Functional study of the soybean stamen-preferentially expressed gene GmFLA22a in regulating male fertility
Received date: 2024-01-24
Revised date: 2024-03-07
Online published: 2024-03-29
Supported by
National Natural Science Foundation of China(32072084);National Science Fund Young Scholars(32101751)
China has a high dependence on soybean imports, yield increase at a faster rate is an urgent problem that need to be solved at present. The application of heterosis is one of the effective ways to significantly increase crop yield. In recent years, the development of an intelligent male sterility system based on recessive nuclear sterile genes has provided a potential solution for rapidly harnessing the heterosis in soybean. However, research on male sterility genes in soybean has been lagged behind. Based on transcriptome data of soybean floral organs in our research group, a soybean stamen-preferentially expressed gene GmFLA22a was identified. It encodes a fasciclin-like arabinogalactan protein with the FAS1 domain, and subcellular localization studies revealed that it may play roles in the endoplasmic reticulum. Take advantage of the gene editing technology, the Gmfla22a mutant was generated in this study. However, there was a significant reduction in the seed-setting rate in the mutant plants at the reproductive growth stage. The pollen viability and germination rate of Gmfla22a mutant plants showed no apparent abnormalities. Histological staining demonstrated that the release of pollen grains in the mutant plants was delayed and incomplete, which may due to the locule wall thickening in the anther development. This could be the reason of the reduced seed-setting rate in Gmfla22a mutants. In summary, our study has preliminarily revealed that GmFLA22a may be involved in regulating soybean male fertility. It provides crucial genetic materials for further uncovering its molecular function and gene resources and theoretical basis for the utilization of heterosis in soybean.
Key words: soybean; heterosis; male sterility; gene editing; reverse genetics
Zhenlin Cao, Jinhong Li, Minhui Zhou, Manting Zhang, Ning Wang, Yifei Chen, Jiaxin Li, Qingsong Zhu, Wenjun Gong, Xuchen Yang, Xiaolong Fang, Jiaxian He, Meina Li . Functional study of the soybean stamen-preferentially expressed gene GmFLA22a in regulating male fertility[J]. Hereditas(Beijing), 2024 , 46(4) : 333 -345 . DOI: 10.16288/j.yczz.24-030
| [1] | Liu SL, Zhang M, Feng F, Tian ZX. Toward a “green revolution” for soybean. Mol Plant, 2020, 13(5): 688-697. |
| [2] | Kim YJ, Zhang DB. Molecular control of male fertility for crop hybrid breeding. Trends Plant Sci, 2018, 23(1): 53-65. |
| [3] | Fang XL, Sun YY, Li JH, Li MN, Zhang CB. Male sterility and hybrid breeding in soybean. Mol Breed, 2023, 43(6): 47. |
| [4] | Wu B, Hu W, Xing YZ. The history and prospect of rice genetic breeding in China. Hereditas (Beijing), 2018, 40(10): 841-857. |
| 吴比, 胡伟, 邢永忠. 中国水稻遗传育种历程与展望. 遗传, 2018, 40(10): 841-857. | |
| [5] | Wu YZ, Fox TW, Trimnell MR, Wang LJ, Xu RJ, Cigan AM, Huffman GA, Garnaat CW, Hershey H, Albertsen MC. Development of a novel recessive genetic male sterility system for hybrid seed production in maize and other cross-pollinating crops. Plant Biotechnol J, 2016, 14(3): 1046-1054. |
| [6] | Deng XW, Wang HY, Tang XY, Zhou JL, Chen HD, He GM, Chen LB, Xu ZH. Hybrid rice breeding welcomes a new era of molecular crop design. Scientia Vitae, 2013, 43(10): 864-868. |
