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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doaj-a14f1aa3208b40858f95789cc8c5a2cf2021-09-20T06:41:56ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-09-011210.3389/fmicb.2021.707281707281Comparative Mitogenomic Analysis and the Evolution of Rhizoctonia solani Anastomosis GroupsRunmao Lin0Yuan Xia1Yao Liu2Danhua Zhang3Xing Xiang4Xianyu Niu5Linjia Jiang6Xiaolin Wang7Aiping Zheng8Aiping Zheng9Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing, ChinaAgriculture College, Sichuan Agricultural University, Chengdu, ChinaRice Research Institute, Sichuan Agricultural University, Chengdu, ChinaAgriculture College, Sichuan Agricultural University, Chengdu, ChinaAgriculture College, Sichuan Agricultural University, Chengdu, ChinaAgriculture College, Sichuan Agricultural University, Chengdu, ChinaAgriculture College, Sichuan Agricultural University, Chengdu, ChinaAgriculture College, Sichuan Agricultural University, Chengdu, ChinaAgriculture College, Sichuan Agricultural University, Chengdu, ChinaState Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Chengdu, ChinaMitochondria 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.https://www.frontiersin.org/articles/10.3389/fmicb.2021.707281/fullRhizoctonia solanimitogenomeexpression patternevolutionpositive selection |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Runmao Lin Yuan Xia Yao Liu Danhua Zhang Xing Xiang Xianyu Niu Linjia Jiang Xiaolin Wang Aiping Zheng Aiping Zheng |
spellingShingle |
Runmao Lin Yuan Xia Yao Liu Danhua Zhang Xing Xiang Xianyu Niu Linjia Jiang Xiaolin Wang Aiping Zheng Aiping Zheng Comparative Mitogenomic Analysis and the Evolution of Rhizoctonia solani Anastomosis Groups Frontiers in Microbiology Rhizoctonia solani mitogenome expression pattern evolution positive selection |
author_facet |
Runmao Lin Yuan Xia Yao Liu Danhua Zhang Xing Xiang Xianyu Niu Linjia Jiang Xiaolin Wang Aiping Zheng Aiping Zheng |
author_sort |
Runmao Lin |
title |
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_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_sort |
comparative mitogenomic analysis and the evolution of rhizoctonia solani anastomosis groups |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Microbiology |
issn |
1664-302X |
publishDate |
2021-09-01 |
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. |
topic |
Rhizoctonia solani mitogenome expression pattern evolution positive selection |
url |
https://www.frontiersin.org/articles/10.3389/fmicb.2021.707281/full |
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