水稻细胞色素c氧化酶亚基5B基因OsCOX5B自然变异通过能量调控种子活力

doi:10.1016/j.jia.2023.06.018

Journal of Integrative Agriculture ›› 2024, Vol. 23 ›› Issue (9): 2898-2910.DOI: 10.1016/j.jia.2023.06.018

水稻细胞色素c氧化酶亚基5B基因OsCOX5B自然变异通过能量调控种子活力

收稿日期:2023-04-18 接受日期:2023-05-23 出版日期:2024-09-20 发布日期:2024-08-19

Natural variation in the cytochrome c oxidase subunit 5B OsCOX5B regulates seed vigor by altering energy production in rice

Chengwei Huang^1*, Zhijuan Ji^{2, 3*}, Qianqian Huang¹, Liling Peng¹, Wenwen Li¹, Dandan Wang¹, Zepeng Wu¹, Jia Zhao¹, Yongqi He^1#, Zhoufei Wang^1#

¹Laboratory of Seed Science and Technology/Guangdong Key Laboratory of Plant Molecular Breeding/State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources/South China Agricultural University, Guangzhou 510642, China
²National Nanfan Research Institute (Sanya), Chinese Academy of Agricultural Sciences, Sanya 572025
³China National Rice Research Institute, Hangzhou 310006, China

Received:2023-04-18 Accepted:2023-05-23 Online:2024-09-20 Published:2024-08-19
About author:Chengwei Huang, E-mail: huangcw2019@stu.scau.edu.cn; Zhijuan Ji, E-mail: zhijuanji@126.com; #Correspondence Zhoufei Wang, Tel: +86-20-85280203, E-mail: wangzf@scau.edu.cn; Yongqi He, Tel: +86-20-85280203, E-mail: hyq@scau.edu.cn * These authors contributed equally to this study. * These authors contributed equally to this study.
Supported by:

This work was supported by the Hainan Province Science and Technology Special Fund, China (ZDYF2023XDNY086), the Project of Sanya Yazhou Bay Science and Technology City, China (SCKJ-JYRC-2022-87), the Natural Science Foundation of Guangdong Province, China (2023A1515012052 and 2023A1515012092), the Guangzhou Science and Technology Plan Project, China (2023A04J1452 and 2023A04J0749), and the Double First-class Discipline Promotion Project, China (2021B10564001).

摘要/Abstract

摘要：

种子活力是直播稻生产的重要性状之一。本研究利用全基因组关联分析方法，挖掘控制水稻种子活力性状包括发芽指数（GI）和发芽势（GP）的遗传因子；鉴定到一个同时控制GI和GP的主效位点qGI6/qGP6。验证qGI6/qGP6候选基因为细胞色素c氧化酶亚基5B基因OsCOX5B；与野生型（WT）粳稻日本晴相比，该基因突变体种子活力显著降低。基因共表达分析表明，OsCOX5B主要通过影响三羧酸循环过程调控种子活力；在种子萌发过程中，Oscox5b突变体葡萄糖含量显著高于WT，而丙酮酸和三磷酸腺苷水平显著降低。此外，OsCOX5B基因优异单倍型通过增强种子萌发过程中其表达水平促进种子活力。因此，在培育适宜直播生产的高活力水稻品种中，OsCOX5B是一个具有潜在育种利用价值的重要基因。

Abstract:

Seed vigor is a crucial trait for the direct seeding of rice. Here we examined the genetic regulation of seed vigor traits in rice, including germination index (GI) and germination potential (GP), using a genome-wide association study approach. One major quantitative trait locus, qGI6/qGP6, was identified simultaneously for both GI and GP. The candidate gene encoding the cytochrome c oxidase subunit 5B (OsCOX5B) was validated for qGI6/qGP6. The disruption of OsCOX5B caused the vigor traits to be significantly lower in Oscox5b mutants than in the japonica Nipponbare wild type (WT). Gene co-expression analysis revealed that OsCOX5B influences seed vigor mainly by modulating the tricarboxylic acid cycle process. The glucose levels were significantly higher while the pyruvic acid and adenosine triphosphate levels were significantly lower in Oscox5b mutants than in WT during seed germination. The elite haplotype of OsCOX5B facilitates seed vigor by increasing its expression during seed germination. Thus, we propose that OsCOX5B is a potential target for the breeding of rice varieties with enhanced seed vigor for direct seeding.

