果树雄性不育研究进展

Advances in research on male sterility in fruit trees

摘要

雄性不育作为果树重要的农艺性状之一，直接关联授粉坐果率，影响果实产量与品质。雄性不育品种需要搭配授粉树或人工辅助授粉，费工费力，但又可省去人工去雄程序，提高杂种纯度和杂交育种效率，降低树体营养消耗，雄性不育还可以促进柑橘无核新品种创制。根据遗传方式的不同，雄性不育通常分为细胞质雄性不育（cytoplasmic male sterility，CMS）和细胞核雄性不育（genic male sterility，GMS）两种类型，但雄性不育相关的生理分子机制仍不甚清楚。本文系统梳理了果树雄性不育在表现形式、鉴定方法、遗传方式、生理及分子调控机制方面的研究进展，旨在为果树省力化栽培与优良无核新品种的选育提供理论参考。

Abstract

In the reproductive biology of fruit trees, male sterility, as an important agronomic trait, is directly related to pollination efficiency and breeding strategies. In the industry, this trait has been utilized for the selection of new varieties and the production of seedless fruits. According to different genetic modes, it is usually manifested as cytoplasmic male sterility (CMS) and nuclear male sterility (GMS). GMS is controlled by a single or a few genes in the nuclear genome and follows Mendelian inheritance laws, while CMS is usually caused by the interaction between genes in the mitochondrial genome and nuclear genes, and exhibits non-Mendelian inheritance characteristics. Male sterility in peach and apricot is of the GMS type, controlled by the Ps and Ms genes, respectively, while citrus belongs to the CMS type. Male sterility affects the efficient and labor-saving cultivation of fruit trees and the progress of seedless breeding. The physiological and molecular mechanisms of male sterility in fruit trees remain unknown. Male sterility in fruit trees exhibits diverse morphological manifestations, primarily including pollen abortion, abnormal tapetum structure, anther degeneration, stamen degeneration or morphological abnormality, microsporangium degeneration, and microspore degeneration, etc. Male sterility in fruit trees can be identified through visual inspection, the staining method, the pollen in vitro culture method, and in vivo identification. As a specific tissue that directly contacts microspores, the tapetum undergoes programmed cell death (PCD) during its development. Abnormalities in the structure or function of the tapetum are one of the key factors leading to male sterility in fruit trees. Tapetal programmed cell death (PCD) provides necessary enzymes, sporopollenin precursors, and other nutrients for the normal maturation of microspores and the formation of the pollen exine. During pollen development, the ability of carbohydrates, other nutrients, plant hormones, and antioxidant systems to remove free radicals significantly affects fertility. In addition, abnormal mitosis and meiosis of microspores during pollen development can also cause male sterility in apricots and citrus. Environmental factors, such as extreme temperatures (either too high or too low), insufficient light, drought or flooding stress, and pollutants in the air or soil, can also affect pollen fertility in fruit trees. During the process of microspore formation in peach, the genes regulating male sterility include the PpABCG26, PpCYP703A2, Pp4CL, and Prupe.6G025000 (CLSE6). In grape, the VvMs1, Vvms2, VviINP1, and VviPPR are involved in the regulation of microspore development. The Pbr035883.1 regulates the microspore development in pear. The genes Barnase, CgAP3.2, and CrMER3 affect pollen development in citrus fruits. The CmTAR regulates pollen development in chestnut. The ATP1 regulates pollen development in jujube. PmGRF7 regulates the formation of male sterility in plum. Additionally, methylation affects the pollen fertility in citrus. This study not only summarizes the research progress on the manifestation forms, identification methods, genetic studies, physiological mechanisms, and gene mining of male sterility in deciduous fruit trees such as peach, pear, grape, cherry, jujube, and chestnut, but also reports the research progress on the physiological mechanisms and gene mining of cytoplasmic male sterility in citrus. However, there are few reports on the molecular mechanisms of male sterility in fruit trees. While extensive research on pollen development in many species has focused on the synthesis and transport of sporopollenin, a comprehensive mechanistic understanding of pollen abortion at the molecular level is perhaps best exemplified by studies in citrus. The miR159a-DUO1 module regulates citrus pollen development by modulating auxin biosynthesis and starch metabolism. In the process of peach pollen development, a possible transcriptional regulatory mechanism involving DYT1-TDF1-AMS-MS188-MS1 exists. The polymerization and establishment of sporopollenin involve two crucial steps: synthesis and transport. The synthesis of sporopollenin refers to the synthesis and secretion of its precursors, while its transport refers to the final delivery to the microspores and the formation of the fine exine structure on the microspores. Sporopollenin is produced and accumulated in the tapetum by Acyl-CoA synthetase 5 (ACOS5), while type Ⅲ lipid transfer proteins (LTPs) function as components to transport it from the tapetum to the pollen exine. In the future, research on male sterility in fruit trees will focus on the exploration of male sterility genes and the analysis of their molecular mechanisms. Subsequently, it will involve the study of the mechanisms through which environmental factors influence the expression of these sterile genes. This study can offer significant theoretical support for the simplified cultivation of fruit trees and the breeding of new germplasm.

