Advances in Research and Application of Male Sterility in Brassica oleracea
Abstract
:1. Introduction
2. Types and Genetic Characteristics of Male Sterility in B. oleracea
2.1. Genic Male Sterility (GMS)
2.2. Cytoplasmic Male Sterility (CMS)
2.2.1. Ogu CMS
2.2.2. Pol CMS
2.2.3. Nig CMS
3. Cytological Study of Male Sterility in B. oleracea
4. Molecular Biological Study of Male Sterility in B. oleracea
4.1. Expression Analysis of Male Sterile Related Genes
4.2. Molecular Markers Associated with Male Sterility
4.3. The Mechanism of Ogu CMS
4.4. The Fertility-Restored Gene Rfo of Ogu CMS
4.5. Other Male Sterile Related Genes in B. oleracea
5. Application of Male Sterility in B. oleracea
5.1. Application of DGMS
5.2. Application of Ogu CMS and Its Fertility-Restored Gene Rfo
6. Perspectives
Author Contributions
Funding
Conflicts of Interest
References
- Liu, S.; Liu, Y.; Yang, X.; Tong, C.; Edwards, D.; Parkin, L.A.P.; Zhao, M.; Ma, J.; Yu, J.; Huang, S.; et al. The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes. Nat. Commun. 2014, 5, 3930. [Google Scholar] [CrossRef]
- Cheng, F.; Sun, R.; Hou, X.; Zheng, H.; Zhang, F.; Zhang, Y.; Liu, B.; Liang, J.; Zhuang, M.; Liu, Y.; et al. Subgenome parallel selection is associated with morphotype diversification and convergent crop domestication in Brassica rapa and Brassica oleracea. Nat. Genet. 2016, 48, 1218–1224. [Google Scholar] [CrossRef] [PubMed]
- Kushad, M.M.; Brown, A.F.; Kurilich, A.C.; Juvik, J.A.; Klein, B.P.; Wallig, M.A.; Jeffery, E.H. Variation of glucosinolates in vegetable crops of Brassica oleracea. J. Agric. Food Chem. 1999, 47, 1541–1548. [Google Scholar] [CrossRef]
- Tanaka, N.; Niikura, S. Genetic analysis of the developmental characteristics related to the earliness of head formation in cabbage (Brassica oleracea L.). Breed. Sci. 2006, 56, 147–153. [Google Scholar] [CrossRef] [Green Version]
- Fang, Z.; Liu, Y.; Yang, L.; Wang, X.; Zhuang, M.; Zhang, Y.; Sun, P. Breeding and seed production technique of dominant genic male sterile (DGMS) line and cytoplasmic male sterile (CMS) line in cabbage. Sci. Agric. Sin. 2004, 37, 717–723. (In Chinese) [Google Scholar]
- Kaul, M.L.H. Male Sterility in Height Plants; Springer: Berlin/Heidelberg, Germany, 1988; pp. 193–220. [Google Scholar]
- Wise, R.P.; Pring, D.R. Nuclear-mediated mitochondrial gene regulation and male fertility in higher plants: Light at the end of the tunnel? Proc. Natl. Acad. Sci. USA 2002, 99, 10240–10242. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vedel, F.; Pla, M.; Vitart, V.; Gutierres, S.; Chetrit, P.; Paepe, R.D. Molecular basis of nuclear and cytoplasmic male sterility in higher plants. Plant Physiol. Biochem. 1994, 32, 601–608. [Google Scholar]
- Fang, Z.; Sun, P.; Liu, Y.; Yang, L.; Wang, X.; Zhuang, M. Investigation of different types of male sterility and application of dominant male sterility in cabbage. China Veg. 2001, 1, 6–10. (In Chinese) [Google Scholar]
- Ji, J.; Yang, L.; Fang, Z.; Zhuang, M.; Zhang, Y.; Lv, H.; Liu, Y.; Li, Z. Recessive male sterility in cabbage (Brassica oleracea var. capitata) caused by loss of function of BoCYP704B1 due to the insertion of a LTR-retrotransposon. Theor. Appl. Genet. 2017, 130, 1441–1451. [Google Scholar] [CrossRef]
