هتروزیس در پنبه: چالش‌ها و فرصت‌های تولید ارقام هیبرید

نوع مقاله : مقاله پژوهشی

نویسندگان

1 بخش تحقیقات علوم زراعی و باغی، مرکز تحقیقات و آموزش کشاورزی و منابع طبیعی خراسان رضوی، سازمان تحقیقات، آموزش و ترویج کشاورزی، مشهد،

2 استادیار موسسه تحقیقات پنبه کشور، سازمان تحقیقات، آموزش و ترویج کشاورزی

10.22092/ijcr.2024.365051.1209

چکیده

پنبه به‌عنوان گیاهی راهبردی و مهمترین گیاه لیفی، یکی ازپرارزش‌ترین گیاهان زراعی است که اهمیت اقتصادی، کشاورزی و تجاری ویژه‌ای در جهان و ایران یافته است، و از گذشته اصلاح ارقام هیبرید در این گیاه مدنظر بوده است. در این مقاله مروری، آخرین پیشرفت‌ها در زمینه هتروزیس پنبه همراه با ساز و کار توسعه ارقام هیبرید به‌صورت سنتی، و استفاده از لاین‌های نرعقیم سیتوپلاسمی(CMS)  و ژنتیکی (GMS) در چند دهه گذشته مورد بررسی قرار خواهند گرفت. در حال حاضر، سه نوع هیبرید حاصل از روش سنتی، CMS و GMS در تولید و کشت و کار پنبه به کار می‌روند. از میان اینها، مطلوب‌ترین روش تولید بذور هیبرید استفاده از لاین GMS یا CMS همراه با گرده‌افشانی به کمک حشرات است و در صورتی که دانه گرده به اندازه کافی وجود داشته باشد، لاین‌های A و B گرده‌افشانی شده به کمک زنبور عسل می‌توانند عملکردهای مساوی از بذر پنبه در مزرعه تولید کنند. در حال حاضر، بیشتر هیبریدهای تجاری با استفاده از روش سنتی و دستی تولید می‌شوند که روشی بسیار پرهزینه است. بنابراین، در بسیاری از نقاط دنیا به دلیل هزینه بالای تولید بذرF1 ، بذر هیبرید  F2به‌طور گسترده‌ کشت می‌شود. عملکرد هیبریدهای نسل F2 معمولاً 5 تا 15 درصد بیشتر از ارقام شاهد است. یکی از مزایای استفاده از نسل F2 این است که با اینکه فقط نیمی از دانه‌های گرده F1 توانایی بازگرداندن باروری را دارند، والدین F2 توانایی بازگرداندن کامل باروری را دارند. با این وجود، گزینش و تأیید هتروزیس بالا در نسل F2 ضرورت دارد؛ زیرا با وجود اینکه هتروزیس بالایی در نسل F1 وجود دارد، برخی از هیبریدهای F2 هتروزیس نشان نمی‌دهند. بعلاوه، در نسل F2 هتروزیس در عملکرد وجود دارد، اما در کیفیت الیاف F2 هتروزیس وجود ندارد. برای توسعه لاین‌های نرعقیم و شناسایی مکانیسم نرعقیمی، ژن‌های GMS مانند ms2 و ms5ms6 و ژن‌های میتوکندریایی (نرعقیمی سیتوپلاسمی) از G. harknessii کلون شده‌اند. از سوی دیگر، شناسایی و بهبود نرعقیمی ژنتیکی حساس به شرایط محیطی القاء شده به‌وسیله عواملی مانند نور و دما این امکان را فراهم ساخته است تا از برخی صفات GMS به‌منظور اصلاح گیاهان هیبرید استفاده شود. لاین EGMS می‌تواند به‌عنوان یک لاین نرعقیم، و همچنین در صورت کنترل شرایط مساعد محیطی و تحقق اصلاح متقاطع دو لاین، به‌عنوان لاین نگهدارنده باروری مورد استفاده قرار گیرد. در این مقاله مروری به چالش‌ها و فرصت‌های استفاده از هتروزیس و توسعه ارقام هیبرید در پنبه پرداخته خواهد شد.

