Skip to main content
Log in

Cytoplasmic male sterility (CMS) in hybrid breeding in field crops

  • Review
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

A comprehensive understanding of CMS/Rf system enabled by modern omics tools and technologies considerably improves our ability to harness hybrid technology for enhancing the productivity of field crops.

Abstract

Harnessing hybrid vigor or heterosis is a promising approach to tackle the current challenge of sustaining enhanced yield gains of field crops. In the context, cytoplasmic male sterility (CMS) owing to its heritable nature to manifest non-functional male gametophyte remains a cost-effective system to promote efficient hybrid seed production. The phenomenon of CMS stems from a complex interplay between maternally-inherited (mitochondrion) and bi-parental (nucleus) genomic elements. In recent years, attempts aimed to comprehend the sterility-inducing factors (orfs) and corresponding fertility determinants (Rf) in plants have greatly increased our access to candidate genomic segments and the cloned genes. To this end, novel insights obtained by applying state-of-the-art omics platforms have substantially enriched our understanding of cytoplasmic-nuclear communication. Concomitantly, molecular tools including DNA markers have been implicated in crop hybrid breeding in order to greatly expedite the progress. Here, we review the status of diverse sterility-inducing cytoplasms and associated Rf factors reported across different field crops along with exploring opportunities for integrating modern omics tools with CMS-based hybrid breeding.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abratti G, Bazzalo ME, Leon A (2008) Mapping a novel fertility restoration gene in sunflower. In: Velasco editor.17th International Sunflower Conference, Cordoba, Spain. pp 617–621

  • Ahmadikhah A, Karlov GI (2006) Molecular mapping of the fertility-restoration gene Rf4 for WA-cytoplasmic male sterility in rice. Plant Breed 125:363–367

    Article  CAS  Google Scholar 

  • Ahmadikhah A, Mirarb M, Pahlevani MH, Nayyeripasand L (2015) Marker-assisted backcrossing (MABC) using CMS-specific, SSR and ISSR markers to develop an elite CMS line in rice. Plant Genome 8:2

    Article  Google Scholar 

  • Ahmed TA, Tsujimoto H, Sasakuma T (2001) QTL analysis of fertility restoration against cytoplasmic male sterility in wheat. Genes Genet Syst 76:33–38

    Article  CAS  PubMed  Google Scholar 

  • Akagi H, Nakamura A, Yokozeki-Misono Y, Inagaki A, Takahashi H, Mori K, Fujimura T (2004) Positional cloning of the rice Rf-1 gene, a restorer of BT-type cytoplasmic male sterility that encodes a mitochondria-targeting PPR protein. Theor Appl Genet 108:1449–1457

    Article  CAS  PubMed  Google Scholar 

  • Allen JO, Fauron CM, Minx P et al (2007) Comparisons among two fertile and three male-sterile mitochondrial genomes of maize. Genetics 177:21173–21192

    Article  CAS  Google Scholar 

  • An H, Yang ZH, Yi B, Wen J, Shen JX, Tu JX, Ma C, Fu T (2014) Comparative transcript profiling of the fertile and sterile flower buds of pol CMS in B. napus. BMC Genom 15:258

    Article  CAS  Google Scholar 

  • Anisimova IN, Gavrilova VA, Rozhkova VT, Port AI, Timofeeva GI, Duka MV (2011) Genetic diversity of sources of sunflower pollen fertility restorer genes. Russ Agric Sci 37:192–196

    Article  Google Scholar 

  • Ariyanayagam RP, Rao AN, Zaveri PP (1993) Gene cytoplasmic male-sterility in pigeonpea. Int Pigeonpea Newsl 18:7–11

    Google Scholar 

  • Arya L, Verma M, Lakhanpaul S (2014) Diagnostic set of microsatellite markers for hybrid purity testing and molecular identification of hybrids and parental lines in sorghum. J Plant Sci Res 1:103

    Google Scholar 

  • Atri C, Kaur B, Sharma S, Gandhi N, Verma H, Goyal A, Banga SS (2016) Substituting nuclear genome of Brassica juncea (L.) Czern & Coss. in cytoplasmic background of Brassica fruticulosa results in cytoplasmic male sterility. Euphytica. 10.1007/s10681-015-1628-4

  • Aya K, Suzuki G, Suwabe K, Hobo T et al (2011) Comprehensive network analysis of anther-expressed genes in rice by the combination of 33 laser microdissection and 143 spatiotemporal microarrays. PLoS One 6:e26162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 549:192–197

    Article  CAS  Google Scholar 

  • Bai YN, Gai JY (2005) Inheritance of male fertility restoration of the cytoplasmic-nuclear male-sterile line NJCMS1A of soybean [Glycine max (L) Merr.]. Euphytica 145:25–32

    Article  CAS  Google Scholar 

  • Bassett MJ, Shuh DM (1982) Cytoplasmic male sterility in common bean. J Am Soc Hortic Sci 107:791–793

    Google Scholar 

  • Bazrkar L, Ali AJ, Babaein NA, Ebadi AA, Allahgholipour M, Kazemitabar K, Nematzadeh G (2008) Tagging of four fertility restorer loci for wild abortive—cytoplasmic male sterility system in rice (Oryza sativa L.) using microsatellite markers. Euphytica 164:669–677

    Article  CAS  Google Scholar 

  • Beckett J (1971) Classification of male sterile cytoplasms in maize. Crop Sci 11:724–726

    Google Scholar 

  • Bentolila S, Stefanov S (2012) A Reevaluation of rice mitochondrial evolution based on the complete sequence of male-fertile and male-sterile mitochondrial genomes. Plant Physiol 158:996–1017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bentolila S, Alfonso AA, Hanson MR (2002) A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants. Proc Natl Acad Sci USA 99:10887–10892

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berthelem P, Guen L (1974) Rapport d activite 1971-1974 INRA. Rennes, France, pp 119–163

    Google Scholar 

  • Bharaj TS, Bains SS, Sidhu GS, Gagneja MR (1991) Genetics of fertility restoration of ‘Wild Abortive’ cytoplasmic male sterility in rice, Oryza sativa L. Euphytica 56:199–203

    Article  Google Scholar 

  • Bharaj TS, Virmani SS, Khush GS (1995) Chromosomal location of fertility restoring genes for ‘wild abortive’ cytoplasmic male sterility using primary trisomics in rice. Euphytica 83:169–173

    Article  Google Scholar 

  • Bird A (2007) Perceptions of epigenetics. Nature 447:396–398

    Article  CAS  PubMed  Google Scholar 

  • Bisht D, 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 35:14

    Article  CAS  Google Scholar 

  • Bohra A, Mallikarjuna N, Saxena K, Upadhyaya H, Vales MI, Varshney RK (2010) Harnessing the potential of crop wild relatives through genomics tools for pigeonpea improvement. J Plant Biol 37:1–16

    Google Scholar 

  • Bohra A, Saxena RK, Gnanesh BN et al (2012) An intra specific consensus genetic map of pigeonpea [Cajanus cajan (L.) Millspaugh] derived from six mapping populations. Theor Appl Genet 125:1325–1338

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 38:13–19

    Article  CAS  Google Scholar 

  • Bond DA, Fyfe JL, Toynke-clarke G (1966) Male sterility with a cytoplasmic type of inheritance in field beans. J Agrl Sci Camb 66:359–367

    Article  Google Scholar 

  • Brown GG, Formanova 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 35:262–272

    Article  CAS  PubMed  Google Scholar 

  • Buchert JG (1961) The stage of the genome-plasmon interaction in the restoration of fertility to cytoplasmically pollen-sterile maize. Proc Natl Acad Sci USA 47:1436–1440

    Article  Google Scholar 

  • Budar F, Touzet P, Pelletier G (2006) Cytoplasmic male sterility. Annual Plant Review 20:148–170

    Google Scholar 

  • Burton GW (1958) Cytoplasmic male-sterility in pearl millet Pennisetum glaucum (L.). Agron J 50:230

    Article  Google Scholar 

  • Castillo A, Atienza SG, Martín AC (2014) Fertility of CMS wheat is restored by two Rf loci located on a recombined acrocentric chromosome. J Exp Bot 65:6667–6677

    Article  PubMed  PubMed Central  Google Scholar 

  • Castillo A, Rodríguez-Suárez C, Martín AC, Pistón F (2015) Contribution of chromosomes 1HchS and 6HchS to fertility restoration in the wheat msH1 CMS system under different environmental conditions. PLoS One 10:e0121479

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chase CD (2007) Cytoplasmic male sterility: a window to the world of plant mitochondrial-nuclear interactions. Trends Genet 23:81–90

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Liu YG (2014) Male sterility and fertility restoration in crops. Annu Rev Plant Biol 65:579–606

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Zhang Y, Liu XP, Chen BY, Tu JX, Fu TD (2007) Detection of QTL for six yield-related traits in oilseed rape (Brassica napus) using DH and immortalized F2 populations. Theor Appl Genet 115:849–858

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Guan R, Chang S, Du T, Zhang H, Xing H (2011) Substoichiometrically different mitotypes coexist in mitochondrial genomes of Brassica napus L. PLoS One 6:e17662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng S, Zhuang J, Fan Y, Du J, Cao L (2007) Progress in research and development on hybrid rice: a super-domesticate in China. Ann Bot 100:959–966

    Article  PubMed  PubMed Central  Google Scholar 

  • Clifton SW, Minx P, Fauron CM et al (2004) Sequence and comparative analysis of the maize NB mitochondrial genome. Plant Physiol 136:3486–3503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cui X, Wise RP, Schnable PS (1996) The rf2 restorer gene of male-sterile T-cytoplasm maize. Science 272:1334–1336

