Mitochondrial genome structural variants and candidate cytoplasmic male sterility-related gene in sugarcane

Abstract Background Sugarcane is a crucial crop for both sugar and bioethanol production. The nobilization breeding and utilization of wild germplasm have significantly enhanced its productivity. However, the pollen sterility in Saccharum officinarum restricts its role to being a female parent in cr...

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Main Authors: Yihan Li, Shuangyu Li, Xiuting Hua, Yi Xu, Shuqi Chen, Zehuai Yu, Gui Zhuang, Yuhong Lan, Wei Yao, Baoshan Chen, Muqing Zhang, Jisen Zhang
Format: Article
Language:English
Published: BMC 2025-01-01
Series:BMC Genomics
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Online Access:https://doi.org/10.1186/s12864-025-11210-y
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author Yihan Li
Shuangyu Li
Xiuting Hua
Yi Xu
Shuqi Chen
Zehuai Yu
Gui Zhuang
Yuhong Lan
Wei Yao
Baoshan Chen
Muqing Zhang
Jisen Zhang
author_facet Yihan Li
Shuangyu Li
Xiuting Hua
Yi Xu
Shuqi Chen
Zehuai Yu
Gui Zhuang
Yuhong Lan
Wei Yao
Baoshan Chen
Muqing Zhang
Jisen Zhang
author_sort Yihan Li
collection DOAJ
description Abstract Background Sugarcane is a crucial crop for both sugar and bioethanol production. The nobilization breeding and utilization of wild germplasm have significantly enhanced its productivity. However, the pollen sterility in Saccharum officinarum restricts its role to being a female parent in crosses with Saccharum spontaneum during nobilization breeding, resulting in a narrow genetic basis for modern sugarcane cultivars. Mitochondria, often referred to as the intracellular “energy factories”, provide energy for plant life activities, and are also implicated in cytoplasmic male sterility (CMS). Results We performed mitochondrial genome assembly and structural analysis of two Saccharum founding species. We discovered that the proportions of repeat sequences are the primary factor contributing to the variations in mitochondrial genome structure and size between the two Saccharum species. Heterologous expression of the mitochondrial chimeric gene ORF113, which is highly expressed in male-sterile S. officinarum flowers, significantly inhibits growth and ATP synthesis in yeast cells, making it a key candidate CMS-related gene in sugarcane. Furthermore, we developed two co-dominant simple sequence repeat (SSR) markers based on the mitochondrial genome, which can effectively distinguish the cytoplasmic types of the two Saccharum species. Conclusion In this study, we identified structural variants and developed SSR molecular markers in the mitochondrial genomes of both S. officinarum and S. spontaneum. We also identified a novel mitochondrial chimeric ORF as a key candidate CMS-related gene. These findings offer valuable insights into variety identification, genetic resource development, and cross-breeding strategies in sugarcane.
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spelling doaj-art-1d7515ce0d0c4758b9f9cbf5af3043522025-01-12T12:09:13ZengBMCBMC Genomics1471-21642025-01-0126111610.1186/s12864-025-11210-yMitochondrial genome structural variants and candidate cytoplasmic male sterility-related gene in sugarcaneYihan Li0Shuangyu Li1Xiuting Hua2Yi Xu3Shuqi Chen4Zehuai Yu5Gui Zhuang6Yuhong Lan7Wei Yao8Baoshan Chen9Muqing Zhang10Jisen Zhang11State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangxi Key Laboratory of Sugarcane Biology, College of Agriculture, Guangxi UniversityFujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Center for Genomics and Biotechnology, Fujian Agriculture and Forestry UniversityState Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangxi Key Laboratory of Sugarcane Biology, College of Agriculture, Guangxi UniversityState Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangxi Key Laboratory of Sugarcane Biology, College of Agriculture, Guangxi UniversityFujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Center for Genomics and Biotechnology, Fujian Agriculture and Forestry UniversityState Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangxi Key Laboratory of Sugarcane Biology, College of Agriculture, Guangxi UniversityState Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangxi Key Laboratory of Sugarcane Biology, College of Agriculture, Guangxi UniversityState Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangxi Key Laboratory of Sugarcane Biology, College of Agriculture, Guangxi UniversityState Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangxi Key Laboratory of Sugarcane Biology, College of Agriculture, Guangxi UniversityState Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangxi Key Laboratory of Sugarcane Biology, College of Agriculture, Guangxi UniversityState Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangxi Key Laboratory of Sugarcane Biology, College of Agriculture, Guangxi UniversityState Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangxi Key Laboratory of Sugarcane Biology, College of Agriculture, Guangxi UniversityAbstract Background Sugarcane is a crucial crop for both sugar and bioethanol production. The nobilization breeding and utilization of wild germplasm have significantly enhanced its productivity. However, the pollen sterility in Saccharum officinarum restricts its role to being a female parent in crosses with Saccharum spontaneum during nobilization breeding, resulting in a narrow genetic basis for modern sugarcane cultivars. Mitochondria, often referred to as the intracellular “energy factories”, provide energy for plant life activities, and are also implicated in cytoplasmic male sterility (CMS). Results We performed mitochondrial genome assembly and structural analysis of two Saccharum founding species. We discovered that the proportions of repeat sequences are the primary factor contributing to the variations in mitochondrial genome structure and size between the two Saccharum species. Heterologous expression of the mitochondrial chimeric gene ORF113, which is highly expressed in male-sterile S. officinarum flowers, significantly inhibits growth and ATP synthesis in yeast cells, making it a key candidate CMS-related gene in sugarcane. Furthermore, we developed two co-dominant simple sequence repeat (SSR) markers based on the mitochondrial genome, which can effectively distinguish the cytoplasmic types of the two Saccharum species. Conclusion In this study, we identified structural variants and developed SSR molecular markers in the mitochondrial genomes of both S. officinarum and S. spontaneum. We also identified a novel mitochondrial chimeric ORF as a key candidate CMS-related gene. These findings offer valuable insights into variety identification, genetic resource development, and cross-breeding strategies in sugarcane.https://doi.org/10.1186/s12864-025-11210-ySugarcaneMitochondrial genomeRepeat sequencesCytoplasmic male sterility (CMS)Simple sequence repeat (SSR)
spellingShingle Yihan Li
Shuangyu Li
Xiuting Hua
Yi Xu
Shuqi Chen
Zehuai Yu
Gui Zhuang
Yuhong Lan
Wei Yao
Baoshan Chen
Muqing Zhang
Jisen Zhang
Mitochondrial genome structural variants and candidate cytoplasmic male sterility-related gene in sugarcane
BMC Genomics
Sugarcane
Mitochondrial genome
Repeat sequences
Cytoplasmic male sterility (CMS)
Simple sequence repeat (SSR)
title Mitochondrial genome structural variants and candidate cytoplasmic male sterility-related gene in sugarcane
title_full Mitochondrial genome structural variants and candidate cytoplasmic male sterility-related gene in sugarcane
title_fullStr Mitochondrial genome structural variants and candidate cytoplasmic male sterility-related gene in sugarcane
title_full_unstemmed Mitochondrial genome structural variants and candidate cytoplasmic male sterility-related gene in sugarcane
title_short Mitochondrial genome structural variants and candidate cytoplasmic male sterility-related gene in sugarcane
title_sort mitochondrial genome structural variants and candidate cytoplasmic male sterility related gene in sugarcane
topic Sugarcane
Mitochondrial genome
Repeat sequences
Cytoplasmic male sterility (CMS)
Simple sequence repeat (SSR)
url https://doi.org/10.1186/s12864-025-11210-y
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