Key words: cytochrome c oxidase , natural variation , rice , seed vigor

Chengwei Huang, Zhijuan Ji, Qianqian Huang, Liling Peng, Wenwen Li, Dandan Wang, Zepeng Wu, Jia Zhao, Yongqi He, Zhoufei Wang. 水稻细胞色素c氧化酶亚基5B基因OsCOX5B自然变异通过能量调控种子活力[J]. Journal of Integrative Agriculture, 2024, 23(9): 2898-2910.

Chengwei Huang, Zhijuan Ji, Qianqian Huang, Liling Peng, Wenwen Li, Dandan Wang, Zepeng Wu, Jia Zhao, Yongqi He, Zhoufei Wang. Natural variation in the cytochrome c oxidase subunit 5B OsCOX5B regulates seed vigor by altering energy production in rice[J]. Journal of Integrative Agriculture, 2024, 23(9): 2898-2910.

参考文献

Bewley J D. 1997. Seed germination and dormancy. Plant Cell, 9, 1055–1066.

Bewley J D, Bradford K J, Hilhorst H, Nonogaki H. 2013. Seeds: Physiology of development, germination and dormancy, 3rd edition. Seed Science Research, 23, 289–392.

Capaldi R A. 1990. Structure and function of cytochrome c oxidase. Annual Review of Biochemistry, 59, 569–596.

Cong L, Zhang F. 2015. Genome engineering using CRISPR-Cas9 system. Methods in Molecular Biology , 1239, 197–217.

Dahan J, Tcherkez G, Macherel D, Benamar A, Belcram K, Quadrado M, Arnal N, Mireau H. 2014. Disruption of the CYTOCHROME C OXIDASE DEFICIENT1 gene leads to cytochrome c oxidase depletion and reorchestrated respiratory metabolism in Arabidopsis. Plant Physiology, 166, 1788–1802.

Danecek P, Auton A, Abecasis G, Albers C A, Banks E, Depristo M A, Handsaker R E, Lunter G, Marth G T, Sherry S T, Mcvean G, Durbin R. 2011. The variant call format and VCFtools. Bioinformatics, 27, 2156–2158.

Farooq M, Siddique K H M, Rehman H, Aziz T, Lee D, Wahid A. 2011. Rice direct seeding: Experiences, challenges and opportunities. Soil and Tillage Research, 111, 87–98.

Finch-Savage W E, Bassel G W. 2016. Seed vigour and crop establishment: Extending performance beyond adaptation. Journal of Experimental Botany, 67, 567–591.

Fontanesi F, Soto I C, Barrientos A. 2008. Cytochrome c oxidase biogenesis: New levels of regulation. Iubmb Life, 60, 557–568.

Fujino K, Sekiguchi H, Matsuda Y, Sugimoto K, Ono K, Yano M. 2008. Molecular identification of a major quantitative trait locus, qLTG3-1, controlling low-temperature germinability in rice. Proceedings of the National Academy of Sciences of the United States of America, 105, 12623–12628.

Garcia L, Mansilla N, Ocampos N, Pagani M A, Welchen E, Gonzalez D H. 2019. The mitochondrial copper chaperone COX19 influences copper and iron homeostasis in Arabidopsis. Plant Molecular Biology, 99, 621–638.

Gras D E, Mansilla N, Rodriguez C, Welchen E, Gonzalez D H. 2020. Arabidopsis thaliana SURFEIT1-like genes link mitochondrial function to early plant development and hormonal growth responses. Plant Journal, 103, 690–704.

He Y, Cheng J, He Y, Yang B, Cheng Y, Yang C, Zhang H, Wang Z. 2019a. Influence of isopropylmalate synthase OsIPMS1 on seed vigour associated with amino acid and energy metabolism in rice. Plant Biotechnology Journal, 17, 322–337.