    Article  CAS  PubMed  Google Scholar 

  • Cui P, Liu H, Lin Q, Ding F et al (2009) A complete mitochondrial genome of wheat (Triticum aestivum cv. Chinese Yumai), and fast evolving mitochondrial genes in higher plants. J Genetics 88:299–307

    Article  CAS  Google Scholar 

  • Dahan J, Mireau H (2013) The Rf and Rf-like PPR in higher plants, a fast-evolving subclass of PPR genes. RNA Biol 10:1469–1476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dalmacio RD, Brar DS, Ishii T, Virmani SS (1995) Identification and transfer of a new cytoplasmic male sterility source from Oryza perennis into rice (O. sativa). Euphytica 82:221–225

    Article  Google Scholar 

  • Das P, Mukherjee B, Santra CK, Gupta S, Dasgupta T (2014) Agro-botanical Characterization of some released F1 hybrids in rice (Oryza sativa L.). Int J Sci Res 4:1–9

    CAS  Google Scholar 

  • Desloire S, Gherbi H, Laloui W et al (2003) Identification of the fertility restoration locus, Rfo, in radish, as a member of the pentatricopeptide-repeat protein family. EMBO Rep 4:588–594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dill CL, Wise RP, Schnable PS (1997) Rf8 and Rf* mediate unique T-urf13-transcript accumulation, revealing a conserved motif associated with RNA processing and restoration of pollen fertility in T-cytoplasm maize. Genetics 147:1367–1379

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ding DR, Gai JY, Cui ZL, Yang SP, Qiu JX (1998) Development and verification of the cytoplasmic-nuclear male sterile soybean line NJCMS1A and its maintainer NJCMS1B. Chin Sci Bull 44:191–192

    Article  Google Scholar 

  • 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 Genom 17:24

    Article  Google Scholar 

  • Dong DK, Li Z, Yuan FJ et al (2012) Inheritance and fine mapping of a restorer-of-fertility (Rf) gene for the cytoplasmic male sterility in soybean. Plant Sci 188:36–40

    Article  PubMed  CAS  Google Scholar 

  • Dudhe MY, Moon MK, Lande SS (2011) Study of gene action for restorer lines in Sunflower. Helia 34:159–164

    Article  Google Scholar 

  • Duvick DN (1965) Cytoplasmic pollen sterility in corn. Adv Genetics 13:1–56

    Article  Google Scholar 

  • Ejaz M, Qidi Z, Gaisheng Z, Qunzhu W, Xinbo Z (2013) Analysis of mitochondrial DNA using amplified fragment length polymorphism markers of isonuclear allocytoplasmic male sterile wheat accessions and their maintainer lines. Genet Mol Res 12:5207–5214

    Article  CAS  PubMed  Google Scholar 

  • Elkonin LA, Kozhemyakin VV, Ishin AG (1998) Nuclear-cytoplasmic interactions in restoration of male fertility in the ‘9E’ and A4 CMS-inducing cytoplasms of sorghum. Theor Appl Genet 97:626–632

    Article  Google Scholar 

  • Erichsen AW, Ross JG (1963) Irregularities at microsporogenesis in colchicine-induced male-sterile mutants in Sorghum vulgare Pers. Crop Sci 3:481–483

    Article  Google Scholar 

  • Feng J, Jan CC (2008) Introgression and molecular tagging of Rf4, a new male fertility restoration gene from wild sunflower Helianthus maximiliani L. Theor Appl Genet 117:241–249

    Article  CAS  PubMed  Google Scholar 

  • Feng J, Primomo V, Li Z, Zhang Y, Jan CC, Tulsieram L, Xu SS (2009) Physical localization and genetic mapping of the fertility restoration gene Rfo in canola (Brassica napus L.). Genome 52:401–407

    Article  CAS  PubMed  Google Scholar 

  • 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 128:2341–2350

    Article  CAS  PubMed  Google Scholar 

  • Ferreyra MLF, Rius SP, Casati P (2012) Flavonoids: biosynthesis, biological functions, and biotechnological applications. Front Plant Sci 3:222

    Google Scholar 

  • Fujii S, Toriyama K (2005) Molecular mapping of the fertility restorer gene for rice ms-CW-type cytoplasmic male sterility of rice. Theor Appl Genet 111:696–701

    Article  CAS  PubMed  Google Scholar 

  • Fujii S, Toriyama K (2008) Genome barriers between nuclei and mitochondria exemplified by cytoplasmic male sterility. Plant Cell Physiol 49:1484–1494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujii S, Toriyama K (2009) Suppressed expression of retrograde-regulated male sterility restores pollen fertility in cytoplasmic male sterile rice plants. Proc Natl Acad Sci USA 106:9513–9518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujii S, Kazama T, Yamada M, Toriyama K (2010) Discovery of global genomic re-organization based on comparison of two newly sequenced rice mitochondrial genomes with cytoplasmic male sterility-related genes. BMC Genom 11:209

    Article  CAS  Google Scholar 

  • Fujii S, Toda T, Kikuchi S, Suzuki R, Yokoyama K, Tsuchida H, Yano K, Toriyama K (2011) Transcriptome map of plant mitochondria reveals islands of unexpected transcribed regions. BMC Genom 12:279

    Article  Google Scholar 

  • Fujimura T, Akagi H, Oka M, Nakamura A, Sawada R (1996) Establishment of a rice protoplast culture and application of an asymmetric protoplast fusion technique to hybrid rice breeding. Plant Tissue Cult Lett 13:243–247

    Article  Google Scholar 

  • Chase CD, Gabay-Laughnan, S (2004) Cytoplasmic male sterility and fertility restoration by nuclear genes. In: Daniell H, Chase CD (ed), Molecular biology and biotechnology of plant organelles. Springer-Verlag, pp 593–622

  • Gabay-Laughnan S, Zabala G, Laughnan JR (1995) S-type cytoplasmic male sterility in maize. In: Levings CS, Vasil IK (eds) Advances in cellular and molecular biology of plants, Molecular biology of the mitochondria, vol 2., KluwerDordrecht, The Netherlands, pp 395–432

    Chapter  Google Scholar 

  • Gai JY, Cui ZL, Ji DF, Ren ZJ, Ding DR (1995) A report on the nuclear cytoplasmic male sterility from a cross between two soybean cultivars. Soybean Genet Newsl 22:55–58

    Google Scholar 

  • Gai JY, Ding DR, Cui ZL, Qiu JX (1999) Development and performance of the cytoplasmic-nuclear male-sterile line NJCMS1A of soybean. Sci Agric Sin 32:23–27

    Google Scholar 

  • Gentzbittel L, Vear F, Zhang YX, Berville A, Nicolas P (1995) Development of a consensus linkage RFLP map of cultivated sunflower (Helianthus annuus L.). Theor Appl Genet 90:1079–1086

    Article  CAS  PubMed  Google Scholar 

  • Gentzbittel L, Mestries E, Mouzeyar S, Mazeyrat F, Badaoui S, Vear F, Labrouhe TD, Nicolas P (1999) A composite map of expressed sequences and phenotypic traits of the sunflower (Helianthus annuus L.) genome. Theor Appl Genet 99:218–234

    Article  CAS  Google Scholar 

  • Gerland P, Raftery AE, Sevcikova H et al (2014) World population stabilization unlikely this century. Science 346:234–237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • German MA, Pillay M, Jeong DH et al (2008) Global identification of microRNA–target RNA pairs by parallel analysis of RNA ends. Nature Biotechnol 26:941–946

    Article  CAS  Google Scholar 

  • German MA, Luo S, Schroth G, Meyers BC, Green PJ (2009) Construction of parallel analysis of RNA ends (PARE) libraries for the study of cleaved miRNA targets and the RNA degradome. Nat Protoc 4:356–362

    Article  CAS  PubMed  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

  • Govinda R, Virmani SS (1988) Genetics of fertility restoration of ‘WA’ type cytoplasmic male sterility in rice. Crop Sci 28:787–792

    Article  Google Scholar 

  • Graybosch RA, Palmer RG (1985) Male sterility in soybean (Glycine max) I. Phenotypic expression of the ms2 mutant. Am J Bot 72:1738–1750

    Article  Google Scholar 

  • Griffiths-Jones S (2006) miRBase: the microRNA sequence database. Methods Mol Biol 342:129–138

    CAS  PubMed  Google Scholar 

  • Hanna WW (1989) Characteristics and stability of a new cytoplasmic-nuclear male-sterile source in pearl millet. Crop Sci 29:1457–1459

    Article  Google Scholar 

  • Hanson MR, Bentolila S (2004) Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16:S154–S169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hariprasanna K, Patil JV (2015) Sorghum: origin, classification, biology and improvement. In: Madhusudhana R, Rajendrakumar P, Patil JV (eds) Sorghum molecular breeding. Springer, India, pp 3–22

    Chapter  Google Scholar 

  • Havey M (2004) The use of cytoplasmic male sterility for hybrid seed production. In: Daniell H, Chase C (eds) Molecular biology and biotechnology of plant organelles. Springer Publishers, The Netherlands, pp 617–628

    Google Scholar 

  • Heng S, Wei C, Jing B et al (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 Genom 15:322

