Genic male and female sterility in vegetable crops

Abstract

Vegetable crops are greatly appreciated for their beneficial nutritional and health components. Hybrid seeds are widely used in vegetable crops for advantages such as high yield and improved resistance, which require the participation of male (stamen) and female (pistil) reproductive organs. Male- or female-sterile plants are commonly used for production of hybrid seeds or seedless fruits in vegetables. In this review we will focus on the types of genic male sterility and factors affecting female fertility, summarize typical gene function and research progress related to reproductive organ identity and sporophyte and gametophyte development in vegetable crops [mainly tomato (Solanum lycopersicum) and cucumber (Cucumis sativus)], and discuss the research trends and application perspectives of the sterile trait in vegetable breeding and hybrid production, in order to provide a reference for fertility-related germplasm innovation.

Acknowledgements

We thank Dr Luo Chen for the pictures of lettuce flowers in Fig. 1f–h, and Dr Chen Jie for the image of a tomato floral bud section in Fig. 2. We apologize to authors not cited due to space limitations. This work was supported by National Natural Science Foundation of China (32025033) and (31930097), and the Chinese Universities Scientific Fund (2022TC009).

Author contributions

C.Z. and S.W. wrote the original draft and prepared the figures; Z.X. supervised the work and revised the manuscript. All authors have read and agreed to the published version of the manuscript.

Conflict of interest

The authors declared no conflict of interest.

References

[1] Carrari F, Baxter C, Usadel B. et al. Integrated analysis of metabolite and transcript levels reveals the metabolic shifts that underlie tomato fruit development and highlight regulatory aspects of metabolic network behavior. Plant Physiol 2006; 142: 1380-96.

[2] Raghavan V . Some reflections on double fertilization, from its discovery to the present. New Phytol 2003; 159: 565-83.

[3] Pnueli L, Hareven D, Broday L. et al. The Tm5 Mads box gene mediates organ differentiation in the 3 inner whorls of tomato flowers. Plant Cell 1994; 6: 175-86.

[4] Bai SL, Peng YB, Cui JX. et al. Developmental analyses reveal early arrests of the spore-bearing parts of reproductive organs in unisexual flowers of cucumber (Cucumis sativus L.). Planta 2004; 220: 230-40.

[5] Ning K, Han Y, Chen Z. et al. Genome-wide analysis of MADS-box family genes during flower development in lettuce. Plant Cell Environ 2019; 42: 1868-81.

[6] Yu DL, Gu XF, Zhang SP. et al. Molecular basis of heterosis and related breeding strategies reveal its importance in vegetable breeding. Hortic Res 2021; 8: 120.

[7] Dias J. Guiding strategies for breeding vegetable cultivars. Agric Sci 2014; 5: 9-32.

[8] Gorman SW, McCormick S, Rick C . Male sterility in tomato. Crit Rev Plant Sci 1997; 16: 31-53.

[9] Shifriss C . Male sterility in pepper (Capsicum annuum L). Euphytica 1997; 93: 83-8.

[10] Ying M, Dreyer F, Cai DG. et al. Molecular markers for genic male sterility in Chinese cabbage. Euphytica 2003; 132: 227-34.

[11] Varoquaux F, Blanvillain R, Delseny M et al. Less is better: new approaches for seedless fruit production. Trends Biotechnol 2000; 18: 233-42.

[12] Lukyanenko AN . Parthenocarpy in tomato. Berlin: Springer; 1991.

[13] Baker LR, Scott JW, Wilson JE . Seedless pickles-a new concept. Res Rep Mich State Univ Agric Exp Stn 1973; 14: 167-77.

[14] Gorguet B, van Heusden AW, Lindhout P . Parthenocarpic fruit development in tomato. Plant Biol (Stuttg) 2005; 7: 131-9.

[15] Koltunow AM, Truettner J, Cox KH. et al. Different temporal and spatial gene-expression patterns occur during anther development. Plant Cell 1990; 2: 1201-24.

[16] Sanders PM, Bui AQ, Weterings K. et al. Anther developmental defects in Arabidopsis thaliana male-sterile mutants . Sex Plant Reprod 1999; 11: 297-322.

