Advances in plant male sterility for hybrid seed production: an overview of conditional nuclear male sterile lines and biotechnology-based male sterile systems
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články, přehledy
PubMed
39974728
PubMed Central
PMC11835859
DOI
10.3389/fpls.2025.1540693
Knihovny.cz E-zdroje
- Klíčová slova
- biotechnology-based male sterile (BBMS) systems, environment-sensitive genic male sterility (EGMS), genic male sterility (GMS), long non-coding RNAs (lncRNAs), phased secondary small interfering RNAs (phasiRNAs),
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
Male sterility forms the foundation of hybrid seed production technology in field crops. A variety of genetically controlled male sterility/fertility systems starting with cytoplasmic male sterility (CMS), genic male sterility (GMS) including conditional male sterility and transgenic-based male sterility have been developed and deployed for heterosis breeding over the past century. Here we review environment-sensitive genic male sterility (EGMS) and biotechnology-based male sterility systems and describe the underlying molecular mechanisms. Advances in crop genomics and discovery of a large number of nuclear genes governing anther/pollen development, which are shared across species, are helping design diverse types of male sterile lines suitable for different crop species and situations. In particular, gene editing offers quick and easy route to develop novel male sterility systems for hybrid seed production. We discuss the advantages and challenges of biotechnology-based male sterility systems and present alternative strategies to address concerns of transgenics. Finally, we propose development of functional male sterility systems based on pollen competition as the future area that holds great promise for heterosis breeding.
Bamboo Industry Institute Zhejiang A and F University Lin'an Hangzhou Zhejiang China
Department of Biotechnology ICAR Indian Institute of Rice Research Rajendranagar Hyderabad India
Department of Pharmacy Mangalayatan University Jabalpur Jabalpur Madhya Pradesh India
Faculty of Forestry and Wood Sciences Czech University of Life Sciences Prague Prague Czechia
ICAR National Institute for Plant Biotechnology New Delhi India
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Aarts M., Keijzer C. J., Stiekema W. J., Pereira A. (1995). Molecular characterization of the CER1 gene of arabidopsis involved in epicuticular wax biosynthesis and pollen fertility. Plant Cell 7, 2115–2127. doi: 10.1105/tpc.7.12.2115 PubMed DOI PMC
An X., Ma B., Duan M., Dong Z., Liu R., Yuan D., et al. . (2020). Molecular regulation of ZmMs7 required for maize male fertility and development of a dominant male-sterility system in multiple species. Proc. Natl. Acad. Sci. U.S.A. 117, 23499–23509. doi: 10.1073/pnas.2010255117 PubMed DOI PMC
Anjani K. (2005). Stabilization and maintenance of male sterility percent in recessive genetic male sterile line. s of safflower (Carthamus tinctorius L.). Indian J. Genet. Plant Breed. 65, 141–142.
Ariizumi T., Hatakeyama K., Hinata K., Inatsugi R., Nishida I., Sato S., et al. . (2004). Disruption of the novel plant protein NEF1 affects lipid accumulation in the plastids of the tapetum and exine formation of pollen, resulting in male sterility in Arabidopsis thaliana . Plant J. 39, 170–181. doi: 10.1111/j.1365-313X.2004.02118.x PubMed DOI
Besnard G., Khadari B., Villemur P., Bervillé A. (2000). Cytoplasmic male sterility in the olive (Olea europaea L.). Theor. Appl. Genet. 100, 1018–1024. doi: 10.1007/s001220051383 DOI
Blackmore S., Wortley A. H., Skvarla J. J., Rowley J. R. (2007). Pollen wall development in flowering plants. New Phytol. 174, 483–498. doi: 10.1111/j.1469-8137.2007.02060.x PubMed DOI
Budar F., Pelletier G. (2001). Male sterility in plants: occurrence, determinism, significance and use. C. R. Acad. Sci. III. 324, 543–550. doi: 10.1016/S0764-4469(01)01324-5 PubMed DOI
Cai C.-F., Zhu J., Lou Y., Guo Z.-L., Xiong S.-X., Wang K., et al. . (2015). The functional analysis of OsTDF1 reveals a conserved genetic pathway for tapetal development between rice and Arabidopsis . Sci. Bull. 60, 1073–1082. doi: 10.1007/s11434-015-0810-3 DOI
Chamola R., Balyan H. S., Bhat S. R. (2013). Effect of alien cytoplasm and fertility restorer genes on agronomic and physiological traits of Brassica juncea (L.) C zern. Plant Breed. 132, 681–687. doi: 10.1111/pbr.2013.132.issue-6 DOI
Chang Z., Chen Z., Wang N., Xie G., Lu J., Yan W., et al. . (2016). Construction of a male sterility system for hybrid rice breeding and seed production using a nuclear male sterility gene. Proc. Natl. Acad. Sci. U.S.A. 113, 14145–14150. doi: 10.1073/pnas.1613792113 PubMed DOI PMC
Chaubal R., Anderson J. R., Trimnell M. R., Fox T. W., Albertsen M. C., Bedinger P. (2003). The transformation of anthers in the msca1 mutant of maize. Planta 216, 778–788. doi: 10.1007/s00425-002-0929-8 PubMed DOI
Chen L., Liu Y. G. (2014). Male sterility and fertility restoration in crops. Annu. Rev. Plant Biol. 65, 579–606. doi: 10.1146/annurev-arplant-050213-040119 PubMed DOI
Chen X. D., Sun D. F., Rong D. F., Peng J. H., Li C. D. (2011. b). A recessive gene controlling male sterility sensitive to short daylength/low temperature in wheat (Triticum aestivum L.). J. Zhejiang Univ. Sci. B. 12, 943–950. doi: 10.1631/jzus.B1000371 PubMed DOI PMC
Chen Z., Wu J., Deng X. W., Tang X. (2023). Establishment and advances of third-generation hybrid rice technology: a review. Rice 16, 56. doi: 10.1186/s12284-023-00670-z PubMed DOI PMC
Chen W., Yu X.-H., Zhang K., Shi J., De Oliveira S., Schreiber L., et al. . (2011. a). Male Sterile2 encodes a plastid-localized fatty acyl carrier protein reductase required for pollen exine development in Arabidopsis. Plant Physiol. 157, 842–853. doi: 10.1104/pp.111.181693 PubMed DOI PMC
