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Comparative Mitogenomic Analysis and the Evolution of Rhizoctonia solani Anastomosis Groups

Mitochondria are the major energy source for cell functions. However, for the plant fungal pathogens, mitogenome variations and their roles during the host infection processes remain largely unknown. Rhizoctonia solani, an important soil-borne pathogen, forms different anastomosis groups (AGs) and a...

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Autores principales: Lin, Runmao, Xia, Yuan, Liu, Yao, Zhang, Danhua, Xiang, Xing, Niu, Xianyu, Jiang, Linjia, Wang, Xiaolin, Zheng, Aiping
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8488467/
https://www.ncbi.nlm.nih.gov/pubmed/34616376
http://dx.doi.org/10.3389/fmicb.2021.707281
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author Lin, Runmao
Xia, Yuan
Liu, Yao
Zhang, Danhua
Xiang, Xing
Niu, Xianyu
Jiang, Linjia
Wang, Xiaolin
Zheng, Aiping
author_facet Lin, Runmao
Xia, Yuan
Liu, Yao
Zhang, Danhua
Xiang, Xing
Niu, Xianyu
Jiang, Linjia
Wang, Xiaolin
Zheng, Aiping
author_sort Lin, Runmao
collection PubMed
description Mitochondria are the major energy source for cell functions. However, for the plant fungal pathogens, mitogenome variations and their roles during the host infection processes remain largely unknown. Rhizoctonia solani, an important soil-borne pathogen, forms different anastomosis groups (AGs) and adapts to a broad range of hosts in nature. Here, we reported three complete mitogenomes of AG1-IA RSIA1, AG1-IB RSIB1, and AG1-IC, and performed a comparative analysis with nine published Rhizoctonia mitogenomes (AG1-IA XN, AG1-IB 7/3/14, AG3, AG4, and five Rhizoctonia sp. mitogenomes). These mitogenomes encoded 15 typical proteins (cox1-3, cob, atp6, atp8-9, nad1-6, nad4L, and rps3) and several LAGLIDADG/GIY-YIG endonucleases with sizes ranging from 109,017 bp (Rhizoctonia sp. SM) to 235,849 bp (AG3). We found that their large sizes were mainly contributed by repeat sequences and genes encoding endonucleases. We identified the complete sequence of the rps3 gene in 10 Rhizoctonia mitogenomes, which contained 14 positively selected sites. Moreover, we inferred a robust maximum-likelihood phylogeny of 32 Basidiomycota mitogenomes, representing that seven R. solani and other five Rhizoctonia sp. lineages formed two parallel branches in Agaricomycotina. The comparative analysis showed that mitogenomes of Basidiomycota pathogens had high GC content and mitogenomes of R. solani had high repeat content. Compared to other strains, the AG1-IC strain had low substitution rates, which may affect its mitochondrial phylogenetic placement in the R. solani clade. Additionally, with the published RNA-seq data, we investigated gene expression patterns from different AGs during host infection stages. The expressed genes from AG1-IA (host: rice) and AG3 (host: potato) mainly formed four groups by k-mean partitioning analysis. However, conserved genes represented varied expression patterns, and only the patterns of rps3-nad2 and nad1-m3g18/mag28 (an LAGLIDADG endonuclease) were conserved in AG1-IA and AG3 as shown by the correlation coefficient analysis, suggesting regulation of gene repertoires adapting to infect varied hosts. The results of variations in mitogenome characteristics and the gene substitution rates and expression patterns may provide insights into the evolution of R. solani mitogenomes.
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spelling pubmed-84884672021-10-05 Comparative Mitogenomic Analysis and the Evolution of Rhizoctonia solani Anastomosis Groups Lin, Runmao Xia, Yuan Liu, Yao Zhang, Danhua Xiang, Xing Niu, Xianyu Jiang, Linjia Wang, Xiaolin Zheng, Aiping Front Microbiol Microbiology Mitochondria are the major energy source for cell functions. However, for the plant fungal pathogens, mitogenome variations and their roles during the host infection processes remain largely unknown. Rhizoctonia solani, an important soil-borne pathogen, forms different anastomosis groups (AGs) and adapts to a broad range of hosts in nature. Here, we reported three complete mitogenomes of AG1-IA RSIA1, AG1-IB RSIB1, and AG1-IC, and performed a comparative analysis with nine published Rhizoctonia mitogenomes (AG1-IA XN, AG1-IB 7/3/14, AG3, AG4, and five Rhizoctonia sp. mitogenomes). These mitogenomes encoded 15 typical proteins (cox1-3, cob, atp6, atp8-9, nad1-6, nad4L, and rps3) and several LAGLIDADG/GIY-YIG endonucleases with sizes ranging from 109,017 bp (Rhizoctonia sp. SM) to 235,849 bp (AG3). We found that their large sizes were mainly contributed by repeat sequences and genes encoding endonucleases. We identified the complete sequence of the rps3 gene in 10 Rhizoctonia mitogenomes, which contained 14 positively selected sites. Moreover, we inferred a robust maximum-likelihood phylogeny of 32 Basidiomycota mitogenomes, representing that seven R. solani and other five Rhizoctonia sp. lineages formed two parallel branches in Agaricomycotina. The comparative analysis showed that mitogenomes of Basidiomycota pathogens had high GC content and mitogenomes of R. solani had high repeat content. Compared to other strains, the AG1-IC strain had low substitution rates, which may affect its mitochondrial phylogenetic placement in the R. solani clade. Additionally, with the published RNA-seq data, we investigated gene expression patterns from different AGs during host infection stages. The expressed genes from AG1-IA (host: rice) and AG3 (host: potato) mainly formed four groups by k-mean partitioning analysis. However, conserved genes represented varied expression patterns, and only the patterns of rps3-nad2 and nad1-m3g18/mag28 (an LAGLIDADG endonuclease) were conserved in AG1-IA and AG3 as shown by the correlation coefficient analysis, suggesting regulation of gene repertoires adapting to infect varied hosts. The results of variations in mitogenome characteristics and the gene substitution rates and expression patterns may provide insights into the evolution of R. solani mitogenomes. Frontiers Media S.A. 2021-09-20 /pmc/articles/PMC8488467/ /pubmed/34616376 http://dx.doi.org/10.3389/fmicb.2021.707281 Text en Copyright © 2021 Lin, Xia, Liu, Zhang, Xiang, Niu, Jiang, Wang and Zheng. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Lin, Runmao
Xia, Yuan
Liu, Yao
Zhang, Danhua
Xiang, Xing
Niu, Xianyu
Jiang, Linjia
Wang, Xiaolin
Zheng, Aiping
Comparative Mitogenomic Analysis and the Evolution of Rhizoctonia solani Anastomosis Groups
title Comparative Mitogenomic Analysis and the Evolution of Rhizoctonia solani Anastomosis Groups
title_full Comparative Mitogenomic Analysis and the Evolution of Rhizoctonia solani Anastomosis Groups
title_fullStr Comparative Mitogenomic Analysis and the Evolution of Rhizoctonia solani Anastomosis Groups
title_full_unstemmed Comparative Mitogenomic Analysis and the Evolution of Rhizoctonia solani Anastomosis Groups
title_short Comparative Mitogenomic Analysis and the Evolution of Rhizoctonia solani Anastomosis Groups
title_sort comparative mitogenomic analysis and the evolution of rhizoctonia solani anastomosis groups
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8488467/
https://www.ncbi.nlm.nih.gov/pubmed/34616376
http://dx.doi.org/10.3389/fmicb.2021.707281
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