[17] Coen ES, Meyerowitz EM . The war of the whorls-genetic interactions controlling flower development. Nature 1991; 353: 31-7.

[18] Weigel D, Meyerowitz EM . The ABCs of floral homeotic genes. Cell 1994; 78: 203-9.

[19] Robles P, Pelaz S . Flower and fruit development in Arabidopsis thaliana. Int J Dev Biol 2005; 49: 633-43.

[20] Brukhin V, Hernould M, Gonzalez N. et al. Flower development schedule in tomato Lycopersicon esculentum cv. sweet cherry . Sex Plant Reprod 2003; 15: 311-20.

[21] Gomez P, Jamilena M, Capel J. et al. Stamenless, a tomato mutant with homeotic conversions in petals and stamens. Planta 1999; 209: 172-9.

[22] de Martino G, Pan I, Emmanuel E. et al. Functional analyses of two tomato APETALA3 genes demonstrate diversification in their roles in regulating floral development. Plant Cell 2006; 18: 1833-45.

[23] Quinet M, Bataille G, Dobrev PI et al. Transcriptional and hormonal regulation of petal and stamen development by STAMENLESS, the tomato (Solanum lycopersicum L.) orthologue to the B-class APETALA3 gene . J Exp Bot 2014; 65: 2243-56.

[24] Cao X, Liu XY, Wang XT. et al. B-class MADS-box TM6 is a candidate gene for tomato male sterile-15(26). Theor Appl Genet 2019; 132: 2125-35.

[25] Geuten K, Irish V . Hidden variability of floral homeotic B genes in Solanaceae provides a molecular basis for the evolution of novel functions. Plant Cell 2010; 22: 2562-78.

[26] Sawhney VK, Greyson RI . Morphogenesis of Stamenless-2 mutant in tomato. 1. Comparative description of flowers and ontogeny of stamens in normal and mutant plants. Am J Bot 1973; 60: 514-23.

[27] Pucci A, Picarella ME, Mazzucato A . Phenotypic, genetic and molecular characterization of 7B-1, a conditional male-sterile mutant in tomato. Theor Appl Genet 2017; 130: 2361-74.

[28] Pnueli L, Hareven AD, Rounsley SD et al. Isolation of the tomato AGAMOUS gene Tag1 and analysis of its homeotic role in transgenic plants. Plant Cell 1994; 6: 163-73.

[29] Ampomah-Dwamena C, Morris BA, Sutherland P. et al. Down-regulation of TM29, a tomato SEPALLATA homolog, causes parthenocarpic fruit development and floral reversion. Plant Physiol 2002; 130: 605-17.

[30] Zhang HM, Li S, Yang L. et al. Gain-of-function of the 1-aminocyclopropane-1-carboxylate synthase gene ACS1G induces female flower development in cucumber gynoecy. Plant Cell 2021; 33: 306-21.

[31] Zhang ZH, Mao LY, Chen HM. et al. Genome-wide mapping of structural variations reveals a copy number variant that determines reproductive morphology in cucumber. Plant Cell 2015; 27: 1595-604.

[32] Li Z, Wang S, Tao Q. et al. A putative positive feedback regulation mechanism in CsACS2 expression suggests a modified model for sex determination in cucumber (Cucumis sativus L.). J Exp Bot 2012; 63: 4475-84.

[33] Boualem A, Troadec C, Camps C. et al. A cucurbit androecy gene reveals how unisexual flowers develop and dioecy emerges. Science 2015; 350: 688-91.

[34] Kater MM, Franken J, Carney KJ. et al. Sex determination in the monoecious species cucumber is confined to specific floral whorls. Plant Cell 2001; 13: 481-93.

[35] Sun JJ, Li F, Wang DH. et al. CsAP3: a cucumber homolog to Arabidopsis APETALA3 with novel characteristics . Front Plant Sci 2016; 7: 1181.

[36] Sather DN, Jovanovic M, Golenberg EM . Functional analysis of B and C class floral organ genes in spinach demonstrates their role in sexual dimorphism. BMC Plant Biol 2010; 10: 46.

[37] Medina M, Roque E, Pineda B. et al. Early anther ablation triggers parthenocarpic fruit development in tomato. Plant Biotechnol J 2013; 11: 770-9.

