Welcome to Acta Agronomica Sinica,

Acta Agronomica Sinica

   

Comparative analysis of metabolite changes during young panicle development in wheat AL type cytoplasmic male serile line and homologous maintainers

KONG De-Zhen,SANG Wei,NIE Ying-Bin,LI Wei,XU Hong-Jun,LI Jiang-Bo,LIU Peng-Peng,TIAN Xiao-Ming*   

  1. Institute of Crop Research, Xinjiang Academy of Agri-Reclamation Sciences / Key Lab of Xinjiang Production and Construction Corps for Cereal Quality Research and Genetic Improvement, Shihezi 832000, Xinjiang, China
  • Received:2025-02-18 Revised:2025-06-01 Accepted:2025-06-01 Published:2025-06-20
  • Supported by:
    This study was supported by the Xinjiang Production and Construction Corps Financial Science and Technology Plan Project (2023CB007-10, 2024DA022).

Abstract:

To investigate the relationship between the AL-type cytoplasmic male sterile (CMS) wheat line and the metabolome of its maintainer line during spikelet development, and to provide a theoretical foundation for the use of exogenous hormones in regulating fertility restoration, the AL-22A sterile line and the AL-22B homotypic maintainer line were used as experimental materials. Self-seed setting rate was determined using international standard methods. Spike samples were collected at nine developmental stages: young panicle differentiation, double ridge, floret primordium differentiation, pistil and stamen differentiation, chamber formation, tetrad, mononuclear median, uninucleate, binucleate, and trinucleate stages. The levels of endogenous hormones, peroxidase (POD), reactive oxygen species (ROS), and ATP were measured using liquid chromatography-mass spectrometry (LC-MS), and metabolites were analyzed through non-targeted metabolomics. The self-seed setting rate of the sterile line was zero, indicating complete sterility. Compared to the maintainer line, the sterile line showed higher levels of abscisic acid (ABA) and lower levels of indole-3-acetic acid (IAA), zeatin riboside (ZR), and gibberellic acid (GA3). Methyl jasmonate (MeJA) content was lower in the sterile line from the double ridge to tetrad stages but higher after the mononuclear median stage. The IAA/ABA ratio was consistently lower in the sterile line, suggesting that hormone imbalance may contribute to sterility, particularly the elevated levels of ABA and MeJA. No significant differences in ATP and ROS levels were observed between the two lines across developmental stages. However, POD activity was significantly higher in the maintainer line from the double ridge to tetrad stages, while the sterile line showed distinct POD levels at the binucleate and trinucleate stages. Non-targeted metabolomic analysis revealed that the sterile line had more downregulated metabolites during the pistil and stamen differentiation and mononuclear median stages, while other stages showed more upregulated than downregulated metabolites, with significant differences. Clustering analysis of metabolite expression patterns across developmental stages grouped samples into early (I–III), middle (IV–VI), and late (VII–IX) phases. Stage-specific differences in metabolite expression were associated with fertility changes. Pathway enrichment analysis indicated that differential metabolites were primarily concentrated in the floret primordium differentiation, chamber formation, tetrad, uninucleate, and trinucleate stages, mainly involving carboxylic acid metabolism and secondary metabolism. The stages most critical to fertility development occurred in early to mid (II–IV) and mid to late (VI–VIII) phases. These results suggest that the interplay between endogenous hormone balance and abnormal metabolite accumulation may be key factors in CMS. This study provides both theoretical insights and practical references for understanding the physiological and metabolic mechanisms of spikelet development in CMS wheat and for developing strategies to promote fertility restoration in AL-type sterile lines.

Key words: wheat, AL-type, CMS, endogenous hormones, metabolome

[1] 孔德真, 聂迎彬, 徐红军, 穆培源, 崔凤娟, 桑伟, 田笑明. AL型三系交小麦不育相关基因dCAPs标记开发与应用. 分子植物育种, 2023, 21: 3336–3340.

Kong D Z, Nie Y B, Xu H J, Mu P Y, Cui F J, Sang W, Tian X M. Development and application of dCAPs markers related to sterility genes in AL type three-line hybrid wheat. Mol Plant Breed, 2023, 21: 3336–3340 (in Chinese with English abstract).

