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Genic markers for wild abortive (WA) cytoplasm based male sterility and its fertility restoration in rice

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Abstract

Commercial exploitation of heterosis is essential for enhancing productivity of rice. The use of cytoplasmic male sterility (CMS) and fertility restoration system greatly facilitates large scale production of hybrid seed. The wild abortive (WA) cytoplasm is most widely used for hybrid seed production in rice. The present study was undertaken to develop molecular markers for both WA cytoplasm based male sterility and its fertility restoration for use in efficient hybrid breeding. High degree of genetic differentiation of WA-cytoplasm from its normal fertile counterpart was observed due to DNA rearrangements involving five (coxI, coxIII, cob, atp6 and rps3) mitochondrial genes. Cleaved amplified polymorphic sequence (CAPS) markers based on five mitochondrial genes namely, coxIII, cob, atp9, rps3 and 18SrRNA polymorphic between CMS and maintainer line were developed. The utility of these informative markers was demonstrated in purity testing of the CMS line Pusa6A being used in commercial hybrid seed production. Fertility restoration was found to be controlled by a major locus in the Basmati restorer line PRR78, which was mapped to a short marker interval of 0.8 cM and a physical interval of 163.6 kb on rice chromosome 10. A total of 13 pentatricopeptide repeat (PPR) motif containing genes were predicted in a 1.66 Mb region on the long-arm of this chromosome of which, four were present in the marker interval containing the fertility restorer gene. High degree of conservation of gene order was observed between japonica and indica for the predicted PPR genes. A sequence tagged site (STS) and a genic non-coding microsatellite (GNMS) marker were designed based on one of the candidate PPR motif containing genes present in the marker interval, which were validated using F2 population and other known restorer lines. The candidate gene based marker identified in the present study would be useful in marker assisted selection (MAS) for fertility restorer gene in hybrid breeding programme based on WA-CMS of rice.

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References

  • 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 

  • 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 

  • Bailey-Serres J, Dixon LK, Liddell AD, Leaver CJ (1986) Nuclear-mitochondrial interactions in cytoplasmic male-sterile sorghum. Theor Appl Genet 73:252–260

    Article  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 

  • Ewing B, Green P (1998) Base calling of automated sequencer traces using Phred II. Error probabilities. Genome Res 8:186–194

    CAS  PubMed  Google Scholar 

  • Forde BG, Leaver CJ (1980) Nuclear and cytoplasmic genes controlling synthesis of variant mitochondrial polypeptides in male-sterile maize. Proc Natl Acad Sci USA 77:418–422

    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  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  Google Scholar 

  • Geddy R, Brown GG (2007) Genes encoding pentatricopeptide repeat (PPR) proteins are not conserved in location in plant genomes and may be subject to diversifying selection. BMC Genomics 8:130

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Huang W, Wang L, Yi P, Tan X-L, Zhang X-M, Zhang Z-J, Li Y-S, Zhu Y-G (2006) RFLP analysis for mitochondrial genome of CMS-rice. Acta Genetica Sinica 33:330–338

    Article  CAS  PubMed  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 

  • International Rice Genome Sequencing Project (IRGSP) (2005) The map based sequence of rice genome. Nature 436:793–800

    Article  CAS  Google Scholar 

  • Itabashi E, Kazama T, Toriyama K (2009) Characterization of cytoplasmic male sterility of rice with Lead Rice cytoplasm in comparison with that with Chinsurah Boro II cytoplasm. Plant Cell Rep 28:233–239

    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  Google Scholar 

  • Jing R, Li X, Yi P, Zhu Y (2001) Mapping fertility-restoring genes of rice WA cytoplasmic male sterility using SSLP markers. Bot Bull Acad Sin 42:167–171

    CAS  Google Scholar 

  • Kazama T, Toriyama K (2003) A pentatricopeptide repeat-containing gene that promotes the processing of aberrant apt6 RNA of cytoplasmic male-sterile rice. FEBS Lett 544:99–102

    Article  CAS  PubMed  Google Scholar 

  • Kazama T, Nakamura T, Watanabe M, Sugita M, Toriyama K (2008) Suppression mechanism of mitochondrial ORF79 accumulation by Rf1 protein in BT-type cytoplasmic male sterile rice. Plant J 55:619–628

    Article  CAS  PubMed  Google Scholar 

  • Komori T, Ohta S, Murai N, Takakura Y, Kuraya Y, Suzuki S, Hiei Y, Imaseki H, Nitta N (2004) Map-based cloning of a fertility restorer gene, Rf-1, in rice (Oryza sativa L.). Plant J 37:315–325

    Article  CAS  PubMed  Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg LA (1987) MAPMAKER: An interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  CAS  PubMed  Google Scholar 