[38] Roque E, Gomez MD, Ellul P. et al. The PsEND1 promoter: a novel tool to produce genetically engineered male-sterile plants by early anther ablation. Plant Cell Rep 2007; 26: 313-25.

[39] McCormick S. Male gametophyte development. Plant Cell 1993; 5: 1265-75.

[40] Walbot V, Egger RL . Pre-meiotic anther development: cell fate specification and differentiation. Annu Rev Plant Biol 2016; 67: 365-95.

[41] Hao S, Ariizumi T, Ezura H . SEXUAL STERILITY is essential for both male and female gametogenesis in tomato. Plant Cell Physiol 2017; 58: 22-34.

[42] Ito T, Wellmer F, Yu H. et al. The homeotic protein AGAMOUS controls microsporogenesis by regulation of SPOROCYTELESS. Nature 2004; 430: 356-60.

[43] Schiefthaler U, Balasubramanian S, Sieber P. et al. Molecular analysis of NOZZLE, a gene involved in pattern formation and early sporogenesis during sex organ development in Arabidopsis thaliana. Proc Natl Acad Sci USA 1999; 96: 11664-9.

[44] Yang WC, Ye D, Xu J. et al. The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein . Genes Dev 1999; 13: 2108-17.

[45] Liu XF, Ning K, Che G. et al. CsSPL functions as an adaptor between HD-ZIPIII and CsWUS transcription factors regulating anther and ovule development in Cucumis sativus (cucumber). Plant J 2018; 94: 535-47.

[46] Jeong HJ, Kang JH, Zhao MA. et al. Tomato male sterile 10(35) is essential for pollen development and meiosis in anthers. J Exp Bot 2014; 65: 6693-709.

[47] Cheng Q, Wang P, Liu JQ. et al. Identification of candidate genes underlying genic male-sterile msc-1 locus via genome resequencing in Capsicum annuum L. Theor Appl Genet 2018; 131: 1861-72.

[48] Liu XY, Yang MX, Liu XL. et al. A putative bHLH transcription factor is a candidate gene for male sterile 32, a locus affecting pollen and tapetum development in tomato. Hortic Res 2019; 6: 88.

[49] Zhang R, Chang J, Li J. et al. Disruption of the bHLH transcription factor Abnormal Tapetum 1 causes male sterility in watermelon. Hortic Res 2021; 8: 258.

[50] Zhu E, You C, Wang S. et al. The DYT1-interacting proteins bHLH010, bHLH089 and bHLH091 are redundantly required for Arabidopsis anther development and transcriptome . Plant J 2015; 83: 976-90.

[51] Zhang W, Sun YJ, Timofejeva L. et al. Regulation of Arabidopsis tapetum development and function by dysfunctional tapetum1 (dyt1) encoding a putative bHLH transcription factor . Development 2006; 133: 3085-95.

[52] Sorensen AM, Krober S, Unte US. et al. The Arabidopsis ABORTED MICROSPORES (AMS) gene encodes a MYC class transcription factor . Plant J 2003; 33: 413-23.

[53] Wilson ZA, Morroll SM, Dawson J. et al. The Arabidopsis MALE STERILITY1 (MS1) gene is a transcriptional regulator of male gametogenesis, with homology to the PHD-finger family of transcription factors . Plant J 2001; 28: 27-39.

[54] Lou Y, Zhou HS, Han Y. et al. Positive regulation of AMS by TDF1 and the formation of a TDF1-AMS complex are required for anther development in Arabidopsis thaliana. New Phytol 2018; 217: 378-91.

[55] Zhu J, Lou Y, Xu XF. et al. A genetic pathway for tapetum development and function in Arabidopsis. J Integr Plant Biol 2011; 53: 892-900.

[56] Zhang SY, Wang J, Chen GH. et al. Functional analysis of a MYB transcription factor BrTDF1 in the tapetum development of Wucai (Brassica rapa ssp.). Sci Hortic 2019; 257, 108728.

[57] Cheng Q, Li T, Ai Y. et al. Phenotypic, genetic, and molecular function of msc-2, a genic male sterile mutant in pepper (Capsicum annuum L.). Theor Appl Genet 2020; 133: 843-55.