- Fang, Z.; Sun, P.; Liu, Y.; Yang, L.; Wang, X.; Hou, A.; Bian, C. A male sterile line with dominant gene (MS) in cabbage (Brassica oleracea var. capitata) and its utilization for hybrid seed production. Euphytica 1997, 97, 265–268. [Google Scholar]
- Ogura, H. Studies on the new male sterility in Japanese radish with special reference to the utilization of this sterility towards the practical raising of hybrid seeds. Mem. Fac. Agric. Kagoshima Univ. 1968, 6, 39–78. [Google Scholar]
- Bannerot, H.; Boulidard, L.; Cauderon, Y.; Tempe, J. Transfer of cytoplasmatic male sterility from Raphanus sativus to Brassica oleracea. Proc. Eucarpia Meet Crucif. Crop Sect. 1974, 25, 52–54. [Google Scholar]
- Walters, W.T.; Mustschler, A.M.; Eaele, D.E. Protoplast fusion-derived Ogura male-sterile cauliflower with cold tolerance. Plant Cell Rep. 1992, 10, 624–628. [Google Scholar] [CrossRef] [PubMed]
- Wang, Q.; Zhang, Y.; Fang, Z.; Liu, Y.; Yang, L.; Zhuang, M. Chloroplast and mitochondrial SSR help to distinguish allo-cytoplasmic male sterile types in cabbage (Brassica oleracea L. var. capitata). Mol. Breed. 2012, 30, 709–716. [Google Scholar] [CrossRef]
- Pelletier, G.; Budar, F. Brassica Ogu-INRA cytoplasmic male sterility: An example of successful plant somatic fusion for hybrid seed production. In Somatic Genome Manipulation; Springer: New York, NY, USA, 2015; pp. 199–216. [Google Scholar] [CrossRef]
- Fu, T. Production and research on rapeseed in the People’s Republic of China. Crucif. Newslett. 1981, 6, 6–7. [Google Scholar]
- Fu, T.; Yang, X.; Yang, G. Development and studies on polima cytoplasmic male sterile “three lines” in Brassica napus L. J. Huazhong Agric. Univ. 1989, 8, 201–207. (In Chinese) [Google Scholar]
- Yang, G.; Fu, T. The inheritance of polima cytoplasmic male sterility in Brassica napus L. Plant Breed. 1990, 104, 121–124. [Google Scholar]
- Yarrow, S.; Burnett, L.; Wildeman, R.; Kemble, R.J. The transfer of polima cytoplasmic male sterility from oil seed rape (B. napus) to broccoli (B. oleracea) by protoplast fusion. Plant Cell Rep. 1990, 9, 185–188. [Google Scholar] [CrossRef]
- Yang, G.; Fu, T.; Yang, X. Studies on the ecotypical male sterile line of Brassica napus L. Acta Agron. Sin. 1995, 21, 129–135. (In Chinese) [Google Scholar]
- Pearson, O.H. Cytoplasmically inherited make sterility characters and flavor components from the species cross B.nigra Koch×B.oleracea L. J. Am. Soc. Hortic. Sci. 1972, 97, 397–402. [Google Scholar]
- Lou, P.; Kang, J.; Zhang, G.; Bonnema, G.; Fang, Z.; Wang, X. Transcript profiling of a dominant male sterile mutant (Ms-cd1) in cabbage during flower bud development. Plant Sci. 2007, 172, 111–119. [Google Scholar] [CrossRef]
- Ma, Y.; Kang, J.; Wu, J.; Zhu, Y.; Wang, X. Identification of tapetum-specific genes by comparing global gene expression of four different male sterile lines in Brassica oleracea. Plant Mol. Biol. 2015, 87, 541–554. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pacini, E. Tapetum character states: Analytical keys for tapetum types and activities. Can. J. Bot. 1997, 75, 1448–1459. [Google Scholar] [CrossRef]
