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Journal of Integrative Agriculture  2025, Vol. 24 Issue (10): 3909-3925    DOI: 10.1016/j.jia.2025.02.018
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Multiple chromosomal configurations and phylogenetic implications in Saccharum mitochondrial genomes

Guilong Lu1, 2, Chang Zhang2, Qibin Wu2, 3, Tingting Sun2, Shaolin Yang2, 3, Erya Wei1, Junhui Li1, Youxiong Que2, 3#

1 School of Horticulture and Landscape Architecture, Henan Institute of Science and Technology, Xinxiang 453003, China

2 State Key Laboratory of Tropical Crop Breeding, Institute of Tropical Bioscience and Biotechnology, Sanya Research Institute, Chinese Academy of Tropical Agricultural Sciences, Sanya 572024, China

3 State Key Laboratory of Tropical Crop Breeding, Sugarcane Research Institute, Yunnan Academy of Agricultural Sciences, Kaiyuan 661699, China

 Highlights 
Mitochondria integrally influence plant growth, fertility and adaptation.
Multiple chromosomal configurations are present in Saccharum complex mitogenomes.
There are substantial genomic reorganization and gene transfer events throughout evolution.
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摘要  
线粒体在植物生长发育、配子育性和生态适应性方面扮演着重要角色。甘蔗(Saccharum spp. hybrids)是世界上最为重要的糖料和能源作物,割手密(S. Spontaneum)和斑茅(S. arundinaceum)是改良甘蔗品种特性和拓宽遗传基础的优异种质资源,但其线粒体基因组及相关研究却鲜有报道。我们的研究对斑茅1-6,割手密2-2和甘蔗杂交种GT42、GT44、LC05-136、LC1541与YZ08-1609的线粒体基因组进行了组装和深入解析。结果表明,这些基因组全长445,578-533,662 bp,编码33个蛋白编码基因(protein coding genes, PCGs),GC含量为43.43%-43.82%。斑茅、割手密和甘蔗杂交种的线粒体基因组主结构分别为三环、单环+线性和双环类型,且由重复序列介导重组产生多种潜在构象。基于线粒体基因的内含子序列开发了可区分斑茅、割手密和甘蔗杂交种的分子标记SAnad4i3。在这些物种的PCGs中鉴定到了540-581个C到U的RNA编辑位点,其中在斑茅中有6个编辑与创造起始或终止密码子有关,而在割手密和甘蔗杂交种中只鉴定到5个相关位点。进一步,在线粒体基因组中鉴定到了30-37个叶绿体基因组同源片段,其中以割手密数量最多、斑茅最少。进化分析显示,甘蔗在长期进化中可能经历了多次基因组重组和基因转移事件,并丢失了8个PCGs。以上研究揭示了“甘蔗复合体”线粒体基因组的遗传多样性和复杂性,为物种分类和高倍体作物遗传进化研究提供了科学基础。


Abstract  


Mitochondria play a crucial role in plant growth, fertility, and adaptation.  Sugarcane (Saccharum hybrids) represents the world’s primary sugar and energy crop, while Sspontaneum and Sarundinaceum serve as valuable parental germplasm.  Despite their importance, limited research exists regarding the mitochondrial genomes of sugarcane and related species.  This study presents the assembly of mitogenomes from one Sarundinaceum, one Sspontaneum, and five sugarcane cultivars.  Analysis revealed that these mitogenomes, encoding 33 protein-coding genes (PCGs), ranged from 445,578 to 533,662 bp, with GC content between 43.43–43.82%.  The primary structures of Sarundinaceum consisted of three small rings, while Sspontaneum exhibited one ring and one linear structure, and sugarcane displayed two rings; multiple potential conformations emerged due to repeat-mediated recombination.  Additionally, this research developed an intron marker SAnad4i3 capable of species differentiation.  The analysis identified between 540 and 581 C to U RNA editing sites in the PCGs, with six RNA editing sites linked to start or stop codon creation in Sarundinaceum, and five sites each in Sspontaneum and sugarcane hybrids.  Significantly, 30–37 fragments homologous to chloroplast DNA were identified, with Sspontaneum containing the highest number.  These mitogenomes appear to have undergone substantial genomic reorganization and gene transfer events throughout evolution, including the loss of eight PCGs.  This comprehensive study illuminates the genetic diversity and complexity of the Saccharum complex, establishing a foundation for future germplasm identification and evolutionary research.


Keywords:  Saccharum       mitogenome        germplasm classification        RNA editing        gene transfer  
Received: 28 July 2024   Online: 17 February 2025   Accepted: 17 January 2025
Fund: This work was supported by the Chinese Academy of Tropical Agricultural Sciences for Science and Technology Innovation Team of National Tropical Agricultural Science Center (CATASCXTD202402), the Science and Technology Major Project of Guangxi, China (Guike AA23073001), the National Key Research and Development Program of China (2022YFD2301100), the Project of State Key Laboratory of Tropical Crop Breeding, China (NKLTCBCXTD24, NKLTCBHZ04, NKLTCB-RC202401 and SKLTCBYWF202504), the China Agriculture Research System of MOF and MARA  (CARS-17), and the Scientific Research Start-up Fund for High-level Introduced Talents of Henan Institute of Science and Technology, China (103020224001/073).
About author:  Guilong Lu, E-mail: luguilong666@126.com; #Correspondence Youxiong Que, E-mail: queyouxiong@126.com

Cite this article: 

Guilong Lu, Chang Zhang, Qibin Wu, Tingting Sun, Shaolin Yang, Erya Wei, Junhui Li, Youxiong Que. 2025. Multiple chromosomal configurations and phylogenetic implications in Saccharum mitochondrial genomes. Journal of Integrative Agriculture, 24(10): 3909-3925.

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