Chen H., Zhang Z., Ni E., Lin J., Peng G., Huang J., et al. . (2020). HMS1 interacts with HMS1I to regulate very-long-chain fatty acid biosynthesis and the humidity-sensitive genic male sterility in rice (Oryza sativa). New Phytol. 225, 2077–2093. doi: 10.1111/nph.v225.5 PubMed DOI
Chen X., Zhang H., Sun H., Luo H., Zhao L., Dong Z., et al. . (2017). IRREGULAR POLLEN EXINE1 Is a novel factor in anther cuticle and pollen exine formation. Plant Physiol. 173, 307–325. doi: 10.1104/pp.16.00629 PubMed DOI PMC
Chen R., Zhao X., Shao Z., Wei Z., Wang Y., Zhu L., et al. . (2007). Rice UDP-glucose pyrophosphorylase1 is essential for pollen callose deposition and its cosuppression results in a new type of thermosensitive genic male sterility. Plant Cell 19, 847–861. doi: 10.1105/tpc.106.044123 PubMed DOI PMC
Cheng X.-Q., Zhang X.-Y., Xue F., Zhu S.-H., Li Y.-J., Zhu Q.-H., et al. . (2020). Characterization and transcriptome analysis of a dominant genic male sterile cotton mutant. BMC Plant Biol. 20, 1–14. doi: 10.1186/s12870-020-02522-0 PubMed DOI PMC
Chueasiri C., Chunthong K., Pitnjam K., Chakhonkaen S., Sangarwut N., Sangsawang K., et al. . (2014). Rice ORMDL controls sphingolipid homeostasis affecting fertility resulting from abnormal pollen development. PloS One 9, e106386. doi: 10.1371/journal.pone.0106386 PubMed DOI PMC
Cole R. A., Synek L., Zarsky V., Fowler J. E. (2005). SEC8, a subunit of the putative Arabidopsis exocyst complex, facilitates pollen germination and competitive pollen tube growth. Plant Physiol. 138, 2005–2018. doi: 10.1104/pp.105.062273 PubMed DOI PMC
Colombo N., Galmarini C. R. (2017). The use of genetic, manual and chemical methods to control pollination in vegetable hybrid seed production: a review. Plant Breed. 136, 287–299. doi: 10.1111/pbr.2017.136.issue-3 DOI
Deng Y., Srivastava R., Quilichini T. D., Dong H., Bao Y., Horner H. T., et al. . (2016). IRE1, a component of the unfolded protein response signaling pathway, protects pollen development in Arabidopsis from heat stress. Plant J. 88, 193–204. doi: 10.1111/tpj.2016.88.issue-2 PubMed DOI
De Souza P. F., Dos Santos C. M. R., Ree J., Guerra M. P., Pescador R. (2020). Male sterility in Bambusa tuldoides Munro. Protoplasma 257, 911–920. doi: 10.1007/s00709-019-01479-8 PubMed DOI
Ding J., Lu Q., Ouyang Y., Mao H., Zhang P., Yao J., et al. . (2012. a). A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice. Proc. Natl. Acad. Sci. U.S.A. 109, 2654–2659. doi: 10.1073/pnas.1121374109 PubMed DOI PMC
Ding J., Shen J., Mao H., Xie W., Li X., Zhang Q. (2012. b). RNA-directed DNA methylation is involved in regulating photoperiod-sensitive male sterility in rice. Mol. Plant 5, 1210–1216. doi: 10.1093/mp/sss095 PubMed DOI
Dong X., Hong Z., Sivaramakrishnan M., Mahfouz M., Verma D. P. (2005). Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis. Plant J. 42, 315–328. doi: 10.1111/j.1365-313X.2005.02379.x PubMed DOI
Dong X., Nou I. S., Yi H., Hur Y. (2015). Suppression of ASKβ (AtSK32), a Clade III Arabidopsis GSK3, leads to the pollen defect during late pollen development. Mol. Cells 38, 506–517. doi: 10.14348/molcells.2015.2323 PubMed DOI PMC
Dong N., Subudhi P., Luong P., Quang V., Quy T., Zheng H., et al. . (2000). Molecular mapping of a rice gene conditioning thermosensitive genic male sterility using AFLP, RFLP and SSR techniques. Theor. Appl. Genet. 100, 727–734. doi: 10.1007/s001220051345 DOI
Du M., Zhou K., Liu Y., Deng L., Zhang X., Lin L., et al. . (2020). A biotechnology-based male-sterility system for hybrid seed production in tomato. Plant J. 102, 1090–1100. doi: 10.1111/tpj.v102.5 PubMed DOI PMC
Enns L. C., Kanaoka M. M., Torii K. U., Comai L., Okada K., Cleland R. E. (2005). Two callose synthases, GSL1 and GSL5, play an essential and redundant role in plant and pollen development and in fertility. Plant Mol. Biol. 58, 333–349. doi: 10.1007/s11103-005-4526-7 PubMed DOI
Fan Y., Yang J., Mathioni S. M., Yu J., Shen J., Yang X., et al. . (2016). PMS1T, producing phased small-interfering RNAs, regulates photoperiod-sensitive male sterility in rice. Proc. Natl. Acad. Sci. U.S.A. 113, 15144–15149. doi: 10.1073/pnas.1619159114 PubMed DOI PMC
Fan Y., Zhang Q. (2018). Genetic and molecular characterization of photoperiod and thermo-sensitive male sterility in rice. Plant Reprod. 31, 3–14. doi: 10.1007/s00497-017-0310-5 PubMed DOI
Fang C., Li L., He R., Wang D., Wang M., Hu Q., et al. . (2019). Identification of S23 causing both interspecific hybrid male sterility and environment-conditioned male sterility in rice. Rice 12, 10. doi: 10.1186/s12284-019-0271-4 PubMed DOI PMC
Fernandez-Gomez J., Talle B., Wilson Z. A. (2020). Increased expression of the MALE STERILITY1 transcription factor gene results in temperature-sensitive male sterility in barley. J. Exp. Bot. 71, 6328–6339. doi: 10.1093/jxb/eraa382 PubMed DOI PMC
Fernandez Gomez J., Wilson Z. A. (2014). A barley PHD finger transcription factor that confers male sterility by affecting tapetal development. Plant Biotechnol. J. 12, 765–777. doi: 10.1111/pbi.12181 PubMed DOI
Fiebig A., Mayfield J. A., Miley N. L., Chau S., Fischer R. L., Preuss D. (2000). Alterations in CER6, a gene identical to CUT1, differentially affect long-chain lipid content on the surface of pollen and stems. Plant Cell 12, 2001–2008. doi: 10.1105/tpc.12.10.2001 PubMed DOI PMC
Fu Z., Yu J., Cheng X., Zong X., Xu J., Chen M., et al. . (2014). The rice basic helix-loop-helix transcription factor TDR INTERACTING PROTEIN2 is a central switch in early anther development. Plant Cell 26, 1512–1524. doi: 10.1105/tpc.114.123745 PubMed DOI PMC
Gao C. (2021). Genome engineering for crop improvement and future agriculture. Cell 184, 1621–1635. doi: 10.1016/j.cell.2021.01.005 PubMed DOI