- Scott, R.J.; Spielman, M.; Dickinson, H.G. Stamen structure and function. Plant Cell 2004, 16, S46–S60. [Google Scholar] [CrossRef] [PubMed]
- Huang, M.D.; Hsing, Y.I.; Huang, A.H. Transcriptomes of the anther sporophyte: Availability and use. Plant Cell Physiol. 2011, 52, 1459–1466. [Google Scholar] [CrossRef] [Green Version]
- Ji, J.; Yang, L.; Fang, Z.; Zhuang, M.; Zhang, Y.; Lv, H.; Liu, Y.; Li, Z. Complementary transcriptome and proteome profiling in cabbage buds of a recessive male sterile mutant provides new insights into male reproductive development. J. Proteom. 2018, 179, 80–91. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; Lou, P.; Bonnema, G.; Yang, B.; He, H.; Zhang, Y.; Fang, Z. Linkage mapping of a dominant male sterility gene DGMS in Barssica oleracea. Genome 2005, 48, 848–854. [Google Scholar] [CrossRef]
- Zhang, X.; Wu, J.; Zhang, H.; Ma, Y.; Guo, A.; Wang, X. Fine mapping of a male sterility gene MS-cd1 in Brassica oleracea. Theor. Appl. Genet. 2011, 123, 231–238. [Google Scholar] [CrossRef] [PubMed]
- Han, F.; Zhang, X.; Yuan, K.; Fang, Z.; Yang, L.; Zhuang, M.; Zhang, Y.; Wang, Y.; Liu, Y.; Li, Z.; et al. A user-friendly KASP molecular marker developed for the DGMS-based breeding system in Brassica oleracea species. Mol. Breed. 2019, 39, 90–96. [Google Scholar] [CrossRef]
- Han, F.; Yuan, K.; Kong, C.; Zhang, X.; Yang, L.; Zhuang, M.; Zhang, Y.; Li, Z.; Wang, Y.; Fang, Z.; et al. Fine mapping and candidate gene identifcation of the genic male sterile gene ms3 in cabbage 51S. Theor. Appl. Genet. 2018, 131, 2651–2661. [Google Scholar] [CrossRef] [PubMed]
- Singh, M.; Rown, G.G. Haracterization of expression of a mitochondrial gene associated with the Brassica polima CMS developmental influences. Curr. Genet. 1993, 24, 316–322. [Google Scholar] [CrossRef]
- Brown, G.G.; Domaj, M.; Dupauw, M.; Jean, M.; Li, X.Q.; Landry, B.S. Molecular analysis of Brassica CMS and its application to hybrid seed production. Acta Hortic. 1998, 459, 265–274. [Google Scholar] [CrossRef]
- Hanson, M.; Bentolila, S. Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 2004, 16 (Suppl. 1), S154–S169. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, J.; Zhang, H.; Yu, X.; Wang, S.; Cao, J. Molecular identification of the cytoplasmic male sterile (CMS) type in common head cabbage. Mol. Plant Breed. 2009, 7, 1149–1153. (In Chinese) [Google Scholar]
- Zhang, Y.; Wang, X.; Li, C.; Song, H.; Ren, X.; Si, J. Molecular identification of Brassica oleracea CMS and the morphology response of flower to nuclear background. Acta Hortic. Sin. 2010, 37, 915–922. (In Chinese) [Google Scholar]
- Zhang, Y.; Fang, Z.; Wang, Q.; Liu, Y.; Yang, L.; Zhuang, M.; Sun, P. Molecular distinction of two Ogura CMS sources in Brassica oleracea var. capitata L. Sci. Agric. Sin. 2011, 44, 2959–2965. (In Chinese) [Google Scholar]