[58] Sheng YY, Wang YD, Jiao SQ. et al. Mapping and preliminary analysis of ABORTED MICROSPORES (AMS) as the candidate gene underlying the male sterility (MS-5) mutant in melon (Cucumis melo L.). Front Plant Sci 2017; 8: 902.

[59] Guo JJ, Liu C, Wang P. et al. The aborted microspores (AMS)-like gene is required for anther and microspore development in pepper (Capsicum annuum L.). Int J Mol Sci 2018; 19: 1341.

[60] Niu HH, Liu XF, Tong C. et al. The WUSCHEL-related homeobox1 gene of cucumber regulates reproductive organ development. J Exp Bot 2018; 69: 5373-87.

[61] Takei H, Shinozaki Y, Yano R. et al. Loss-of-function of a tomato receptor-like kinase impairs male fertility and induces parthenocarpic fruit set. Front Plant Sci 2019; 10: 403.

[62] Fernandes JB, Seguela-Arnaud M, Larcheveque C. et al. Unleashing meiotic crossovers in hybrid plants. Proc Natl Acad Sci USA 2018; 115: 2431-6.

[63] Zhang PP, Zhang YX, Sun LP. et al. The rice AAA-ATPase OsFIGNL1 is essential for male meiosis. Front Plant Sci 2017; 8: 1639.

[64] Mieulet D, Aubert G, Bres C. et al. Unleashing meiotic crossovers in crops. Nat Plants 2018; 4: 1010-6.

[65] Reddy TV, Kaur J, Agashe B. et al. The DUET gene is necessary for chromosome organization and progression during male meiosis in Arabidopsis and encodes a PHD finger protein . Development 2003; 130: 5975-87.

[66] Han Y, Zhao F, Gao S. et al. Fine mapping of a male sterility gene ms-3 in a novel cucumber (Cucumis sativus L.) mutant . Theor Appl Genet 2018; 131: 449-60.

[67] McCormick S. Control of male gametophyte development. Plant Cell 2004; 16: S142-53.

[68] Chen L, Yang D, Zhang Y. et al. Evidence for a specific and critical role of mitogen-activated protein kinase 20 in uni-to-binucleate transition of microgametogenesis in tomato. New Phytol 2018; 219: 176-94.

[69] Wang J, Li M, Zhuo S. et al. Mitogen-activated protein kinase 4 is obligatory for late pollen and early fruit development in tomato. Hortic Res 2022; 9: uhac048.

[70] Yang DD, Liu Y, Ali M. et al. Phytochrome interacting factor 3 regulates pollen mitotic division through auxin signalling and sugar metabolism pathways in tomato. New Phytol 2022; 234: 560-77.

[71] Zhang Y, Zhang B, Yang TW. et al. The GAMYB-like gene SlMYB33 mediates flowering and pollen development in tomato. Hortic Res 2020; 7: 133.

[72] Sun LL, Sui XL, Lucas WJ. et al. Down-regulation of the sucrose transporter CsSUT1 causes male sterility by altering carbohydrate supply. Plant Physiol 2019; 180: 986-97.

[73] Cheng JT, Wang ZY, Yao FZ. et al. Down-regulating CsHT1, a cucumber pollen-specific hexose transporter, inhibits pollen germination, tube growth, and seed development. Plant Physiol 2015; 168: 635-47.

[74] Nashilevitz S, Melamed-Bessudo C, Aharoni A. et al. The legwd mutant uncovers the role of starch phosphorylation in pollen development and germination in tomato. Plant J 2009; 57: 1-13.

[75] Sinha R, Rajam MV . RNAi silencing of three homologues of S-adenosylmethionine decarboxylase gene in tapetal tissue of tomato results in male sterility. Plant Mol Biol 2013; 82: 169-80.

[76] Gan ZY, Feng Y, Wu T. et al. Downregulation of the auxin transporter gene SlPIN8 results in pollen abortion in tomato. Plant Mol Biol 2019; 99: 561-73.

[77] Keijzer CJ . The processes of anther dehiscence and pollen dispersal: II. The formation and the transfer mechanism of pollenkitt, cell-wall development of the loculus tissues and a function of orbicules in pollen dispersal. New Phytol 1987; 105: 499-507.