[2] Zhang S W, Zhang D, Fan S, Du L S, Shen Y W, Xing L B, Li Y M, Ma J J, Han M Y. Effect of exogenous GA3 and its inhibitor paclobutrazol on floral formation, endogenous hormones, and flowering-associated genes in ‘Fuji’ apple (Malus domestica Borkh.). Plant Physiol Biochem, 2016, 107: 178–186.

[3] 李罗江, 茹振刚, 高庆荣, 姜辉, 郭凤芝, 吴世文, 孙哲. BNS小麦的雄性不育性及其温光特性. 中国农业科学, 2009, 42: 3019–3027.

Li L J, Ru Z G, Gao Q R, Jiang H, Guo F Z, Wu S W, Sun Z. Male sterility and thermo-optical characteristics of BNS wheat. Sci Agric Sin, 2009, 42: 3019–3027 (in Chinese with English abstract).

[4] 周美兰, 宋雪薇, 朱潇, 姜辉, 郭凤芝, 吴世文, 孙哲. 小麦温敏不育系BNS366育性转换的敏感期研究. 麦类作物学报, 2015, 35: 7–15.

Zhou M L, Song X W, Zhu X, Jiang H, Guo F Z, Wu S W, Sun Z. Study on sensitive period of fertility transition of wheat temperature-sensitive sterile line BNS366. J Triticeae Crops, 2015, 35: 7–15 (in Chinese with English abstract).

[5] 刘海英, 冯必得, 茹振钢, 陈向东, 黄培新, 邢晨涛, 潘茵茵, 甄俊琦. BNSBNS366小麦雄性不育与内源激素的关系. 中国农业科学, 2021, 54(1): 1–18.

Liu H Y, Feng B D, Ru Z G, Chen X D, Huang P X, Xing C T, Pan Y Y, Zhen J Q. Relationship between BNS and BNS366 wheat male sterility and endogenous hormones. Sci Agric Sin, 2021, 54: 1–18 (in Chinese with English abstract).

[6] 李英贤, 张爱民, 梁振兴. 小麦雄性不育的发生与花药组织内激素平衡的关系. 农业生物技术学报, 1998, 6(1): 71–75.

Li Y X, Zhang A M, Liang Z X. Relationship between BNS and BNS366 wheat male sterility and endogenous hormones. J Agric Biotechnol, 1998, 6(1): 71–75(in Chinese with English abstract).

[7] 张自刚, 马小飞, 张红霞, 王震, 张思妮, 郭冬, 张永鹏, 马翎健. 小麦光温敏雄性不育系BNS育性转换与内源激素的关系研究. 植物遗传资源学报, 2016, 17: 913–919.

Zhang Z G, Ma X F, Zhang H X, Wang Z, Zhang S N, Guo D, Zhang Y P, Ma L J. Relationship between fertility transition and endogenous hormones in wheat temperature-sensitive male sterile line BNS. J Plant Genet Resour, 2016, 17: 913–919 (in Chinese with English abstract).

[8] 张龙雨, 袁蕾, 杨书玲, 张改生, 王俊生, 宋瑜龙, 赵卓军, 牛娜, 马守才. 小麦雄性不育系中TaPDC-E1α及其调节酶基因的表达特征. 作物学报, 2011, 37: 620–628.

Zhang L Y, Yuan L, Yang S L, Zhang G S, Wang J S, Song Y L, Zhao Z J, Niu N, Ma S C. Expression characteristics of TaPDC-E1α and its regulatory enzyme gene in male sterile wheat lines. Acta Agron Sin, 2011, 37: 620–628 (in Chinese with English abstract).

[9] 苗锦山, 杨文才, 刘彩霞, 李美芹, 乔宁, 沈火林. 葱胞质雄性不育花蕾生化物质含量和能量代谢酶活性的动态变化特征. 西北植物学报, 2010, 30: 1142–1148.

Miao J S, Yang W C, Liu C X, Li M Q, Qiao N, Shen H L. Dynamic changes of biochemical substances content and energy metabolizing enzyme activity in cytoplasmic male sterile flower buds of Allium allium L. Acta Bot Boreali-Occident Sin, 2010, 30: 1142–1148(in Chinese with English abstract).