    Article  CAS  Google Scholar 

  • Hobo T, Suwabe K, Aya K et al (2008) Various spatiotemporal expression profiles of anther-expressed genes in rice. Plant Cell Physiol 49:1417–1428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horn R, Kusterer B, Lazarescu E, Prufe M, Friedt W (2003) Molecular mapping of the Rf1 gene restoring pollen fertility in PET1-based F1 hybrids in sunflower (Helianthus annuus L.). Theor Appl Genet 106:599–606

    CAS  PubMed  Google Scholar 

  • Horn R, Gupta KJ, Colombo N (2014) Mitochondrion role in molecular basis of cytoplasmic male sterility. Mitochondrion 19:198–205

    Article  CAS  PubMed  Google Scholar 

  • Hu X, Sulliva-Gilbert M, Kubik T, Danielson J, Hnatiuk N, Marchione W (2008) Mapping of the Ogura fertility restorer gene Rfo and development of Rfo allele-specific markers in canola (Brassica napus L.). Mol Breed 22:663–674

    Article  CAS  Google Scholar 

  • Hu J, Wang K, Huang W et al (2012) The rice pentatricopeptide repeat protein Rf5 restores fertility in Hong-Lian cytoplasmic male-sterile lines via a complex with the glycine-rich protein GRP162. Plant Cell 24:109–122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu J, Yi R, Zhang G, Ding Y (2013a) Nucleo-cytoplasmic interactions affect RNA editing of cox2, atp6 and atp9 in alloplasmic male-sterile rice (Oryza sativa L.) lines. Mitochondrion 13:87–95

    Article  CAS  PubMed  Google Scholar 

  • Hu J, Huang W, Huang Q, Qin X, Dan Z, Yao G, Zhu R, Zhu Y (2013b) The mechanism of ORFH79 suppression with the artificial restorer fertility gene Mt-GRP162. New Phytol 199:52–58

    Article  CAS  PubMed  Google Scholar 

  • Hu J, Huang W, Huang Q et al (2014) Mitochondria and cytoplasmic male sterility in plants. Mitochondrion 19:282–288

    Article  CAS  PubMed  Google Scholar 

  • Huang JZ, E ZG, Zhang HL, Shu QY (2014) Workable male sterility systems for hybrid rice: genetics, biochemistry, molecular biology, and utilization. Rice 7:13

  • Huang Q, He Y, Jing R, Zhu R, Zhu Y (2000) Mapping of the nuclear fertility restorer gene for HL cytoplasmic male sterility in rice using microsatellite markers. Chin Sci Bull 45:430–432

    Article  CAS  Google Scholar 

  • Huang J, Hu J, Xu X, Li S, Yi P, Yang D (2003) Fine mapping of the nuclear fertility restorer gene for HL cytoplasmic male sterility in rice. Bot Bull Acad Sin 44:285–289

    CAS  Google Scholar 

  • Huang MD, Caroline Hsing YI, Huang AHC (2011) Transcriptomes of the anther sporophyte: availability and uses. Plant Cell Physiol 9:1459–1466

    Article  CAS  Google Scholar 

  • Huang W, Hu J, Yu C et al (2012) Two non-allelic nuclear genes restore fertility in a gametophytic pattern and enhance abiotic stress tolerance in the hybrid rice plant. Theor Appl Genet 124:799–807

    Article  CAS  PubMed  Google Scholar 

  • Huang W, Yu C, Hu J et al (2015) Pentatricopeptide-repeat family protein RF6 functions with hexokinase 6 to rescue rice cytoplasmic male sterility. Proc Natl Acad Sci USA 112:14984–14989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 129:249–252

    Article  CAS  Google Scholar 

  • Ichikawa N, Kishimoto N, Inagaki A et al (1997) A rapid PCR-aided selection of a rice line containing the Rf-1 gene which is involved in restoration of the cytoplasmic male sterility. Mol Breed 3:195–202

    Article  CAS  Google Scholar 

  • Igarashi K, Kazama T, Motomura K, Toriyama K (2013) Whole genomic sequencing of RT98 mitochondria derived from Oryza rufipogon and northern blot analysis to uncover a cytoplasmic male sterility-associated gene. Plant Cell Physiol 54:237–243

    Article  CAS  PubMed  Google Scholar 

  • Ingale BV, Jambhale ND, Waghmode BD, Dalvi VV (2006) Sahyadri 2, an early rice hybrid for Maharashtra State in India. International Rice Research Notes 31:20–21

    Google Scholar 

  • Itabashi E, Iwata N, Fuji S, Kazama T, Toriyama K (2011) The fertility restorer gene, Rf2, for Lead Rice-type cytoplasmic male sterility of rice encodes a mitochondrial glycine-rich protein. Plant J 65:359–367

    Article  CAS  PubMed  Google Scholar 

  • Iwabuchi M, Kyozuka J, Shimamoto K (1993) Processing followed by complete editing of an altered mitochondrial atp6 RNA restores fertility of cytoplasmic male sterile rice. EMBO J 12:1437–1446

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jan CC, Vick BA, Miller JF, Kahler AL, Butler ET (1998) Construction of an RFLP linkage map for cultivated sunflower. Theor Appl Genet 96:15–22

    Article  CAS  Google Scholar 

  • Janeja HS, Banga SK, Bhaskar PB, Banga SS (2003a) 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 46:792–797

    Article  CAS  PubMed  Google Scholar 

  • Janeja HS, Banga SS, Lakshmikumaran M (2003b) Identification of AFLP markers linked to fertility restorer genes for tournefortii cytoplasmic male-sterility system in Brassica napus. Theor Appl Genet 107:148–154

    CAS  PubMed  Google Scholar 

  • Jean M, Brown GG, Landry BS (1997) Genetic mapping of nuclear fertility restorer genes for the ‘Polima’cytoplasmic male sterility in canola (Brassica napus L.) using DNA markers. Theor Appl Genet 95:321–328

    Article  CAS  Google Scholar 

  • Jenkins MT (1978) Maize breeding during the development and early years of hybrid maize. In: Walden B (ed) Maize breeding and genetics. John Wiley and Sons, New York, pp 13–28

    Google Scholar 

  • 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 30:1679–1688

    Article  CAS  Google Scholar 

  • Jordan DR, Mace ES, Henzell RG, Klien PE, Klein RR (2010) Molecular mapping and candidate gene identification of the Rf2 gene for pollen fertility restoration in sorghum (Sorghum bicolor (L.) Moench). Theor Appl Genet 120:1279–1287

    Article  CAS  PubMed  Google Scholar 

  • Jordan DR, Klein RR, Sakrewski KG, Henzell RG, Klein PE, Mace ES (2011) Mapping and characterization of Rf5: a new gene conditioning pollen fertility restoration in A1 and A2 cytoplasm in sorghum (Sorghum bicolor (L.) Moench). Theor Appl Genet 123:383–396

    Article  CAS  PubMed  Google Scholar 

  • Kalaimagal T, Muthaiah A, Rajarathinam S, Malini S, Nadarajan N, Pechiammal I (2008) Development of new cytoplasmic-genetic male-sterile lines in pigeonpea from crosses between Cajanus cajan (L.) Millsp. and C. scarabaeoides (L.) Thouars. J Appl Genet 49:221–227

    Article  PubMed  Google Scholar 

  • Kamps TL, Chase CD (1997) RFLP mapping of the maize gametophytic restorer of fertility locus (rf3) and aberrant pollen transmission of the nonrestoring rf3 allele. Theor Appl Genet 95:525–531

    Article  CAS  Google Scholar 

  • Kamps TL, McCarty DR, Chase CD (1996) Gametophytic genetics in Zea mays L.: dominance of a restoration-of-fertility allele (Rj3) in diploid pollen. Genetics 142:1001–1007

    CAS  PubMed  PubMed Central  Google Scholar 

  • Katsuo K, Mizushima U (1958) Studies on the cytoplasmic difference among rice varieties, Oryza sativa L. 1. On the fertility of hybrids obtained reciprocally between cultivated and wild varieties. Jpn J Breed 8:1–5

    Article  Google Scholar 

  • Kaul MLH (1988) Male sterility in higher plants Springer Science, The Netherlands

  • Kazama T, Toriyama K (2003) A pentatricopeptide repeat-containing gene that promotes the processing of aberrant atp6 RNA of cytoplasmic male-sterile rice. (Translated from Eng). FEBS Lett 544:99–102

    Article  CAS  PubMed  Google Scholar 

  • Kazama T, Toriyama K (2014) A fertility restorer gene, Rf4, widely used for hybrid rice breeding encodes a pentatricopeptide repeat protein. Rice 7:28

    Article  PubMed  Google Scholar 

  • Khan MH, Dar ZA, Dar SA (2015) Breeding strategies for improving rice yield—A review. Agric Sci 6:467–478

    CAS  Google Scholar 

  • Khera P, Saxena R, Sameerkumar CV, Saxena K, Varshney RK (2015) SSRs and their utility in distinguishing wild species, CMS lines and maintainer lines in pigeonpea (Cajanus cajan L.). Euphytica 206:737–746

    Article  CAS  Google Scholar 

  • Kheyr-Pour A, Gracenz VE, Everett HL (1981) Genetics of fertility restoration in the c group of cytoplasmic male sterility in maize. Genetics 98:379–388

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim JS, Klein PE, Klein RR, Price HJ, Mullet JE, Stelly DM (2005) Molecular cytogenetic maps of sorghum linkage groups 2 and 8. Genetics 169:955–965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim SS, Grienenberger E, Lallemand B et al (2010) LAP6/POLYKETIDE SYNTHASE A and LAP5/POLYKETIDE SYNTHASE B encode hydroxyalkyl alpha-pyrone synthases required for pollen development and sporopollenin biosynthesis in Arabidopsis thaliana. Plant Cell 22:4045–4066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kinoshita T (1995) Report of committee on gene symbolization, nomenclature and linkage groups. Rice Genet Newsl 12:9–153