Gautam R., Shukla P., Kirti P. B. (2023). Male sterility in plants: an overview of advancements from natural CMS to genetically manipulated systems for hybrid seed production. Theor. Appl. Genet. 136, 195. doi: 10.1007/s00122-023-04444-5 PubMed DOI
Guo R. X., Sun D. F., Tan Z. B., Rong D. F., Li C. D. (2006). Two recessive genes controlling thermophotoperiod-sensitive male sterility in wheat. Theor. Appl. Genet. 112, 1271–1276. doi: 10.1007/s00122-006-0228-z PubMed DOI
Hamilton E. S., Haswell E. S. (2017). The tension-sensitive ion transport activity of MSL8 is critical for its function in pollen hydration and germination. Plant Cell Physiol. 58, 1222–1237. doi: 10.1093/pcp/pcw230 PubMed DOI
Han Y., Jiang S. Z., Zhong X., Chen X., Ma C. K., Yang Y. M., et al. . (2023). Low temperature compensates for defective tapetum initiation to restore the fertility of the novel TGMS line ostms15 . Plant Biotechnol. J. 21, 1659–1670. doi: 10.1111/pbi.14066 PubMed DOI PMC
Han Y., Zhou S.-D., Fan J.-J., Zhou L., Shi Q.-S., Zhang Y.-F., et al. . (2021). OsMS188 is a key regulator of tapetum development and sporopollenin synthesis in rice. Rice 14, 1–14. doi: 10.1186/s12284-020-00451-y PubMed DOI PMC
Haslam T. M., Haslam R., Thoraval D., Pascal S., Delude C., Domergue F., et al. . (2015). ECERIFERUM2-LIKE proteins have unique biochemical and physiological functions in very-long-chain fatty acid elongation. Plant Physiol. 167, 682–692. doi: 10.1104/pp.114.253195 PubMed DOI PMC
Hong L., Tang D., Shen Y., Hu Q., Wang K., Li M., et al. . (2012. a). MIL 2 (MICROSPORELESS 2) regulates early cell differentiation in the rice anther. New Phytol. 196, 402–413. doi: 10.1111/j.1469-8137.2012.04270.x PubMed DOI
Hong L., Tang D., Zhu K., Wang K., Li M., Cheng Z. (2012. b). Somatic and reproductive cell development in rice anther is regulated by a putative glutaredoxin. Plant Cell 24, 577–588. doi: 10.1105/tpc.111.093740 PubMed DOI PMC
Hou J., Fan W., Ma R., Li B., Yuan Z., Huang W., et al. . (2022). MALE STERILITY 3 encodes a plant homeodomain-finger protein for male fertility in soybean. J. Integr. Plant Biol. 64, 1076–1086. doi: 10.1111/jipb.13242 PubMed DOI PMC
Hu H., Scheben A., Wang J., Li F., Li C., Edwards D., et al. . (2024). Unravelling inversions: Technological advances, challenges, and potential impact on crop breeding. Plant Biotechnol. J. 22, 544–554. doi: 10.1111/pbi.14224 PubMed DOI PMC
Huang W., Li Y., Du Y., Pan L., Huang Y., Liu H., et al. . (2022). Maize cytosolic invertase INVAN6 ensures faithful meiotic progression under heat stress. New Phytol. 236, 2172–2188. doi: 10.1111/nph.v236.6 PubMed DOI
Huang T.-Y., Wang Z., Hu Y.-G., Shi S.-P., Peng T., Chu X.-D., et al. . (2008). Genetic analysis and primary mapping of pms4, a photoperiod-sensitive genic male sterility gene in rice (Oryza sativa). Rice Sci. 15, 153–156. doi: 10.1016/S1672-6308(08)60035-9 DOI
Huang H., Wang C., Tian H., Sun Y., Xie D., Song S. (2014). Amino acid substitutions of GLY98, LEU245 and GLU543 in COI1 distinctively affect jasmonate-regulated male fertility in Arabidopsis . Sci. China Life Sci. 57, 145–154. doi: 10.1007/s11427-013-4590-1 PubMed DOI
Hussain A. J., Ali J., Siddiq E. A., Gupta V. S., Reddy U. K., Ranjekar P. K. (2011). Mapping of tms8 gene for temperature-sensitive genic male sterility (TGMS) in rice (Oryza sativa L.). Plant Breed. 131, 42–47. doi: 10.1111/j.1439-0523.2011.01897.x DOI
Ishiguro S., Nishimori Y., Yamada M., Saito H., Suzuki T., Nakagawa T., et al. . (2010). The Arabidopsis FLAKY POLLEN1 gene encodes a 3-hydroxy-3-methylglutaryl-coenzyme A synthase required for development of tapetum-specific organelles and fertility of pollen grains. Plant Cell Physiol. 51, 896–911. doi: 10.1093/pcp/pcq068 PubMed DOI
Ito T., Nagata N., Yoshiba Y., Ohme-Takagi M., Ma H., Shinozaki K. (2007). Arabidopsis MALE STERILITY1 encodes a PHD-type transcription factor and regulates pollen and tapetum development. Plant Cell 19, 3549–3562. doi: 10.1105/tpc.107.054536 PubMed DOI PMC
Ito T., Shinozaki K. (2002). The MALE STERILITY1 gene of Arabidopsis, encoding a nuclear protein with a PHD-finger motif, is expressed in tapetal cells and is required for pollen maturation. Plant Cell Physiol. 43, 1285–1292. doi: 10.1093/pcp/pcf154 PubMed DOI
Iwata Y., Fedoroff N. V., Koizumi N. (2008). Arabidopsis bZIP60 Is a proteolysis-activated transcription factor involved in the endoplasmic reticulum stress response. Plant Cell 20, 3107–3121. doi: 10.1105/tpc.108.061002 PubMed DOI PMC
Jagannath A., Arumugam N., Gupta V., Pradhan A., Burma P. K., Pental D. (2002). Development of transgenic barstar lines and identification of a male sterile (barnase)/restorer (barstar) combination for heterosis breeding in Indian oilseed mustard (Brassica juncea). Curr. Sci. 82, 46–52.
Jessen D., Olbrich A., Knufer J., Kruger A., Hoppert M., Polle A., et al. . (2011). Combined activity of LACS1 and LACS4 is required for proper pollen coat formation in Arabidopsis. Plant J. 68, 715–726. doi: 10.1111/j.1365-313X.2011.04722.x PubMed DOI
Jia J., Zhang D., Li C., Qu X., Wang S., Chamarerk V., et al. . (2001). Molecular mapping of the reverse thermo-sensitive genic male-sterile gene (rtms1) in rice. Theor. Appl. Genet. 103, 607–612. doi: 10.1007/PL00002916 DOI
Jiang S. Y., Cai M., Ramachandran S. (2007). ORYZA SATIVA MYOSIN XI B controls pollen development by photoperiod-sensitive protein localizations. Dev. Biol. 304, 579–592. doi: 10.1016/j.ydbio.2007.01.008 PubMed DOI
Jin-Long N. I., De-Zheng W., Da-Hu N. I., Feng-Shun S., Jian-Bo Y., Da-Nian Y. (2022). Characterization and fine mapping of RTMS10, a semi-dominant reverse thermo-sensitive genic male sterile locus in rice. J. Integr. Agric. 21, 316–325. doi: 10.1016/S2095-3119(20)63563-8 DOI