[10] 王保明, 陈永忠, 李红波, 莫华, 黄露波. 植物雄性不育的机制及应用研究进展. 河南农业科学, 2019, 48(5): 1–9.

Wang B M, Chen Y Z, Li H B, Mo H, Huang L B. Research progress on mechanism and application of male sterility in plants. J Henan Agric Sci, 2019, 48(5): 1–9 (in Chinese with English abstract).

[11] 张鹏飞, 宋瑜龙, 张改生, 赵新亮, 巴青松, 刘红占, 祝万万, 李志宽, 王军卫, 牛娜. 小麦雄性不育系绒毡层异常代谢与小孢子败育的关系. 中国农业科学, 2014, 47: 1670–1680.

Zhang P F, Song Y L, Zhang G S, Zhao X L, Ba Q S, Liu H Z, Zhu W W, Li Z K, Wang J W, Niu N. Relationship between abnormal tapetum metabolism and microspore abortion in male sterile lines of wheat. Sci Agric Sin, 2014, 47: 1670–1680 (in Chinese with English abstract).

[12] Li Y, Liu T K, Duan W K, Song X M, Shi G J, Zhang J Y, Deng X H, Zhang S N, Hou X L. Instability in mitochondrial membranes in Polima cytoplasmic male sterility of Brassica rapa ssp. chinensis. Funct Integr Genomics, 2014, 14: 441–451.

[13] 贲蓓倍, 徐维红, 邹德玉, 牟美睿, 杨仁杰, 刘海学. 不同施肥条件下的小麦籽粒代谢组学研究. 麦类作物学报, 2021, 41: 212–219.

Ben B B, Xu W H, Zou D Y, Mu M R, Yang R J, Liu H X. Study on metabolomics of wheat grain under different fertilization conditions. J Triticeae Crops, 2021, 41: 212–219 (in Chinese with English abstract).

[14] 于振文. 作物栽培学各论(北方本). 北京: 中国农业出版社, 2003.

Yu Z W. Crop Cultivation Monographs (Northern Edition). Beijing: China Agricultural Press, 2003 (in Chinese).

[15] 宋喜悦, 何蓓如, 马翎健, 胡银岗, 李宏斌. 小麦温敏不育系A3314温敏不育性的遗传研究. 中国农业科学, 2005, 38: 1095–1099.

Song X Y, He B R, Ma L J, Hu Y G, Li H B. Genetic study on temperature-sensitive sterility of wheat temperature-sensitive sterile line A3314. Sci Agric Sin, 2005, 38: 1095–1099(in Chinese with English abstract).

[16] 李合生. 植物生理生化实验原理和技术. 北京: 高等教育出版社, 2000.

Li H S. Experimental Principles and Techniques of Plant Physiology and Biochemistry. Beijing: Higher Education Press, 2000 (in Chinese).

[17] 王贺正, 张均, 吴金芝, 徐国伟, 陈明灿, 付国占, 李友军. 不同氮素水平对小麦旗叶生理特性和产量的影响. 草业学报, 2013, 22(4): 69–75.

Wang H Z, Zhang J, Wu J Z, Xu G W, Chen M C, Fu G Z, Li Y J. Effects of different nitrogen levels on physiological characteristics and yield of flag leaves of wheat. Acta Pratac Sin, 2013, 22(4): 69–75 (in Chinese with English abstract).

[18] 柏斌, 吴俊, 盛文涛, 庄文, 李莺歌, 邓启云. 育性敏感期低温胁迫对水稻光温敏不育系叶片内源激素的影响. 杂交水稻, 2016, 31(1): 57–61.

Bai B, Wu J, Sheng W T, Zhuang W, Li Y G, Deng Q Y. Effects of different nitrogen levels on physiological characteristics and yield of flag leaves of wheat. Hybrid Rice, 2016, 31(1): 57–61(in Chinese with English abstract).

[19] 张艳玉, 张卫东, 高庆荣, 张保雷, 李楠楠, 高建华, 王慧娜, 赵兰飞. 温光敏雄性不育小麦BNS幼穗发育中的内源激素变化. 西北植物学报, 2013, 33: 1165–1170.