کلیدواژه‌ها

موضوعات


عنوان مقاله [English]

Heterosis in cotton: Challenges and opportunities of hybrid cultivars production

نویسندگان [English]

  • Fatemeh Saeidnia 1
  • Rasmieh Hamid 2
1 Agricultural and Horticultural Science Research Department, Khorasan Razavi Agricultural and Natural Resources Research and Education Center, Agricultural Research, Education and Extension Organization, Mashhad, 91769-83641, Iran.
2 Cotton research institute of Iran
چکیده [English]

Cotton, as a strategic crop and the most important fibre crop, is one of the most valuable agricultural crops that has a special economic, agricultural and commercial importance in the world and in Iran and has long been a subject for hybrid variety breeding. In this review, we have presented the latest advances in theoretical and applied research in the field of cotton heterosis and the methods used to develop hybrid varieties in recent decades. Three types of hybrids produced by manual emasculation, cytoplasmic male sterility and genetic male sterility have been developed and are being cultivated. The most desirable method of producing hybrid seed is to use the GMS or CMS line in combination with insect pollination when sufficient pollen is available to be pollinated by honey bees. The A and B lines can produce the same yield of seed cotton in the field. Currently, most hybrids grown commercially are produced by manual emasculation and pollination. Due to the high cost of producing F1 seed, F2 seed is therefore widely cultivated. The F2 generation of these combinations was 5 to 15 better in yield than the control varieties. One advantage of the F2 generation is that only half of the pollen of the F1 hybrid regains its fertility. However, the selection and certification of high heterosis in the F2 generation is necessary, as some F2 generations show no heterosis, although high heterosis is present in the F1 generation. In addition, there is heterosis in yield but not in fibre quality in F2. GMS genes (ms2 and ms5ms6) used in hybrid seed production and occasional mitochondrial genes for G. harknessii CMS were cloned. On the other hand, the discovery and improvement of environmental male sterility (EGMS), which is induced by environmental factors such as light and temperature, has enabled the utilisation of some GMS traits for hybrid breeding. The EGMS line can be used both as a sterile line and as a maintenance line by controlling the appropriate environment and realising the crossing of two lines. In this review, the challenges and opportunities of heterosis in cotton and the development of hybrid varieties are discussed.

کلیدواژه‌ها [English]