关键词

果树 / 雄性不育 / 花粉 / 绒毡层

Key words

Fruit trees / Male sterility / Pollen / Tapetum

参考文献

[1] 谢勇尧， 汤金涛， 杨博文， 胡骏， 刘耀光， 陈乐天 . 水稻育性调控的分子遗传研究进展[J]. 遗传， 2019， 41(8)： 703-715.

[2] Xie Yongyao， Tang Jintao， Yang Bowen， Hu Jun， Liu Yaoguang， Chen Letian. Current advance on molecular genetic regulation of rice fertility[J]. Hereditas， 2019， 41(8)： 703-715.

[3] Zhang X M， Ding Z P， Lou H B， Han R， Ma C Q， Yang S C . A systematic review and developmental perspective on origin of CMS genes in crops[J]. International Journal of Molecular Sciences， 2024， 25(15)： 8372.

[4] 王文然， 樊秀彩， 王晨， 刘崇怀， 房经贵 . 果树雄性不育的研究进展[J]. 分子植物育种， 2019， 17(1)： 245-254.

[5] Wang Wenran， Fan Xiucai， Wang Chen， Liu Chonghuai， Fang Jinggui. Advances research on male sterility in fruit crops[J]. Molecular Plant Breeding， 2019， 17(1)： 245-254.

[6] 王真， 郭继英， 姜全， 赵剑波， 任飞， 王尚德， 张瑜， 李新越， 郑书旗 . 桃生产成本构成及变化趋势调查研究[J]. 中国果树， 2019(5)： 105-107.

[7] Wang Zhen， Guo Jiying， Jiang Quan， Zhao Jianbo， Ren Fei， Wang Shangde， Zhang Yu， Li Xinyue， Zheng Shuqi. Investigation on producing cost structure and variation trend of peach[J]. China Fruits， 2019(5)： 105-107.

[8] 罗来水， 肖德兴， 霍光华， 刘勇， 辜青青 . 桃雄性不育的表现形式及其败育途径[J]. 果树科学， 2000， 17(2)： 89-96.

[9] Luo Laishui， Xiao Dexing， Huo Guanghua， Liu Yong， Gu Qingqing. Phenotypes of male sterilities and their abortion pathways among peach varieties[J]. Journal of Fruit Science， 2000， 17(2)： 89-96.

[10] Eduardo I， de Tomás C， Alexiou K， Giovannini D， Pietrella M， Carpenedo S， Bassols Raseira M， Batlle I， Cantín C， Aranzana M， Arús P . Fine mapping of the peach pollen sterility gene (Ps/ps) and detection of markers for marker-assisted selection [J]. Molecular Breeding， 2020， 40(6)： 57.