Jung K.-H., Han M.-J., Lee Y.-S., Kim Y.-W., Hwang I., Kim M.-J., et al. . (2005). Rice Undeveloped Tapetum1 is a major regulator of early tapetum development. Plant Cell 17, 2705–2722. doi: 10.1105/tpc.105.034090 PubMed DOI PMC
Kim Y. J., Zhang D. (2018). Molecular control of male fertility for crop hybrid breeding. Trends Plant Sci. 23, 53–65. doi: 10.1016/j.tplants.2017.10.001 PubMed DOI
Koornneef M., Hanhart C., Thiel F. (1989). A genetic and phenotypic description of Eceriferum (cer) mutants in Arabidopsis thaliana . J. Hered. 80, 118–122. doi: 10.1093/oxfordjournals.jhered.a110808 DOI
Kriete G., Niehaus K., Perlick A., Pühler A., Broer I. (1996). Male sterility in transgenic tobacco plants induced by tapetum-specific deacetylation of the externally applied non-toxic compound N-acetyl-l-phosphinothricin. Plant J. 9, 809–818. doi: 10.1046/j.1365-313X.1996.9060809.x PubMed DOI
Kumar P., Vasupalli N., Srinivasan R., Bhat S. R. (2012). An evolutionarily conserved mitochondrial orf108 is associated with cytoplasmic male sterility in different alloplasmic lines of Brassica juncea and induces male sterility in transgenic Arabidopsis thaliana . J. Exp. Bot. 63, 2921–2932. doi: 10.1093/jxb/err459 PubMed DOI
Lee D. S., Chen L. J., Suh H. S. (2005). Genetic characterization and fine mapping of a novel thermo-sensitive genic male-sterile gene tms6 in rice (Oryza sativa L.). Theor. Appl. Genet. 111, 1271–1277. doi: 10.1007/s00122-005-0044-x PubMed DOI
Lee S. K., Kim H., Cho J. I., Nguyen C. D., Moon S., Park J. E., et al. . (2020). Deficiency of rice hexokinase HXK5 impairs synthesis and utilization of starch in pollen grains and causes male sterility. J. Exp. Bot. 71, 116–125. doi: 10.1093/jxb/erz436 PubMed DOI
Lee Y. S., Maple R., Durr J., Dawson A., Tamim S., Del Genio C., et al. . (2021). A transposon surveillance mechanism that safeguards plant male fertility during stress. Nat. Plants 7, 34–41. doi: 10.1038/s41477-020-00818-5 PubMed DOI
Li H., Li S., Abdelkhalik S., Shahzad A., Gu J., Yang Z., et al. . (2020). Development of thermo-photo sensitive genic male sterile lines in wheat using doubled haploid breeding. BMC Plant Biol. 20, 246. doi: 10.1186/s12870-020-02458-5 PubMed DOI PMC
Li H., Yuan Z., Vizcay-Barrena G., Yang C., Liang W., Zong J., et al. . (2011). PERSISTENT TAPETAL CELL1 encodes a PHD-finger protein that is required for tapetal cell death and pollen development in rice. Plant Physiol. 156, 615–630. doi: 10.1104/pp.111.175760 PubMed DOI PMC
Li J., Zhang H., Si X., Tian Y., Chen K., Liu J., et al. . (2017). Generation of thermosensitive male-sterile maize by targeted knockout of the ZmTMS5 gene. J. Genet. Genom. 44, 465–468. doi: 10.1016/j.jgg.2017.02.002 PubMed DOI
Li W.-Q., Zhang X.-Q., Xia C., Deng Y., Ye D. (2010). MALE GAMETOPHYTE DEFECTIVE 1, encoding the FAd subunit of mitochondrial F1F0-ATP synthase, is essential for pollen formation in Arabidopsis thaliana . Plant Cell Physiol. 51, 923–935. doi: 10.1093/pcp/pcq066 PubMed DOI
Li Y. F., Zhao C. P., Zhang F. T., Sun H., Sun D. F. (2006). Fertility alteration in the photo-thermo-sensitive male sterile line BS20 of wheat (Triticum aestivum L.). Euphytica 151, 207–213. doi: 10.1007/s10681-006-9141-4 DOI
Liang-Bi C., Guang-Qia Z., Yu-Xiang H. (1994). Effects of temperature and photoperiod on fertility and physiological activities of rice Annong S-1 and Hengnong S-1. J. Integr. Plant Biol. 36, 119.
Lin S., Liu Z., Sun S., Xue F., Li H., Tursun A., et al. . (2023). Rice HEAT SHOCK PROTEIN60-3B maintains male fertility under high temperature by starch granule biogenesis. Plant Physiol. 192, 2301–2317. doi: 10.1093/plphys/kiad136 PubMed DOI PMC
Lin X., Xie H., Xi Z., Hu Y., Zhao G., Duan L., et al. . (2009). Identification and mapping of a thermo-sensitive genic self-incompatibility gene in maize. Genes Genom. 31, 227–234. doi: 10.1007/BF03191194 DOI
Liping Z., Changping Z., Fuhua S., Fengting Z., Zhijie Y. (2009). The mixed genetic analysis of photoperiod-temperature sensitive male sterility of BS210 in wheat. Zuowu Xuebao 33, 1553–1557.
Liu Z., Bao W., Liang W., Yin J., Zhang D. (2010. b). Identification of gamyb-4 and analysis of the regulatory role of GAMYB in rice anther development. J. Integr. Plant Biol. 52, 670–678. doi: 10.1111/j.1744-7909.2010.00959.x PubMed DOI
Liu Y. J., Li D., Gong J., Wang Y. B., Chen Z. B., Pang B. S., et al. . (2021). Comparative transcriptome and DNA methylation analysis in temperature-sensitive genic male sterile wheat BS366. BMC Genom. 22, 911. doi: 10.1186/s12864-021-08163-3 PubMed DOI PMC
Liu X., Li X., Zhang X., Wang S. (2010. a). Genetic analysis and mapping of a thermosensitive genic male sterility gene, tms6(t), in rice (Oryza sativa L.). Genome 53, 119–124. doi: 10.1139/G09-092 PubMed DOI
Liu D., Shi J., Liang W., Zhang D. (2023). Molecular mechanisms underlying plant environment-sensitive genic male sterility and fertility restoration. Seed Biol. 2, 13. doi: 10.48130/SeedBio-2023-0013 DOI
Lu P., Chai M., Yang J., Ning G., Wang G., Ma H. (2014). The Arabidopsis CALLOSE DEFECTIVE MICROSPORE1 gene is required for male fertility through regulating callose metabolism during microsporogenesis. Plant Physiol. 164, 1893–1904. doi: 10.1104/pp.113.233387 PubMed DOI PMC
Ma X.-D., Wang J.-S., Lu Y.-Q., Li S.-Y., Liu G.-Q., Hou S.-L., et al. . (2012). Characterization of fertility and pollen abortion of sorghum sterile line Ji 130A under different temperature conditions. J. Plant Genet. Res. 13, 212–218.
Ma J., Wei H., Liu J., Song M., Pang C., Wang L., et al. . (2013). Selection and characterization of a novel photoperiod-sensitive male sterile line in upland cotton. J. Integr. Plant Biol. 55, 608–618. doi: 10.1111/jipb.12067 PubMed DOI
Manjappa M., Rangaiah S., Gowda M. (2015). Assessment of heterotic potential of hybrids using a novel partial male sterile mutant (PS 1) in finger millet (Eleusine coracana (L.) Geartn.). Mysore J. Agric. Sci. 49, 266–269.