Zhang Y Y, Zhang W D, Gao Q R, Zhang B L. Li N N, Gao J H, Wang H N, Zhao L F. Endogenous hormone changes in young ear development of temperature-photosensitive male sterile wheat BNS. Acta Bot Boreali-Occident Sin, 2013, 33: 1165–1170 (in Chinese with English abstract).

[20] 陈建国, 王建波, 胡如忠, 陈钊德, 杨振智, 丁丁, 郭大芳, 谢晋云, 安开宇, . 烟草胞质雄性不育系与保持系内源植物激素水平差异性研究. 安徽农业科学, 2018, 46(9): 54–57.

Chen J G, Wang J B, Hu R Z, Chen Z D, Yang Z Z, Ding D, Guo D F, Xie J Y, An K Y, et al. Study on the difference of endogenous plant hormone levels between cytoplasmic male sterile line and maintainer line of tobacco. J Anhui Agric Sci, 2018, 46(9): 54–57 (in Chinese with English abstract).

[21] 杨海燕. 温光敏核不育小麦育性转换与激素间关系的研究. 西南大学硕士学位论文, 重庆, 2006.

Yang H Y. Study on the Relationship between Fertility Conversion and Hormones in Temperature-photosensitive Sterile Wheat. MS Thesis of Southwest University, Chongqing, China, 2006 (in Chinese with English abstract).

[22] 贺晓敏, 周美兰, 余传启, 蒋敏明, 茹振刚. 温敏雄性不育小麦BNS366花粉败育的细胞学观察. 麦类作物学报, 2014, 34: 460–466.

He X M, Zhou M L, Yu C Q, Jiang M M, Ru Z G. Cytological observation of pollen abortion in Wenmin male sterile wheat BNS366. J Triticeae Crops, 2014, 34: 460–466 (in Chinese with English abstract).

[23] 刘海英, 甄俊琦, 胡铁柱, 茹振钢, 李珍, 胡雪寒, 邢晨涛, 高远. 小麦温敏雄性不育系BNS366小孢子发育和花粉育性检测方法研究. 麦类作物学报, 2018, 38: 379–385.

Liu H Y, Zhen J Q, Hu T Z, Ru Z G, Li Z, Hu X H, Xing S T, Gao Y. Study on detection methods of microspore development and pollen fertility of wheat temperature-sensitive male sterile line BNS366. J Triticeae Crops, 2018, 38: 379–385 (in Chinese with English abstract).

[24] 丛庆, 张琪, 宋丽莉, 陈月, 蔡洪生, 郭长虹. 激素在植物冷胁迫应答中的角色. 核农学报, 2016, 30: 614–619.

Cong Q, Zhang Q, Song L L, Chen Y, Cai H S, Guo C H. The role of hormones in plant response to cold stress. J Nucl Agric Sci, 2016, 30: 614–619(in Chinese with English abstract).

[25] 孙佳尧, 李资文, 崔天宇, 刘鹏, 赵丽梅, 李志刚. 大豆不育系花器官发育过程中内源激素动态变化研究. 大豆科学, 2020, 39: 891–897.

Sun J Y, Li Z W, Cui T Y, Liu P, Zhao L M, Li Z G. Dynamic changes of endogenous hormones during flower organ development in sterile soybean lines. Soybean Sci, 2020, 39: 891–897 (in Chinese with English abstract).

[26] 邓继新, 刘文芳, 肖翊华. HPGMR花粉发育期花药ATP含量及核酸与蛋白质的合成研究. 武汉大学学报(自然科学版), 1990, 36(3): 85–88.

Deng J X, Liu W F, Xiao Y H. Study on anther ATP content and synthesis of nucleic acid and protein in HPGMR pollen during its development. J Wuhan Univ (Nat Sci Edn), 1990, 36(3): 85–88(in Chinese with English abstract).

[27] 周凯, 司龙亭, 张琪. 萝卜细胞质雄性不育系与保持系光合特性和呼吸特性的比较试验. 北方园艺, 2007, (6): 3–5.

Zhou K, Si L T, Zhang Q. Comparative study on photosynthetic and respiratory characteristics of cytoplasmic male sterile line and maintainer line of turnip. North Hortic, 2007, (6): 3–5 (in Chinese with English abstract).