    Google Scholar 

  • Klein RR, Klein PE, Chhabra AK et al (2001) Molecular mapping of the rf1 gene for pollen fertility restoration in sorghum (Sorghum bicolor L.). Theor Appl Genet 102:1206–1212

    Article  CAS  Google Scholar 

  • Klein RR, Klein PE, Mullet JE, Minx P, Rooney WL, Schertz KF (2005) Fertility restorer locus Rf1 of sorghum (Sorghum bicolor L.) encodes a pentatricopeptide repeat protein not present in the colinear region of rice chromosome 12. Theor Appl Genet 111:994–1012

    Article  CAS  PubMed  Google Scholar 

  • Klein RR, Monsma S, Keough B, Mead D, Small I, Mace E, Jordan DR (2015) Closing and finishing the mitochondrial and chloroplast genomes of sorghum male sterile a1 cytoplasm using long span NGS read technology. In Plant and Animal Genome XXIII, January 10–14, 2015, San Diego, CA. P 1096. (https://pag.confex.com/pag/xxiii/webprogram/Paper16193.html)

  • Kohel RJ, Quisenberry JE, Dilbeck RE (1984) Linkage analysis of the male-fertility restorer gene, Rf, in cotton. Crop Sci 24:992–994

    Article  Google Scholar 

  • Koizuka N, Imai R, Fujimoto H et al (2003) Genetic characterization of a pentatricopeptide repeat protein gene, orf687, that restores fertility in the cytoplasmic male sterile Kosena radish. Plant J 34:407–415

    Article  CAS  PubMed  Google Scholar 

  • Kojima T, Tsujimoto H, Ogihara Y (1997) High-resolution RFLP mapping of the fertility restoration (Rf3) gene against Triticum timopheevi cytoplasm located on chromosome 1BS of common wheat. Genes Genet Syst 72:353–359

    Article  CAS  Google Scholar 

  • Komori T, Yamamoto T, Takemori N, Kashihara M, Matsushima H, Nitta N (2003) Fine genetic mapping of the nuclear gene, Rf-1, that restores the BT-type cytoplasmic male sterility in rice (Oryza sativa L.) by PCR-based markers. Euphytica 29:241–247

    Article  Google Scholar 

  • Komori T, Ohta S, Murai N et al (2004) Map-based cloning of a fertility restore gene, Rf-1, in rice (Oryza sativa L.). Plant J 37:315–325

    Article  CAS  PubMed  Google Scholar 

  • Kubo T, Kitazaki K, Matsunaga M, Kagami H, Mikami T (2011) Male sterility-inducing mitochondrial genomes: how do they differ? Crit Rev Plant Sci 30:378–400

    Article  CAS  Google Scholar 

  • Kuhlman LC, Pring DR, Rooney WL, Tang HV (2006) Allelic frequency at the Rf3 and Rf4 loci and the genetics of A3 cytoplasmic fertility restoration in converted sorghum lines. Crop Sci 46:1576–1580

    Article  CAS  Google Scholar 

  • Kusterer B, Horn R, Friedt W (2005) Molecular mapping of the fertility restoration locus Rf1 in sunflower and development of diagnostic markers for the restorer gene. Euphytica 143:35–42

    Article  CAS  Google Scholar 

  • Landry BS, Hubert N, Etoh T, Harada JJ, Lincoln SE (1991) A genetic map for Brassica napus based on restriction fragment length polymorphisms detected with expressed DNA sequences Genome 34:543–552

    CAS  Google Scholar 

  • Langer S, Longin CFH, Würschum T (2014) Phenotypic evaluation of floral traits with relevance for hybrid breeding in wheat (Triticum aestivum L.). Plant Breed 133-433-441

  • Laser KD, Lersten NR (1972) Anatomy and cytology of microsporogenesis in cytoplasmic male sterile angiosperms. Bot Rev 38:425–454

    Article  Google Scholar 

  • Laughnan JR, Gaby SJ (1978) Nuclear and cytoplasmic mutations to fertility in S male-sterile maize. In: Waldin DB (ed) Maize breeding and genetics. Wiley, New York, pp 427–446

    Google Scholar 

  • Leclercq P (1969) Une sterilite male cytoplasmic chez le tournesol. Ann Amelior Plantes 19:99–106

    Google Scholar 

  • Léon J (1994) Mating system and the effect of heterogeneity and heterozygosity on phenotypic stability. In: van Ooijen JW, Jansen J (eds) Biometrics in plant breeding: Applications of molecular markers. Proceedings of the 9th meeting of the eUCArPIA section biometrics in plant breeding, Wageningen, pp 19–31

  • Levings CS (1993) III. Thoughts on cytoplasmic male sterility in CMS-T maize. Plant Cell 5:1285–1290

    Article  PubMed  PubMed Central  Google Scholar 

  • Li L, Yang QF, Hu YM, Zhu LH, Ge HX (1995) Discovery of parent interaction sterile material of soybean cultivar and its genetic inference. J Anhui Agric Sci 23:304–306

    Google Scholar 

  • Li XQ, Jean M, Landry B, Brown GG (1998) Restorer genes for different forms of Brassica cytoplasmic male sterility map to a single nuclear locus that modifies transcripts of several mitochondrial genes. Proc Natl Acad Sci USA 95:10032–10037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li XL, Liu LK, Hou N, Liu GQ, Liu CG (2005) SSR and SCAR markers linked to the fertility-restoring gene for a D2-type cytoplasmic male-sterile line in wheat. Plant Breed 124:413–415

    Article  CAS  Google Scholar 

  • Li YF, Zheng Y, Addoquaye C et al (2010) Transcriptome wide identification of microRNA targets in rice. Plant J 62:742–759

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Liu Z, Cai Q, Yang GS, He QB, Liu PW (2011) Identification of a microsatellite marker linked to the fertility-restoring gene for a polima cytoplasmic male-sterile line in Brassica napus L. Afr J Biotechnol 10:9563–9569

    CAS  Google Scholar 

  • Li J, Han S, Ding X, He T, Dai J, Yang S, Gai J (2015) Comparative transcriptome analysis between the cytoplasmic male sterile line NJCMS1A and its maintainer NJCMS1B in soybean (Glycine max (L.) Merr.). PLoS One 10:e0126771

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lin SC, Yuan LP (1980) Hybrid rice breeding in China. In: Innovative approaches to Rice breeding. Selected papers from the 1979 International Rice Research Conference The International Rice Research Institute, Philippines pp 35–52

  • Lin C, Zhang C, Zhao H, Xing S, Wang Y, Liu X (2014) Sequencing of the chloroplast genomes of cytoplasmic male-sterile and male-fertile lines of soybean and identification of polymorphic markers. Plant Sci 229:208–214

    Article  CAS  PubMed  Google Scholar 

  • Link W, Ederer W, Gumberg RK, Melchinger AE (1997) Detection and characterization of two new CMS system in Faba bean. Plant Breed 116:158–162

    Article  Google Scholar 

  • Link W, Hanafy M, Malenica N, Jacobsen HJ, Jelenic S (2008) Fababean Compendium of transgenic crop plants: Transgenic legume grain and legumes. Blackwell publisher pp 71–88

  • Liu F, Cui X, Horner HT, Weiner H, Schnable PS (2001) Mitochondrial aldehyde dehydrogenase activity is required for male fertility in maize. Plant Cell 13:1063–1078

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu L, Guo W, Zhu X, Zhang T (2003) Inheritance and fine mapping of fertility restoration for cytoplasmic male sterility in Gossypium hirsutum L. Theor Appl Genet 106:461–469

    CAS  PubMed  Google Scholar 

  • Liu XQ, Xu X, Tan YP et al (2004) Inheritance and molecular mapping of two fertility-restoring loci for Honglian gametophytic cytoplasmic male sterility in rice (Oryza sativa L.). Mol Gen Genomics 271:586–594

    Article  CAS  Google Scholar 

  • Liu Y, Dong ZS, Zhang GS et al (2005) Cytological study on growth of anther of CMS 212A in Brassica napus L. Acta Agric Boreali-Occident Vin 14:33–37

    Google Scholar 

  • Liu CG, Hou N, Liu LK, Liu JC, Kang XS, Zhang AM (2006) A YA-type cytoplasmic male sterile source in common wheat. Plant Breed 125:437–440

    Article  Google Scholar 

  • 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 Genom 12:163

    Article  CAS  Google Scholar 

  • Liu Z, Liu P, Long F, Hong D, He Q, Yang G (2012a) Fine mapping and candidate gene analysis of the nuclear restorer gene Rfp for pol CMS in rapeseed (Brassica napus L.). Theor Appl Genet 125:773–779

    Article  CAS  PubMed  Google Scholar 

  • Liu Z, Wang D, Feng J, Seiler GJ, Cai X, Jan CC (2013a) Diversifying sunflower germplasm by integration and mapping of a novel male fertility restoration gene. Genetics 193:727–737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu C, Ma N, Wang PY, Fu N, Shen HL (2013b) Transcriptome sequencing and De Novo analysis of a cytoplasmic male sterile line and its near-isogenic restorer line in chili pepper (Capsicum annuum L.). PLoS One 8:e65209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Z, Mulpuri S, Feng J, Vick BA, Jan CC (2012b) Molecular mapping of the Rf3 fertility restoration gene to facilitate its utilization in breeding confection sunflower. Mol Breed 29:275–284