Marchant D. B., Walbot V. (2022). Anther development—The long road to making pollen. Plant Cell 34, 4677–4695. doi: 10.1093/plcell/koac287 PubMed DOI PMC
Mariani C., Beuckeleer M. D., Truettner J., Leemans J., Goldberg R. B. (1990). Induction of male sterility in plants by a chimaeric ribonuclease gene. nature 347, 737–741. doi: 10.1038/347737a0 DOI
Mariani C., Gossele V., Beuckeleer M. D., Block M. D., Goldberg R. B., Greef W. D., et al. . (1992). A chimaeric ribonuclease-inhibitor gene restores fertility to male sterile plants. Nature 357, 384–387. doi: 10.1038/357384a0 DOI
Mei M., Chen L., Zhang Z., Li Z., Xu C., Zhang Q. (1999). pms3 is the locus causing the original photoperiod-sensitive male sterility mutation of’Nongken 58S’. Sci. China Life Sci. 42, 316–322. doi: 10.1007/BF03183609 PubMed DOI
Millar A. A., Gubler F. (2005). The Arabidopsis GAMYB-like genes, MYB33 and MYB65 , are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell 17, 705–721. doi: 10.1105/tpc.104.027920 PubMed DOI PMC
Mitterreiter M. J., Bosch F. A., Brylok T., Schwenkert S. (2020). The ER luminal C-terminus of AtSec62 is critical for male fertility and plant growth in Arabidopsis thaliana . Plant J. 101, 5–17. doi: 10.1111/tpj.v101.1 PubMed DOI
Moon S., Kim S. R., Zhao G., Yi J., Yoo Y., Jin P., et al. . (2013. b). Rice glycosyltransferase1 encodes a glycosyltransferase essential for pollen wall formation. Plant Physiol. 161, 663–675. doi: 10.1104/pp.112.210948 PubMed DOI PMC
Moon J., Skibbe D., Timofejeva L., Wang C. J. R., Kelliher T., Kremling K., et al. . (2013. a). Regulation of cell divisions and differentiation by MALE STERILITY 32 is required for anther development in maize. Plant J. 76, 592–602. doi: 10.1111/tpj.2013.76.issue-4 PubMed DOI PMC
Mou Z., Wang X., Fu Z., Dai Y., Han C., Ouyang J., et al. . (2002). Silencing of phosphoethanolamine N-methyltransferase results in temperature-sensitive male sterility and salt hypersensitivity in Arabidopsis. Plant Cell 14, 2031–2043. doi: 10.1105/tpc.001701 PubMed DOI PMC
Muratore C., Espen L., Prinsi B. (2021). Nitrogen uptake in plants: The plasma membrane root transport systems from a physiological and proteomic perspective. Plants 10, 681. doi: 10.3390/plants10040681 PubMed DOI PMC
Murmu J., Bush M. J., Delong C., Li S., Xu M., Khan M., et al. . (2010). Arabidopsis basic leucine-zipper transcription factors TGA9 and TGA10 interact with floral glutaredoxins ROXY1 and ROXY2 and are redundantly required for anther development. Plant Physiol. 154, 1492–1504. doi: 10.1104/pp.110.159111 PubMed DOI PMC
Nan G.-L., Zhai J., Arikit S., Morrow D., Fernandes J., Mai L., et al. . (2017). MS23, a master basic helix-loop-helix factor, regulates the specification and development of the tapetum in maize. Development 144, 163–172. doi: 10.1242/dev.140673 PubMed DOI
Ni E., Deng L., Chen H., Lin J., Ruan J., Liu Z., et al. . (2021). OsCER1 regulates humidity-sensitive genic male sterility through very-long-chain (VLC) alkane metabolism of tryphine in rice. Funct. Plant Biol. 48, 461–468. doi: 10.1071/FP20168 PubMed DOI
Nishikawa S., Zinkl G. M., Swanson R. J., Maruyama D., Preuss D. (2005). Callose (beta-1,3 glucan) is essential for Arabidopsis pollen wall patterning, but not tube growth. BMC Plant Biol. 5, 22. doi: 10.1186/1471-2229-5-22 PubMed DOI PMC
Nonomura K.-I., Miyoshi K., Eiguchi M., Suzuki T., Miyao A., Hirochika H., et al. . (2003). The MSP1 gene is necessary to restrict the number of cells entering into male and female sporogenesis and to initiate anther wall formation in rice. Plant Cell 15, 1728–1739. doi: 10.1105/tpc.012401 PubMed DOI PMC
Omidvar V., Mohorianu I., Dalmay T., Zheng Y., Fei Z., Pucci A., et al. . (2017). Transcriptional regulation of male-sterility in 7B-1 male-sterile tomato mutant. PloS One 12, e0170715. doi: 10.1371/journal.pone.0170715 PubMed DOI PMC
Palve S., Santhy V., Bhat S., Laxman S., Rajesh Patil R. P., Khadi B., et al. . (2011). Thermosensitive genetic male Sterility system in cotton (G. arboreum L.). World Cotton Res. Conf. Technol. Prosperity, 62–68.
Pei Q., Liu J., Guo C., Ma X., Liu X., You C., et al. . (2024). Morphological and cytological assessments reveal pollen degradation causes pollen abortion in cotton cytoplasmic male sterility lines. J. Cotton Sci. 7, 26. doi: 10.1186/s42397-024-00189-8 DOI
Peng G., Liu Z., Zhuang C., Zhou H. (2023). Environment-sensitive genic male sterility in rice and other plants. Plant Cell Environ. 46, 1120–1142. doi: 10.1111/pce.14503 PubMed DOI
Peng H. F., Zhang Z. F., Wu B., Chen X. H., Zhang G. Q., Zhang Z. M., et al. . (2008). Molecular mapping of two reverse photoperiod-sensitive genic male sterility genes (rpms1 and rpms2) in rice (Oryza sativa L.). Theor. Appl. Genet. 118, 77–83. doi: 10.1007/s00122-008-0877-1 PubMed DOI
Perez-Prat E., Van Lookeren Campagne M. M. (2002). Hybrid seed production and the challenge of propagating male-sterile plants. Trends Plant Sci. 7, 199–203. doi: 10.1016/S1360-1385(02)02252-5 PubMed DOI
Qi Y., Liu Q., Zhang L., Mao B., Yan D., Jin Q., et al. . (2014). Fine mapping and candidate gene analysis of the novel thermo-sensitive genic male sterility tms9-1 gene in rice. Theor. Appl. Genet. 127, 1173–1182. doi: 10.1007/s00122-014-2289-8 PubMed DOI
Reddy O., Siddiq E., Sarma N., Ali J., Hussain A., Nimmakayala P., et al. . (2000). Genetic analysis of temperature-sensitive male sterilty in rice. Theor. Appl. Genet. 100, 794–801. doi: 10.1007/s001220051354 DOI
Ren W., Si J., Chen L., Fang Z., Zhuang M., Lv H., et al. . (2022). Mechanism and utilization of ogura cytoplasmic male sterility in cruciferae crops. Int. J. Mol. Sci. 23, 9099. doi: 10.3390/ijms23169099 PubMed DOI PMC
Ren L., Zhao T., Zhang L., Du G., Shen Y., Tang D., et al. . (2020). Defective microspore development 1 is required for microspore cell integrity and pollen wall formation in rice. Plant J. 103, 1446–1459. doi: 10.1111/tpj.v103.4 PubMed DOI
Rick C. M., Boynton J. E. (1967). A temperature-sensitive male-sterile mutant of the tomato. Am. J. Bot. 54, 601–611. doi: 10.1002/j.1537-2197.1967.tb10683.x DOI