He Y, Yang B, He Y, Zhan C, Cheng Y, Zhang J, Zhang H, Cheng J, Wang Z. 2019b. A quantitative trait locus, qSE3, promotes seed germination and seedling establishment under salinity stress in rice. Plant Journal, 97, 1089–1104.

He Y, Zhao J, Yang B, Sun S, Peng L, Wang Z. 2020. Indole-3-acetate beta-glucosyltransferase OsIAGLU regulates seed vigour through mediating crosstalk between auxin and abscisic acid in rice. Plant Biotechnology Journal, 18, 1933–1945.

Howell K A, Narsai R, Carroll A, Ivanova A, Lohse M, Usadel B, Millar A H, Whelan J. 2009. Mapping metabolic and transcript temporal switches during germination in rice highlights specific transcription factors and the role of RNA instability in the germination process. Plant Physiology, 149, 961–980.

Li W, Yang B, Xu J, Peng L, Sun S, Huang Z, Jiang X, He Y, Wang Z. 2021. A genome-wide association study reveals that the 2-oxoglutarate/malate translocator mediates seed vigor in rice. Plant Journal, 108, 478–491.

Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2^–∆∆CT method. Methods, 25, 402–408.

Lu Q, Zhang M, Niu X, Wang C, Xu Q, Feng Y, Wang S, Yuan X, Yu H, Wang Y, Wei X. 2016. Uncovering novel loci for mesocotyl elongation and shoot length in indica rice through genome-wide association mapping. Planta, 243, 645–657.

Lv Y, Guo Z, Li X, Ye H, Li X, Xiong L. 2016. New insights into the genetic basis of natural chilling and cold shock tolerance in rice by genome-wide association analysis. Plant Cell and Environment, 39, 556–570.

Mansilla N, Garcia L, Gonzalez D H, Welchen E. 2015. AtCOX10, a protein involved in haem o synthesis during cytochrome c oxidase biogenesis, is essential for plant embryogenesis and modulates the progression of senescence. Journal of Experimental Botany, 66, 6761–6775.

Mansilla N, Welchen E, Gonzalez D H. 2019. Arabidopsis SCO proteins oppositely influence cytochrome c oxidase levels and gene expression during salinity stress. Plant and Cell Physiology, 60, 2769–2784.

McCouch S R, Wright M H, Tung C W, Maron L G, Mcnally K L, Fitzgerald M, Singh N, Declerck G, Agosto-Perez F, Korniliev P, Greenberg A J, Naredo M E, Mercado S M, Harrington S E, Shi Y, Branchini D A, Kuser-Falcao P R, Leung H, Ebana K, Yano M, Eizenga G, Mcclung A, Mezey J. 2016. Open access resources for genome-wide association mapping in rice. Nature Communications, 7, 10532. (not found in text? In method 2.8)

Peng L, Sun S, Yang B, Zhao J, Li W, Huang Z, Li Z, He Y, Wang Z. 2022. Genome-wide association study reveals that the cupin domain protein OsCDP3.10 regulates seed vigour in rice. Plant Biotechnology Journal, 20, 485–498.

Saish D, Nakazono M, Lee K H, Tsutsumi N, Akita S, Hirai A. 2001. The gene for alternative oxidase-2 (AOX2) from Arabidopsis thaliana consists of five exons unlike other AOX genes and is transcribed at an early stage during germination. Genes & Genetic Systems, 76, 89–97.

Schwender J, Ohlrogge J B, Shachar-Hill Y. 2003. A flux model of glycolysis and the oxidative pentosephosphate pathway in developing Brassica napus embryos. Journal of Biological Chemistry, 278, 29442–29453.

Smiri M, Chaoui A, Rouhier N, Gelhaye E, Jacquot J P, El F E. 2010. Effect of cadmium on resumption of respiration in cotyledons of germinating pea seeds. Ecotoxicological and Environmental Safety, 73, 1246–1254.