  • Sporophytic
  • gametophytic
  • restorer line
  • cytoplasmic male sterility
  • genetic male sterility
  1. Bohra, A., Jha, U. C., Adhimoolam, P., Bisht, D., & Singh, N. P. (2016). Cytoplasmic male sterility (CMS) in hybrid breeding in field crops. Plant Cell Reports, 35, 967–993. doi: 10.1007/s00299-016-1949-3.
  2. Budar, F., & Pelletier, G. (2001). Male sterility in plants: occurrence, determinism, significance and use. Comptes Rendus de l'Académie des Sciences - Series III, 324, 543–550. https://doi.org/10.1016/S0764-4469(01)01324-5
  3. Chen, L., & Liu, Y. G. (2014). Male sterility and fertility restoration in crops. Annual Review of Plant Biology, 65, 579–606. DOI: 1146/annurev-arplant-050213-040119
  4. Chen, D. Y., Ding, Y. Z., Guo, W. Z., & Zhang, T. Z. (2009). Molecular mapping of genic male-sterile genes ms15, ms5 and ms6 in tetraploid cotton. Plant Breeding, 128, 193–198. DOI: 1111/j.1439-0523.2008.01562.x
  5. Feng, F. Z. (1990). Primary studies on insect pollination male sterile line to produce hybrid seeds. China Cottons, 17(5), 16.
  6. Feng, C. D., Stewart, J. M., & Zhang, J. F. (2005). STS markers linked to the Rf1 fertility restorer gene of cotton. Theoretical and Applied Genetics, 110, 237–243. doi: 10.1007/s00122-004-1817-3.
  7. Feng, J., Zhang, X., Zhang, M., Guo, L., Qi, T., Tang, H., Zhu, H., Wang, H., Qiao, X., Xing, C., & Wu, J. (2021). Physical mapping and InDel marker development for the restorer gene Rf2 in cytoplasmic male sterile CMS-D8 cotton. BMC Genomics, 22, 24. https://doi.org/10.1186/s12864-020-07342-y.
  8. Feng, C., Guo, J., Nie, Y., Wu, Z., Zhang, X., Zhang, J., & Stewart, J. M. (2000). Cytoplasmic-nuclear male sterility in cotton: comparative RFLP analysis of mitochondrial DNA. Proceedings Beltwide Cotton Production Research Conference, San Antonio, USA, pp. 511–512.
  9. Gao, B., Ren, G., Wen, T., Li, H., Zhang, X., & Lin, Z. (2022). A super PPR cluster for restoring fertility revealed by genetic mapping, homocap-seq and de novo assembly in cotton. Theoretical and Applied Genetics, 135, 637–652. doi: 10.1007/s00122-021-03990-0.
  10. Guo, W. Z., Zhang, T. Z., Pan, J. J., & Kohel, R. J. (1998). Identification of RAPD marker linked with fertility-restoring gene of cytoplasmic male sterile lines in upland cotton. Chinese Science Bulletin, 43, 52–54. https://doi.org/10.1007/BF02885512.
  11. Guo, X. M., Tan, L. W., & Liu, Z. D. (2002). Evaluating germplasm resource value of Zhongmian 12. China Cotton, 29, 12–14
  12. Guo, S. D., Zhang, R., & Wang, Y. (2007). Research on genetic basis of three-line cotton. Bulletin of Agricultural Science and Technology, 12, 11–12
  13. Hamid, R., Marashi, H., Tomar, R. S., Malekzadeh Shafaroudi, S., & Sabara, P. H. (2019). Transcriptome analysis identified aberrant gene expression in pollen developmental pathways leading to CGMS in cotton (Gossypium hirsutum). PloS one,14(6), p.e0218381. https://doi.org/10.1371/journal.pone.0218381.
  14. Hamid, R., Tomar, R. S., Marashi, H., Shafaroudi, S. M., Golakiya, B. A., & Mohsenpour, M. (2018). Transcriptome profiling and cataloging differential gene expression in floral buds of fertile and sterile lines of cotton (Gossypium hirsutum). Gene, 660, 80-91. DOI: 10.1016/j.gene.2018.03.070
  15. Horn, R., Gupta, K. J., & Colombo, N. (2014). Mitochondrion role in molecular basis of cytoplasmic male sterility. Mitochondrion, 19, 198–205. doi: 10.1016/j.mito.2014.04.004.
