Abstract
Key message
A candidate gene cytochrome b5 for the major QTL qSRMP9 for rice seed reserve mobilization was validated during seed germination using a genome-wide association study approach.
Abstract
Seed reserve mobilization plays important roles in the early seedling growth in rice. However, the genetic basis underlying this process is poorly understood. In this study, the genetic architecture of variation in seed reserve mobilization during seed germination was studied using a genome-wide association study approach in rice. Three quantitative trait loci (QTL) including qSRMP6, qSRMP9, and qSRMP12 for seed reserve mobilization percentage were identified. In which, the candidate gene cytochrome b5 (OsCyb5) for the major QTL qSRMP9 was validated. Disruption of this gene in Oscyb5 mutants reduced the seed reserve mobilization and seedling growth compared with wild-type (WT) in rice. There were no significant differences of grain size, starch, protein and total soluble sugar content in the mature grains between Oscyb5 mutants and WT. However, the α-amylase activity in the germinating seeds of Oscyb5 mutants was significantly decreased compared to that of WT, and then, the starch and sugar mobilization and the glucose accumulation during seed germination were significantly decreased in Oscyb5 mutants. Two elite haplotypes of OsCyb5 associated with the higher seed reserve mobilization percentage and its elite single nucleotide polymorphism variations were mainly existed in the INDICA and AUS accessions. The natural variation of OsCyb5 contributing to seed reserve mobilization might be useful for the future rice breeding.
Similar content being viewed by others
References
Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21:263–265
Bewley JD, Bradford KJ, Hilhorst HWM, Nonogaki H (2013) Seeds: physiology of development, germination and dormancy, 3rd edn. Springer, New York, Heidelberg, Dordrecht, London
Bockous WW, Shroyer JP (1996) Effect of seed size on seedling vigor and forage production of winter wheat. Can J Plant Sci 76:101–105
Cheng X, Cheng J, Huang X, Lai Y, Wang L, Du W, Wang Z, Zhang H (2013) Dynamic quantitative trait loci analysis of seed reserve utilization during three germination stages in rice. PLoS ONE 8:e80002
Cheng J, Cheng X, Wang L, He Y, An C, Wang Z, Zhang H (2015) Physiological characteristics of seed reserve utilization during the early seedling growth in rice. Braz J Bot 38:751–759
Fujino K, Sekiguchi H, Sato T, Kiuchi H, Nonoue Y, Takeuchi Y, Ando T, Lin SY, Yano M (2004) Mapping of quantitative trait loci controlling low temperature germinability in rice (Oryza sativa L.). Theor Appl Genet 108:794–799
Gallardo K, Job C, Groot SP, Puype M, Demol H, Vandekerckhove J, Job D (2002) Proteomics of Arabidopsis seed germination. A comparative study of wild-type and gibberellin-deficient seeds. Plant Physiol 129:823–837
He Y, Yang B, He Y, Zhan C, Cheng Y, Zhang J, Zhang H, Cheng J, Wang Z (2019) A quantitative trait locus, qSE3, promotes seed germination and seedling establishment under salinity stress in rice. Plant J 97:1089–1104
Howell KA, Millar AH, Whelan J (2006) Ordered assembly of mitochondria during rice germination begins with promitochondrial structures rich in components of the protein import apparatus. Plant Mol Biol 60:201–223
Ichie T, Ninomiya I, Ogino K (2001) Utilization of seed reserves during germination and early seedling growth by Dryobalanops lanceolata (Dipterocarpaceae). J Trop Ecol 17:371–378
Li Y, Li LL, Fan RC, Peng CC, Sun HL, Zhu SY, Wang XF, Zhang LY, Zhang DP (2012) Arabidopsis sucrose transporter SUT4 interacts with cytochrome b5–2 to regulate seed germination in response to sucrose and glucose. Mol Plant 5:1029–1041