Taylor N L, Howell K A, Heazlewood J L, Tan T Y, Narsai R, Huang S, Whelan J, Millar A H. 2010. Analysis of the rice mitochondrial carrier family reveals anaerobic accumulation of a basic amino acid carrier involved in arginine metabolism during seed germination. Plant Physiology, 154, 691–704.

Villani G, Attardi G. 1997. In vivo control of respiration by cytochrome c oxidase in wild-type and mitochondrial DNA mutation-carrying human cells. Proceedings of the National Academy of Sciences of the United States of America, 94, 1166–1171.

Villani G, Attardi G. 2000. In vivo control of respiration by cytochrome c oxidase in human cells. Free Radical Biology and Medicine, 29, 202–210.

Wang L, Xie W, Chen Y, Tang W, Yang J, Ye R, Liu L, Lin Y, Xu C, Xiao J, Zhang Q. 2010. A dynamic gene expression atlas covering the entire life cycle of rice. Plant Journal, 61, 752–766.

Wang W Q, Xu D Y, Sui Y P, Ding X H, Song X J. 2022. A multiomic study uncovers a bZIP23-PER1A-mediated detoxification pathway to enhance seed vigor in rice. Proceedings of the National Academy of Sciences of the United States of America, 119, e2026355119.

Welchen E, Chan R L, Gonzalez D H. 2004. The promoter of the Arabidopsis nuclear gene COX5b-1, encoding subunit 5b of the mitochondrial cytochrome c oxidase, directs tissue-specific expression by a combination of positive and negative regulatory elements. Journal of Experimental Botany, 55, 1997–2004.

Yang W, Guo Z, Huang C, Duan L, Chen G, Jiang N, Fang W, Feng H, Xie W, Lian X, Wang G, Luo Q, Zhang Q, Liu Q, Xiong L. 2014. Combining high-throughput phenotyping and genome-wide association studies to reveal natural genetic variation in rice. Nature Communications, 5, 5087.

Yano K, Yamamoto E, Aya K, Takeuchi H, Lo P C, Hu L, Yamasaki M, Yoshida S, Kitano H, Hirano K, Matsuoka M. 2016. Genome-wide association study using whole-genome sequencing rapidly identifies new genes influencing agronomic traits in rice. Nature Genetics, 48, 927–934.

Yin G, Whelan J, Wu S, Zhou J, Chen B, Chen X, Zhang J, He J, Xin X, Lu X. 2016. Comprehensive mitochondrial metabolic shift during the critical node of seed ageing in rice. PLoS ONE, 11, e148013.

Yuan Z, Fan K, Wang Y, Tian L, Zhang C, Sun W, He H, Yu S. 2021. OsGRETCHENHAGEN3-2 modulates rice seed storability via accumulation of abscisic acid and protective substances. Plant Physiology, 186, 469–482.

Zhao H, Yao W, Ouyang Y, Yang W, Wang G, Lian X, Xing Y, Chen L, Xie W. 2015. RiceVarMap: A comprehensive database of rice genomic variations. Nucleic Acids Research, 43, D1018–D1022.

Zhao J, He Y, Huang S, Wang Z. 2021a. Advances in the identification of quantitative trait loci and genes involved in seed vigor in rice. Frontiers in Plant Science, 12, 659307.

Zhao J, Li W, Sun S, Peng L, Huang Z, He Y, Wang Z. 2021b. The rice small auxin-up RNA gene OsSAUR33 regulates seed vigor via sugar pathway during early seed germination. International Journal of Molecular Sciences, 22, 1562.

Zhou Y, Zhou S, Wang L, Wu D, Cheng H, Du X, Mao D, Zhang C, Jiang X. 2020. MiR164c and miR168a regulate seed vigor in rice. Journal of Integrative Plant Biology, 62, 470–486.

水稻细胞色素c氧化酶亚基5B基因OsCOX5B自然变异通过能量调控种子活力

Natural variation in the cytochrome c oxidase subunit 5B OsCOX5B regulates seed vigor by altering energy production in rice

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