  16. Hou, L., Xiao, Y., Li, X., Wang, W., Luo, X., & Pei, Y. (2002). The cDNA-AFLP differential display in developing anthers between cotton male sterile and fertile line of “Dong A.” Journal of Genetics and Genomics, 29, 359–363.
  17. Hu, J., Huang, W., Huang, Q., Qin, X., Yu, C., Wang, L., Li, S., Zhu, R., & Zhu, Y. (2014). Mitochondria and cytoplasmic male sterility in plants. Mitochondrion, 19, 282–288. doi: 10.1016/j.mito.2014.02.008.
  18. Hu, Y., Chen, J., Fang, L., Zhang, Z., Ma, W., Niu, Y., Ju, L., Deng, J., Zhao, T., Lian, J., Baruch, K., Fang, D., Liu, X., Ruan, Y-L., Rahman, M-U., Han, J., Wang, K., Wang, Q., Wu, H., Mei, G., Zang, Y., Han, Z., Xu, C., Shen, W., Yang, D., Si, Z., Dai, F., Zou, L., Huang, F., Bai, Y., Zhang, Y., Brodt, A., Ben-Hamo, H., Zhu, X., Zhou, B., Guan, X., Zhu, S., Chen, X., & Zhang, T. Z. (2019). Gossypium barbadense and Gossypium hirsutum genomes provide insights into the origin and evolution of allotetraploid cotton. Nature Genetics, 51, 739–748. doi: 10.1038/s41588-019-0371-5.
  19. Huang, Z. K. (2007). Cotton Varieties and Their Genealogy in China. China Agric Sci Press, Beijing.
  20. Huang, G. W., & Shi, X. Z. (1988). Chuanzha 4, a cotton hybrid by genic male sterile line. China Cottons, 15(3), 19.
  21. Jia, Z. C. (1990). Selection of a male-sterile line 104–7A of cotton and its complete set of three lines. China Cottons, 6, 11.
  22. Jiang, H., Lu, Q., Qiu, S., Yu, H., Wang, Z., Yu, Z., Lu, Y., Wang, L., Xia, F., Wu, Y., Li, F., Zhang, Q., Liu, G., Song, D., Ma, C., Ding, Q., Zhang, X., Zhang, L., Zhang, X., Li, X., Zhang, J., Xiao, J., Li, X., Wang, N., Ouyang, Y., Zhou, F., & Zhang, Q. (2022). Fujian cytoplasmic male sterility and the fertility restorer gene OsRf19 provide a promising breeding system for hybrid rice. Proceedings of the National Academy of Sciences, USA, 119(34), e2208759119.
  23. Jing, B., Heng, S., Tong, D., Wan, Z., Fu, T., Tu, J., Ma, C., Yi, B., Wen, J., & Shen, J. (2012). A male sterility-associated cytotoxic protein ORF288 in Brassica juncea causes aborted pollen development. Journal of Experimental Botany, 63, 1285–1295. doi: 1093/jxb/err355.
  24. Jing, S. R., Liu, S. L., Yuan, Y. L., & Xing, C. Z. (1994). Studies of utilization of genetic double recessive male sterile hirsutum L. Acta Gossypii Sinica, 6, 28–30.
  25. Justus, N., & Leinweber, L. (1960). A heritable partially male-sterile character in cotton. Journal of Heredity, 51, 192–192. https://doi.org/10.1093/oxfordjournals.jhered.a106987.
  26. Khan, A., Kong, X., Liao, X., Zheng, J., You, J., Li, M., Hussain, R. M., Raza, H., & Zhou, R. (2022). Mitochondrial gene expression analysis reveals aberrant transcription of cox3 in Gossypium barbadense CMS line H276A. Development Genes and Evolution, 232, 15–23. DOI: 1007/s00427-022-00687-2.
  27. Kim, Y. J., & Zhang, D. (2018). Molecular control of male fertility for crop hybrid breeding. Trends in Plant Science, 23, 53–65. DOI: 1016/j.tplants.2017.10.001.
  28. Kime, P. H., & Tilley, R. H. (1947). Hybrid vigor in Upland cotton-effect on yield and quality. Journal of American Society of Agronomy, 39, 308–317.
  29. Kohel, R. J., & Lewis, C. F. (1984). Cotton. American Society of Agronomy, Madison, Wisconsin.
  30. Li, S., Chen, Z., Zhao, N., Wang, Y., Nie, H., & Hua, J. (2018). The comparison of four mitochondrial genomes reveals cytoplasmic male sterility candidate genes in cotton. BMC Genomics, 19(1), 1–15. doi: 10.1186/s12864-018-5122-y.
  31. Li, M., Chen, L., Khan, A., Kong, X., Khan, M. R., Rao, M. J., Wang, J., Wang, L., & Zhou, R. (2021). Transcriptome and MiRNA omics analyses identify genes associated with cytoplasmic male sterility in cotton (Gossypium hirsutum L). International Journal of Molecular Sciences, 22(9), 4684. doi: 3390/ijms22094684.