[78] Gorguet B, Schipper D, van Lammeren A. et al. Ps-2, the gene responsible for functional sterility in tomato, due to non-dehiscent anthers, is the result of a mutation in a novel polygalacturonase gene. Theor Appl Genet 2009; 118: 1199-209.

[79] Gorguet B, Schipper D, van Heusden AW. et al. High-resolution fine mapping of ps-2, a mutated gene conferring functional male sterility in tomato due to non-dehiscent anthers. Theor Appl Genet 2006; 113: 1437-48.

[80] Leide J, Hildebrandt U, Reussing K. et al. The developmental pattern of tomato fruit wax accumulation and its impact on cuticular transpiration barrier properties: effects of a deficiency in a beta-ketoacyl-coenzyme a synthase (LeCER6). Plant Physiol 2007; 144: 1667-79.

[81] Smirnova A, Leide J, Riederer M . Deficiency in a very-long-chain fatty acid beta-ketoacyl-coenzyme a synthase of tomato impairs microgametogenesis and causes floral organ fusion. Plant Physiol 2013; 161: 196-209.

[82] Chen KY, Cong B, Wing R. et al. Changes in regulation of a transcription factor lead to autogamy in cultivated tomatoes. Science 2007; 318: 643-5.

[83] Marti C, Orzaez D, Ellul P. et al. Silencing of DELLA induces facultative parthenocarpy in tomato fruits. Plant J 2007; 52: 865-76.

[84] Garcia-Hurtado N, Carrera E, Ruiz-Rivero O. et al. The characterization of transgenic tomato overexpressing gibberellin 20-oxidase reveals induction of parthenocarpic fruit growth, higher yield, and alteration of the gibberellin biosynthetic pathway. J Exp Bot 2012; 63: 5803-13.

[85] Cheng MZ, Gong C, Zhang B. et al. Morphological and anatomical characteristics of exserted stigma sterility and the location and function of SlLst (Solanum lycopersicum Long styles) gene in tomato . Theor Appl Genet 2021; 134: 505-18.

[86] Pan CT, Yang DD, Zhao XL. et al. Tomato stigma exsertion induced by high temperature is associated with the jasmonate signalling pathway. Plant Cell Environ 2019; 42: 1205-21.

[87] Mazzucato A, Cellini F, Bouzayen M. et al. A TILLING allele of the tomato aux/IAA9 gene offers new insights into fruit set mechanisms and perspectives for breeding seedless tomatoes. Mol Breeding 2015; 35: 22.

[88] Mounet F, Moing A, Kowalczyk M. et al. Down-regulation of a single auxin efflux transport protein in tomato induces precocious fruit development. J Exp Bot 2012; 63: 4901-17.

[89] Du LM, Bao CL, Hu TH. et al. SmARF8, a transcription factor involved in parthenocarpy in eggplant. Mol Gen Genomics 2016; 291: 93-105.

[90] Cai XD, Fu J, Deng XX. et al. Production and molecular characterization of potential seedless cybrid plants between pollen sterile Satsuma mandarin and two seedy citrus cultivars. Plant Cell Tiss Org 2007; 90: 275-83.

[91] Guo WW, Prasad D, Cheng YJ. et al. Targeted cybridization in citrus: transfer of Satsuma cytoplasm to seedy cultivars for potential seedlessness. Plant Cell Rep 2004; 22: 752-8.

[92] Wang X, Gao DL, Sun JJ. et al. An exon skipping in a SEPALLATA-like gene is associated with perturbed floral and fruits development in cucumber. J Integr Plant Biol 2016; 58: 766-71.

[93] Qu LJ, Li L, Lan Z et al. Peptide signalling during the pollen tube journey and double fertilization. J Exp Bot 2015; 66: 5139-50.

[94] Crawford BCW, Yanofsky MF . The formation and function of the female reproductive tract in flowering plants. Curr Biol 2008; 18: R972-8.

[95] Heisler MGB, Atkinson A, Bylstra YH. et al. SPATULA, a gene that controls development of carpel margin tissues in Arabidopsis, encodes a bHLH protein . Development 2001; 128: 1089-98.

[96] Wu MF, Tian Q, Reed JW . Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction . Development 2006; 133: 4211-8.

