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Recent Advances in Cytoplasmic Male Sterility (CMS) in Crop Brassicas

  • Hitesh Kumar
  • Javed Akhatar
  • Shabir Hussain Wani
Chapter
  • 39 Downloads

Abstract

Brassicas are widely used for different purposes as vegetable oil, condiments, vegetables, biofuels, and animal feed. The cultivated rapeseed-mustard species are adapted in diverse agro-climatic situation ranged from warmer semitropical to cooler temperate regions of the world represented in China, Canada, India, Germany, the UK, France, Australia, Poland, and the USA. Cytoplasmic male sterility (CMS) is one of the extensively studied and useful examples of nucleo-cytoplasmic interactions. CMS is attributed by failure of plant to produce functional/viable pollen grain. CMS is a consequence of conflict/miscoordination between the organelles (mitochondria) and nuclear genes that arises due to instinctively mutation mt DNA and production of alloplasmic substitutions with widely differentiated wild spp. In this chapter, we will discuss the various cytoplasmic male sterility systems with fertility restorer (Rf) genes and advancement in the understanding of fertility restoration mechanism of fertility restorer genes.

Keywords

Cytoplasmic male sterile Fertility restorer Mitochondria Brassica genome High-throughput sequencing Hybrid breeding 

References

  1. Atri C, Kaur B, Sharma S et al (2016) Substituting nuclear genome of Brassica juncea (L.) Czern & Coss. In cytoplasmic background of Brassica fruticulosa results in cytoplasmic male sterility. Euphytica 209(1):31–40CrossRefGoogle Scholar
  2. Ba Q, Zhang G, Niu N, Ma S, Wang J (2015) Cytoplasmic effects on DNA methylation between male sterile lines and the maintainer in wheat (Triticum aestivum L.). Gene 549:192–197CrossRefGoogle Scholar
  3. Banga SS (1993) Heterosis and utilization. In: Labana KS, Banga SS, Banga SK (eds) Breeding oilseed brassicas. Monographs on theoretical and applied genetics, vol 19. Springer, Berlin, pp 21–43CrossRefGoogle Scholar
  4. Banga SS, Banga SK (1997) Enarthrocarpus lyratus cytoplasm causes male sterility in oilseed rape. In: The genetics and exploitation of heterosis in crops. Abs. CIMMYT international symposium, Mexico, 7–22 Aug 1997, pp 120–121Google Scholar
  5. Banga S, Kumar PR, Bhajan R, Singh D, Banga SS (2015) Genetics and breeding. In: Kumar A, Banga SS, Meena PD, Kumar PR (eds) Brassica oilseeds: breeding and management. CABI, Wallingford, pp 11–41CrossRefGoogle Scholar
  6. Bannerot H, Boulidard L, Cauderon Y, Temp J. (1974) Transfer of cytoplasmic male sterility from Raphanus sativus to Brassica oleracea. In: Eucarpia Meeting Cruciferae, Dundee, Scotland, pp 52–54Google Scholar
  7. Bentolila S, Alfonso AA, Hanson MR (2002) A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants. Proc Natl Acad Sci U S A 99(16):10887–10892PubMedPubMedCentralCrossRefGoogle Scholar
  8. Bird A (2007) Perceptions of epigenetics. Nature 447:396–398PubMedCrossRefPubMedCentralGoogle Scholar
  9. Bisht DS, Chamola R, Nath M, Bhat SR (2015) Molecular mapping of fertility restorer gene of an alloplasmic CMS system in Brassica juncea containing Moricandia arvensis cytoplasm. Mol Breed 35:14CrossRefGoogle Scholar
  10. Bohra A, Singh IP, Yadav AK, Pathak A, Soren KR, Chaturvedi SK, Nadarajan N (2015) Utility of informative SSR markers in the molecular characterization of cytoplasmic genetic male sterility-based hybrid and its parents in pigeonpea. Natl Acad Sci Lett 38:13–19CrossRefGoogle Scholar