[11] Cai Y M， Ma Z S， Ogutu C O， Zhao L， Liao L， Zheng B B， Zhang R X， Wang L， Han Y P . Potential association of reactive oxygen species with male sterility in peach[J]. Frontiers in Plant Science， 2021， 12： 653256.

[12] Huang Z Y， Shen F， Chen Y L， Cao K， Wang L R . Preliminary identification of key genes controlling peach pollen fertility using genome-wide association study[J]. Plants， 2021， 10(2)： 242.

[13] 曹庆芹， 伊华林， 邓秀新 . 果树雄性不育研究进展[J]. 果树学报， 2005， 22(6)： 678-681.

[14] Cao Qingqin， Yi Hualin， Deng Xiuxin. Advances in research on male sterility in fruit crops[J]. Journal of Fruit Science， 2005， 22(6)： 678-681.

[15] 刘穆 . 种子植物形态解剖学导论[M]. 5 版 . 北京： 科学出版社， 2010.

[16] Liu Mu. Introduction to the morphological anatomy of seed plants[M]. 5th ed. Beijing：Science Press， 2010.

[17] 范眸天， 李树云， 李云 . 芒果雄性不育现象及花粉萌发研究初报[J]. 云南农业大学学报， 1996， 11(1)： 25-27.

[18] Fan Moutian， Li Shuyun， Li Yun. Stuies on the male sterility and pollen sprouting of mango[J]. Journal of Yunnan Agricultural University， 1996， 11(1)： 25-27.

[19] 曹珂， 王思倩， 朱更瑞， 方伟超， 陈昌文， 王力荣 . 桃花粉育性与花药颜色的关系及其 SSR 分子标记[J]. 植物遗传资源学报， 2010， 11(6)： 817-822.

[20] Cao Ke， Wang Siqian， Zhu Gengrui， Fang Weichao， Chen Changwen， Wang Lirong. Study on relationship between pollen fertility and anther color and its SSR marker screening in peach[J]. Journal of Plant Genetic Resources， 2010， 11(6)： 817-822.

[21] 沈元月， 王东昌 . “川中岛”白桃雄性不育小孢子发育的细胞形态学[J]. 应用与环境生物学报， 2002， 8(4)： 435-437.

[22] Shen Yuanyue， Wang Dongchang. Cytomorphology of microsporogenesis in male sterile of“Chuanzhongdao”white peach[J]. Chinese Journal of Applied & Environmental Biology， 2002， 8(4)： 435-437.

[23] 万淑媛. 桃花粉不育的细胞学特征及关键候选基因的鉴定[D]. 杨凌： 西北农林科技大学， 2021.

[24] Wan Shuyuan. Cytological characteristics and identification of key candidate genes of peach pollen sterility[D]. Yangling： Northwest A & F University， 2021.

[25] 李六林 . ‘新高’梨花粉败育的细胞学和生理特性研究[D]. 南京： 南京农业大学， 2007.

[26] Li Liulin. Studies on cytological and physiological characteristics of pollen abortion of‘Niitaka’(Pyrus pyrifolia Nakai) [D]. Nanjing： Nanjing Agricultural University， 2007.

[27] 唐宁浩 . 南方枣品种花粉育性规律的研究[D]. 长沙： 中南林业科技大学， 2010.

[28] Tang Ninghao. The studies on the rhythmic of pollen fertility of southern jujube cultivar[D]. Changsha： Central South University of Forestry & Technology， 2010.

[29] Scott D H， Weinberger J H . Inheritance of pollen sterility in some peach varieties[J]. Proceedings of the American Society for Horticultural Science， 1944， 9： 187-188.

[30] 闫芬芬， 王玖瑞， 吴翠云， 刘孟军 . 枣雄性不育种质‘JMS2’杂交子代开花结实性状的遗传分析[J]. 北方园艺， 2020(20)： 9-15.

[31] Yan Fenfen， Wang Jiurui， Wu Cuiyun， Liu Mengjun. Genetic analysis of flowering and fruit traits in hybrid progeny of male sterile germplasm‘JMS2’in Chinese jujube[J]. Northern Horticulture， 2020(20)： 9-15.