  32. Liu, L. W., Guo, W. Z., Zhu, X. F., & Zhang, T. Z. (2003). Inheritance and fine mapping of fertility restoration for cytoplasmic male sterility in Gossypium hirsutum Theoretical and Applied Genetics, 106, 461–469. doi: 10.1007/s00122-002-1084-0.
  33. Liu, R. Z., Wang, B. H., Guo, W. Z., Qin, Y. S., Wang, L. G., Zhang, Y. M., & Zhang, T. Z. (2012). Quantitative trait loci mapping for yield and its components by using two immortalized populations of a heterotic hybrid in Gossypium hirsutum Molecular Breeding, 29, 297–311. DOI: 10.1007/s11032-011-9547-0
  34. Liu, J., Pang, C., Wei, H., Song, M., Meng, Y., Fan, S., & Yu, S. (2014). Proteomic analysis of anthers from wild-type and photosensitive genetic male sterile mutant cotton (Gossypium hirsutum ). BMC Plant Biology, 14, 390. https://doi.org/10.1186/s12870-014-0390-4.
  35. Luo, D., Xu, H., Liu, Z., Guo, J., Li, H., Chen, L., Fang, C., Zhang, Q., Bai, M., Yao, N., Wu, H., Wu, H., Ji, C., Zheng, H., Chen, Y., Ye, S., Li, X., Zhao, X., Li, R., & Liu, Y. G. (2013). A detrimental mitochondrial-nuclear interaction causes cytoplasmic male sterility in rice. Nature Genetics, 45, 573–577. doi: 10.1038/ng.2570.
  36. Ma, X., Xing, C., Guo, L., Gong, Y., Wang, H., Zhao, Y., & Wu, J. (2007). Analysis of differentially expressed genes in genic male sterility cotton (Gossypium hirsutum ) using cDNA-AFLP. Journal of Genetics and Genomics, 34, 536–543. https://doi.org/10.1016/S1673-8527(07)60059-9.
  37. Ma, H., Wu, Y., Lv, R., Chi, H., Zhao, Y., Li, Y., Liu, H., Ma, Y., Zhu, L., Guo, X., Kong, J., Wu, J., Xing, C., Zhang, X., & Min, L. (2022). Cytochrome P450 mono-oxygenase CYP703A2 plays a central role in sporopollenin formation and ms5ms6 fertility in cotton. Journal of Integrative Plant Biology, 64, 2009–2025. doi: 10.1111/jipb.13340.
  38. Mao, Y., Dai, F., Si, Z. F., Fang, L., & Zhang, T. Z. (2022). Duplicate mutations of GhCYP450 lead to the production of ms5m6 male sterile line in cotton. Theoretical and Applied Genetics, 136(1), 2. doi: 10.1007/s00122-023-04296-z. DOI: 1007/s00122-023-04296-z.
  39. Melonek, J., Duarte, J., Martin, J., Beuf, L., Murigneux, A., Varenne, P., Comadran, J., Specel, S., Levadoux, S., Bernath-Levin, K., Torney, F., Pichon, J. P., Perez, P., & Small, I. (2021). The genetic basis of cytoplasmic male sterility and fertility restoration in wheat. Nature Communications, 12, 1036. doi: 10.1038/s41467-021-21225-0.
  40. Meyer, V. G. (1975). Male-sterility from Gossypium-harknessii. Journal of Heredity, 66, 23–27. https://doi.org/10.1093/oxfordjournals.jhered.a108566.
  41. Meyer, V. G., & Meyer, J. R. (1965). Cytoplasmically controlled male sterility in cotton. Crop Science, 5, 444–448.
  42. Munir, S., Hussain, S. B., Manzoor, H., Quereshi, M. K., Zubair, M., Nouman, W., Shehzad, A. N., Rasul, S., & Manzoor, S. A. (2016). Heterosis and correlation in interspecific and intraspecific hybrids of cotton. Genetics and Molecular Research, 15(2), 15028083. http://dx.doi.org/10.4238/gmr.15028083.
  43. Raja, D., Kumar, M. S., Devi, P. R., Loganathan, S., Ramya, K., Kannan, N., & Subramanian, V. (2018). Identification of molecular markers associated with genic male sterility in tetraploid cotton (Gossypium hirsutum ) through bulk segregant analysis using a cotton SNP 63K array. Czech Journal of Genetics and Plant Breeding, 54, 154–160. DOI: 10.17221/25/2017-CJGPB.