  11. Brown GG, Formanová N, Jin H et al (2003) The radish Rfo restorer gene of Ogura cytoplasmic male sterility encodes a protein with multiple pentatricopeptide repeats. Plant J 35:262–272PubMedCrossRefPubMedCentralGoogle Scholar
  12. Budar F, Touzet P, De Paepe R (2003) The nucleo-mitochondrial conflict in cytoplasmic male sterilities revisited. Genetica 117:3–16PubMedCrossRefPubMedCentralGoogle Scholar
  13. Chase CD (2007) Cytoplasmic male sterility: a window to the world of plant mitochondrial-nuclear interactions. Trends Genet 23:81–90PubMedCrossRefPubMedCentralGoogle Scholar
  14. Chen L, Liu YG (2014) Male sterility and fertility restoration in crops. Annu Rev Plant Biol 65:579–606CrossRefGoogle Scholar
  15. Dahan J, Mireau H (2013) The Rf and Rf-like PPR in higher plants, a fast-evolving subclass of PPR genes. RNA Biol 10(9):1469–1476PubMedPubMedCentralCrossRefGoogle Scholar
  16. Deol S, Shivanna JR, Prakash K, Banga SS, Robbelen G (2008) Enarthrocarpus lyratus-based cytoplasmic male sterility and fertility restorer system in Brassica rapa. Plant Breed 122:438–440CrossRefGoogle Scholar
  17. Dieterich JH, Braun HP, Schmitz UK (2003) Alloplasmic male sterility in Brassica napus (CMS ‘Tournefortii-Stiewe’) is associated with a special gene arrangement around a novel atp9 gene. Mol Genet Genomics 269(6):723–731PubMedCrossRefPubMedCentralGoogle Scholar
  18. Ding X, Li J, Zhang H, He T, Han S, Li Y, Yang S, Gai J (2016) Identification of miRNAs and their targets by high-throughput sequencing and degradome analysis in cytoplasmic male-sterile line NJCMS1A and its maintainer NJCMS1B of soybean. BMC Genomics 17:24PubMedPubMedCentralCrossRefGoogle Scholar
  19. Fan Z, Stefansson BR, Sernyk JL (1986) Maintainers and restorers for three male-sterility-inducing cytoplasms in rape (Brassica napus L.). Can J Plant Sci 66:229–234CrossRefGoogle Scholar
  20. Feng Y, Zheng Q, Song H, Wang Y, Wang H, Jiang L, Zheng Y, Yue B (2015) Multiple loci not only Rf3 involved in the restoration ability of pollen fertility, anther exsertion and pollen shedding to S type cytoplasmic male sterile in maize. Theor Appl Genet 128:2341–2350PubMedCrossRefPubMedCentralGoogle Scholar
  21. Flavell R (1974) A model for the mechanism of cytoplasmic male sterility in plants, with special reference to maize. Plant Sci Lett 3(4):259–263CrossRefGoogle Scholar
  22. Food and Agriculture Organization (FAO) (2017) FAOSTAT statistical database of the United Nation Food and Agriculture Organization (FAO) Statistical Division, Rome. Available at: http://www.fao.org/faostat/en/#data/QC. Accessed Jan 2019
  23. Fu TD (1981) Production and research of rapeseed in the People’s Republic of China. Eucarpia Cruciferae Newslett 6:6–7Google Scholar
  24. Fu TD, Yang GS, Yang N (1987) Some investigation on Polima cytoplasmic male sterility in B. napus. Eucarpia Cruciferae Newslett 12:46–47Google Scholar
  25. Fujii S, Toriyama K (2008) Genome barriers between nuclei and mitochondria exemplified by cytoplasmic male sterility. Plant Cell Physiol 49:1484–1494PubMedPubMedCentralCrossRefGoogle Scholar
  26. Gaborieau L, Brown GG (2016) Comparative genomic analysis of the compound Brassica napus Rf locus. BMC Genomics 17(1):834PubMedPubMedCentralCrossRefGoogle Scholar