Ronspies M., Dorn A., Schindele P., Puchta H. (2021). CRISPR-Cas-mediated chromosome engineering for crop improvement and synthetic biology. Nat. Plants 7, 566–573. doi: 10.1038/s41477-021-00910-4 PubMed DOI
Ru Z.-G., Zhang L.-P., Hu T.-Z., Liu H.-Y., Yang Q.-K., Weng M.-L., et al. . (2014). Genetic analysis and chromosome mapping of a thermo-sensitive genic male sterile gene in wheat. Euphytica 201, 321–327. doi: 10.1007/s10681-014-1218-x DOI
Ruiz O. N., Daniell H. (2005). Engineering cytoplasmic male sterility via the chloroplast genome by expression of β-ketothiolase. Plant Physiol. 138, 1232–1246. doi: 10.1104/pp.104.057729 PubMed DOI PMC
Schmidt C., Pacher M., Puchta H. (2019). Efficient induction of heritable inversions in plant genomes using the CRISPR/Cas system. Plant J. 98, 577–589. doi: 10.1111/tpj.2019.98.issue-4 PubMed DOI
Schuhmann P., Engstler C., Klopfer K., Gugel I. L., Abbadi A., Dreyer F., et al. . (2022). Two wrongs make a right: heat stress reversion of a male-sterile Brassica napus line. J. Exp. Bot. 73, 3531–3551. doi: 10.1093/jxb/erac082 PubMed DOI PMC
Shearman J. R., Sangsrakru D., Ruang-Areerate P., Sonthirod C., Uthaipaisanwong P., Yoocha T., et al. . (2014). Assembly and analysis of a male sterile rubber tree mitochondrial genome reveals DNA rearrangement events and a novel transcript. BMC Plant Biol. 14, 1–11. doi: 10.1186/1471-2229-14-45 PubMed DOI PMC
Sheng Z., Wei X., Shao G., Chen M., Song J., Tang S., et al. . (2013). Genetic analysis and fine mapping of tms9, a novel thermosensitive genic male-sterile gene in rice (Oryza sativa L.). Plant Breed. 132, 159–164. doi: 10.1111/pbr.2013.132.issue-2 DOI
Shi Q. S., Lou Y., Shen S. Y., Wang S. H., Zhou L., Wang J. J., et al. . (2021). A cellular mechanism underlying the restoration of thermo/photoperiod-sensitive genic male sterility. Mol. Plant 14, 2104–2114. doi: 10.1016/j.molp.2021.08.019 PubMed DOI
Shi C., Zhang J., Wu B., Jouni R., Yu C., Meyers B. C., et al. . (2022). Temperature-sensitive male sterility in rice determined by the roles of AGO1d in reproductive phasiRNA biogenesis and function. New Phytol. 236, 1529–1544. doi: 10.1111/nph.v236.4 PubMed DOI
Shukla P., Singh N. K., Gautam R., Ahmed I., Yadav D., Sharma A., et al. . (2017). Molecular approaches for manipulating male sterility and strategies for fertility restoration in plants. Mol. Biotechnol. 59, 445–457. doi: 10.1007/s12033-017-0027-6 PubMed DOI
Si F., Luo H., Yang C., Gong J., Yan B., Liu C., et al. . (2023). Mobile ARGONAUTE 1d binds 22-nt miRNAs to generate phasiRNAs important for low-temperature male fertility in rice. Sci. China Life Sci. 66, 197–208. doi: 10.1007/s11427-022-2204-y PubMed DOI
Song X. Y., Qian H. H., Zhang L. L. (2013). Cytogenetic analysis of cytoplasmic male sterility in wheat line KTP116A and molecular mapping of two thermo-sensitive restoration genes. Euphytica 196, 129–136. doi: 10.1007/s10681-013-1020-1 DOI
Steiner-Lange S., Unte U. S., Eckstein L., Yang C., Wilson Z. A., Schmelzer E., et al. . (2003). Disruption of Arabidopsis thaliana MYB26 results in male sterility due to non-dehiscent anthers. Plant J. 34, 519–528. doi: 10.1046/j.1365-313x.2003.01745.x PubMed DOI
Subudhi P., Borkakati R., Virmani S., Huang N. (1997). Molecular mapping of a thermosensitive genetic male sterility gene in rice using bulked segregant analysis. Genome 40, 188–194. doi: 10.1139/g97-027 PubMed DOI
Tang J. H., Fu Z. Y., Hu Y. M., Li J. S., Sun L. L., Ji H. Q. (2006). Genetic analyses and mapping of a new thermo-sensitive genic male sterile gene in maize. Theor. Appl. Genet. 113, 11–15. doi: 10.1007/s00122-006-0262-x PubMed DOI
Tang Z., Zhang L., Yang D., Zhao C., Zheng Y. (2011). Cold stress contributes to aberrant cytokinesis during male meiosis I in a wheat thermosensitive genic male sterile line. Plant Cell Environ. 34, 389–405. doi: 10.1111/j.1365-3040.2010.02250.x PubMed DOI
Teng C., Zhang H., Hammond R., Huang K., Meyers B. C., Walbot V. (2020). Dicer-like 5 deficiency confers temperature-sensitive male sterility in maize. Nat. Commun. 11, 2912. doi: 10.1038/s41467-020-16634-6 PubMed DOI PMC
Vasupalli N., Kumar V., Bhattacharya R., Bhat S. R. (2021). Analysis of mitochondrial recombination in the male sterile Brassica juncea cybrid Og1 and identification of the molecular basis of fertility reversion. Plant Mol. Biol. 106, 109–122. doi: 10.1007/s11103-021-01132-0 PubMed DOI
Vasupalli N., Singh S. K., Watts A., Kumar P., Kumar V., Rao K. R. S. S., et al. . (2016). Mutations in the mitochondrial orf108 render Moricandia arvensis restorer ineffective in restoring male fertility to Brassica oxyrrhina-based cytoplasmic male sterile line of B. juncea . Mol. Breed. 36, 67. doi: 10.1007/s11032-016-0489-4 DOI
Vernoud V., Laigle G., Rozier F., Meeley R. B., Perez P., Rogowsky P. M. (2009). The HD-ZIP IV transcription factor OCL4 is necessary for trichome patterning and anther development in maize. Plant J. 59, 883–894. doi: 10.1111/j.1365-313X.2009.03916.x PubMed DOI
Wan X., Wu S., Li Z., Dong Z., An X., Ma B., et al. . (2019). Maize genic male-sterility genes and their applications in hybrid breeding: Progress and perspectives. Mol. Plant 12, 321–342. doi: 10.1016/j.molp.2019.01.014 PubMed DOI
Wan L., Zha W., Cheng X., Liu C., Lv L., Liu C., et al. . (2011). A rice β-1, 3-glucanase gene Osg1 is required for callose degradation in pollen development. Planta 233, 309–323. doi: 10.1007/s00425-010-1301-z PubMed DOI
Wang B., Fang R., Zhang J., Han J., Chen F., He F., et al. . (2020). Rice LecRK5 phosphorylates a UGPase to regulate callose biosynthesis during pollen development. J. Exp. Bot. 71, 4033–4041. doi: 10.1093/jxb/eraa180 PubMed DOI PMC
Wang D., Li J., Sun L., Hu Y., Yu J., Wang C., et al. . (2021). Two rice MYB transcription factors maintain male fertility in response to photoperiod by modulating sugar partitioning. New Phytol. 231, 1612–1629. doi: 10.1111/nph.v231.4 PubMed DOI
Wang H., Lu Y., Jiang T., Berg H., Li C., Xia Y. (2013). The Arabidopsis U-box/ARM repeat E3 ligase AtPUB4 influences growth and degeneration of tapetal cells, and its mutation leads to conditional male sterility. Plant J. 74, 511–523. doi: 10.1111/tpj.2013.74.issue-3 PubMed DOI