- Zhu, Q.; Kang, Z.; Jian, Y.; Ding, Y.; Kang, J. The molecular characteristics of Ogura cytoplasmic male sterility related gene orf138 in cabbage (Brassica oleracea var. capitata). Chin. Agric. Sci. Bull. 2012, 28, 104–109. (In Chinese) [Google Scholar]
- Fujii, S.; Toriyam, K. Genome barriers between nuclei and mitochondria exemplified by cytoplasmic male sterility. Plant Cell Physiol. 2008, 49, 1484–1494. [Google Scholar] [CrossRef] [Green Version]
- Chen, L.; Liu, Y. Male sterility and fertility restoration in crops. Ann. Rev. Plant Biol. 2014, 65, 579–606. [Google Scholar] [CrossRef]
- Domblides, E.A.; Domblides, A.S.; Zayachkovskaya, T.V.; Bondareva, L.L. Identification of cytoplasm types in accessions of the family Brassicaceae (Brassicaceae Burnett) with DNA markers. Vavilov J. Genet. Breed. 2015, 19, 529. [Google Scholar] [CrossRef]
- Yamagishi, H.; Terachi, T. Intra-and inter-specifc variations in the mitochondrial gene orf138 of Ogura-type male sterile cytoplasm from Raphanus sativus and Raphanus raphanistrum. Theor. Appl. Genet. 2001, 103, 725–732. [Google Scholar] [CrossRef]
- Bonhomme, S.; Budar, F.; Ferault, M.; Pelletier, G. A 2.5kb Nco I fragment of Ogura radish mitochondrial DNA is correlated with cytoplasmic male-sterility in Brassica cybrids. Curr. Genet. 1991, 19, 121–127. [Google Scholar] [CrossRef]
- Bonhomme, S.; Budar, F.; Lancelin, D.; Small, I.; Defrance, M.C.; Pelletier, G. Sequence and transcript analysis of the Nco2.5 Ogura-specific fragment correlated with cytoplasmic male sterility in Brassica cybrids. Mol. Gen. Genet. 1992, 235, 340–348. [Google Scholar] [CrossRef]
- Krishnasamy, S.; Makaroff, C.A. Characterization of the radish mitochondrial orfB locus: Possible relationship with male sterility in Ogura radish. Curr. Genet. 1993, 24, 156–163. [Google Scholar] [CrossRef] [PubMed]
- Krishnasamy, S.; Makaroff, C.A. Organ-specific reduction in the abundance of a mitochondrial protein accompanies fertility restoration in cytoplasmic male-sterile radish. Plant Mol. Biol. 1994, 26, 935–946. [Google Scholar] [CrossRef]
- Duroc, Y.; Gaillard, C.; Hiard, S.; Defrance, M.C.; Pelletier, G.; Budar, F. Biochemical and functional characterization of orf138, a mitochondrial protein responsible for Ogura cytoplasmic male sterility in Brassiceae. Biochimie 2005, 87, 1089. [Google Scholar] [CrossRef]
- Tanaka, Y.; Tsuda, M.; Yasumoto, K.; Yamagishi, H.; Terachi, T. A complete mitochondrial genome sequence of Ogura-type male-sterile cytoplasm and its comparative analysis with that of normal cytoplasm in radish (Raphanus sativus L.). BMC Genom. 2012, 13, 352. [Google Scholar] [CrossRef] [Green Version]
- Xing, M.; Sun, C.; Li, H.; Hu, S.; Lei, L.; Kang, J. Integrated analysis of transcriptome and proteome changes related to the Ogura cytoplasmic male sterility in cabbage. PLoS ONE 2018, 13, e0193462. [Google Scholar] [CrossRef] [Green Version]
- Nieuwhof, M. Cytoplasmic-genetic male sterility in radish (Raphanus sativus L.). Identification of maintainers, inheritance of male sterility and effect of environmental factors. Euphytica 1990, 47, 171–177. [Google Scholar]