  27. Grelon M, Bonhomme FBS, Pelletier G (1994) Ogura cytoplasmic male-sterility [CMS]-associated orf138 is translated into a mitochondrial membrane polypeptide in male-sterile Brassica cybrids. Mol Gen Genet 243:540–547PubMedCrossRefPubMedCentralGoogle Scholar
  28. Hanson MR, Bentolila S (2004) Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16:154–169CrossRefGoogle Scholar
  29. Heng S, Wei C, Jing B, Wan Z, Wen J, Yi B, Ma C, Tu J, Fu T, Shen J (2014) Comparative analysis of mitochondrial genomes between the hau cytoplasmic male sterility (CMS) line and its iso-nuclear maintainer line in Brassica juncea to reveal the origin of the CMS-associated gene orf288. BMC Genomics 15:322PubMedPubMedCentralCrossRefGoogle Scholar
  30. Heng S, Liu S, Xia C, Tang HY, Xie F, Fu T, Wan Z (2018a) Morphological and genetic characterization of a new cytoplasmic male sterility system (oxa CMS) in stem mustard (Brassica juncea). Theor Appl Genet 131(1):59–66PubMedCrossRefPubMedCentralGoogle Scholar
  31. Heng S, Liu S, Xia C et al (2018b) Morphological and genetic characterization of a new cytoplasmic male sterility system (oxa CMS) in stem mustard (Brassica juncea). Theor Appl Genet 131(1):59–66PubMedCrossRefPubMedCentralGoogle Scholar
  32. Heyn FW (1976) Transfer of restorer genes from Raphanus to cytoplasmic male sterile Brassica napus. Cruciferae Newslett 1:15–16Google Scholar
  33. Horn R, Gupta KJ, Colombo N (2014) Mitochondrion role in molecular basis of cytoplasmic male sterility. Mitochondrion 19:198–205CrossRefGoogle Scholar
  34. Hu X, Sullivan-Gilbert M, Kubik T, Danielson J, Hnatiuk N, Marchione W, Greene T, Thompson S (2008) Mapping of the Ogura fertility restorer gene Rfo and development of Rfo allele-specific markers in canola (Brassica napus L.). Mol Breed 22:663–674CrossRefGoogle Scholar
  35. Hu J, Huang W, Huang Q, Qin X, Dan Z, Yao G, Zhu R, Zhu Y (2013) The mechanism of ORFH79 suppression with the artificial restorer fertility gene Mt-GRP162. New Phytol 199:52–58PubMedCrossRefPubMedCentralGoogle Scholar
  36. Ichii M, Hong DL, Ohara Y, Zhao CM, Taketa S (2003) Characterization of CMS and maintainer lines in indica rice (Oryza sativa L.) based on RAPD marker analysis. Euphytica 129:249–252CrossRefGoogle Scholar
  37. Janeja HS, Banga SK, Bhasker PB, Banga SS (2003) Alloplasmic male sterile Brassica napus with Enarthrocarpus lyratus cytoplasm: introgression and molecular mapping of an E. Lyratus chromosome segment carrying a fertility restoring gene. Genome 46:792–797PubMedCrossRefPubMedCentralGoogle Scholar
  38. Jarl CI, Bornman CH (1988) Correction of chlorophyll-defective, male sterile winter oilseed rape (Brassica napus) through organelle exchange: phenotypic evaluation of progeny. Hereditas 108:97–102CrossRefGoogle Scholar
  39. Jiang H, Feng Y, Bao L et al (2012) Improving blast resistance of Jin 23B and its hybrid rice by marker-assisted gene pyramiding. Mol Breed 30:1679–1688CrossRefGoogle Scholar
  40. Kang L, Li P, Wang A, Ge X, Li Z (2017) A novel cytoplasmic male sterility in Brassica napus (inap CMS) with Carpelloid Stamens via protoplast fusion with Chinese Woad. Front Plant Sci 8:529PubMedPubMedCentralGoogle Scholar
  41. Kirti PB, Narasimhulu SB, Mohapatra T, Prakash S, Chopra VL (1993) Correction of chlorophyll deficiency in alloplasmic male sterile Brassica juncea through recombination between chloroplast genome. Genet Res 62:11–14CrossRefGoogle Scholar
  42. Kirti PB, Banga SS, Prakash S, Chopra VL (1995a) Transfer of Ogu cytoplasmic male sterility to Brassica juncea and improvement of male sterile through somatic cell fusion. Theor Appl Genet 91:517–521PubMedCrossRefPubMedCentralGoogle Scholar