  • Longin CFH, Mühleisen J, Maurer HP, Zhang H, Gowda M, Reif JC (2012) Hybrid breeding in autogamous cereals. Theor Appl Genet 125:1087–1096

    Article  PubMed  Google Scholar 

  • Longin CF, Reif JC, Würschum T (2014) Long-term perspective of hybrid versus line breeding in wheat based on quantitative genetic theory. Theor Appl Genet 127:1635–1641

    Article  PubMed  Google Scholar 

  • Longin CFH, Mi X, Würschum T (2015) Genomic selection in wheat: optimum allocation of test resources and comparison of breeding strategies for line and hybrid breeding. Theor Appl Genet 128:1297–1306

    Article  PubMed  Google Scholar 

  • Luo D, Xu H, Liu Z et al (2013) A detrimental mitochondrial-nuclear interaction causes cytoplasmic male sterility in rice. Nat Genet 45:573–577

    Article  CAS  PubMed  Google Scholar 

  • Ma ZQ, Sorrells ME (1995) Genetic analysis of fertility restoration in wheat using restriction fragment length polymorphisms. Crop Sci 35:1137–1143

    Article  CAS  Google Scholar 

  • Mackenzie SA, Pring DR, Bassett MJ, Chase CD (1988) Mitochondrial DNA rearrangement associated with fertility restoration and cytoplasmic reversion to fertility in cytoplasmic male sterile Phaseolus vulgaris L. Proc Natl Acad Sci USA 85:2714–2717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mallikarjuna N, Saxena KB (2002) Production of hybrids between Cajanus acutifolius and C. cajan. Euphytica 124:107–110

    Article  CAS  Google Scholar 

  • Mallikarjuna N, Saxena KB (2005) A new cytoplasmic nuclear male-sterility system derived from cultivated pigeonpea cytoplasm. Euphytica 142:143–148

    Article  Google Scholar 

  • Mallikarjuna N, Jadhav D, Reddy P (2006) Introgression of Cajanus platycarpus genome into cultivated pigeonpea genome. Euphytica 19:161–167

    Article  CAS  Google Scholar 

  • Manickam S, Gururajan KN, Gopalakrishnan N (2010) Development of isogenic restorer line in extra long staple cotton variety Suvin. Electronic J Plant Breed 1:632–636

    Google Scholar 

  • Mantione KJ, Kream RM, Kuzelova H, Ptacek R, Raboch J, Samuel JM, Stefano GB (2014) Comparing bioinformatic gene expression profiling methods: microarray and RNA-Seq. Med Sci Monit Basic Res 20:138–141

    Article  PubMed  PubMed Central  Google Scholar 

  • Martin AC, Atienza SG, Ramireza MC, Barro F, Martin A (2008) Male fertility restoration of wheat in Hordeum chilense cytoplasm is associated with 6HchS chromosome addition. Austr J Agric Res 59:206–213

    Article  CAS  Google Scholar 

  • Matsuhira H, Kagami H, Kurata M et al (2012) Unusual and typical features of a novel restorer-of-fertility gene of sugar beet (Beta vulgaris L.). Genetics 192:1347–1358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mette MF, Gils M, Longin CFH, Reif JC (2016) Hybrid breeding in wheat. In: Takumi S, Handa H (eds) Ogihara Y. Advances in wheat genetics, From genome to field. Springer Japan, pp 225–232

    Google Scholar 

  • Meyer VG (1975) Male sterility from Gossypium harknessii. J Hered 66:23–27

    Google Scholar 

  • Meyer J, Pei D, Wise PR (2011) Rf8-mediated T-urf13 transcript accumulation coincides with a pentatricopeptide repeat cluster on maize chromosome 2L. Plant Genome 4:283–299

    Article  CAS  Google Scholar 

  • Millar AA, 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller DA, Pickett RC (1964) Inheritance of partial male-fertility in Sorghum vulgare Pers. Crop Sci 4:1–4

    Article  Google Scholar 

  • Mühleisen J, Piepho HP, Maurer HP, Longin CFH, Reif JC (2014) Yield stability of hybrids versus lines in wheat, barley, and triticale. Theor Appl Genet 127:309–316

    Article  PubMed  Google Scholar 

  • Mühleisen J, Piepho H, Maurer HP, Reif JC (2015) Yield performance and stability of CMS-based triticale hybrids. Theor Appl Genet 128:291–301

    Article  PubMed  CAS  Google Scholar 

  • 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 26:275–292

    Article  CAS  Google Scholar 

  • Ogura H (1968) Studies on the new male-sterility in Japanese radish, with special reference to the utilization of this sterility towards practical raising of hybrid seed. Mem Fac Agric Kagoshima Univ 6:39–78

    Google Scholar 

  • Ohtsu K, Takahashi H, Schnable PS, Nakazono M (2007) Cell type-specific gene expression profiling in plants by using a combination of laser microdissection and high-throughput technologies. Plant Cell Physiol 48:3–7

    Article  CAS  PubMed  Google Scholar 

  • 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 54:1560–1568

    Article  CAS  PubMed  Google Scholar 

  • Palmer RG, Gai J, Sun H, Burton JW (2010) Production and evaluation of hybrid soybean. Plant Breed Rev 21:263–299

    Google Scholar 

  • Palmer RG, Gai J, Dalvi VA, Suso MJ (2011) Male sterility and hybrid production Technology. In: Pratap A, Kumar J (ed) Biology and breeding of food legumes. CAB International pp 193–206

  • Peng X, Wang K, Hu C et al (2010) The mitochondrial gene orfH79 plays a critical role in impairing both male gametophyte development and root growth in CMS-Honglian rice. BMC Plant Biol 10:125

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pradhan SB, Ratho SN, Jachuck PJ (1990) New sources of cytoplasmic-genetic male sterility in cultivated indica rices. Euphytica 48:215–218

    Article  Google Scholar 

  • Prakash S, Kirti PB, Bhat SR, Gaikwad K, Kumar VD, Chopra VL (1998) A Moricandia arvensis based cytoplasmic male sterility and fertility restoration systems in Brassica juncea. Theor Appl Genet 97:488–492

    Article  CAS  Google Scholar 

  • Praveen M, Anurag UG, Suneetha N, Umakanth A, Patil JV, Madhusudana R (2015) Inheritance and molecular mapping of Rf6 locus with pollen fertility restoration ability on A1 and A2 cytoplasms in sorghum. Plant Sci 238:73–80

    Article  CAS  PubMed  Google Scholar 

  • Primard-Brisset C, Poupard JP, Horvais R, Eber F, Pelletier G, Renard M Delourne R (2005) A new recombined double low restorer line for the Ogu-INRA cms in rapeseed Brassica napus L. Theor Appl Genet 111:736–746

  • Pring DR, Tang HV, Chen W, Howad W, Kempken F (1999) A unique two-gene gametophytic male sterility system in sorghum involving a possible role of RNA editing in fertility restoration. J Hered 90:386–393

    Article  CAS  PubMed  Google Scholar 

  • Qi LL, Seiler GJ, Vick BA, Gulya TJ (2012) Genetics and mapping of the R11 gene conferring resistance to recently emerged rust races, tightly linked to male fertility restoration, in sunflower (Helianthus annuus L.). Theor Appl Genet 125:921–932

    Article  CAS  PubMed  Google Scholar 

  • Quinby JR (1980) Interaction of genes and cytoplasm in male sterility in Sorghum. In proceedings of 35th corn and sorghum research conference, American Seed Trade Assoc. Chicago, Illinois, USA

  • Rai KN (1995) A new cytoplasmic-nuclear male sterility system in pearl millet. Plant Breed 114:445–447

    Article  Google Scholar 

  • Rai KN, Anandkumar K, Andres DJ, Rao AS (2001) Commercial viability of alternative cytoplasmic-nuclear male sterility systems in pearl millet. Euphytica 121:107–114

    Article  Google Scholar 

  • Rajendrakumar P, Biswal AK, Balachandran SM, Ramesha MS, Viraktamath BC, Sundaram RM (2007) A mitochondrial repeat specific marker for distinguishing wild abortive type cytoplasmic male sterile rice lines from their cognate isogenic maintainer lines. Crop Sci 47:207–211

    Article  CAS  Google Scholar 

  • Ramesh S, Reddy BV, Reddy B, Ramaiah B (2006) Influence of cytoplasmic-nuclear male sterility on agronomic performance of sorghum hybrids. Int Sorghum Millets Newslett 47:21–25

    Google Scholar 

  • Rao NGP, Tripathi DP, Rana BS (1984) Genetic analysis of cytoplasmic systems in sorghum. Indian J Genet 44:48–49

    Google Scholar 

  • Rasmusson AG, Heiser V, Zabaleta E, Brennicke A, Grohmann L (1998) Physiological, biochemical and molecular aspects of mitochondrial complex I in plants. Biochim Biophys Acta 1364:101–111

    Article  CAS  PubMed  Google Scholar 

  • Rathnaswamy R, Yolanda JL, Kalaimagal T, Suryakumar M, Sassikumar D (1999) Cytoplasmic-genic male-sterility in pigeonpea (Cajanus cajan). Ind J Agric Sci 69:159–160

    Google Scholar 

  • Reddy BVS, Sharma HC, Thakur RP, Ramesh S, Rattunde F, Mgonja M (2006) Sorghum hybrid parents research at ICRIAT—strategies, status, and impacts. SAT ejournal 2:24