- Yamagishi, H. Distribution and allelism of restorer genes for Ogura cytoplasmic male sterility in wild and cultivated radishes. Genes Genet. Syst. 1998, 73, 79–83. [Google Scholar] [CrossRef] [Green Version]
- Zhang, L.; Shen, X.; Zhao, G. Inheritance of male sterility in spring-summer radish. Acta Hortic. Sin. 1999, 26, 238–243. (In Chinese) [Google Scholar]
- Bellaoui, M.; Pelletier, G.; Budar, F. The steady-level of mRNA from the Ogura cytoplasmic male sterility locus in Brassica cybrids is determined post-transcriptionally by its 3′ region. EMBO J. 1997, 16, 5057–5068. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brown, G.G.; Formanova, N.; Jin, H.; Wargachuk, R.; Dendy, C.; Pati, P.; Lafores, M.; Zhang, J.; Cheung, W.Y.; Landry, B.S. The radish Rfo restorer gene of Ogura cytoplasmic male sterility encodes a protein with multiple pentatricopeptide repeats. Plant J. 2003, 35, 262–272. [Google Scholar] [CrossRef] [PubMed]
- Desloire, S.; Gherbi, H.; Laloui, W.; Marhadour, S.; Clouet, V.; Cattolico, L.; Falentin, C.; Giancola, S.; Renard, M.; Budar, F.; et al. Identification of the fertility restoration locus Rfo in radish, as a member of the pentatricopeptide-repeat protein family. EMBO Rep. 2003, 4, 588–594. [Google Scholar] [CrossRef] [Green Version]
- Uyttewaal, M.; Arnal, N.; Quadrado, M.; Martin-Canadell, A.; Vrielynck, N.; Hiard, S.; Gherbi, H.; Bendahmane, A.; Budar, F.; Mireau, H. Characterization of Raphanus sativus pentatricopeptide repeat proteins encoded by the fertility restorer locus for Ogura cytoplasmic male sterility. Plant Cell 2008, 20, 3331–3345. [Google Scholar] [CrossRef] [Green Version]
- Koizuka, N.; Imai, R.; Fujimoto, H.; Hayakawa, T.; Kimura, Y.; Kohno-Murase, J.; Sakai, T.; Kawasaki, S.; Imamura, J. Genetic characterization of a pentatricopeptide repeat protein gene, orf687, that restores fertility in the cytoplasmic male-sterile Kosena radish. Plant J. 2003, 34, 407–415. [Google Scholar] [CrossRef]
- Yasumoto, K.; Terachi, T.; Yamagishi, H. A novel Rf gene controlling fertility restoration of Ogura male sterility by RNA processing of orf138 found in Japanese wild radish and its STS markers. Genome 2009, 52, 495–504. [Google Scholar] [CrossRef]
- Wang, Z.; Zhang, Y.; Xiang, C.; Mei, S.; Zhou, Y.; Chen, G.; Wang, T. A new fertility restorer locus linked closely to the Rfo locus for cytoplasmic male sterility in radish. Theor. Appl. Genet. 2008, 117, 313–320. [Google Scholar] [CrossRef]
- Wang, Z.; Zhang, L.; Chen, J.; Xiang, C.; Mei, S.; Zhou, Y.; Wang, T. A chimeric Rfo gene generated by intergenic recombination cosegregates with the fertility restorer phenotype for cytoplasmic male sterility in radish. Mol. Breed. 2010, 25, 339–349. [Google Scholar] [CrossRef]
- Wang, Z.; De, W.; Gao, L.; Mei, S.; Zhou, Y.; Xiang, C.; Wang, T. Heterozygous alleles restore male fertility to cytoplasmic male-sterile radish (Raphanus sativus L.): A case of overdominance. J. Exp. Bot. 2013, 64, 2041. [Google Scholar] [CrossRef] [Green Version]
- Wang, Z.; Wang, C.; Mei, S.; Gao, L.; Zhou, Y.; Wang, T. An insertion-deletion at a pentatricopeptide repeat locus linked to fertility transition to cytoplasmic male sterility in radish (Raphanus sativus L.). Mol. Breed. 2015, 35, 108. [Google Scholar] [CrossRef]