[97] Gremski K, Ditta G, Yanofsky MF . The HECATE genes regulate female reproductive tract development in Arabidopsis thaliana. Development 2007; 134: 3593-601.

[98] Crawford BCW, Ditta G, Yanofsky MF . The NTT gene is required for transmitting-tract development in carpels of Arabidopsis thaliana. Curr Biol 2007; 17: 1101-8.

[99] Crawford BCW, Yanofsky MF . HALF FILLED promotes reproductive tract development and fertilization efficiency in Arabidopsis thaliana. Development 2011; 138: 2999-3009.

[100] Liu N, Wu S, Van Houten J. et al. Down-regulation of AUXIN RESPONSE FACTORS 6 and 8 by microRNA 167 leads to floral development defects and female sterility in tomato. J Exp Bot 2014; 65: 2507-20.

[101] Cheng Z, Song X, Liu X. et al. SPATULA and ALCATRAZ confer female sterility and fruit cavity via mediating pistil development in cucumber. Plant Physiol 2022; 189: 1553-69.

[102] Schneitz K, Hulskamp M, Kopczak SD. et al. Dissection of sexual organ ontogenesis: a genetic analysis of ovule development in Arabidopsis thaliana. Development 1997; 124: 1367-76.

[103] Schneitz K, Hulskamp M, Pruitt RE . Wild-type ovule development in Arabidopsis thaliana: a light-microscope study of cleared whole-mount tissue . Plant J 1995; 7: 731-49.

[104] Yadegari R, Drews GN . Female gametophyte development. Plant Cell 2004; 16: S133-41.

[105] Liu XF, Hao N, Li HY. et al. PINOID is required for lateral organ morphogenesis and ovule development in cucumber. J Exp Bot 2019; 70: 5715-30.

[106] Otsuga D, DeGuzman B, Prigge MJ. et al. REVOLUTA regulates meristem initiation at lateral positions. Plant J 2001; 25: 223-36.

[107] Barro-Trastoy D, Carrera E, Banos J. et al. Regulation of ovule initiation by gibberellins and brassinosteroids in tomato and Arabidopsis: two plant species, two molecular mechanisms . Plant J 2020; 102: 1026-41.

[108] Gomez MD, Barro-Trastoy D, Escoms E. et al. Gibberellins negatively modulate ovule number in plants. Development 2018; 145- 55.

[109] Sicard A, Petit J, Mouras A et al. Meristem activity during flower and ovule development in tomato is controlled by the mini zinc finger gene INHIBITOR OF MERISTEM ACTIVITY. Plant J 2008; 55: 415-27.

[110] Takisawa R, Nakazaki T, Nunome T. et al. The parthenocarpic gene Pat-k is generated by a natural mutation of SlAGL6 affecting fruit development in tomato (Solanum lycopersicum L.). BMC Plant Biol 2018; 18: 72.

[111] Pinyopich A, Ditta GS, Savidge B. et al. Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 2003; 424: 85-8.

[112] Ocarez N, Mejia N . Suppression of the D-class MADS-box AGL11 gene triggers seedlessness in fleshy fruits. Plant Cell Rep 2016; 35: 239-54.

[113] Schubert R, Dobritzsch S, Gruber C. et al. Tomato MYB21 acts in ovules to mediate jasmonate-regulated fertility. Plant Cell 2019; 31: 1043-62.

[114] da Silva EM, Silva GFFE, Bidoia DB. et al. microRNA159-targeted SIGAMYB transcription factors are required for fruit set in tomato. Plant J 2017; 92: 95-109.

[115] Clepet C, Devani RS, Boumlik R. et al. The miR166-SlHB15A regulatory module controls ovule development and parthenocarpic fruit set under adverse temperatures in tomato. Mol Plant 2021; 14: 1185-98.

[116] Mecchia MA, Santos-Fernandez G, Duss NN. et al. RALF4/19 peptides interact with LRX proteins to control pollen tube growth in Arabidopsis. Science 2017; 358: 1600-3.

[117] Ge ZX, Bergonci T, Zhao YL. et al. Arabidopsis pollen tube integrity and sperm release are regulated by RALF-mediated signaling . Science 2017; 358: 1596-600.