| [7] | Sun XY, Wang YF, Wang YH, Lin JY, Li JH, Qun YT, Fang XL, Kong FJ, Li MN. Progress on genic male sterility gene in soybean. Hereditas (Beijing), 2021, 43(1): 52-65. |
| 孙小媛, 王一帆, 王韫慧, 蔺佳雨, 李金红, 丘远涛, 方小龙, 孔凡江, 李美娜. 大豆细胞核雄性不育基因研究进展. 遗传, 2021, 43(1): 52-65. | |
| [8] | Fang XL, Sun XY, Yang XD, Li Q, Lin CJ, Xu J, Gong WJ, Wang YF, Liu L, Zhao LM, Liu BH, Qin J, Zhang CB, Kong FJ, Li MN. MS1 is essential for male fertility by regulating the microsporocyte cell plate expansion in soybean. Sci China Life Sci, 2021, 64(9): 1533-1545. |
| [9] | Jiang BJ, Chen L, Yang CY, Wu TT, Yuan S, Wu CX, Zhang MC, Gai JY, Han TF, Hou WS, Sun S. The cloning and CRISPR/Cas9-mediated mutagenesis of a male sterility gene MS1 of soybean. Plant Biotechnol J, 2021, 19(6): 1098-1100. |
| [10] | Nadeem M, Chen AD, Hong HL, Li DD, Li JJ, Zhao D, Wang W, Wang XB, Qiu LJ. GmMs1 encodes a kinesin-like protein essential for male fertility in soybean (Glycine max L.). J Integr Plant Biol, 2021, 63(6): 1054-1064. |
| [11] | Fang XL, Feng XC, Sun XY, Yang XD, Li Q, Yang XL, Xu J, Zhou MH, Lin CJ, Sui Y, Zhao LM, Liu BH, Kong FJ, Zhang CB, Li MN. Natural variation of MS2 confers male fertility and drives hybrid breeding in soybean. Plant Biotechnol J, 2023, 21(11): 2322-2332. |
| [12] | Hou JJ, Fan WW, Ma RR, Li B, Yuan ZH, Huang WX, Wu YY, Hu Q, Lin CJ, Zhao XQ, Peng B, Zhao LM, Zhang CB, Sun LJ. MALE STERILITY 3 encodes a plant homeodomain-finger protein for male fertility in soybean. J Integr Plant Biol, 2022, 64(5): 1076-1086. |
| [13] | Thu SW, Rai KM, Sandhu D, Rajangam A, Balasubramanian VK, Palmer RG, Mendu V. Mutation in a PHD-finger protein MS4 causes male sterility in soybean. BMC Plant Biol, 2019, 19(1): 1-12. |
| [14] | Zhang WN, Yang J, Yang XL, Gao MM, Lin CJ, Liu P, Li ZG, Yang XD, Zhang CB. Functional identification of a nuclear male sterility gene MS6 and creation of new sterile germplasms in soybean. J Plant Genet Res, 2023, 24(3): 801-807. |
| 张万年, 杨静, 杨绪磊, 高萌萌, 林春晶, 刘鹏, 李志刚, 杨向东, 张春宝. 大豆细胞核雄性不育基因MS6的功能验证及不育新种质创制. 植物遗传资源学报, 2023, 24(3): 801-807. | |
| [15] | Yu JP, Zhao GL, Li W, Zhang Y, Wang P, Fu AG, Zhao LM, Zhang CB, Xu M. A single nucleotide polymorphism in an R2R3 MYB transcription factor gene triggers the male sterility in soybean ms6 (Ames1). Theor Appl Genet, 2021, 134(11): 3661-3674. |
| [16] | Ma YX, Johnson K. Arabinogalactan proteins- multifunctional glycoproteins of the plant cell wall. Cell Surf, 2023, 9: 100102. |
| [17] | Seifert GJ. Fascinating fasciclins: a surprisingly widespread family of proteins that mediate interactions between the cell exterior and the cell surface. Int J Mol Sci, 2018, 19(6): 1628. |
| [18] | Li J, Yu M, Geng LL, Zhao J. The fasciclin‐like arabinogalactan protein gene, FLA3, is involved in microspore development of Arabidopsis. Plant J, 2010, 64(3): 482-497. |
| [19] | Miao YJ, Cao JS, Huang L, Yu YJ, Lin S.FLA14 is required for pollen development and preventing premature pollen germination under high humidity in Arabidopsis. BMC Plant Biol, 2021, 21(1): 254. |
| [20] | Deng Y, Wan YC, Liu WC, Zhang LS, Zhou K, Feng P, He GH, Wang N. OsFLA1 encodes a fasciclin-like arabinogalactan protein and affects pollen exine development in rice. Theor Appl Genet, 2022, 135(4): 1247-1262. |
| [21] | Huang HT, Miao YJ, Zhang YT, Huang L, Cao JS, Lin S. Comprehensive analysis of arabinogalactan protein- encoding genes reveals the involvement of three BrFLA genes in pollen germination in Brassica rapa. Int J Mol Sci, 2021, 22(23): 13142. |