- Wang, Z.; Wang, C.; Cai, Q.; Mei, S.; Gao, L.; Zhou, Y. Identification of promoter exchange at a male fertility restorer locus for cytoplasmic male sterility in radish (Raphanus sativus L.). Mol. Breed. 2017, 37, 82. [Google Scholar] [CrossRef]
- Goldberg, R.B.; Beals, T.P.; Snaders, P.M. Anhter development: Basic principles and practical applications. Plant Cell 1993, 5, 1217–1229. [Google Scholar]
- Liu, H.; Kang, J.; Xie, J.; Jian, Y.; Ding, Y. Cloning an expression of an Ogu CMS-related anther-preferential transcription factor in Brassica oleracea. Acta Hortic. Sin. 2010, 37, 1953–1960. (In Chinese) [Google Scholar]
- Guo, Y.; Xie, J.; Jian, Y.; Yu, J.; Kang, J. Cloning and functional analysis of Ogu CMS-related gene BoMF1 Promoter in Brassica oleracea. Acta Hortic. Sin. 2013, 40, 887–895. (In Chinese) [Google Scholar]
- Kang, J.; Guo, Y.; Chen, Y.; Li, H.; Zhang, L.; Liu, H. Upregulation of the AT-hook DNA binding gene BoMF2 in OguCMS anthers of Brassica oleracea suggests that it encodes a transcriptional regulatory factor for anther development. Mol. Biol. Rep. 2014, 41, 512–527. [Google Scholar] [CrossRef]
- Zhang, L.; Kang, Z.; Liu, H.; Kang, J. Cloning and expression of an Ogura cytoplasmic male sterile (Ogu CMS) related MYB transcription factor in Brassica oleracea var. capitata. J. Agric. Biotech. 2012, 20, 627–635. (In Chinese) [Google Scholar]
- Chen, Y.; Xie, J.; Guo, Y.; Kang, J. Transcriptional activation analysis of an OguCMS-related gene BoMYB1 in Brassica oleracea. Acta Agric. Boreal. Occident. Sin. 2014, 23, 120–126. (In Chinese) [Google Scholar]
- Yan, H.; Fang, Z.; Liu, Y.; Yang, L.; Zhuang, M.; Zhang, Y. In vitro conservation technique for the dominant genic male sterile materials in cabbage. Chin. J. Trop. Agric. 2013, 33, 35–39. (In Chinese) [Google Scholar]
- Yu, H.; Fang, Z.; Liu, Y.; Yang, L.; Zhuang, M.; Lv, H.; Li, Z.; Han, F.; Liu, X.; Zhang, Y. Development of a novel allele-specific Rfo marker and creation of Ogura CMS fertility-restored interspecific hybrids in Brassica oleracea. Theor. Appl. Genet. 2016, 129, 1625–1637. [Google Scholar] [CrossRef]
- Ren, W.; Li, Z.; Han, F.; Zhang, B.; Li, X.; Fang, Z.; Yang, L.; Zhuang, M.; Lv, H.; Liu, Y.; et al. Utilization of Ogura CMS germplasm with the clubroot resistance gene by fertility restoration and cytoplasm replacement in Brassica oleracea L. Hortic. Res. 2020, 7, 61. [Google Scholar] [CrossRef] [PubMed]
- Ullstrup, A.J. The impact of the southern corn leaf blight of epidemics 1970–1971. Annu. Rev. Phytopathol. 1972, 10, 37–50. [Google Scholar] [CrossRef]
- Kempken, F. Engineered Male Sterility. In Genetic Modification of Plants. Biotechnology in Agriculture and Forestry; Kempken, F., Jung, C., Eds.; Springer: Berlin/Heidelberg, Germany, 2010; Volume 64. [Google Scholar] [CrossRef]
- Mariani, C.; Beuckeleer, M.D.; Truettner, J.; Leemans, J.; Goldberg, R. Induction of male sterility in plants by a chimeric ribonuclease gene. Nature 1990, 347, 737–741. [Google Scholar] [CrossRef]