[118] Ge XC, Chang F, Ma H . Signaling and transcriptional control of reproductive development in Arabidopsis. Curr Biol 2010; 20: R988-97.

[119] Chevalier E, Loubert-Hudon A, Matton DP . ScRALF3, a secreted RALF-like peptide involved in cell-cell communication between the sporophyte and the female gametophyte in a solanaceous species. Plant J 2013; 73: 1019-33.

[120] Loubert-Hudon A, Mazin BD, Chevalier É. et al. The ScRALF3 secreted peptide is involved in sporophyte to gametophyte signalling and affects pollen mitosis I. Plant Biol 2020; 22: 13-20.

[121] Tian S, Ge J, Ai G. et al. A 2.09 Mb fragment translocation on chromosome 6 causes abnormalities during meiosis and leads to less seed watermelon. Hortic Res 2021; 8: 256.

[122] Oka H, Watanabe T, Nishiyama I . Reciprocal translocation as a new approach to breeding seedless watermelon. Canadian J Genet Cytol 1967; 9: 482- 9.

[123] Martin G, Carreel F, Coriton O. et al. Evolution of the banana genome (Musa acuminata) is impacted by large chromosomal translocations . Mol Biol Evol 2017; 34: 2140-52.

[124] Schijlen EG, de Vos CH, Martens S. et al. RNA interference silencing of chalcone synthase, the first step in the flavonoid biosynthesis pathway, leads to parthenocarpic tomato fruits. Plant Physiol 2007; 144: 1520-30.

[125] Deslous P, Bournonville C, Decros G. et al. Overproduction of ascorbic acid impairs pollen fertility in tomato. J Exp Bot 2021; 72: 3091-107.

[126] Nieves-Cordones M, Lara A, Silva M. et al. Root high-affinity K(+) and Cs(+) uptake and plant fertility in tomato plants are dependent on the activity of the high-affinity K(+) transporter SlHAK5. Plant Cell Environ 2020; 43: 1707-21.

[127] Pechar GS, Donaire L, Gosalvez B. et al. Editing melon eIF4E associates with virus resistance and male sterility. Plant Biotechnol J 2022; 20: 2006-22.

[128] Jung YJ, Kim DH, Lee HJ. et al. Knockout of SlMS10 gene (Solyc02g079810) encoding bHLH transcription factor using CRISPR/Cas9 system confers male sterility phenotype in tomato. Plants (Basel) 2020; 9: 9.

[129] Du M, Zhou K, Liu Y. et al. A biotechnology-based male-sterility system for hybrid seed production in tomato. Plant J 2020; 102: 1090-100.

[130] He YB, Zhang T, Sun H. et al. A reporter for noninvasively monitoring gene expression and plant transformation. Hortic Res 2020; 7: 152.

[131] He Y, Zhu M, Wang L. et al. Programmed self-elimination of the CRISPR/Cas9 construct greatly accelerates the isolation of edited and transgene-free rice plants. Mol Plant 2018; 11: 1210-3.

[132] He Y, Zhao Y . Technological breakthroughs in generating transgene-free and genetically stable CRISPR-edited plants. aBIOTECH 2020; 1: 88-96.

[133] Wang BK, Li N, Wang J. et al. iTRAQ-based proteomics reveals that the tomato ms10(35) gene causes male sterility through compromising fat acid metabolism. Proteomics 2020; 20: 1900213-24.

[134] Huang SY, Wang BK, Li N. et al. iTRAQ and PRM-based proteomics analysis for the identification of differentially abundant proteins related to male sterility in ms-7 mutant tomato (Solanum lycoperscium) plants . J Proteome 2022; 261: 104557.

[135] Kim JS, Ezura K, Lee J. et al. Genetic engineering of parthenocarpic tomato plants using transient SlIAA9 knockdown by novel tissue-specific promoters. Sci Rep 2019; 9: 18871.

[136] Feder A, Jensen S, Wang AQ. et al. Tomato fruit as a model for tissue-specific gene silencing in crop plants. Hortic Res 2020; 7: 142.

[137] Wan X, Wu S, Li X . Breeding with dominant genic male-sterility genes to boost crop grain yield in the post-heterosis utilization era. Mol Plant 2021; 14: 531-4.