  43. Kirti PB, Mohapatra T, Prakash S, Chopra VL (1995b) Development of a stable cytoplasmic male sterile line of Brassica juncea from the somatic hybrid Trachystoma balli + Brassica juncea. Plant Breed 113:21–24Google Scholar
  44. Koizuka N, Imai R, Fujimoto H, Hayakawa T, Kimura Y, Kohno-Murase J, Sakai T, Kawasaki S, Imamura J (2003) Genetic characterization of a pentatricopeptide repeat protein gene, orf687, that restores fertility in the cytoplasmic male-sterile Kosena radish. Plant J 34:407–415PubMedCrossRefPubMedCentralGoogle Scholar
  45. Kubo T, Kitazaki K, Matsunaga M, Kagami H, Mikami T (2011) Male sterility-inducing mitochondrial genomes: how do they differ? Crit Rev Plant Sci 30:378–400CrossRefGoogle Scholar
  46. Kumar P, Vasupalli N, Srinivasan R, Bhat SR (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 63:2921–2932PubMedCrossRefPubMedCentralGoogle Scholar
  47. L’Homme Y, Stahl RJ, Xiu-Qing Li Hameed A, Brown GG (1997) Brassica napus cytoplasmic male sterility is associated with expression of a mtDNA region containing a chimeric gene similar to the pol CMS-associated orf224 gene. Curr Genet 31:325–335PubMedCrossRefPubMedCentralGoogle Scholar
  48. Labana KS, Banga SS (1984) Floral biology in Indian mustard (Brassica juncea (L.) Coss). Genet Agrar 38:131–138Google Scholar
  49. Landgren M, Zetterstrand M, Sundberg E, Glimelius K (1996) Alloplasmic male-sterile Brassica lines containing B. tournefortii mitochondria express an ORF 3′ of the atp6gene and a 32 kDa protein Plant. Mol Biol 32(5):879–890CrossRefGoogle Scholar
  50. Langer S, Longin CFH, Wurschum T (2014) Phenotypic evaluation of floral traits with relevance for hybrid breeding in wheat (Triticum aestivum L.). Plant Breed 133:433–441CrossRefGoogle Scholar
  51. Liu H, Cui P, Zhan K et al (2011) Comparative analysis of mitochondrial genomes between a wheat K-type cytoplasmic male sterility line and its maintainer line. BMC Genomics 12:163PubMedPubMedCentralCrossRefGoogle Scholar
  52. Liu Z, Liu P, Long F, Hong D, He Q, Yang G (2012) Fine mapping and candidate gene analysis of the nuclear restorer gene Rfp for pol CMS in rapeseed (Brassica napus L.). Theor Appl Genet 125:773–779PubMedCrossRefPubMedCentralGoogle Scholar
  53. Liu Z, Dong F, Wang X, Wang T, Su R, Hong D, Yang G (2017) A pentatricopeptide repeat protein restores nap cytoplasmic male sterility in Brassica napus. J Exp Bot 68(15):4115–4123PubMedPubMedCentralCrossRefGoogle Scholar
  54. Longin CF, Reif JC, Wurschum T (2014) Long-term perspective of hybrid versus line breeding in wheat based on quantitative genetic theory. Theor Appl Genet 127:1635–1641PubMedCrossRefPubMedCentralGoogle Scholar
  55. 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 YG (2013) A detrimental mitochondrial-nuclear interaction causes cytoplasmic male sterility in rice. Nat Genet 45(5):573–577PubMedCrossRefPubMedCentralGoogle Scholar
  56. Menczel L, Morgan A, Brown S, Maliga P (1987) Fusion-mediated combination of Ogura-type cytoplasmic male sterility with Brassica napus plastids using X-irradiated CMS protoplasts. Plant Cell Rep 6:98–101PubMedPubMedCentralGoogle Scholar
  57. Murayama S, Yamagishi H, Terachi T (1999) Identification of RAPD and SCAR markers linked to a restorer gene for Ogura cytoplasmic Male sterility in radish (Raphanus sativus L.) by bulked segregant analysis. Breed Sci 49:115–121CrossRefGoogle Scholar