[32] 张立彬， 肖啸， 王学东， 戴刚 . 大久保桃自交后代若干性状的变异和遗传倾向[J]. 果树学报， 2004， 21(4)： 308-310.

[33] Zhang Libin， Xiao Xiao， Wang Xuedong， Dai Gang. Variability and inheritance of some characters in self-crossed progeny of Okubo peach cultivar[J]. Journal of Fruit Science， 2004， 21(4)： 308-310.

[34] Werner D J， Creller M A . Genetic studies in peach：Inheritance of sweet kernel and male sterility[J]. Journal of the American Society for Horticultural Science， 1997， 122(2)： 215-217.

[35] 俞明亮 . 桃性状遗传评价和分子标记技术研究[D]. 南京： 南京农业大学， 2004.

[36] Yu Mingliang. Genetic evaluation of main characters and study of molecular marker technique in peach[D]. Nanjing： Nanjing Agricultural University， 2004.

[37] 赵恺 . 桃花粉育性与果实性状的关系及花粉育性基因的定位[D]. 延吉： 延边大学， 2007.

[38] Zhao Kai. Relationship between peach pollen fertility and fruit traits and mapping of pollen fertilitygenes[D]. Yanji： Yanbian University， 2007.

[39] Soylu A . Heredity of male sterility in some chestnut cultivars (Castanea sativa Mill.) [J]. Acta Horticulturae， 1992(317)： 181-186.

[40] Marinoni D， Akkak A， Bounous G， Edwards K J， Botta R . Development and characterization of microsatellite markers in Castanea sativa (Mill.) [J]. Molecular Breeding， 2003， 11(2)： 127-136.

[41] Parish R W， Li S F . Death of a tapetum：A programme of developmental altruism[J]. Plant Science， 2010， 178(2)： 73-89.

[42] 罗来水， 霍光华， 刘勇， 肖德兴， 辜青青 . 桃雄性育性与花器官内游离氨基酸含量的关系[J]. 果树科学， 2000， 17(4)： 255-260.

[43] Luo Laishui， Huo Guanghua， Liu Yong， Xiao Dexing， Gu Qingqing. The relation between male fertility and free amino acid content of flower organ in peach[J]. Journal of Fruit Science， 2000， 17(4)： 255-260.

[44] 叶茂， 刘春生， 刘亚婷， 张曼， 苏凯， 张晨光， 李晓颖， 王海静， 肖啸， 张立彬， 杨清， 武军凯 . 转录组分析揭示 PpCYP703A2、Pp4CL 和 PpABCG26 参与调控桃花粉育性[J]. 农业生物技术学报， 2023， 31(7)： 1405-1418.

[45] Ye Mao， Liu Chunsheng， Liu Yating， Zhang Man， Su Kai， Zhang Chenguang， Li Xiaoying， Wang Haijing， Xiao Xiao， Zhang Libin， Yang Qing， Wu Junkai. Transcriptomic analysis reveals the involvement of PpCYP703A2，Pp4CL，and PpABCG26 in regulating peach (Prunus persica) pollen fertility [J]. Journal of Agricultural Biotechnology， 2023， 31(7)： 1405-1418.

[46] 王新鑫 . 西伯利亚杏雄性不育花解剖结构与生理特性研究[D]. 沈阳： 沈阳农业大学， 2023.

[47] Wang Xinxin. Study of anatomical structure and physiological characteristics of male sterility flowers in Prunus sibirica [D]. Shenyang： Shenyang Agricultural University， 2023.

[48] 齐国辉， 李保国， 郭素萍， 李冬至 . 黄金梨小孢子败育的解剖学观察[J]. 河北林果研究， 2009， 24(4)： 427-429.

[49] Qi Guohui， Li Baoguo， Guo Suping， Li Dongzhi. Anatomical study on the microspore abortion in Whangkeumbae[J]. Hebei Journal of Forestry and Orchard Research， 2009， 24(4)： 427-429.

