Mitochondrial Genome Structural Variants and Candidate Cytoplasmic Male Sterility-related Gene in Sugarcane

Overview

Journal BMC Genomics

Publisher Biomed Central

Date 2025 Jan 10

PMID 39794692

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

Affiliations

Soon will be listed here.

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.

References

Alverson A, Rice D, Dickinson S, Barry K, Palmer J . Origins and recombination of the bacterial-sized multichromosomal mitochondrial genome of cucumber. Plant Cell. 2011; 23(7):2499-513. PMC: 3226218. DOI: 10.1105/tpc.111.087189. View

Igarashi K, Kazama T, Motomura K, Toriyama K . Whole genomic sequencing of RT98 mitochondria derived from Oryza rufipogon and northern blot analysis to uncover a cytoplasmic male sterility-associated gene. Plant Cell Physiol. 2012; 54(2):237-43. DOI: 10.1093/pcp/pcs177. View

Zhang D, Gao F, Jakovlic I, Zou H, Zhang J, Li W . PhyloSuite: An integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Mol Ecol Resour. 2019; 20(1):348-355. DOI: 10.1111/1755-0998.13096. View

Epstein C, Waddle J, Hale 4th W, Dave V, Thornton J, Macatee T . Genome-wide responses to mitochondrial dysfunction. Mol Biol Cell. 2001; 12(2):297-308. PMC: 30944. DOI: 10.1091/mbc.12.2.297. View

Tang H, Zheng X, Li C, Xie X, Chen Y, Chen L . Multi-step formation, evolution, and functionalization of new cytoplasmic male sterility genes in the plant mitochondrial genomes. Cell Res. 2016; 27(1):130-146. PMC: 5223224. DOI: 10.1038/cr.2016.115. View

Wolfe K, Li W, Sharp P . Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci U S A. 1987; 84(24):9054-8. PMC: 299690. DOI: 10.1073/pnas.84.24.9054. View

Rice D, Alverson A, Richardson A, Young G, Sanchez-Puerta M, Munzinger J . Horizontal transfer of entire genomes via mitochondrial fusion in the angiosperm Amborella. Science. 2013; 342(6165):1468-73. DOI: 10.1126/science.1246275. View

Toriyama K . Molecular basis of cytoplasmic male sterility and fertility restoration in rice. Plant Biotechnol (Tokyo). 2021; 38(3):285-295. PMC: 8562580. DOI: 10.5511/plantbiotechnology.21.0607a. View

Yang H, Xue Y, Li B, Lin Y, Li H, Guo Z . The chimeric gene atp6c confers cytoplasmic male sterility in maize by impairing the assembly of the mitochondrial ATP synthase complex. Mol Plant. 2022; 15(5):872-886. DOI: 10.1016/j.molp.2022.03.002. View

10.

Kobayashi Y, Odahara M, Sekine Y, Hamaji T, Fujiwara S, Nishimura Y . Holliday Junction Resolvase MOC1 Maintains Plastid and Mitochondrial Genome Integrity in Algae and Bryophytes. Plant Physiol. 2020; 184(4):1870-1883. PMC: 7723093. DOI: 10.1104/pp.20.00763. View

11.

Tillich M, Lehwark P, Pellizzer T, Ulbricht-Jones E, Fischer A, Bock R . GeSeq - versatile and accurate annotation of organelle genomes. Nucleic Acids Res. 2017; 45(W1):W6-W11. PMC: 5570176. DOI: 10.1093/nar/gkx391. View

12.

Wick R, Schultz M, Zobel J, Holt K . Bandage: interactive visualization of de novo genome assemblies. Bioinformatics. 2015; 31(20):3350-2. PMC: 4595904. DOI: 10.1093/bioinformatics/btv383. View

13.

Frazer K, Pachter L, Poliakov A, Rubin E, Dubchak I . VISTA: computational tools for comparative genomics. Nucleic Acids Res. 2004; 32(Web Server issue):W273-9. PMC: 441596. DOI: 10.1093/nar/gkh458. View

14.

Wang Z, Zou Y, Li X, Zhang Q, Chen L, Wu H . Cytoplasmic male sterility of rice with boro II cytoplasm is caused by a cytotoxic peptide and is restored by two related PPR motif genes via distinct modes of mRNA silencing. Plant Cell. 2006; 18(3):676-87. PMC: 1383642. DOI: 10.1105/tpc.105.038240. View

15.

Li Z, Wang G, Liu X, Wang Z, Zhang M, Zhang J . Genome-wide identification and expression profiling of DREB genes in Saccharum spontaneum. BMC Genomics. 2021; 22(1):456. PMC: 8212459. DOI: 10.1186/s12864-021-07799-5. View

16.

Sloan D, Warren J, Williams A, Wu Z, Abdel-Ghany S, Chicco A . Cytonuclear integration and co-evolution. Nat Rev Genet. 2018; 19(10):635-648. PMC: 6469396. DOI: 10.1038/s41576-018-0035-9. View

17.

Chan P, Lowe T . tRNAscan-SE: Searching for tRNA Genes in Genomic Sequences. Methods Mol Biol. 2019; 1962:1-14. PMC: 6768409. DOI: 10.1007/978-1-4939-9173-0_1. View

18.

Oldenburg D, Bendich A . DNA maintenance in plastids and mitochondria of plants. Front Plant Sci. 2015; 6:883. PMC: 4624840. DOI: 10.3389/fpls.2015.00883. View

19.

Li Z, Hua X, Zhong W, Yuan Y, Wang Y, Wang Z . Genome-Wide Identification and Expression Profile Analysis of WRKY Family Genes in the Autopolyploid Saccharum spontaneum. Plant Cell Physiol. 2019; 61(3):616-630. DOI: 10.1093/pcp/pcz227. View

20.

Zhang J, Zhang X, Tang H, Zhang Q, Hua X, Ma X . Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L. Nat Genet. 2018; 50(11):1565-1573. DOI: 10.1038/s41588-018-0237-2. View