  58. U (1935) Genome analysis in Brassica with special reference to the experimental formation of B. Napus and peculiar mode of fertilization. Jpn J Bot 7:389–452Google Scholar
  59. Ngangkham U, Parida SK, De S, Kumar KAR, Singh AK, Singh NK, Mohapatra T (2010) Genic markers for wild abortive (WA) cytoplasm based male sterility and its fertility restoration in rice. Mol Breed 26:275–292CrossRefGoogle Scholar
  60. Ogura H (1968) Studies on the new male sterility in Japanese radish, with special references to the utilization of this sterility towards the practical raising of hybrid seeds. Mem Fac Agric Kagoshima Univ 6:39–78Google Scholar
  61. Okazaki M, Kazama T, Murata H, Motomura K, Toriyama K (2013) Whole mitochondrial genome sequencing and transcriptional analysis to uncover an RT102-type cytoplasmic male sterility-associated candidate gene derived from Oryza rufipogon. Plant Cell Physiol 54:1560–1568PubMedCrossRefPubMedCentralGoogle Scholar
  62. Pathania A, Bhat SR, Dinesh Kumar V et al (2003) Cytoplasmic male sterility in alloplasmic Brassica juncea carrying Diplotaxis catholica cytoplasm: molecular characterization and genetics of fertility restoration. Theor Appl Genet 107(3):455–461PubMedCrossRefPubMedCentralGoogle Scholar
  63. Pei X, Jing Z, Tang Z, Zhu Y (2017) Comparative transcriptome analysis provides insight into differentially expressed genes related to cytoplasmic male sterility in broccoli (Brassica oleracea var. italica). Sci Hortic 217:234–242CrossRefGoogle Scholar
  64. Pelletier G, Primard C, Vedel F, Chétrit P, Rémy R, Rousselle P, Renard M (1983) Intergeneric cytoplasmic hybridization in Cruciferae by protoplast fusion. Mol Gen Genet 191:244–250CrossRefGoogle Scholar
  65. Prakash S, Chopra VL (1988) Synthesis of alloplasmic Brassica campestris as a new source of cytoplasmic male sterility. Plant Breed 101:253–255CrossRefGoogle Scholar
  66. Prakash S, Kirti PB, Bhat SR, Gaikwad K, Kumar VD, Chopra VL (1998a) A Moricandia arvensis-based cytoplasmic male sterility and fertility restoration system in Brassica juncea. Theor Appl Genet 97:488–492CrossRefGoogle Scholar
  67. Prakash S, Kirti P, Bhat S et al (1998b) A Moricandia arvensis–based cytoplasmic male sterility and fertility restoration system in Brassica juncea. Theor Appl Genet 97(3):488–492CrossRefGoogle Scholar
  68. Prakash S, Ahuja I, Upreti HC, Dinesh Kumar V, Bhat SR, Kirti PB, Chopra VL (2001) Expression of male sterility in allplasmic Brassica juncea with Erucastrum canariense cytoplasm and the development of a fertility restorer system. Plant Breed 120:479–482CrossRefGoogle Scholar
  69. Rao GU, Batra VS, Prakash S, Shivanna KR (1994) Development of a new cytoplasmic male sterility system in Brassica juncea through wide hybridization. Plant Breed 112:171–174CrossRefGoogle Scholar
  70. Rawat DS, Anand IJ (1979) Male sterility in Indian mustard. J Genet Plant Breed 39:412–415Google Scholar
  71. Sabar M, Gagliardi D, Balk J, Leaver CJ (2003) ORFB is a subunit of F1F(O)-ATP synthase: insight into the basis of cytoplasmic male sterility in sunflower. EMBO Rep 4:381–386PubMedPubMedCentralCrossRefGoogle Scholar
  72. Sarria R, Lyznik A, Vallejos CE, Mackenzie SA (1998) A cytoplasmic male sterility–associated mitochondrial peptide in common bean is post-translationally regulated. Plant Cell 10:1217–1228PubMedPubMedCentralGoogle Scholar
