liuhui
Lu, Yanan
Xing, Guozhen
Wang, Xiaodong
Zhang, Gengyun
Qian, Huimin
Shen, Yilin
Zhang, Yibo
Yao, Wen
Cheng, Kun
Ma, Zhenling
Liu, Na
Wang, Daowen
Zheng, Wenming
author_sort Li, Chuang
collection PubMed
description Chromosome evolution drives species evolution, speciation, and adaptive radiation. Accurate genome assembly is crucial to understanding chromosome evolution of species, such as dikaryotic fungi. Rust fungi (Pucciniales) in dikaryons represent the largest group of plant pathogens, but the evolutionary process of adaptive radiation in Pucciniales remains poorly understood. Here, we report a gapless genome for the wheat leaf rust fungus Puccinia triticina determined using PacBio high-fidelity (HiFi) sequencing. This gapless assembly contains two sets of chromosomes, showing that one contig represents one chromosome. Comparisons of homologous chromosomes between the phased haplotypes revealed that highly frequent small-scale sequence divergence shapes haplotypic variation. Genome analyses of Puccinia triticina along with other rusts revealed that recent transposable element bursts and extensive segmental gene duplications synergistically highlight the evolution of chromosome structures. Comparative analysis of chromosomes indicated that frequent chromosomal rearrangements may act as a major contributor to rapid radiation of Pucciniales. This study presents the first gapless, phased assembly for a dikaryotic rust fungus and provides insights into adaptive evolution and species radiation in Pucciniales. IMPORTANCE Rust fungi (Pucciniales) are the largest group of plant pathogens. Adaptive radiation is a predominant feature in Pucciniales evolution. Chromosome evolution plays an important role in adaptive evolution. Accurate chromosome-scale assembly is required to understand the role of chromosome evolution in Pucciniales. We took advantage of HiFi sequencing to construct a gapless, phased genome for Puccinia triticina. Further analyses revealed that the evolution of chromosome structures in rust lineage is shaped by the combination of transposable element bursts and segmental gene duplications. Chromosome comparisons of Puccinia triticina and other rusts suggested that frequent chromosomal arrangements may make remarkable contributions to high species diversity of rust fungi. Our results present the first gapless genome for Pucciniales and shed light on the feature of chromosome evolution in Pucciniales.
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spelling pubmed-99275012023-02-15 Gapless Genome Assembly of Puccinia triticina Provides Insights into Chromosome Evolution in Pucciniales Li, Chuang Qiao, Liuhui Lu, Yanan Xing, Guozhen Wang, Xiaodong Zhang, Gengyun Qian, Huimin Shen, Yilin Zhang, Yibo Yao, Wen Cheng, Kun Ma, Zhenling Liu, Na Wang, Daowen Zheng, Wenming Microbiol Spectr Research Article Chromosome evolution drives species evolution, speciation, and adaptive radiation. Accurate genome assembly is crucial to understanding chromosome evolution of species, such as dikaryotic fungi. Rust fungi (Pucciniales) in dikaryons represent the largest group of plant pathogens, but the evolutionary process of adaptive radiation in Pucciniales remains poorly understood. Here, we report a gapless genome for the wheat leaf rust fungus Puccinia triticina determined using PacBio high-fidelity (HiFi) sequencing. This gapless assembly contains two sets of chromosomes, showing that one contig represents one chromosome. Comparisons of homologous chromosomes between the phased haplotypes revealed that highly frequent small-scale sequence divergence shapes haplotypic variation. Genome analyses of Puccinia triticina along with other rusts revealed that recent transposable element bursts and extensive segmental gene duplications synergistically highlight the evolution of chromosome structures. Comparative analysis of chromosomes indicated that frequent chromosomal rearrangements may act as a major contributor to rapid radiation of Pucciniales. This study presents the first gapless, phased assembly for a dikaryotic rust fungus and provides insights into adaptive evolution and species radiation in Pucciniales. IMPORTANCE Rust fungi (Pucciniales) are the largest group of plant pathogens. Adaptive radiation is a predominant feature in Pucciniales evolution. Chromosome evolution plays an important role in adaptive evolution. Accurate chromosome-scale assembly is required to understand the role of chromosome evolution in Pucciniales. We took advantage of HiFi sequencing to construct a gapless, phased genome for Puccinia triticina. Further analyses revealed that the evolution of chromosome structures in rust lineage is shaped by the combination of transposable element bursts and segmental gene duplications. Chromosome comparisons of Puccinia triticina and other rusts suggested that frequent chromosomal arrangements may make remarkable contributions to high species diversity of rust fungi. Our results present the first gapless genome for Pucciniales and shed light on the feature of chromosome evolution in Pucciniales. American Society for Microbiology 2023-01-23 /pmc/articles/PMC9927501/ /pubmed/36688678 http://dx.doi.org/10.1128/spectrum.02828-22 Text en Copyright © 2023 Li 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
Li, Chuang
Qiao, Liuhui
Lu, Yanan
Xing, Guozhen
Wang, Xiaodong
Zhang, Gengyun
Qian, Huimin
Shen, Yilin
Zhang, Yibo
Yao, Wen
Cheng, Kun
Ma, Zhenling
Liu, Na
Wang, Daowen
Zheng, Wenming
Gapless Genome Assembly of Puccinia triticina Provides Insights into Chromosome Evolution in Pucciniales
title Gapless Genome Assembly of Puccinia triticina Provides Insights into Chromosome Evolution in Pucciniales
title_full Gapless Genome Assembly of Puccinia triticina Provides Insights into Chromosome Evolution in Pucciniales
title_fullStr Gapless Genome Assembly of Puccinia triticina Provides Insights into Chromosome Evolution in Pucciniales
title_full_unstemmed Gapless Genome Assembly of Puccinia triticina Provides Insights into Chromosome Evolution in Pucciniales
title_short Gapless Genome Assembly of Puccinia triticina Provides Insights into Chromosome Evolution in Pucciniales
title_sort gapless genome assembly of puccinia triticina provides insights into chromosome evolution in pucciniales
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9927501/
https://www.ncbi.nlm.nih.gov/pubmed/36688678
http://dx.doi.org/10.1128/spectrum.02828-22
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