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Comparative analysis of mitochondrial genomes of maize CMS-S subtypes provides new insights into male sterility stability

BACKGROUND: Cytoplasmic male sterility (CMS) is a trait of economic importance in the production of hybrid seeds. In CMS-S maize, exerted anthers appear frequently in florets of field-grown female populations where only complete male-sterile plants were expected. It has been reported that these reve...

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Autores principales: Xiao, Senlin, Xing, Jingfeng, Nie, Tiange, Su, Aiguo, Zhang, Ruyang, Zhao, Yanxin, Song, Wei, Zhao, Jiuran
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9526321/
https://www.ncbi.nlm.nih.gov/pubmed/36180833
http://dx.doi.org/10.1186/s12870-022-03849-6
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author Xiao, Senlin
Xing, Jingfeng
Nie, Tiange
Su, Aiguo
Zhang, Ruyang
Zhao, Yanxin
Song, Wei
Zhao, Jiuran
author_facet Xiao, Senlin
Xing, Jingfeng
Nie, Tiange
Su, Aiguo
Zhang, Ruyang
Zhao, Yanxin
Song, Wei
Zhao, Jiuran
author_sort Xiao, Senlin
collection PubMed
description BACKGROUND: Cytoplasmic male sterility (CMS) is a trait of economic importance in the production of hybrid seeds. In CMS-S maize, exerted anthers appear frequently in florets of field-grown female populations where only complete male-sterile plants were expected. It has been reported that these reversions are associated with the loss of sterility-conferring regions or other rearrangements in the mitochondrial genome. However, the relationship between mitochondrial function and sterility stability is largely unknown. RESULTS: In this study, we determined the ratio of plants carrying exerted anthers in the population of two CMS-S subtypes. The subtype with a high ratio of exerted anthers was designated as CMS-Sa, and the other with low ratio was designated as CMS-Sb. Through next-generation sequencing, we assembled and compared mitochondrial genomes of two CMS-S subtypes. Phylogenetic analyses revealed strong similarities between the two mitochondrial genomes. The sterility-associated regions, S plasmids, and terminal inverted repeats (TIRs) were intact in both genomes. The two subtypes maintained high transcript levels of the sterility gene orf355 in anther tissue. Most of the functional genes/proteins were identical at the nucleotide sequence and amino acid sequence levels in the two subtypes, except for NADH dehydrogenase subunit 1 (nad1). In the mitochondrial genome of CMS-Sb, a 3.3-kilobase sequence containing nad1-exon1 was absent from the second copy of the 17-kb repeat region. Consequently, we detected two copies of nad1-exon1 in CMS-Sa, but only one copy in CMS-Sb. During pollen development, nad1 transcription and mitochondrial biogenesis were induced in anthers of CMS-Sa, but not in those of CMS-Sb. We suggest that the impaired mitochondrial function in the anthers of CMS-Sb is associated with its more stable sterility. CONCLUSIONS: Comprehensive analyses revealed diversity in terms of the copy number of the mitochondrial gene nad1-exon1 between two subtypes of CMS-S maize. This difference in copy number affected the transcript levels of nad1 and mitochondrial biogenesis in anther tissue, and affected the reversion rate of CMS-S maize. The results of this study suggest the involvement of mitochondrial robustness in modulation of sterility stability in CMS-S maize. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-022-03849-6.
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spelling pubmed-95263212022-10-02 Comparative analysis of mitochondrial genomes of maize CMS-S subtypes provides new insights into male sterility stability Xiao, Senlin Xing, Jingfeng Nie, Tiange Su, Aiguo Zhang, Ruyang Zhao, Yanxin Song, Wei Zhao, Jiuran BMC Plant Biol Research BACKGROUND: Cytoplasmic male sterility (CMS) is a trait of economic importance in the production of hybrid seeds. In CMS-S maize, exerted anthers appear frequently in florets of field-grown female populations where only complete male-sterile plants were expected. It has been reported that these reversions are associated with the loss of sterility-conferring regions or other rearrangements in the mitochondrial genome. However, the relationship between mitochondrial function and sterility stability is largely unknown. RESULTS: In this study, we determined the ratio of plants carrying exerted anthers in the population of two CMS-S subtypes. The subtype with a high ratio of exerted anthers was designated as CMS-Sa, and the other with low ratio was designated as CMS-Sb. Through next-generation sequencing, we assembled and compared mitochondrial genomes of two CMS-S subtypes. Phylogenetic analyses revealed strong similarities between the two mitochondrial genomes. The sterility-associated regions, S plasmids, and terminal inverted repeats (TIRs) were intact in both genomes. The two subtypes maintained high transcript levels of the sterility gene orf355 in anther tissue. Most of the functional genes/proteins were identical at the nucleotide sequence and amino acid sequence levels in the two subtypes, except for NADH dehydrogenase subunit 1 (nad1). In the mitochondrial genome of CMS-Sb, a 3.3-kilobase sequence containing nad1-exon1 was absent from the second copy of the 17-kb repeat region. Consequently, we detected two copies of nad1-exon1 in CMS-Sa, but only one copy in CMS-Sb. During pollen development, nad1 transcription and mitochondrial biogenesis were induced in anthers of CMS-Sa, but not in those of CMS-Sb. We suggest that the impaired mitochondrial function in the anthers of CMS-Sb is associated with its more stable sterility. CONCLUSIONS: Comprehensive analyses revealed diversity in terms of the copy number of the mitochondrial gene nad1-exon1 between two subtypes of CMS-S maize. This difference in copy number affected the transcript levels of nad1 and mitochondrial biogenesis in anther tissue, and affected the reversion rate of CMS-S maize. The results of this study suggest the involvement of mitochondrial robustness in modulation of sterility stability in CMS-S maize. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-022-03849-6. BioMed Central 2022-10-01 /pmc/articles/PMC9526321/ /pubmed/36180833 http://dx.doi.org/10.1186/s12870-022-03849-6 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Xiao, Senlin
Xing, Jingfeng
Nie, Tiange
Su, Aiguo
Zhang, Ruyang
Zhao, Yanxin
Song, Wei
Zhao, Jiuran
Comparative analysis of mitochondrial genomes of maize CMS-S subtypes provides new insights into male sterility stability
title Comparative analysis of mitochondrial genomes of maize CMS-S subtypes provides new insights into male sterility stability
title_full Comparative analysis of mitochondrial genomes of maize CMS-S subtypes provides new insights into male sterility stability
title_fullStr Comparative analysis of mitochondrial genomes of maize CMS-S subtypes provides new insights into male sterility stability
title_full_unstemmed Comparative analysis of mitochondrial genomes of maize CMS-S subtypes provides new insights into male sterility stability
title_short Comparative analysis of mitochondrial genomes of maize CMS-S subtypes provides new insights into male sterility stability
title_sort comparative analysis of mitochondrial genomes of maize cms-s subtypes provides new insights into male sterility stability
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9526321/
https://www.ncbi.nlm.nih.gov/pubmed/36180833
http://dx.doi.org/10.1186/s12870-022-03849-6
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