[50] 谭智文， 金炳奎， 曹后男， 宗成文 . 延边小香水梨雄性不育细胞学研究[J]. 延边大学农学学报， 2013， 35(1)： 28-31.

[51] Tan Zhiwen， Jin Bingkui， Cao Hounan， Zong Chengwen. Cytological study on male sterility in Pyrus ussuriensis‘Xiaoxiangshui’ [J]. Journal of Agricultural Science Yanbian University， 2013， 35(1)： 28-31.

[52] 李彬， 蔡宇良， 赵晓军， 宛甜， 高天翔 . ‘马哈利’樱桃雄性不育细胞学观察[J]. 西北植物学报， 2015， 35(10)： 2007-2011.

[53] Li Bin， Cai Yuliang， Zhao Xiaojun， Wan Tian， Gao Tianxiang. Cytological observation of male sterile in Prunus mahaleb [J]. Acta Botanica Boreali-Occidentalia Sinica， 2015， 35(10)： 2007-2011.

[54] 郭艳玲， 张绍铃， 李六林， 马凯 . ‘新高’梨雄性不育与碳水化合物代谢研究[J]. 上海农业学报， 2007， 23(2)： 68-71.

[55] Guo Yanling， Zhang Shaoling， Li Liulin， Ma Kai. Study on the male sterility and carbohydrate metabolism of the pear variety‘Niitaka’[J]. Acta Agriculturae Shanghai， 2007， 23(2)： 68-71.

[56] 李皓 . ‘新梨七号’雄性不育机制及花粉直感效应研究[D]. 阿拉尔： 塔里木大学， 2025.

[57] Li Hao. Male sterility mechanism and pollen xenia effect of‘Xinli No.7’[D]. Alar： Tarim University， 2025.

[58] 张彦昌， 赵德英， 马骏 . 果树雄性不育机理研究进展[J]. 河北林果研究， 2008， 23(1)： 66-69.

[59] Zhang Yanchang， Zhao Deying， Ma Jun. Study on male sterility of fruit trees[J]. Hebei Journal of Forestry and Orchard Research， 2008， 23(1)： 66-69.

[60] 刘阳 . 生长素介导的板栗雄花序败育的机理研究[D]. 北京： 北京林业大学， 2022.

[61] Liu Yang. Mechanism of auxin mediated on staminate catkins abortion in Chinese chestnut (Castanea mollissima) [D]. Beijing： Beijing Forestry University， 2022.

[62] Li P， Tian J， Guo C K， Luo S P， Li J . Interaction of gibberellin and other hormones in almond anthers：Phenotypic and physiological changes and transcriptomic reprogramming[J]. Horticulture Research， 2021， 8(1)： 94.

[63] 洪奔， 陶建敏， 农慧兰， 徐颖一， 耿艺宁， 凌千惠， 郑焕 . ‘阳光玫瑰’雄性不育株花蕾发育期抗氧化酶活性和内源激素含量的变化[J]. 西北植物学报， 2022， 42(3)： 444-452.

[64] Hong Ben， Tao Jianmin， Nong Huilan， Xu Yingyi， Geng Yining， Ling Qianhui， Zheng Huan. Analysis of antioxidant enzymes activities and endogenous hormone contents in male sterile plant of‘Shine Muscat’seeding during bud development[J]. Acta Botanica Boreali-Occidentalia Sinica， 2022， 42(3)： 444-452.

[65] 郑焕 . ‘钟山红’葡萄雄性不育形成机理研究[D]. 南京： 南京农业大学， 2013.

[66] Zheng Huan. Studies the mechanism of male sterile in new gapevine selection‘Zhong Shan Hong’[D]. Nanjing： Nanjing Agricultural University， 2013.

[67] 王玖瑞 . 枣树雄性不育和胚败育研究[D]. 保定： 河北农业大学， 2004.