  44. Rhyne, C. L. (1991). Male-steriles ms5ms5ms6ms6 and ms8ms8ms9ms9. Proceedings Beltwide Cotton Production Research Conference, USA, pp. 532-533.
  45. Schnable, P. S., & Springer, N. M. (2013). Progress toward understanding heterosis in crop plants. Annual Review of Plant Biology, 64, 71–88. DOI: 1146/annurev-arplant-042110-103827.
  46. Stewart, J. M. (1992). A new cytoplasmic male sterile and restorer for cotton. Proceedings Beltwide Cotton Production Research Conference, National Cotton Council, Memphis TN, p. 610.
  47. Tian, S. H., Xu, X., Zhu, X. F., Wang, F., Song, X. L., & Zhang, T. Z. (2019). Over-dominance is the major genetic basis of lint yield heterosis in interspecific hybrids between hirsutum and G. barbadense. Heredity, 123, 384–394. https://doi.org/10.1038/s41437-019-0211-5.
  48. Turcotte, E. L., & Feaster, C. V. (1979). Linkage tests in American Pima cotton. Crop Science, 19, 119–120. https://doi.org/10.2135/cropsci1979.0011183X001900010030x.
  49. Wang, X. D. (2000). Analyses of mitochondrial protein and DNA from cytoplasmic male sterile cotton. Acta Agronomica Sinica, 26, 35–39.
  50. Wang, X. D., Zhang, T. Z., & Pan, J. J. (1997). Cytoplasmic effects of cytoplasmic male sterile Upland cotton. Acta Agronomica Sinica, 23, 393–399.
  51. Wang, X. D., Zhang, T. Z., & Pan, J. J. (1998). Cytological observation of microsporogenesis and RAPD analysis of mitochondrial DNAs for cytoplasmic male sterile cotton lines. Scientia Agricultura Sinica, 31, 70–75.
  52. Wang, X. D., Zhu, Y. G., Zhao, P. O., & Ni, X. Y. (2003). Relationship between glutathione S-transferase activity of restorer anthers and pollen fertility of F1 hybrid in Upland cotton. Acta Agronomica Sinica, 29, 693–696.
  53. Wang, B. H., Wu, Y. T., Guo, W. Z., Zhu, X. F., Huang, N. T., & Zhang, T. Z. (2007a). QTL analysis and epistasis effects dissection of fiber qualities in an elite cotton hybrid grown in second generation. Crop Science, 47, 1384–1392. https://doi.org/10.2135/cropsci2006.10.0647.
  54. Wang, F., Stewart, J. M., & Zhang, J. (2007b). Molecular markers linked to the Rf2 fertility restorer gene in cotton. Genome, 50, 818–824. doi: 10.1139/g07-061.
  55. Wang, F., Feng, C., O’Connell, M. A., Stewart, J. M., & Zhang, J. F. (2009a). RFLP analysis of mitochondrial DNA in two cytoplasmic male sterility systems (CMS-D2 and CMS-D8) of cotton. Euphytica, 172, 93–99. https://doi.org/10.1007/s10681-009-0055-9.
  56. Wang, F., Yue, B., Hu, J., Stewart. J. M., & Zhang, J. F. (2009b). A target region amplified polymorphism marker for fertility restorer gene Rf1 and chromosomal localization of Rf1 and Rf2 in cotton. Crop Science, 49, 1602–1608. https://doi.org/10.2135/cropsci2008.09.0531.
  57. Wei, M., Song, M., Fan, S., & Yu, S. (2013). Transcriptomic analysis of differentially expressed genes during anther development in genetic male sterile and wild type cotton by digital gene expression profiling. BMC Genomics, 14, 97. https://doi.org/10.1186/1471-2164-14-97.
  58. Wu, Y. T., Yin, J. M., Guo, W. Z., Zhu, X. F., & Zhang, T. Z. (2004). Heterosis performance of yield and fiber quality in F1 and F2 hybrids in Upland cotton. Plant Breeding, 123(3), 285–289. DOI: 1111/j.1439-0523.2004.00990.x.
  59. Wu, J., Cao, X., Guo, L., Qi, T., Wang, H., Tang, H., Zhang, J., & Xing, C. (2014). Development of a candidate gene marker for Rf1 based on a PPR gene in cytoplasmic male sterile CMS-D2 Upland cotton. Molecular Breeding, 34, 231–240. https://doi.org/10.1007/s11032-014-0032-4.