    Google Scholar 

  • Reddy CVCM, Sinha B, Reddy AVV, Reddy YR (2008) Maintenance of male sterility and fertility restoration in different CMS sources of sunflower (Helianthus annuus L.). Asian J Plant Sci 7:762–766

    Article  Google Scholar 

  • Reddy BVS, Kumar AA, Sharma HC et al (2012) Sorghum improvement (1980–2010): status and way forward. J SAT Agri Res 10:1–14

    Google Scholar 

  • Rogers J, Edwardson J (1952) The utilization of cytoplasmic male inbred lines in production of corn hybrids. Agron J 44:8–13

    Article  Google Scholar 

  • Ross WM, Heckerott HL (1972) Registration of seven iso-cytoplasmic sorghum germplasm lines. Crop Sci 12:720

    Article  Google Scholar 

  • Rutley N, Twell D (2015) A decade of pollen transcriptomics. Plant Reprod 28:73–89

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sane AP, Seth P, Ranade SA, Nath P, Sane PV (1997) RAPD analysis of isolated mitochondrial DNA reveals heterogeneity in elite wild abortive (WA) cytoplasm in rice. Theor Appl Genet 95:1098–1103

    Article  CAS  Google Scholar 

  • Sattari M, Kathiresan A, Gregorio GB, Hernandez JE, Nas TM, Virman SS (2007) Development and use of a two-gene marker-aided selection system for fertility restorer genes in rice. Euphytica 153:35–42

    Article  CAS  Google Scholar 

  • Saxena KB (2013) A novel CMS source in pigeonpea derived from Cajanus reticulates. Indian J Genet 73:259–263

    Google Scholar 

  • Saxena KB, Kumar RV (2003) Development of a cytoplasmic nuclear male sterility system in pigeonpea using C. scarabaeoides (L.) Thours. Indian J Genet Plant Breed 63:225–229

    Google Scholar 

  • Saxena KB, Nadarajan N (2010) Prospects of pigeonpea hybrids in Indian agriculture. Electronic J Plant Breed 1:1107–1117

    Google Scholar 

  • Saxena KB, Kumar RV, Srivastava N, Bao S (2005) A cytoplasmic-nuclear male-sterility system derived from a cross between Cajanus cajanifolius and Cajanus cajan. Euphytica 145:289–294

    Article  Google Scholar 

  • Saxena KB, Sultana R, Mallikarjuna N, Saxena RK, Kumar RV, Sawargaonkar KL (2010a) Male-sterility systems in pigeonpea and their role in enhancing yield. Plant Breed 129:125–134

    Article  Google Scholar 

  • Saxena RK, Saxena K, Varshney RK (2010b) Application of SSR markers for molecular characterization of hybrid parents and purity assessment of ICPH 2438 hybrid of pigeonpea [Cajanus cajan (L.) Millspaugh]. Mol Breed 26:371–380

    Article  CAS  Google Scholar 

  • Saxena MK, Saxena U, Saxena KB, Khandalkar VS, Sultana R (2011) Profitability and production cost of hybrid pigeonpea seed. Electronic J Plant Breed 2:409–412

    Google Scholar 

  • Saxena KB, Kumar RV, Tikle AN et al (2013) ICPH2671—the world’s first commercial food legume hybrid. Plant Breed 132:479–485

  • Schertz KF, Ritchey JM (1978) Cytoplasmic-genic male-sterility systems in sorghum. Crop Sci 18:890–893

    Article  Google Scholar 

  • Schertz KF, Sivaramakrishnan S, Hanna WW et al (1997) Alternate cytoplasms and apomixis of sorghum and pearl millet. In Proc. Intl. Conf. Genetic Improvement of Sorghum and Pearl Millet. INTSORMIL/ICRISAT, Lubbock, TX.pp 213–223

  • Schnable U, Engelmann U, Horn R (2008) Development of markers for the use of the PEF1 cytoplasm in sunflower hybrid breeding. Plant Breed 127:587–591

    Article  CAS  Google Scholar 

  • Selinski J, Scheibe R (2014) Pollen tube growth: where does the energy come from? Plant Signal Behav 9: e977200-1-e977200-9

  • Serieys H (1996) Identification, study and utilization in breeding programs on new CMS sources. Helia 19:144–160

    Google Scholar 

  • Serieys H, Vincourt P (1987) Characterization of new cytoplasmic male sterility sources from Helianthus genus. Helia 10:9–13

    Google Scholar 

  • 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 167:217–227

    Article  CAS  Google Scholar 

  • Shemesh-Mayer E, Ben-Michael T, Rotem N et al (2015) Garlic (Allium sativum L.) fertility: transcriptome and proteome analyses provide insight into flower and pollen development. Front. Plant Sci 6:271

    Google Scholar 

  • Shinjyo C (1975) Genetical studies of cytoplasmic male sterility and fertility restoration in rice, Oryza sativa L. Sci Bull Coll Agric Univ Ryukyus 22:1–57

    Google Scholar 

  • Shinjyo C, Omura T (1966) Cytoplasmic-genetic male sterility in cultivated rice, Oryza sativa L. I. Fertilities of F1, F2 and offspring’s obtained from their mutual reciprocal backcrosses and segregation of completely male sterile plants. Jpn J Breed 16:179–180

    Article  Google Scholar 

  • Shinjyo C, Sato S (1994) Chromosomal location of a fertility restoration gene Rf2 in rice, Oryza sativa L. Rice Genet Newsl 11:93–95

    Google Scholar 

  • Singh SD (1995) Downy mildew of pearl millet. Plant Dis 79:545–549

    Article  Google Scholar 

  • Singh HP, Lohithaswa HC (2006) Sorghum. In: Kole C (ed) Genome Mapping & Molecular Breeding in Plants. Springer- Verlag, Berlin, Heidelberg, pp 257–302

    Google Scholar 

  • Singh SP, Singh SP, Pandey T, Singh RK, Sawant SV (2015) A novel male sterility-fertility restoration system in plants for hybrid seed production. Sci Rep 5:11274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sinha P, Tomar SM, Vinod Singh VK, Balyan HS (2013) Genetic analysis and molecular mapping of a new fertility restorer gene Rf8 for Triticum timopheevi cytoplasm in wheat (Triticum aestivum L.) using SSR markers. Genetica 141:431–441

    Article  CAS  PubMed  Google Scholar 

  • Sinha P, Saxena KB, Saxena RK et al (2015) Association of nad7a gene with cytoplasmic male sterility in pigeonpea. Plant Genome 8:2

    Article  Google Scholar 

  • Sisco PH (1991) Duplications complicate genetic mapping of Rf4, a restorer gene for CMS-C cytoplasmic male sterility in corn. Crop Sci 31:1263–1266

    Article  CAS  Google Scholar 

  • Stephens JC, Holland RF (1954) Cytoplasmic male sterility for hybrid sorghum seed production. Agron J 46:20–23

    Article  Google Scholar 

  • Stewart JM (1992). A new cytoplasmic male sterile and restorer for cotton. Proc Beltwide Cotton Prod Res Conf, p 610

  • Stewart JM, Zhang J (1996) Cytoplasmic influence on the inheritance of the D8 restorer gene. Proc. Beltwide Cotton Conf, Nashville, pp 622–623

    Google Scholar 

  • Stewart JM, Black-Brown CE, Zhang J (1996) Sporophytic and gametic male dysfunction conditioned by the D8 cytoplasm of cotton. In: Agronomy Abstracts. ASA, Madison, WI, p 86

  • Sun H, Zhao LM, Huang H (1994) Studies on the cytoplasmic nuclear male sterile soybean. Chin Sci Bull 39:175–176

    Google Scholar 

  • Sun H, Zhao LM, Huang M (2001) Cytoplasmic genetic male sterile soybean and method for producing hybrid soybean. United States Patent 6,320,098 B1

  • Sun Q, Hu C, Hu J, Li S, Zhu Y (2009) Quantitative proteomic analysis of CMS-related changes in Honglian CMS rice anther. Protein J 28:341–348

    Article  CAS  PubMed  Google Scholar 

  • Sundaram RM, Naveenkumar B, Biradar SK et al (2008) Identification of informative SSR markers capable of distinguishing hybrid rice parental lines and their utilization in seed purity assessment. Euphytica 63:215–224

    Article  Google Scholar 

  • Suresh PB, Srikanth B, Kishore VH et al (2012) Fine mapping of Rf3 and Rf4 fertility restorer loci of WA-CMS of rice (Oryza sativa L.) and validation of the developed marker system for identification of restorer lines. Euphytica 187:421–435

    Article  CAS  Google Scholar 

  • Suwabe K, Suzuki G, Takahashi H et al (2008) Separated transcriptomes of male gametophyte and tapetum in rice: validity of a laser microdissection (LM) microarray. Plant Cell Physiol 49:1407–1416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki H, Rodriguez-Uribe L, Xu J, Zhang J (2013) Transcriptome analysis of cytoplasmic male sterility and restoration in CMS-D8 cotton. Plant Cell Rep 32:1531–1542

    Article  CAS  PubMed  Google Scholar 

  • Tan XL, Vanavichit A, Amornsilpa S, Trangoonrung S (1998a) Genetic analysis of rice CMS-WA fertility restoration based on QTL mapping. Theor Appl Genet 97:994–999

    Article  CAS  Google Scholar 

  • Tan XL, Vanavichit P, Amornsilpa S, Trangoonrung S (1998b) Mapping of rice Rf gene by bulked line analysis. DNA Res 5:15–18