Wang C.-J. R., Nan G.-L., Kelliher T., Timofejeva L., Vernoud V., Golubovskaya I. N., et al. . (2012). Maize multiple archesporial cells 1 (mac1), an ortholog of rice TDL1A, modulates cell proliferation and identity in early anther development. Development 139, 2594–2603. doi: 10.1242/dev.077891 PubMed DOI PMC
Wang B., Xu W., Wang J., Wu W., Zheng H., Yang Z., et al. . (1995). Tagging and mapping the thermo-sensitive genic male-sterile gene in rice (Oryza sativa L.) with molecular markers. Theor. Appl. Genet. 91, 1111–1114. doi: 10.1007/BF00223928 PubMed DOI
Wang K. Q., Yu Y. H., Jia X. L., Zhou S. D., Zhang F., Zhao X., et al. . (2022). Delayed callose degradation restores the fertility of multiple P/TGMS lines in Arabidopsis . J. Integr. Plant Biol. 64, 717–730. doi: 10.1111/jipb.13205 PubMed DOI
Wang Y., Zha X., Zhang S., Qian X., Dong X., Sun F., et al. . (2010). Down-regulation of the OsPDCD5 gene induced photoperiod-sensitive male sterility in rice. Plant Sci. 178, 221–228. doi: 10.1016/j.plantsci.2009.12.001 DOI
Wei D., Liu M., Chen H., Zheng Y., Liu Y., Wang X., et al. . (2018). INDUCER OF CBF EXPRESSION 1 is a male fertility regulator impacting anther dehydration in Arabidopsis . PloS Genet. 14, e1007695. doi: 10.1371/journal.pgen.1007695 PubMed DOI PMC
Wei W., Wang P., Li S., Fan G., Zhao F., Zhang X., et al. . (2021). Rapid identification of candidate genes controlling male-sterility in Foxtail millet (Setaria italica). Mol. Breed. 41, 73. doi: 10.1007/s11032-021-01269-2 PubMed DOI PMC
Wen J., Zeng Y., Chen Y., Fan F., Li S. (2021). Genic male sterility increases rice drought tolerance. Plant Sci. 312, 111057. doi: 10.1016/j.plantsci.2021.111057 PubMed DOI
Wheeler M. J., Franklin-Tong V. E., Franklin F. C. H. (2001). The molecular and genetic basis of pollen-pistil interactions. New Phytol. 151, 565–584. doi: 10.1046/j.0028-646x.2001.00229.x PubMed DOI
Wolf C., Hennig M., Romanovicz D., Steinebrunner I. (2007). Developmental defects and seedling lethality in apyrase AtAPY1 and AtAPY2 double knockout mutants. Plant Mol. Biol. 64, 657–672. doi: 10.1007/s11103-007-9184-5 PubMed DOI
Wu Y., Fox T. W., Trimnell M. R., Wang L., Xu R. J., Cigan A. M., et al. . (2016). Development of a novel recessive genetic male sterility system for hybrid seed production in maize and other cross-pollinating crops. Plant Biotechnol. J. 14, 1046–1054. doi: 10.1111/pbi.2016.14.issue-3 PubMed DOI PMC
Wu L., Jing X., Zhang B., Chen S., Xu R., Duan P., et al. . (2022). A natural allele of OsMS1 responds to temperature changes and confers thermosensitive genic male sterility. Nat. Commun. 13, 2055. doi: 10.1038/s41467-022-29648-z PubMed DOI PMC
Xing S., Zachgo S. (2008). ROXY1 and ROXY2, two Arabidopsis glutaredoxin genes, are required for anther development. Plant J. 53, 790–801. doi: 10.1111/j.1365-313X.2007.03375.x PubMed DOI
Xu L., Tang Y., Yang Y., Wang D., Wang H., Du J., et al. . (2023). Microspore-expressed SCULP1 is required for p-coumaroylation of sporopollenin, exine integrity, and pollen development in wheat. New Phytol. 239, 102–115. doi: 10.1111/nph.v239.1 PubMed DOI
Xu F., Zheng L., Yang Z., Zhang S. (2020). Arabidopsis ECERIFERUM3 (CER3) functions to maintain hydration for pollen–stigma recognition during fertilization. J. Plant Biol. 63, 347–359. doi: 10.1007/s12374-020-09257-3 DOI
Xue Z., Xu X., Zhou Y., Wang X., Zhang Y., Liu D., et al. . (2018). Deficiency of a triterpene pathway results in humidity-sensitive genic male sterility in rice. Nat. Commun. 9, 604. doi: 10.1038/s41467-018-03048-8 PubMed DOI PMC
Yamaguchi Y., Hirasawa H., Minami M., Ujihara A. (1997). ). Linkage analysis of thermosensitive genic male sterility gene, tms-2 in rice (Oryza sativa L.). Japanese J. Breed. 47, 371–373. doi: 10.1270/jsbbs1951.47.371 DOI
Yan J., Li H., Li S., Yao R., Deng H., Xie Q., et al. . (2013). The Arabidopsis F-box protein CORONATINE INSENSITIVE1 is stabilized by SCFCOI1 and degraded via the 26S proteasome pathway. Plant Cell 25, 486–498. doi: 10.1105/tpc.112.105486 PubMed DOI PMC
Yan W., Yuan S., Zu Y., Chang Z., Li Y., Chen Z., et al. . (2023). Ornithine δ-aminotransferase OsOAT is critical for male fertility and cold tolerance during rice plant development. Plant J. 114, 1301–1318. doi: 10.1111/tpj.v114.6 PubMed DOI
Yan X., Zeng X., Wang S., Li K., Yuan R., Gao H., et al. . (2016). Aberrant meiotic prophase i leads to genic male sterility in the novel TE5A mutant of Brassica napus . Sci. Rep. 6, 33955. doi: 10.1038/srep33955 PubMed DOI PMC
Yang S.-L., Jiang L., Puah C. S., Xie L.-F., Zhang X.-Q., Chen L.-Q., et al. . (2005). Overexpression of TAPETUM DETERMINANT1 alters the cell fates in the Arabidopsis carpel and tapetum via genetic interaction with excess EXCESS ICROSPOROCYTES1/EXTRA SPOROGENOUS CELLS . Plant Physiol. 139, 186–191. doi: 10.1104/pp.105.063529 PubMed DOI PMC
Yang H., Li Y., Cao Y., Shi W., Xie E., Mu N., et al. . (2022). Nitrogen nutrition contributes to plant fertility by affecting meiosis initiation. Nat. Commun. 13, 485. doi: 10.1038/s41467-022-28173-3 PubMed DOI PMC
Yang Z., Liu L., Sun L., Yu P., Zhang P., Abbas A., et al. . (2019). OsMS1 functions as a transcriptional activator to regulate programmed tapetum development and pollen exine formation in rice. Plant Mol. Biol. 99, 175–191. doi: 10.1007/s11103-018-0811-0 PubMed DOI
Yang L., Qian X., Chen M., Fei Q., Meyers B. C., Liang W., et al. . (2016). Regulatory role of a receptor-like kinase in specifying anther cell identity. Plant Physiol. 171, 2085–2100. doi: 10.1104/pp.16.00016 PubMed DOI PMC
Yang K. Z., Xia C., Liu X. L., Dou X. Y., Wang W., Chen L. Q., et al. . (2009). A mutation in Thermosensitive Male Sterile 1, encoding a heat shock protein with DnaJ and PDI domains, leads to thermosensitive gametophytic male sterility in Arabidopsis. Plant J. 57, 870–882. doi: 10.1111/j.1365-313X.2008.03732.x PubMed DOI