[28] 冯小磊, 范光宇, 苏旭, 宋国亮, 史高雷, 王峰, 邱风仓, 王晓明, 赵治海. 植物雄性不育生理生化研究进展. 作物杂志, 2012, (3): 6–11.

Feng X L, Fan G Y, Su X, Song G L, Shi G L, Wang F, Qiu F C, Wang X M, Zhao Z H. Advances in physiological and biochemical studies of male sterility in plants. Crops, 2012, (3): 6–11 (in Chinese with English abstract).

[29] 刘金兵, 侯喜林, 陈晓峰, 张静宜, 王述彬, 潘宝贵. 甜椒胞质雄性不育系及其保持系生化特性研究. 园艺学报, 2006, 33: 629–631.

Liu J B, Hou X L, Chen X F, Zhang J Y, Wang S B, Pan B G. Study on biochemical characteristics of cytoplasmic male sterile line and its maintainer line of sweet pepper. Acta Hortic Sin, 2006, 33: 629–631(in Chinese with English abstract).

[30] Wang S P, Zhang Y X, Song Q L, Fang Z W, Chen Z, Zhang Y M, Zhang L L, Zhang L, Niu N, Ma S C, et al. Mitochondrial dysfunction causes oxidative stress and tapetal apoptosis in chemical hybridization reagent-induced male sterility in wheat. Front Plant Sci, 2018, 8: 2217.

[31] 刘玉平, 茹振刚, 陈希勇, 李辉, 李亚军, 赵爱菊, 宿振起. 小麦不育系BNS在石家庄地区育性转换规律的研究. 河北农业科学, 2011, 15(6): 46–49.

Liu Y P, Ru Z G, Chen X Y, Li H, Li Y J, Zhao A J, Su Z Q. Study on fertility conversion of wheat sterile line BNS in Shijiazhuang area. J Hebei Agric Sci, 2011, 15(6): 46–49 (in Chinese with English abstract).