    Article  CAS  PubMed  Google Scholar 

  • 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 16:45

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tang HV, Pring DR (2003) Conversion of fertility restoration of the sorghum IS1112C (A3) male-sterile cytoplasm from two genes to one gene. Crop Sci 43:1747–1753

    Article  CAS  Google Scholar 

  • Tang HV, Pring DR, Shaw LC et al (1996) Transcript processing internal to a mitochondrial open reading frame is correlated with fertility restoration in male-sterile sorghum. Plant J 10:123–133

    Article  CAS  PubMed  Google Scholar 

  • Tang HV, Chang R, Pring DR (1998) Cosegregation of single genes associated with fertility restoration and transcript processing of sorghum mitochondrial orf107 and urf209. Genetics 150:383–391

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tang HV, Pedersen JF, Chase CD, Pring DR (2007) Fertility restoration of the sorghum A3 male-sterile cytoplasm through a sporophytic mechanism derived from Sudan grass. Crop Sci 47:943–950

    Article  CAS  Google Scholar 

  • Tang H, Luo D, Zhou D, Zhang Q, Tian D, Zheng X, Chen L, Liu YG (2014) The Rice Restorer Rf4 for wild-abortive cytoplasmic male sterility encodes a PPR protein that functions in reduction of WA352 transcripts. Mol Plant 7:1497–1500

    Article  CAS  PubMed  Google Scholar 

  • Tao D, Xu P, Li J, Hu F, Yang Y, Zhou J, Tan XL, Jones MP (2004) Inheritance and mapping of male sterility restoration gene in upland japonica restorer lines. Euphytica 38:247–254

    Article  Google Scholar 

  • Teng LS, Shen ZT (1994) Inheritance of fertility restoration for cytoplasmic male sterility in rice. Rice Genet Newslett 11:95–99

    Google Scholar 

  • 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. Mol Breed 34:1361–1371

    Article  CAS  Google Scholar 

  • Tikka SBS, Parmar LD, Chauhan RM (1997) First record of cytoplasmic-genic male-sterility system in pigeonpea [Cajanus cajan (L.) Millsp.] through wide hybridization. Gujarat Agri Univ Res J 22:10–162

    Google Scholar 

  • Touzet P, Budar F (2004) Unveiling the molecular arms race between two conflicting genomes in cytoplasmic male sterility? Trends Plant Sci 9:568–570

    Article  CAS  PubMed  Google Scholar 

  • Touzet P, Meyer EH (2014) Cytoplasmic male sterility and mitochondrial metabolism in plants. Mitochondrion 19:166–171

    Article  CAS  PubMed  Google Scholar 

  • Tsunewaki K (2015) Fine mapping of the first multi-fertility-restoring gene, Rf (multi), of wheat for three Aegilops plasmons, using 1BS-1RS recombinant lines. Theor Appl Genet 128:723–732

    Article  CAS  PubMed  Google Scholar 

  • Tuteja R, Saxena RK, Davila J et al (2013) Cytoplasmic male sterility associated chimeric open reading frames identified by mitochondrial genome sequencing of four Cajanus genotypes. DNA Res 20:485–495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wan ZJ, Jing B, Tu J et al (2008) Genetic characterization of a new cytoplasmic male sterility system (hau) in Brassica juncea and its transfer to B. napus. Theor Appl Genet 116:355–362

    Article  PubMed  Google Scholar 

  • Wang Z, Zou Y, Li X et al (2006) Cytoplasmic male sterility of rice with Boro II cytoplasm is caused by a cytotoxic peptide and is restored by two related PPR motif genes via distinct modes of mRNA silencing. Plant Cell 18:676–687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang F, Stewart JM, Zhang J (2007) Molecular markers linked to the Rf2 fertility restorer gene in cotton. Genome 50:818–824

    Article  CAS  PubMed  Google Scholar 

  • Wang F, Yue B, Hu J, Stewart JMD, Zhang J (2009) A target region amplified polymorphism marker for fertility restorer gene Rf1 and chromosomal localization of Rf1 and Rf2 in cotton. Crop Sci 49:1602–1608

    Article  CAS  Google Scholar 

  • Wang Y, Zhao L, Wang X, Sun H (2010a) Molecular mapping of a fertility restorer gene for cytoplasmic male sterility in soybean. Plant Breed 129:9–12

    Article  CAS  Google Scholar 

  • Wang F, Feng C, O’Connell MA, Stewart JM, Zhang J (2010b) RFLP analysis of mitochondrial DNA in two cytoplasmic male sterility systems (CMS-D2 and CMS-D8) of cotton. Euphytica 172:93–99

    Article  CAS  Google Scholar 

  • Wang K, Peng X, Ji Y, Yang P, Zhu Y, Li S (2013a) Gene, Protein and network of male sterility in rice. Front Plant Sci 92:1–10

    CAS  Google Scholar 

  • Wang K, Gao F, Ji Y, Liu Y, Dan Z, Yang P, Zhu Y, Li S (2013b) orfh79 impairs mitochondrial function via interaction with a subunit of electron transport chain complex III in Honglian cytoplasmic male sterile rice. New Phytol 198:408–418

    Article  CAS  PubMed  Google Scholar 

  • Wang ZW, Wang C, Gao L, Mei SY, Zhou Y, Xiang CP, Wang T (2013c) Heterozygous alleles restore male fertility to cytoplasmic male-sterile radish (Raphanus sativus L.) a case of overdominance. J Exp Bot 64:2041–2048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wanjari KB, Patil AN, Manapure P, Manjaya JG, Manish P (1999) Cytoplasmic male-sterility in pigeonpea with cytoplasm from Cajanus volubilis. Ann Plant Physiol 13:170–174

    Google Scholar 

  • Watanabe Y, Sakaguchi S, Kudo M (1968) On the male sterile rice plant possessing the cytoplasm of Burmese variety ‘Lead Rice’. Jpn J Breed 18:77–78

    Article  Google Scholar 

  • Watanabe Y, Tomita M, Kanai A (2007) Computational methods for microRNA target prediction. Meth Enzymol 427:65–86

    Article  CAS  PubMed  Google Scholar 

  • Weaver DB, Weaver JB (1977) Inheritance of pollen fertility restoration in cytoplasmic male-sterile upland cotton. Crop Sci 17:497–499

    Article  Google Scholar 

  • Webster OJ, Singh SP (1964) Breeding behaviour and histological structure of a non dehiscent anther character in Sorghum vulgare Pers. Crop Sci 4:656–658

    Article  Google Scholar 

  • Weeraratne H (1954) Hybridization technique in rice. Trop Agric (Colombo) 110:93–97

    Google Scholar 

  • Wei M, Wei H, Wu M, Song M, Zhang J, Yu J, Fan S, Yu S (2013) Comparative expression profiling of miRNA during anther development in genetic male sterile and wild type cotton. BMC Plant Biol 13:66

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wen L, Tang HV, Chen W, Chang R, Pring DR, Klein PE, Childs KL, Klein RR (2002) Development and mapping of AFLP markers linked to the sorghum fertility restorer gene rf4. Theor Appl Genet 104:577–585

    Article  CAS  PubMed  Google Scholar 

  • Wen L, Liu G, Li S, Wan C, Tao J, Xu K, Zhang JZ, Zhu YG (2007) Proteomic analysis of anthers from Honglian cytoplasmic male sterility line rice and its corresponding maintainer and hybrid. Bot Stud 48:293–309

    CAS  Google Scholar 

  • Wesołowski W, Szklarczyk M, Szalonek M, Słowińska J (2015) Analysis of the mitochondrial proteome in cytoplasmic male-sterile and male-fertile beets. J Proteomics 119:61–74

    Article  PubMed  CAS  Google Scholar 

  • Whelan EDP (1981) Cytoplasmic Male Sterility in Helianthus giganteus L. × H. annuus L. Interspecific hybrids. Crop Sci 21:855–858

    Article  Google Scholar 

  • Whitford R, Fleury D, Reif JC, Garcia M, Okada T, Korzun V, Langridge P (2013) Hybrid breeding in wheat: technologies to improve hybrid wheat seed production. J Exp Bot 64:5411–5428

    Article  CAS  PubMed  Google Scholar 

  • Wilson JA, Ross WM (1962) Male sterility interaction of the Triticum aestivum nucleus and Triticum timopheevii cytoplasm. Wheat Inf Serv 14:29–30

    Google Scholar 

  • Wise RP, Schnable PS (1994) Mapping complementary genes in maize: positioning the rf1 and rf2 nuclear-fertility restorer loci of Texas (T) cytoplasm relative to RFLP and visible markers. Theor Appl Genet 88:785–795

    Article  CAS  PubMed  Google Scholar 

  • Wise RP, Dill CL, Schnable PS (1996) Mutator-induced mutations of the rf1 nuclear fertility restorer of T-cytoplasm maize alters the accumulation of T-urf13 mitochondrial transcripts. Genetics 143:1383–1394

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wise RP, Gobelman-Werner K, Peil D, Dill CL, Schnable PS (1999) Mitochondrial transcript processing and restoration of male fertility in T-cytoplasm maize. J Hered 90:380–385

    Article  CAS  PubMed  Google Scholar 

  • Worstell JV, Kidd HJ Schertz KC (1984) Relationships among male sterility inducing cytoplasms of sorghum. Crop Sci 24:186–189

  • Wu MF, Tian Q, Reed JW (2006) Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133:4211–4218

    Article  CAS  PubMed  Google Scholar 

  • Wu J, Gong Y, Cui M, Qi T, Guo L, Zhang J, Xing C (2011) Molecular characterization of cytoplasmic male sterility conditioned by Gossypium harknessii cytoplasm (CMS-D2) in upland cotton. Euphytica 181:17–29