[138] Fang ZY, Sun PT, Liu YM. et al. A male sterile line with dominant gene (Ms) in cabbage (Brassica oleracea var. capitata) and its utilization for hybrid seed production . Euphytica 1997; 97: 265-8.

[139] Liang J, Ma Y, Wu J. et al. Map-based cloning of the dominant genic male sterile Ms-cd1 gene in cabbage (Brassica oleracea). Theor Appl Genet 2017; 130: 71-9.

[140] Han FQ, Zhang XL, Yuan KW. et al. A user-friendly KASP molecular marker developed for the DGMS-based breeding system in Brassica oleracea species . Mol Breed 2019; 39: 90.

[141] Deng Y, Liu S, Zhang Y. et al. A telomere-to-telomere gap-free reference genome of watermelon and its mutation library provide important resources for gene discovery and breeding. Mol Plant 2022; 15: 1268-84.

[142] Wan XY, Wu SW, Li ZW. et al. Maize genic male-sterility genes and their applications in hybrid breeding: progress and perspectives. Mol Plant 2019; 12: 321-42.

[143] Feng PC, Qi Y, Chiu T. et al. Improving hybrid seed production in corn with glyphosate-mediated male sterility. Pest Manag Sci 2014; 70: 212-8.

[144] Rao GS, Rao TAK, KV. Development of an inducible male-sterility system in rice through pollen-specific expression of L-ornithinase (argE) gene of E. coli. Plant Sci 2017; 256: 139-47.

[145] Kriete G, Niehaus K, Perlick AM. et al. Male sterility in transgenic tobacco plants induced by tapetum-specific deacetylation of the externally applied non-toxic compound N-acetyl-L-phosphinothricin. Plant J 1996; 9: 809-18.

[146] Hawkes T, Pline-Srnic W, Dale R et al. D-glufosinate as a male sterility agent for hybrid seed production. Plant Biotechnol J 2011; 9: 301-14.

[147] Hochholdinger F, Baldauf JA . Heterosis in plants. Curr Biol 2018; 28: R1089-92.

[148] He H. Analyses of plant character in Hubei photoperiod-sensitive genie male-sterile rice (HPGMR) under different light and temperature conditions. Hybrid Rice 1989; 5: 1-9.

[149] Xu FY, Yang XD, Zhao N. et al. Exploiting sterility and fertility variation in cytoplasmic male sterile vegetable crops. Hortic Res 2022; 9: uhab039.

[150] Wei XC, Lv YY, Zhao YY. et al. Comparative transcriptome analysis in Chinese cabbage (Brassica rapa ssp. pekinesis) for DEGs of Ogura-, Polima-CMS and their shared maintainer . Physiol Mol Biol Plants 2020; 26: 719-31.

[151] Wang CD, Lezhneva L, Arnal N. et al. The radish Ogura fertility restorer impedes translation elongation along its cognate CMS-causing mRNA. Proc Natl Acad Sci USA 2021; 118: 1-9.

[152] Desloire S, Gherbi H, Laloui W. et al. Identification of the fertility restoration locus, Rfo, in radish, as a member of the pentatricopeptide-repeat protein family. EMBO Rep 2003; 4: 588-94.

[153] Yang JH, Liu XY, Yang XD. et al. Mitochondrially-targeted expression of a cytoplasmic male sterility-associated orf220 gene causes male sterility in Brassica juncea. BMC Plant Biol 2010; 10: 231.

[154] Zhao N, Xu XY, Wamboldt Y. et al. MutS HOMOLOG1 silencing mediates ORF220 substoichiometric shifting and causes male sterility in Brassica juncea. J Exp Bot 2016; 67: 435-44.

[155] Kuwabara K, Arimura SI, Shirasawa K. et al. orf137 triggers cytoplasmic male sterility in tomato. Plant Physiol 2022; 189: 465-8.

[156] Lu Y, Zhu HL . The regulation of nutrient and flavor metabolism in tomato fruit. Vegetable Res 2022; 2: 5.

[157] Wang MF, Yang SL, Sun L. et al. A CBL4-CIPK6 module confers salt tolerance in cucumber. Vegetable Res 2022; 2: 7.