  73. Sheeba NK, Viraktamath BC, Sivaramakrishnan S, Gangashetti MG, Khera P, Sundaram RM (2009) Validation of molecular markers linked to fertility restorer gene(s) for WA-CMS lines of rice. Euphytica 167:217–227CrossRefGoogle Scholar
  74. Shi HQ, Gong RF, Zhuan LL, Long XP (1991) Studies on the utilization of heterosis in mustard (Brassica juncea). Acta Agron Sin 17:32–41Google Scholar
  75. Shinada T, Kikuchi Y, Fujimoto R, Kishitani S (2006) An alloplasmic male-sterile line of Brassica oleracea harboring the mitochondria from Diplotaxis muralis expresses a novel chimeric open reading frame, orf72. Plant Cell Physiol 47(4):549–553PubMedCrossRefPubMedCentralGoogle Scholar
  76. Tan Y, Xu X, Wang C, Cheng G, Li S, Liu X (2015) Molecular characterization and application of a novel cytoplasmic male sterility-associated mitochondrial sequence in rice. BMC Genet 16:45PubMedPubMedCentralCrossRefGoogle Scholar
  77. Tang CY, Yang MK, Wu FY, Zhao H, Pang YJ, Yang RW, Lu GH, Yang YH (2015) Identification of miRNAs and their targets in transgenic Brassica napus and its acceptor (Westar) by high-throughput sequencing and degradome analysis. RSC Adv 5:85383–85394CrossRefGoogle Scholar
  78. Tian E, Roslinsky V, Cheng B (2014) Molecular marker-assisted breeding for improved Ogura cms restorer line (RfoRfo) and mapping of the restorer gene (Rfo) in Brassica juncea. Molecular Breed 34(3):1361–1371CrossRefGoogle Scholar
  79. Touzet P, Meyer EH (2014) Cytoplasmic male sterility and mitochondrial metabolism in plants. Mitochondrion 19:166–171PubMedCrossRefPubMedCentralGoogle Scholar
  80. Walters TW, Mutschler MA, Earle ED (1992) Protoplast fusion-derived Ogura male sterile cauliflower with cold tolerance. Plant Cell Rep 10(12):624–628PubMedCrossRefPubMedCentralGoogle Scholar
  81. Warmke HE, Lee SL (1978) Pollen abortion in T cytoplasmic male-sterile corn (Zea mays): a suggested mechanism. Science 200:561–563PubMedCrossRefPubMedCentralGoogle Scholar
  82. Xie F, He Z, Esguerra MQ, Qiu F, Ramanathan V (2013) Determination of heterotic groups for tropical Indica hybrid rice germplasm. Theor Appl Genet 127:407–417CrossRefGoogle Scholar
  83. Yang JH, Zhang MF, Yu JQ, Zhang S, Wang T, Chen ZJ (2005) Identification of alloplasmic cytoplasmic male-sterile line of leaf mustard synthesized by intra-specific hybridization. Plant Sci 168:865–871CrossRefGoogle Scholar
  84. Yang J, Liu X, Xu B, Zhao N, Yang X, Zhang M (2013) Identification of miRNAs and their targets using high-throughput sequencing and degradome analysis in cytoplasmic male-sterile and its maintainer fertile lines of Brassica juncea. BMC Genome 14:9CrossRefGoogle Scholar
  85. Yuan LP (1985) A concise course in hybrid rice. Hunan Science and Technology Publishing House, Hunan, p 168Google Scholar
  86. Zhang H, Wu J, Dai Z, Qin M, Hao L, Ren Y, Li Q, Zhang L (2017) Allelism analysis of BrRfp locus in different restorer lines and map-based cloning of a fertility restorer gene, BrRfp1, for pol CMS in Chinese cabbage (Brassica rapa L.). Theor Appl Genet 130(3):539–547PubMedCrossRefPubMedCentralGoogle Scholar

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© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Banda University of Agriculture and TechnologyBandaIndia
  2. 2.Punjab Agricultural UniversityLudhianaIndia
  3. 3.Mountain Research Centre for Field Crops, Sher-e-Kashmir University of Agricultural Sciences and Technology of KashmirKhudwaniIndia

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