| [22] | Zhang M, Wei HL, Liu J, Bian YJ, Ma Q, Mao GZ, Wang HT, Wu AM, Zhang JJ, Chen PY, Ma L, Fu XK, Yu SX. Non-functional GoFLA19s are responsible for the male sterility caused by hybrid breakdown in cotton (Gossypium spp.). Plant J, 2021, 107(4): 1198-1212. |
| [23] | Chen K, Dou H, Ouyang YD. Paraffin embedding rice tissues and sectioning. Bio-101, 2018, e1010140. |
| 程珂, 都浩, 欧阳亦聃. 水稻组织石蜡切片. Bio-101, 2018, e1010140. | |
| [24] | Chen LY, Nan HY, Kong LP, Yue L, Yang H, Zhao QS, Fang C, Li HY, Cheng Q, Lu SJ, Kong FJ, Liu BH, Dong LD. Soybean AP1 homologs control flowering time and plant height. J Integr Plant Biol, 2020, 62(12): 1868-1879. |
| [25] | Ma XL, Zhang QY, Zhu QL, Liu W, Chen Y, Qiu R, Wang B, Yang ZF, Li HY, Lin YR, Xie YY, Shen RX, Chen SF, Wang Z, Chen YL, Guo JX, Chen LT, Zhao XC, Dong ZC, Liu YG. A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol Plant, 2015, 8: 1274-1284. |
| [26] | Yang J, Xing GJ, Du X, Sui L, Guo DQ, Niu L, Yang XD. Effects of different soybean genotypes on the transformation efficiency of soybean and analysis of the T-DNA insertions in the soybean genome. Soybean Sci, 2016, 35(4): 562-567. |
| 杨静, 邢国杰, 杜茜, 隋丽, 郭东全, 牛陆, 杨向东. 不同大豆基因型对大豆遗传转化效率的影响及外源T-DNA插入分析. 大豆科学, 2016, 35(4): 562-567. | |
| [27] | Yao SE, Wang YF, Wang N, Zhou MH, Chen YF, Zhang MT, Li JX, Gong WJ, Fang XL, Li MN. The soybean stamen-preferentially expressed gene GmARFA1a regulates seed setting rate by controlling pollen germination. J Plant Genet Res, 2024, 1: 1-16. |
| 姚士恩, 王一帆, 王宁, 周铭辉, 陈一飞, 张曼婷, 李嘉欣, 宫雯珺, 方小龙, 李美娜. 大豆雄蕊优势表达基因GmARFA1a通过调控花粉萌发影响结实率. 植物遗传资源学报, 2024, 1: 1-16. | |
| [28] | Letunic I, Khedkar S, Bork P. SMART: recent updates, new developments and status in 2020. Nucleic Acids Res, 2021, 49(D1): D458-D460. |
| [29] | Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG.Clustal W and Clustal X version 2.0. Bioinformatics, 2007, 23(21): 2947-2948. |
| [30] | Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol, 2018, 35(6): 1547-1549. |
| [31] | He JD, Zhao H, Cheng ZL, Ke YW, Liu JX, Ma HL. Evolution analysis of the fasciclin-like arabinogalactan proteins in plants shows variable fasciclin-AGP domain constitutions. Int J Mol Sci, 2019, 20(8): 1945. |
| [32] | Johnson KL, Jones BJ, Bacic A, Schultz CJ. The fasciclin-like arabinogalactan proteins of Arabidopsis. A multigene family of putative cell adhesion molecules. Plant Physiol, 2003, 133(4): 1911-1925. |
| [33] | Lin JY, Li JH, Feng XC, Zhou MH, Wang N, Chen YF, Li MN. Effects of AtFLA22 gene on fertility in Arabidopsis thaliana. Heilongjiang Agric Scis, 2023, (8): 1-7. |
| 蔺佳雨, 李金红, 冯湘池, 周铭辉, 王宁, 陈一飞, 李美娜. AtFLA22基因对拟南芥育性的影响. 黑龙江农业科学, 2023, (8): 1-7. | |
| [34] | Zang LN, Zheng TC, Su XH. Advances in research of fasciclin-like arabinogalactan proteins (FLAs) in plants. Plant Omics, 2015, 8(2): 190-194. |
| [35] | Hromadová D, Soukup A, Tylová E. Arabinogalactan proteins in plant roots--an update on possible functions. Front Plant Sci, 2021, 12: 674010. |
| [36] | Tan HX, Liang WQ, Hu JP, Zhang DB. MTR1 encodes a secretory fasciclin glycoprotein required for male reproductive development in rice. Dev Cell, 2012, 22(6): 1127-1137. |
| [37] | Huber O, Sumper M. Alga-CAMs: isoforms of a cell adhesion molecule in embryos of the alga Volvox with homology to Drosophila fasciclin I. EMBO J, 1994, 13(18): 4212-4222. |
/
| 〈 |
|
〉 |