[68] Wang Jiurui. Studies on male sterility and embryo abortion of Chinese jujube (Ziziphus jujuba Mill.) [D]. Baoding： Hebei Agricultural University， 2004.

[69] 刘丽华， 沈广宁， 张倩， 赵永孝， 许琳 . ‘浮来无花’板栗雄花序败育的生理特性研究[J]. 山东农业科学， 2007， 39(5)： 45-47.

[70] LIU Lihua， SHEN Guangning， ZHANG Qian， ZHAO Yongxiao， XU Lin. Study on physiological characteristics of male inflorescence abortion in‘Fulaiwuhua’chestnut[J]. Shandong Agricultural Sciences， 2007， 39(5)： 45-47.

[71] 叶丽霞 . 多组学解析‘华农’无籽椪柑花粉败育机制[D]. 武汉： 华中农业大学， 2021.

[72] Ye Lixia. Multi-omics analysis of the mechanism of pollen abortion in‘Hua Nong’seedless ponkan[D]. Wuhan： Huazhong Agricultural University， 2021.

[73] 彭宇 . 观赏海棠雄性不育鉴定及其生理生化机制探讨[D]. 新乡： 河南科技学院， 2025.

[74] Peng Yu. Identification of male sterility in flowering crabapple and exploration of its physiological and biochemical mechanism[D]. Xinxiang： Henan Institute of Science and Technology， 2025.

[75] 俞狄虎 . 转录组和蛋白质组关联分析‘无子瓯柑’雄性不育分子机理[D]. 杭州： 浙江农林大学， 2018.

[76] Yu Dihu. An integrative analysis of the transcriptome and proteome of‘Wuzi ougan’(Citrus suavissima Hort. ex Tanaka‘Seedless’) and the wild type improves our understanding of male sterility [D]. Hangzhou： Zhejiang A & F University， 2018.

[77] Zhang S S， Pingcuo G S， Ying H， Zhao F， Cui Y N， Zeng X L . Male sterility is linked to the flavonoid biosynthesis pathways in Prunus mira [J]. Bioinformation， 2020， 16(5)： 363-374.

[78] Fan Y J， Du Z Z， He X Y， Liu Z A， Zhuang J X， Xiao G A， Duan Y Y， Tan F Q， Xie K D， Jiao W B， Zhang F， Yang C， Guo W W， Wu X M . Somatic variations in the meiosis-specific gene CrMER3 confer seedlessness in a citrus bud sport [J]. Journal of Integrative Plant Biology， 2025， 67(6)： 1649-1664.

[79] 叶正文， 杜纪红， 苏明申， 周慧娟 . 高温对桃小孢子产生及花粉发育的影响[C]//中国园艺学会桃分会 . 中国园艺学会桃分会第三届学术研讨会论文集 . 西安： 2011： 219-225.

[80] Ye Zhengwen， Du Jihong， Su Mingshen， Zhou Huijuan. Effects of high temperature on microsporogenesis and pollen development in peach[C]//Peach Branch of Chinese Society for Horticultural Science. Proceedings of the Third Academic Symposium of Peach Branch of Chinese Society for Horticultural Science. Xi’an： 2011： 219-225.

[81] 杨雅婷， 苏立新， 范明霞 . 植物花粉发育响应高温胁迫的研究进展[J]. 世界热带农业信息， 2025(2)： 16-18.

[82] Yang Yating， Su Lixin， Fan Mingxia. Research progress on plant pollen development in response to high temperature stress[J]. World Tropical Agriculture Information， 2025(2)： 16-18.

[83] Huang Z Y， Bie H L， Li M， Xia L H， Chen L， Chen Y L， Wang L R， Gan Z Y， Cao K . Integrated GWAS BSA-seq，and RNA-seq analyses to identify candidate genes associated with male fertility trait in peach[J]. Plant Physiology and Biochemistry， 2025， 220： 109525.