- Reynaerts, A.; van de Wiele, H.; de Sutter, G.; Janssens, J. Engineered genes for fertility control and their application in hybrid seed production. Sci. Hortic. 1993, 55, 125. [Google Scholar] [CrossRef]
- Shen, G.; Wang, X.; Zhu, Y.; Yang, H.; Lu, G.; Wang, J.; Wan, X.; Zhang, J. Male sterile transgenic cabbage plants with TA29-barnase gene. Acta Phytophysiol. Sin. 2001, 27, 43–48. (In Chinese) [Google Scholar]
- He, Y.; Xiong, X.; Guan, C.; Li, X.; Lin, L.; Chen, S.; Liu, Z.; Li, W.; Zhong, J.; Liu, C.; et al. The pTA29-Barnase chimeric gene transformation of Brassica napus mediated by agrobacterium. Acta Agron. Sin. 2003, 29, 615–620. (In Chinese) [Google Scholar]
- Li, C.; He, S.; Lan, C.; Ren, X.; Si, J.; Li, C.; Song, H. Transgenic male sterile cabbage plants induced by BcA9-Barnase transformation. J. SW Univ. 2015, 37, 52–58. (In Chinese) [Google Scholar]
- Curtis, I.S.; He, C.; Scott, R.; Power, J.B.; Davey, M.R. Genomic male sterility in lettuce, a base line for the production of F1 hybrids. Plant Sci. 1996, 113, 113–119. [Google Scholar] [CrossRef]
- He, S.; Abad, A.R.; Gelvin, S.B.; Mackenzie, S.A. A cytoplasmic male sterility-associated mitochondrial protein causes pollen disruption in transgenic tobacco. Proc. Natl. Acad. Sci. USA 1996, 93, 11763–11768. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Y.H.; Shewry, P.H.; Barcelo, P.; Lazzeri, P.A.; Halfold, N.G. Expression of antisense SnRK1 protein kinase sequence causes abnormal pollen development and male sterility in transgenic barley. Plant J. 2001, 28, 431–441. [Google Scholar] [CrossRef] [Green Version]
- Perez-Prat, E.; van Lookeren Campagne, M. Hybrid seed production and the challenge of propagating male-sterile plants. Trends Plant Sci. 2002, 7, 199–203. [Google Scholar] [CrossRef]
- Brink, K.; Crowgey, E.; Dietrich, N.; Hondred, D.; Young, J.K.; Zhong, C.X. Plant Genome DNA Flanking SPT Event and Methods for Identifying SPT Event. U.S. Patent No. 8,257,930, 4 September 2012. [Google Scholar]
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Ji, J.; Huang, J.; Yang, L.; Fang, Z.; Zhang, Y.; Zhuang, M.; Lv, H.; Wang, Y.; Liu, Y.; Li, Z.; et al. Advances in Research and Application of Male Sterility in Brassica oleracea. Horticulturae 2020, 6, 101. https://doi.org/10.3390/horticulturae6040101
Ji J, Huang J, Yang L, Fang Z, Zhang Y, Zhuang M, Lv H, Wang Y, Liu Y, Li Z, et al. Advances in Research and Application of Male Sterility in Brassica oleracea. Horticulturae. 2020; 6(4):101. https://doi.org/10.3390/horticulturae6040101
Chicago/Turabian StyleJi, Jialei, Jianxin Huang, Limei Yang, Zhiyuan Fang, Yangyong Zhang, Mu Zhuang, Honghao Lv, Yong Wang, Yumei Liu, Zhansheng Li, and et al. 2020. "Advances in Research and Application of Male Sterility in Brassica oleracea" Horticulturae 6, no. 4: 101. https://doi.org/10.3390/horticulturae6040101
APA StyleJi, J., Huang, J., Yang, L., Fang, Z., Zhang, Y., Zhuang, M., Lv, H., Wang, Y., Liu, Y., Li, Z., & Han, F. (2020). Advances in Research and Application of Male Sterility in Brassica oleracea. Horticulturae, 6(4), 101. https://doi.org/10.3390/horticulturae6040101