Yang X., Ye J., Niu F., Feng Y., Song X. (2021). Identification and verification of genes related to pollen development and male sterility induced by high temperature in the thermo-sensitive genic male sterile wheat line. Planta 253, 83. doi: 10.1007/s00425-021-03601-8 PubMed DOI
Yi J., Moon S., Lee Y. S., Zhu L., Liang W., Zhang D., et al. . (2016). Defective Tapetum Cell Death 1 (DTC1) regulates ros levels by binding to metallothionein during tapetum degeneration. Plant Physiol. 170, 1611–1623. doi: 10.1104/pp.15.01561 PubMed DOI PMC
Yu J., Han J., Kim Y. J., Song M., Yang Z., He Y., et al. . (2017). Two rice receptor-like kinases maintain male fertility under changing temperatures. Proc. Natl. Acad. Sci. U.S.A. 114, 12327–12332. doi: 10.1073/pnas.1705189114 PubMed DOI PMC
Yu Q., Liang C., Wang X., Du Y., Masuda M., Murakami K. (2015). Study on the pollen thermo-sensitive and stigma exsertion male sterile line tomato (Lycopersicon esculentum Mill.) cv. Da107. Am. J. Plant Sci. 06, 2535–2539. doi: 10.4236/ajps.2015.616255 DOI
Yu B., Liu L., Wang T. (2019). Deficiency of very long chain alkanes biosynthesis causes humidity-sensitive male sterility via affecting pollen adhesion and hydration in rice. Plant Cell Environ. 42, 3340–3354. doi: 10.1111/pce.v42.12 PubMed DOI
Yu C., Xu X., Ge J., Guo Y., Dong J., Dong Z. (2016). Premature breakdown of tapetum associated with reverse thermo-sensitive genic male-sterile line Huiyou50S in rapeseed (Brassica napus). Acta Physiol. Plant 38, 54. doi: 10.1007/s11738-015-2039-9 DOI
Zhan H., Xiong H., Wang S., Yang Z. N. (2018). Anther endothecium-derived very-long-chain fatty acids facilitate pollen hydration in Arabidopsis . Mol. Plant 11, 1101–1104. doi: 10.1016/j.molp.2018.05.002 PubMed DOI
Zhang J.-K., Dong J., Zong X.-F., Yu G.-D., Dai X.-M., Ruan R.-W. (2009). Fertility alternation of thermo-photo-sensitive genic male sterile (TGMS) wheat line C412S and its association with adenine phosphoribosyltransferase gene expression. Acta Phys. Sin. 35, 662–671. doi: 10.1016/S1875-2780(08)60077-2 DOI
Zhang Y. F., Li Y. L., Zhong X., Wang J. J., Zhou L., Han Y., et al. . (2022. b). Mutation of glucose-methanol-choline oxidoreductase leads to thermosensitive genic male sterility in rice and Arabidopsis. Plant Biotechnol. J. 20, 2023–2035. doi: 10.1111/pbi.v20.10 PubMed DOI PMC
Zhang H., Liang W., Yang X., Luo X., Jiang N., Ma H., et al. . (2010). Carbon starved anther encodes a MYB domain protein that regulates sugar partitioning required for rice pollen development. Plant Cell 22, 672–689. doi: 10.1105/tpc.109.073668 PubMed DOI PMC
Zhang M., Liu J., Ma Q., Qin Y., Wang H., Chen P., et al. . (2020. b). Deficiencies in the formation and regulation of anther cuticle and tryphine contribute to male sterility in cotton PGMS line. BMC Genom. 21, 825. doi: 10.1186/s12864-020-07250-1 PubMed DOI PMC
Zhang C., Liu C., Weng J., Cheng B., Liu F., Li X., et al. . (2017). Creation of targeted inversion mutations in plants using an RNA-guided endonuclease. Crop J. 5, 83–88. doi: 10.1016/j.cj.2016.08.001 DOI
Zhang C., Ren M. Y., Han W. J., Zhang Y. F., Huang M. J., Wu S. Y., et al. . (2022. a). Slow development allows redundant genes to restore the fertility of rpg1, a TGMS line in Arabidopsis. Plant J. 109, 1375–1385. doi: 10.1111/tpj.v109.6 PubMed DOI
Zhang Q., Shen B., Dai X., Mei M., Saghai Maroof M., Li Z. (1994). Using bulked extremes and recessive class to map genes for photoperiod-sensitive genic male sterility in rice. Proc. Natl. Acad. Sci. U.S.A. 91, 8675–8679. doi: 10.1073/pnas.91.18.8675 PubMed DOI PMC
Zhang W., Sun Y., Timofejeva L., Chen C., Grossniklaus U., Ma H. (2006). Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encoding a putative bHLH transcription factor. Development 133, 3085–3095. doi: 10.1242/dev.02463 PubMed DOI
Zhang D., Wu S., An X., Xie K., Dong Z., Zhou Y., et al. . (2018). Construction of a multicontrol sterility system for a maize male-sterile line and hybrid seed production based on the ZmMs7 gene encoding a PHD-finger transcription factor. Plant Biotechnol. J. 16, 459–471. doi: 10.1111/pbi.2018.16.issue-2 PubMed DOI PMC
Zhang H., Xu C., He Y., Zong J., Yang X., Si H., et al. . (2013). Mutation in CSA creates a new photoperiod-sensitive genic male sterile line applicable for hybrid rice seed production. Proc. Natl. Acad. Sci. U.S.A. 110, 76–81. doi: 10.1073/pnas.1213041110 PubMed DOI PMC
Zhang C., Xu T., Ren M. Y., Zhu J., Shi Q. S., Zhang Y. F., et al. . (2020. a). Slow development restores the fertility of photoperiod-sensitive male-sterile plant lines. Plant Physiol. 184, 923–932. doi: 10.1104/pp.20.00951 PubMed DOI PMC
Zhang L., Yang M., Wei K., Yang W., Li S., Wang X., et al. . (2024). Fine-Mapping of Tomato male sterile-24 Locus and Marker Development for ms-24 and Its Alleles, ms-10, ms-35, and ms-36 . Horticulturae 10, 1322. doi: 10.3390/horticulturae10121322 DOI
Zhao D.-Z., Wang G.-F., Speal B., Ma H. (2002). The excess microsporocytes1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes Dev. 16, 2021–2031. doi: 10.1101/gad.997902 PubMed DOI PMC
Zhou M., Deng L., Yuan G., Zhao W., Ma M., Sun C., et al. . (2023). Rapid generation of a tomato male sterility system and its feasible application in hybrid seed production. Theor. Appl. Genet. 136, 197. doi: 10.1007/s00122-023-04428-5 PubMed DOI
Zhou L.-Z., Juranić M., Dresselhaus T. (2017). Germline development and fertilization mechanisms in maize. Mol. Plant 10, 389–401. doi: 10.1016/j.molp.2017.01.012 PubMed DOI
Zhou H., Liu Q., Li J., Jiang D., Zhou L., Wu P., et al. . (2012). Photoperiod- and thermo-sensitive genic male sterility in rice are caused by a point mutation in a novel noncoding RNA that produces a small RNA. Cell Res. 22, 649–660. doi: 10.1038/cr.2012.28 PubMed DOI PMC
Zhou H., Zhou M., Yang Y., Li J., Zhu L., Jiang D., et al. . (2014). RNase ZS1 processes UbL40 mRNAs and controls thermosensitive genic male sterility in rice. Nat. Commun. 5, 4884. doi: 10.1038/ncomms5884 PubMed DOI
Zhu J., Lou Y., Shi Q. S., Zhang S., Zhou W. T., Yang J., et al. . (2020). Slowing development restores the fertility of thermo-sensitive male-sterile plant lines. Nat. Plants 6, 360–367. doi: 10.1038/s41477-020-0622-6 PubMed DOI