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−DDC(T) 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
McCouch SR, Wright MH, Tung CW, Maron LG, McNally KL, Fitzgerald M, Singh N, DeClerck G, Agosto-Perez F, Korniliev P, Greenberg AJ, Naredo ME, Mercado SM, Harrington SE, Shi Y, Branchini DA, Kuser-Falcão PR, Leung H, Ebana K, Yano M, Eizenga G, McClung A, Mezey J (2016) Open access resources for genome-wide association mapping in rice. Nat Commun 7:10532
Mohammadi H, Soltani A, Sadeghipour HR, Zeinali E (2011) Effects of seed aging on subsequent seed reserve utilization and seedling growth in soybean. Int J Plant Prod 5:65–70
Ostergaard O, Finnie C, Laugesen S, Roepstorff P, Svennson B (2004) Proteome analysis of barley seeds: identification of major proteins from two-dimensional gels (pI 4–7). Proteomics 4:2437–2447
Pritchard SL, Charlton WL, Baker A, Graham IA (2002) Germination and storage reserve mobilization are regulated independently in Arabidopsis. Plant J 31:639–647
Soltani A, Gholipoor A, Zeinali E (2006) Seed reserve utilization and seedling growth of wheat as affected by drought and salinity. Environ Exp Bot 55:195–200
Wang Z, Wang J, Bao Y, Wang F, Zhang H (2010) Quantitative trait loci analysis for rice seed vigor during the germination stage. J Zhejiang Univ-SC B 11:958–964
Wang Z, Wang J, Bao Y, Wu Y, Zhang H (2011) Quantitative trait loci controlling rice seed germination under salt stress. Euphytica 178:297–307
Wayne LL, Wallis JG, Kumar R, Markham JE, Browse J (2013) Cytochrome b5 reductase encoded by CBR1 is essential for a functional male gametophyte in Arabidopsis. Plant Cell 25:3052–3066
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 Commun 5:5087
Yano K, Yamamoto E, Aya K, Takeuchi H, Lo PC, 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. Nat Genet 48:927–934
Zeeman SC, Kossmann J, Smith AM (2010) Starch: its metabolism, evolution, and biotechnological modification in plants. Annu Rev Plant Biol 61:209–234
Zhao K, Tung CW, Eizenga GC, Wright MH, Ali ML, Price AH, Norton GJ, Islam MR, Reynolds A, Mezey J, McClung AM, Bustamante CD, McCouch SR (2011) Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa. Nature Commun 2:467
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 Res 43:D1018–D1022
Zheng H, Li X, Shi L, Jing Y, Song Q, Chen Y, He L, Wang F, Gao J, Bi Y (2019) Genome-wide identification and analysis of the cytochrome b5 protein family in Chinese Cabbage (Brassica rapa L. ssp. Pekinensis). Int J Genom 2019:2102317
Acknowledgements
The authors would like to thank USDA-ARS for seeds of the Rice Diversity Panel. This work was supported by the National Natural Science Foundation of China (Grant No. 32172052, 31971995, 31901601, and 31771889), the Natural Science Foundation of Guangdong Province (Grant No. 2020A1515011053), the Key-Area Research and Development Program of Guangdong Province (Grant No. 2018B020202012 and 2020B020219004), the Science and Technology Support Program of Huzhou (2018GZ07) and the startup funding from South China Agricultural University.
Author information
Authors and Affiliations
Contributions
ZW and JF planned the research. ZH and YH performed all important experiments. LP, SS, and CH performed physiological assay. CL performed seed germination experiments. ZW, YH, and ZH analyzed the data and wrote the paper.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Communicated by Takuji Sasaki.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Huang, Z., Ying, J., Peng, L. et al. A genome-wide association study reveals that the cytochrome b5 involved in seed reserve mobilization during seed germination in rice. Theor Appl Genet 134, 4067–4076 (2021). https://doi.org/10.1007/s00122-021-03948-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-021-03948-2