  60. Wu, Y., Min, L., Wu, Z., Yang, L., Zhu, L., Yang, X., Yuan, D., Guo, X., & Zhang, X. L. (2015). Defective pollen wall contributes to male sterility in the male sterile line 1355A of cotton. Scientific Reports, 5, 9608. https://doi.org/10.1038/srep09608.
  61. Wu, J., Zhang, M., Zhang, X., Guo, L., Qi, T., Wang, H., Tang, H., Zhang, J., & Xing, C. (2017). Development of InDel markers for the restorer gene Rf1 and assessment of their utility for marker-assisted selection in cotton. Euphytica, 213(11), 1–8. https://doi.org/10.1007/s10681-017-2043-9.
  62. Wu, Y., Li, X., Li, Y., Ma, H., Chi, H., Ma, Y., Yang, J., Xie, S., Zhang, R., Liu, L., Su, X., Lv, R., Khan, A. H., Kong, J., Guo, X., Lindsey, K., Min, L., & Zhang, X. L. (2022). Degradation of de-esterified pctin/homogalacturonan by the polygalacturonase GhNSP is necessary for pollen exine formation and male fertility in cotton. Plant Biotechnology Journal, 20, 1054–1068. doi: 10.1111/pbi.13785.
  63. Xing, C. Z., Jing, S. L., Guo, L. P., Yuan, Y. L., Liu, S. L., & Wang, H. L. (1999). Nuclear sterile ms5ms6 of Upland cotton resistant to cotton bollworm-Zhongkang A. China Cottons, 26(6), 27.
  64. Xing, C. Z., Guo, L. P., Miao, C. D., Wang, H. L., & Lou, B. Q. (2005). Study on effects of producing cotton hybrids by bees pollination. Cotton Science, 17, 207–210.
  65. Xing, C. Z., Guo, L. P., Li, W., Wu, J. Y., Yang, D. G., Qi, T. T., Ma, X. F., & Zhang, X. X. (2017). Ten-year achievements and future development of cotton heterosis utilization. Cotton Science, 29, 28–36.
  66. Xuan, L. S., Qi, G. A., Li, X., Yan, S., Cao, Y., Huang, C., He, L., Zhang, T. Z., Shang, H., & Hu, Y. (2022). Comparison of mitochondrial genomes between a cytoplasmic male-sterile line and its restorer line for identifying candidate CMS genes in Gossypium hirsutum. International Journal of Molecular Sciences, 23(16), 9198. doi: 10.3390/ijms23169198.
  67. Yamagishi, H., Tanaka, Y., Shiiba, S., Hashimoto, A., Fukunaga, A., & Terachi, T. (2019). Mitochondrial orf463 causing male sterility in radish is possessed by cultivars belonging to the ‘Niger’ group. Euphytica, 215(6), 1–8. https://doi.org/10.1007/s10681-019-2437-y.
  68. Yang, L. M., Zhu, H. Y., Guo, W. Z., & Zhang, T. Z. (2010). Molecular cloning and characterization of five genes encoding pentatricopeptide repeat proteins from Upland cotton (Gossypium hirsutum ). Molecular Biology Reports, 37, 801–808. doi: 10.1007/s11033-009-9610-7.
  69. Yang, H., Xue, Y., Li, B., Lin, Y., Li, H., Guo, Z., Li, W., Fu, Z., Ding, D., & Tang, J. (2022). The chimeric gene atp6c confers cytoplasmic male sterility in maize by impairing the assembly of the mitochondrial ATP synthase complex. Molecular Plant, 15, 872–886. doi: 10.1016/j.molp.2022.03.002.
  70. Yin, J. M., Guo, W. Z., Yang, L. M., Liu, L. W., & Zhang, T. Z. (2006). Physical mapping of the Rf1 fertility-restoring gene to a 100 kb region in cotton. Theoretical and Applied Genetics, 112, 1318–1325. doi: 10.1007/s00122-006-0234-1.
  71. You, J., Li, M., Li, H., Bai, Y., Zhu, X., Kong, X., Chen, X., & Zhou, R. (2022). Integrated methylome and transcriptome analysis widen the knowledge of cytoplasmic male sterility in cotton (Gossypium barbadense ). Frontiers in Plant Science, 13, 770098. doi: 10.3389/fpls.2022.770098.
  72. Zaidi, S. S., Naqvi, R. Z., Asif, M., Strickler, S., Shakir, S., Shafiq, M., Khan, A. M., Amin, I., Mishra, B., Mukhtar, M. S., Scheffler, B. E., Scheffler, J. A., Mueller, L. A., & Mansoor, S. (2020). Molecular insight into cotton leaf curl geminivirus disease resistance in cultivated cotton (Gossypium hirsutum). Plant Biotechnology Journal, 18, 691–706. doi: 10.1111/pbi.13236.