[84] 郑焕， 张计育， 王新卫， 章镇， 季晨飞， 陶建敏 . 葡萄雌能花相关基因 VvMS2 的克隆及表达分析 [J]. 中国农业科学， 2013， 46(14)： 2953-2962.

[85] Zheng Huan， Zhang Jiyu， Wang Xinwei， Zhang Zhen， Ji Chenfei， Tao Jianmin. Cloning and expression analysis of a male sterility-related gene VvMS2 from grapes [J]. Scientia Agricultura Sinica， 2013， 46(14)： 2953-2962.

[86] Massonnet M， Cochetel N， Minio A， Vondras A M， Lin J， Muyle A， Garcia J F， Zhou Y F， Delledonne M， Riaz S， Figueroa-Balderas R， Gaut B S， Cantu D . The genetic basis of sex determination in grapes[J]. Nature Communications， 2020， 11： 2902.

[87] 梁月婷 . 葡萄 VviPPR 基因调控雄性育性的功能验证 [D]. 南京： 南京农业大学， 2023.

[88] Liang Yueting. Functional verification of grape VviPPR gene in regulating male fertility [D]. Nanjing： Nanjing Agricultural University， 2023.

[89] Jiang N， Feng M Q， Cheng L C， Kuang L H， Li C C， Yin Z P， Wang R， Xie K D， Guo W W， Wu X M . Spatiotemporal profiles of gene activity in stamen delineate nucleo-cytoplasmic interaction in a male-sterile somatic cybrid citrus[J]. Horticulture Research， 2023， 10(7)： uhad105.

[90] Koltunow A M， Brennan P， Bond J E， Barker S J . Evaluation of genes to reduce seed size in shape Arabidopsis and tobacco and their application to shape Citrus [J]. Molecular Breeding， 1998， 4(3)： 235-251.

[91] 冯春芳， 张力曼， 赵锦， 刘志国， 王玖瑞， 刘孟军 . 枣 ATP1 基因克隆及其在雄性可育和不育品种中的表达分析 [J]. 河北农业大学学报， 2017， 40(3)： 59-64.

[92] Feng Chunfang， Zhang Liman， Zhao Jin， Liu Zhiguo， Wang Jiurui， Liu Mengjun. ATP1 gene cloning and its expression in male-sterile and male-fertile cultivars of Chinese jujube (Ziziphus jujuba Mill.) [J]. Journal of Agricultural University of Hebei， 2017， 40(3)： 59-64.

[93] Badenes M L， Hurtado M A， Sanz F， Archelos D M， Burgos L， Egea J， Llácerl G . Searching for molecular markers linked to male sterility and self-compatibility in apricot[J]. Plant Breeding， 2000， 119(2)： 157-160.

[94] Lian X D， Zhang H P， Jiang C， Gao F， Yan L， Zheng X B， Cheng J， Wang W， Wang X B， Ye X， Li J D， Zhang L L， Li Z Q， Tan B， Feng J C . De novo chromosome-level genome of a semi-dwarf cultivar of Prunus persica identifies the aquaporin PpTIP2 as responsible for temperature-sensitive semi-dwarf trait and PpB3-1 for flower type and size [J]. Plant Biotechnology Journal， 2022， 20(5)： 886-902.

[95] Donoso J M， Eduardo I， Picañol R， Batlle I， Howad W， Aranzana M J， Arús P . High-density mapping suggests cytoplasmic male sterility with two restorer genes in almond × peach progenies[J]. Horticulture Research， 2015， 2： 15016.

[96] 王蕊 . 梅 PmGRF7 基因功能鉴定及 miR396 的调控分析 [D]. 南京： 南京农业大学， 2022.

[97] Wang Rui. Functional identification of PmGRF7 gene and regulation analysis of miR396 in Japanese apricot [D]. Nanjing： Nanjing Agricultural University， 2022.