[1] LI Shi-Peng, CHEN Cai-Wu, ZHANG Jing, LYU Tian, FU Ting-Dong, YI Bin. Identification of fertility levels and quantification of the temperature-fertility relationship in rapeseed pol TCMS lines using an improved U-Net++ model [J]. Acta Agronomica Sinica, 2025, 51(6): 1423-1434.
[2] LYU Guo-Feng, FAN Jin-Ping, WU Su-Lan, ZHANG Xiao, ZHAO Ren-Hui, LI Man, WANG Ling, GAO De-Rong, BIE Tong-De, LIU Jian. Genetic analysis of key target traits in the early-maturing wheat cultivar Yangmai 37 [J]. Acta Agronomica Sinica, 2025, 51(6): 1538-1547.
[3] WU Mei-Juan, ZHANG Yin-Hui, LI Yuan-Hao, LIU Hai-Xia, HUANG Yi-Lin, LI Tian, LIU Hong-Xia, ZHANG Xue-Yong, HAO Chen-Yang, GUO Jie, HOU Jian. Functional dissection of sucrose synthase gene TaSUS2 regulating grain starch synthesis and quality in wheat [J]. Acta Agronomica Sinica, 2025, 51(6): 1514-1525.
[4] YANG Si-Jie, DU Qi-Di, CHAI Shou-Xi, XIONG Hong-Chun, XIE Yong-Dun, ZHAO Lin-Shu, GU Jia-Yu, GUO Hui-Jun, LIU Lu-Xiang. Genetic mapping of mutant genes on flag leaf length and width in wheat [J]. Acta Agronomica Sinica, 2025, 51(6): 1548-1557.
[5] ZHAO Gang, ZHANG Jian-Jun, DANG Yi, FAN Ting-Lu, WANG Lei, ZHOU Gang, WANG Shu-Ying, LI Xing-Mao, NI Sheng-Li, MI Wen-Bo, ZHOU Xu-Jiao, CHENG Wan-Li, LI Shang-Zhong. Effects of straw mulching on soil water temperature effect and winter wheat yield in different rainfall years in Dryland Loess Plateau [J]. Acta Agronomica Sinica, 2025, 51(6): 1643-1653.
[6] MENG Xiang-Yu, DIAO Deng-Chao, LIU Ya-Rui, LI Yun-Li, SUN Yu-Chen, WU Wei, ZHAO Wen, WANG Yu, WU Jian-Hui, LI Chun-Lian, ZENG Qing-Dong, HAN De-Jun, ZHENG Wei-Jun. Genetic analysis of high yield and yield stability characteristics of new wheat variety Xinong 877 [J]. Acta Agronomica Sinica, 2025, 51(5): 1261-1276.
[7] WANG Qing, WANG Yi-Xiu, LI Yue-Nan, LYU Yong-Hui, ZHANG Hai-Bo, LIU Na, CHENG Hong-Yan. Differences in transcriptomic responses to cadmium stress in high/low-Cd- accumulation wheat [J]. Acta Agronomica Sinica, 2025, 51(5): 1230-1247.
[8] WANG Jia-Jie, WANG Zheng-Nan, BATOOL Maria, WANG Wang-Nian, WEN Jing, REN Chang-Zhong, HE Feng, WU You-You, XU Zheng-Hua, WANG Jing, KUAI Jie, WANG Bo, ZHOU Guang-Sheng, FU Ting-Dong. Comparison of physiological characteristics of salt and alkali tolerance between rapeseed and wheat [J]. Acta Agronomica Sinica, 2025, 51(5): 1215-1229.
[9] WANG Dong, WANG Sen, SHANG Li, FENG Hao-Wei, ZHANG Yong-Qiao, CUI Jia-Ming, LI Shuang, ZHANG Jia-Cong, CHE Huan. Effect of supplementary irrigation on winter wheat yield and water use efficiency in semi humid areas of the Loess Plateau [J]. Acta Agronomica Sinica, 2025, 51(5): 1312-1325.
[10] LI Pei-Hua, LI Jie, MENG Xiang-Yu, SUN Yu-Chen, FENG Yong-Jia, LI Yun-Li, DIAO Deng-Chao, ZHAO Wen, WU Wei, HAN De-Jun, ZHANG Song-Wu, ZHENG Wei-Jun. Evaluation of stress tolerance and physiological response of cold-type wheat under heat stress [J]. Acta Agronomica Sinica, 2025, 51(4): 1118-1130.
[11] LI Qiao, YE Yang-Chun, CHANG Xu-Hong, WANG De-Mei, WANG Yan-Jie, YANG Yu-Shuang, MA Rui-Qi, ZHAO Guang-Cai, CAI Rui-Guo, ZHANG Min, LIU Xi-Wei. Effects of high temperature and drought stresses on photosynthetic characteristics and yield of winter wheat after anthesis [J]. Acta Agronomica Sinica, 2025, 51(4): 1077-1090.
[12] WANG Jiao, BAI Hai-Xia, HAN Yu-Yan, LIANG Hui, FENG Ya-Nan, ZHANG Dong-Sheng, LI Ping, ZONG Yu-Zheng, SHI Xin-Rui, HAO Xing-Yu. Effects of elevated CO2 concentration, increased temperature and their interaction on the carbon and nitrogen metabolism in Liangxing 99 winter wheat leaves [J]. Acta Agronomica Sinica, 2025, 51(4): 1061-1076.
[13] CHENG Hong-Na, QIN Dan-Dan, XU Fu-Chao, XU Qing, PENG Yan-Chun, SUN Long-Qing, XU Le, GUO Ying, YANG Xin-Quan, XU De-Ze, DONG Jing. Comparative analysis of metabolomics of colored hulless barley and colored wheat grains [J]. Acta Agronomica Sinica, 2025, 51(4): 932-942.
[14] LI Hui-Min, XING Zhi-Peng, ZHANG Hai-Peng, WEI Hai-Yan, ZHANG Hong-Cheng, LI Guang-Yan. Application of chemical regulators and other cultivation measures in lodging resistance and high-yield cultivation of wheat [J]. Acta Agronomica Sinica, 2025, 51(4): 847-862.
[15] ZHANG Heng, FENG Ya-Lan, TIAN Wen-Zhong, GUO Bin-Bin, ZHANG Jun, MA Chao. Identification of TaSnRK gene family and expression analysis under localized root zone drought in wheat [J]. Acta Agronomica Sinica, 2025, 51(3): 632-649.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
No Suggested Reading articles found!