  73. Zhang, T. Z. (1995). A discussion on the inheritance of Dong-A male sterility and its fertility-maintaining line(Mb) in Upland cotton. Hereditas (Beijing), 17(6), 30–33.
  74. Zhang, T. Z., & Jing, S. L. (1997). Theory and Practice of Hybrid Cotton Development Via Male Sterile Lines in Cotton. China Agricultural Press, Beijing.
  75. Zhang, T. Z., & Pan, J. J. (1990). A genetic male sterile line with virescent marker character in Upland cotton. Euphytica, 48, 233–237.
  76. Zhang, J. F. & Stewart, J. M. (2001). Inheritance and genetic relationships of the D8 and D2–2 restorer genes for cotton cytoplasmic male sterility. Crop Science, 41, 289–294. https://doi.org/10.2135/cropsci2001.412289x.
  77. Zhang, J., & Stewart, J. M. (2004). Identification of molecular markers linked to the fertility restorer genes for CMS-D8 in cotton. Crop Science, 44, 1209–1217. https://doi.org/10.2135/cropsci2004.1209
  78. Zhang, T. Z., & Zhu, X. F. (2004). Breeding and cultivation technology of Nannong6 (NAU6). China Cottons, 31(8), 18–19.
  79. Zhang, T. Z., & Zhu, X. F. (2005). Breeding and cultivation technology of Nannong9 (NAU9). China Cottons 32(8), 19.
  80. Zhang, T., Xuan, L., Mao, Y., & Hu, Y. (2023). Heterosis and hybrid cultivar development. Theoretical and Applied Genetics, 136, 89. https://doi.org/10.1007/s00122-023-04334-w.
  81. Zhang, B., Zhang, X., Guo, L., Qi, T., Wang, H., Tang, H., Qiao, X., Shahzad, K., Xing, C., & Wu, J. (2018). Genome-wide analysis of Rf-PPR-like (RFL) genes and a new InDel marker development for Rf1 gene in cytoplasmic male sterile CMS-D2 Upland cotton. Journal of Cotton Research, 1(1), 1–11. https://doi.org/10.1186/s42397-018-0013-y.
  82. Zhang, M., Liu, J., Ma, Q., Qin, Y., Wang, H., Chen, P., Ma, L., Fu, X., Zhu, L., Wei, H., & Yu, S. (2020). Deficiencies in the formation and regulation of anther cuticle and tryphine contribute to male sterility in cotton PGMS line. BMC Genomics, 21, 825. https://doi.org/10.1186/s12864-020-07250-1.
  83. Zhang, Y., Han, Y., Zhang, M., Zhang, X., Guo, L., Qi, T., Li, Y., Feng, J., Wang, H., Tang, H., Qiao, X., Chen, L., Song, X., Xing. C., & Wu, J. (2022). The cotton mitochondrial chimeric gene orf610a causes male sterility by disturbing the dynamic balance of ATP synthesis and ROS burst. The Crop Journal, 10, 1683–1694. https://doi.org/10.1016/j.cj.2022.02.008.
  84. Zhang, T. Z., & Pan, J. J. (1999). Hybrid seed production in cotton. In: Basra R.S. (Ed.) Hybrid Seed Production in Crops. Food Production Press, New York, USA. pp. 149–184.
  85. Zhou, H., Liu, Q., Li, J., Jiang, D., Zhou, L., Wu, P., Lu, S., Li, F., Zhu, L., Liu, Z., Chen, L., Liu, Y-G., & Zhuang, C. (2012). Photoperiod- and thermosensitive genic male sterility in rice are caused by a point mutation in a novel noncoding RNA that produces a small RNA. Cell Research, 22, 649–660. https://doi.org/10.1038/cr.2012.28.
  86. Zhu, X. F., Wang, X. D., Sun, J., Zhang, T. Z., & Pan, J. J. (1998). Assessment of cytoplasmic effects of cytoplasmic male-sterile lines in upland cotton. Plant Breeding, 117, 549–552. https://doi.org/10.1111/j.1439-0523.1998.tb02205.x
  87. Zhu, S. J., Tong, X. H., Hong, C. X., Ji, D. F., Wu, W., & Wang, R. H. (2006). A new combination of three-line hybrid cotton “Zheza 2.” China Cottons, 5, 12–13.
  88. Zhu, C. S., Wu, J. T., Zhou, D. G., Li, Y., Peng, F. J., Gong, Y. C., & Zhou, S. X. (2013). Breeding and utilization of cotton cytoplasmic sterile line “Xiangyuan A.” China Cotton Association, Beijing, pp. 192–194.