    Article  CAS  Google Scholar 

  • 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. Mol Breed 34:231–240

    Article  CAS  Google Scholar 

  • Xian-Hua S, Song Y, Ren-liang H, Shan Z, Hong-lian X, Lin-jun S (2013) Development of novel cytoplasmic male sterile source from dongxiang wild rice (Oryza rufipogon). Rice 20:379–382

    Article  Google Scholar 

  • Xie F, He Z, Esguerra MQ, Qiu F, Ramanathan V (2013) Determination of heterotic groups for tropical Indica hybrid rice germplasm. Theor Appl Genet 127:407–417

    Article  Google Scholar 

  • Yamagishi H, Bhat SR (2014) Cytoplasmic male sterility in Brassicaceae crops. Breed Sci 64:38–47

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan X, Dong C, Yu J et al (2013) Transcriptome profile analysis of young floral buds of fertile and sterile plants from the self-pollinated offspring of the hybrid between novel restorer line NR1 and Nsa CMS line in Brassica napus. BMC Genom 14:26

    Article  CAS  Google Scholar 

  • Yan J, Tian H, Wang S, Shao J, Zheng Y, Zhang H, Guo L, Ding Y (2014) Pollen developmental defects in ZD-CMS rice line explored by cytological, molecular and proteomic approaches. J Proteomics 108C:110–123

    Article  CAS  Google Scholar 

  • Yan J, Zhang H, Zheng Y, Ding Y (2015) Comparative expression profiling of miRNAs between the cytoplasmic male sterile line Meixiang A and its maintainer line Meixiang B during rice anther development. Planta 241:109–123

    Article  CAS  PubMed  Google Scholar 

  • Yang SP, Duan MP, Meng QC, Qui J, Fan JM, Zhao TJ, Yu DY, Gai JY (2007) Inheritance and gene tagging of male fertility restoration of cytoplasmic-nuclear male-sterile line NJCMS1A in soybean. Plant Breed 126:302–305

    Article  CAS  Google Scholar 

  • 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 Genom 14:9

    Article  CAS  Google Scholar 

  • Yang P, Han J, Huang J (2014) Transcriptome sequencing and de novo analysis of cytoplasmic male sterility and maintenance in JA-CMS cotton. PLoS One 9:e112320

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yao FY, Xu CG, Yu SB, Li JX, Gao YJ, Li XH, Zhang Q (1997) Mapping and genetic analysis of two fertility restorer loci in the wild-abortive cytoplasmic male sterility system of rice (Oryza sativa L). Euphytica 98:183–187

    Article  CAS  Google Scholar 

  • Yashitola J, Sundaram RM, Biradar SK et al (2004) A sequence specific PCR marker for distinguishing rice lines on the basis of Wild Abortive cytoplasm from their cognate maintainer lines. Crop Sci 44:920–924

    Article  CAS  Google Scholar 

  • Ylstra B, Muskens M, Tunen AJ (1996) Flavonols are not essential for fertilization in Arabidopsis thaliana. Plant Mol Biol 32:1155–1158

    Article  CAS  PubMed  Google Scholar 

  • Yuan LP (1985) A concise course in hybrid rice. Hunan Science and Technology Publishing House, China, p 168

  • Yue B, Vick BA, Cai X, Hu J (2010) Genetic mapping for the Rf1 (fertility restoration) gene in sunflower (Helianthus annuus L.) by SSR and TRAP markers. Plant Breed 129:24–28

    Article  CAS  Google Scholar 

  • Zabala G, Gabay-Laughnan S, Laughnan JR (1997) The nuclear gene Rf3 affects the expression of the mitochondrial chimeric sequence R implicated in S-type male sterility in Maize. Genetics 147:847–860

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhan XD, Zhou HP, Chai RY, Zhuang JY, Cheng SH, Li CY (2012) Breeding of R8012, a Rice restorer line resistant to blast and bacterial blight through marker-assisted selection. Rice Sci 19:29–35

    Article  CAS  Google Scholar 

  • Zhang L, Dai OH (1997) Selection and breeding of nucleocytoplasmic male sterile line W931A in soybean. Sci Agric Sin 30:90–91

    Google Scholar 

  • Zhang JF, Stewart JM (2001a) Inheritance and genetic relationships of the D8 and D2-2 restorer genes for cotton cytoplasmic male sterility. Crop Sci 41:289–294

    Article  Google Scholar 

  • Zhang JF, Stewart JM (2001b) CMS-D8 restoration in cotton is conditioned by one dominant gene. Crop Sci 41:283–288

    Article  Google Scholar 

  • Zhang JF, Stewart JM (2004) Identification of molecular markers linked to the fertility restorer genes for CMS-D8 in cotton (Gossypium hirsutum L.). Crop Sci 44:1209–1217

    Article  CAS  Google Scholar 

  • Zhang G, Bharaj TS, Lu Y, Virmani SS, Huang N (1997) Mapping of the Rf-3 nuclear fertility-restoring gene for WA cytoplasmic male sterility in rice using RAPD and RFLP markers. Theor Appl Genet 94:27–33

    Article  CAS  PubMed  Google Scholar 

  • Zhang QY, Liu YG, Zhang GQ, Mei MT (2002) Molecular mapping of the fertility restorer gene Rf-4 for WA cytoplasmic male sterility in rice. Yi Chuan Xue Bao 29:1001–1004

    PubMed  Google Scholar 

  • Zhang C, Wang HY, Shen YZ, Zhao BC, Zhu ZG, Huang ZJ (2003) Location of the fertility restorer gene for T-type CMS wheat by microsatellite marker. Yi Chuan Xue Bao 30:459–464

    CAS  PubMed  Google Scholar 

  • Zhang JF, Stewart JM, Wang TH (2005) Linkage analysis between gametophytic restorer Rf2 gene and genetic markers in cotton. Crop Sci 45:147–156

    Google Scholar 

  • Zhang ZF, Wang Y, Zheng YL (2006) AFLP and PCR-based markers linked to Rf3, a fertility restorer gene for S cytoplasmic male sterility in maize. Mol Gen Genet 276:162–169

    Article  CAS  Google Scholar 

  • Zhang X, Meng Z, Zhou T, Sun G, Shi J, Yu Y, Zhang R, Guo S (2012) Mitochondrial SCAR and SSR markers for distinguishing cytoplasmic male sterile lines from their isogenic maintainer lines in cotton. Plant Breed 131:563–570

    Article  CAS  Google Scholar 

  • Zhao TJ, Gai JY (2006) Discovery of new male-sterile cytoplasm sources and development of a new cytoplasmic-nuclear male sterile line NJCMS3A in soybean. Euphytica 152:387–396

    Article  CAS  Google Scholar 

  • Zhao LM, Sun H, Huang M (1998) The development and preliminary studies on cytoplasmic male sterile soybean line ZA. Soybean Sci 17:268–270

    Google Scholar 

  • Zhao LM, Wang YM, Sun H et al (2007) Identification of SSR markers linked to the fertility restorer gene for the CMS in soybean. Soybean Sci 26:835–839

    Google Scholar 

  • Zhao ZQ, Liu PW, Yang GS (2008) Identification of AFLP and SCAR markers linked to the fertility restorer gene for the ‘Polima’ CMS in Brassica napus. Genes Genom 30:191–196

    CAS  Google Scholar 

  • Zhao Y, Li Z, Liu G et al (2015) Genome-based establishment of a high-yielding heterotic pattern for hybrid wheat breeding. Proc Natl Acad Sci USA 112:15624–15629

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou T (1983) Analysis of R genes in hybrid indica rice of ‘WA’ type. Acta Agron Sin 9:241–247

    Google Scholar 

  • Zhou PH, Tan YF, He YQ, Xu CG, Zhang Q (2003) Simultaneous improvement for four quality traits of Zhenshan 97, an elite parent of hybrid rice, by molecular marker-assisted selection. Theor Appl Genet 106:326–331

    CAS  PubMed  Google Scholar 

  • Zhou W, Kolb FL, Domier LL, Wang S (2005) SSR markers associated with fertility restoration genes against Triticum timopheevii cytoplasm in Triticum aestivum. Euphytica 141:33–40

    Article  CAS  Google Scholar 

  • Zhou M, Gu L, Li P, Song X, Wei L, Chen Z, Cao X (2010) Degradome sequencing reveals endogenous small RNA targets in rice (Oryza sativa L. ssp. indica). Front Biol 5:67–90

    Article  CAS  Google Scholar 

  • Zhu Q, Zhang X, Ejaz M et al (2013) Analysis of three wheat cytoplasmic male sterile lines mitochondrial DNA by AFLP. Sheng Wu Gong Cheng Xue Bao 29:646–656

    CAS  PubMed  Google Scholar 

  • Zhu Q, Song Y, Zhang G et al (2015) De novo assembly and transcriptome analysis of wheat with male sterility induced by the chemical hybridizing agent SQ-1. PLoS One 10(4):e0123556

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgments

Authors acknowledge support from Indian Council of Agricultural Research (ICAR), India.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Abhishek Bohra.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Communicated by N. Stewart.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 119 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bohra, A., Jha, U.C., Adhimoolam, P. et al. Cytoplasmic male sterility (CMS) in hybrid breeding in field crops. Plant Cell Rep 35, 967–993 (2016). https://doi.org/10.1007/s00299-016-1949-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-016-1949-3

Keywords

Navigation