[98] 师小舒， 谢善鹏， 解凯东， 周锐， 陈鹏， 戴亚， 郭玲霞， 伍小萌， 郭文武 . 以雄性不育华柚 2 号为母本有性杂交创制柚潜在无核新种质[J]. 果树学报， 2024， 41(12)： 2389-2396.

[99] Shi Xiaoshu， Xie Shanpeng， Xie Kaidong， Zhou Rui， Chen Peng， Dai Ya， Guo Lingxia， Wu Xiaomeng， Guo Wenwu. Production of potential seedless pummelo sexual progenies via sexual hybridization using male-sterile cybrid Huayou No. 2 as the female parent [J]. Journal of Fruit Science， 2024， 41(12)： 2389-2396.

[100] Wang R， Shi Y C， Xie K D， Xie Z Z， Wu X M， Guo W W . The citrus somatic cybrids exhibit various degrees of male sterility conferred by mitochondrial genome of Satsuma mandarin (Citrus unshiu) [J]. Scientia Horticulturae， 2024， 338： 113624.

[101] Wang N， Li C C， Kuang L H， Wu X M， Xie K D， Zhu A D， Xu Q， Larkin R M， Zhou Y F， Deng X X， Guo W W . Pan-mitogenomics reveals the genetic basis of cytonuclear conflicts in citrus hybridization，domestication，and diversification[J]. Proceedings of the National Academy of Sciences of the United States of America， 2022， 119(43)： e2206076119.

[102] 邱文明， 张祖铭， 徐育海， 何秀娟， 孙中海， 仝铸， 肖翠， 吴黎明， 郭文武 . 柑橘雄性不育类蛋白基因 MSLP 的克隆与分析 [J]. 园艺学报， 2019， 46(12)： 2323-2334.

[103] Qiu Wenming， Zhang Zuming， Xu Yuhai， He Xiujuan， Sun Zhonghai， Tong Zhu， Xiao Cui， Wu Liming， Guo Wenwu. Cloning and functional analysis of male sterile 2-like protein gene (MSLP) in Citrus [J]. Acta Horticulturae Sinica， 2019， 46(12)： 2323-2334.

[104] 胡志勇 . ‘无核瓯柑’、温州蜜柑无核的细胞及分子机理研究[D]. 武汉： 华中农业大学， 2007.

[105] Hu Zhiyong. Studies on the cytological and molecular mechanism referring seedlessness of‘Ougan’and Satsuma mandarin[D]. Wuhan： Huazhong Agricultural University， 2007.

[106] Xu Y H， Tian W X， Yin M Q， Cai Z M， Zhang L， Yuan D Y， Yi H L， Wu J X . The miR159a- DUO1 module regulates pollen development by modulating auxin biosynthesis and starch metabolism in citrus [J]. Journal of Integrative Plant Biology， 2024， 66(7)： 1351-1369.

[107] Wang K， Guo Z L， Zhou W T， Zhang C， Zhang Z Y， Lou Y， Xiong S X， Yao X Z， Fan J J， Zhu J， Yang Z N . The regulation of sporopollenin biosynthesis genes for rapid pollen wall formation[J]. Plant Physiology， 2018， 178(1)： 283-294.

[108] Ariizumi T， Toriyama K . Genetic regulation of sporopollenin synthesis and pollen exine development[J]. Annual Review of Plant Biology， 2011， 62： 437-460.

[109] Ríos G， Tadeo F R， Leida C， Badenes M L . Prediction of components of the sporopollenin synthesis pathway in peach by genomic and expression analyses[J]. BMC Genomics， 2013， 14(1)： 40.

[110] 苏振新， 周鹊， 楼悦 . 花药绒毡层发育及调控的分子研究进展[J]. 中国科学：生命科学， 2025， 55(2)： 206-225.

[111] Su Zhenxin， Zhou Que， Lou Yue. Advance in the anther tapetum development and their regulatory mechanisms[J]. Scientia Sinica (Vitae)， 2025， 55(2)： 206-225.

基金资助

国家自然科学基金项目(32402512)

河北省自然科学青年基金项目(C2024407070)