  • Lin H, Ouyang S, Egan A, Nobuta K, Haas BJ, Zhu W, Gu X, Silva JC, Meyers BC, Buell CR (2008) Characterization of paralogous protein families in rice. BMC Plant Biol 8:18

    Article  PubMed  CAS  Google Scholar 

  • Liu X-Q, Xu X, Tan Y-P, Li S-Q, Hu J, Huang J-Y, Yang D-C, Li Y-S, Zhu Y-G (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 Z-L, Xu H, Guo J-X, Liu Y-G (2007) Structural and expressional variations of the mitochondrial genome conferring the Wild Abortive type of cytoplasmic male sterility in rice. J Integr Plant Biol 49:908–914

    Article  CAS  Google Scholar 

  • Mather K (1951) The measurement of linkage in heredity, 2nd edn. Wiley, New York, p 149

    Google Scholar 

  • McCouch SR, Teytelman L, Xu Y, Lobos KB, Clare K, Walton M, Fu B, Maghirang R, Li Z, Xing Y, Zhang Q, Kono I, Yano M, Fjellstrom R, DeClerck G, Schneider D, Cartinhour S, Ware D, Stein L (2002) Development and mapping of 2, 240 new SSR markers for rice (Oryza sativa L.). DNA Res 9:199–207

    Article  CAS  PubMed  Google Scholar 

  • Mishra GP, Singh RK, Mohapatra T, Singh AK, Prabhu KV, Zaman FU, Sharma RK (2003) Molecular mapping of a gene for fertility restoration of wild abortive cytoplasmic male sterility using a Basmati rice restorer line. J Plant Biochem Biotech 12:37–42

    CAS  Google Scholar 

  • Narayanan KK, Senthilkumar P, Sridhar VV, Thomas G, Thomas J (1995) Organization of the mitochondrial cob2 pseudogene in different lines of rice. Theor Appl Genet 90:1087–1093

    Article  CAS  Google Scholar 

  • Narayanan KK, Senthikumar P, Venmadhi S, Thomas G, Thomas J (1996) Molecular genetics studies on the rice mitochondrial genome. In: Khush GS (Ed) Rice genetics III. Proceedings of third international rice genet symposium, international rice research institute, Los Bonos, Manila, The Philippines, pp 689–695

  • Newton ΚJ (1988) Plant mitochondrial genomes: organization, expression and variation. Annu Rev Plant Physiol Plant Mol Biol 39:503–532

    Article  CAS  Google Scholar 

  • O’Toole N, Hattori M, Andres C, Iida K, Lurin C, Schmitz-Linneweber C, Sugita M, Small I (2008) On the expansion of the pentatricopeptide repeat gene family in plants. Mol Biol Evol 25:1120–1128

    Article  PubMed  CAS  Google Scholar 

  • Parida SK, Dalal V, Singh AK, Singh NK, Mohapatra T (2009) Genic non-coding microsatellites in the rice genome: characterization, marker design and use in assessing genetic and evolutionary relationships among domesticated groups. BMC Genomics 10:140

    Article  PubMed  CAS  Google Scholar 

  • Pathania A, Kumar R, Kumar DV, Ashutosh, Dwivedi KK, Kirti PB, Prakash S, Chopra VL, Bhat SR (2007) A duplex coxI gene is associated with cytoplasmic male sterility in an alloplasmic Brassica juncea line derived from somatic hybridization with Diplotaxis catholica. J Genet 86:93–101

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Rice Chromosomes 11, 12 Sequencing Consortia (RCSC) (2005) The sequence of rice chromosomes 11 and 12 rich in disease resistance genes and recent gene duplications. BMC Biol 3:20

    Article  CAS  Google Scholar 

  • Rosamma CA, Vijayakumar NK (2005) Maintainers and restorers for CMS lines of rice. J Trop Agric 43:75–77

    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 

  • Sang T, Ge Song (2007) The puzzle of rice domestication. J Int Plant Biol 49:760–768

    Article  CAS  Google Scholar 

  • Schmitz-Linneweber C, Small I (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci 13:663–670

    Article  CAS  PubMed  Google Scholar 

  • Schnable PS, Wise RP (1998) The molecular basis of cytoplasmic male sterility and fertility restoration. Trends Plant Sci 3:175–180

    Article  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 

  • Tian X, Zheng J, Hu S, Yu J (2006) The rice mitochondrial genomes and their variations. Plant Physiol 140:401–410

    Article  CAS  PubMed  Google Scholar 

  • Vedel F, Pla M, Vitart V, Guteirres S, Chetrit P, De Paepe R (1994) Molecular basis of nuclear and cytoplasmic male sterility in higher plants. Plant Physiol Biochem 32:601–618

    CAS  Google Scholar 

  • Wang Z, Zou Y, Li X, Zhang Q, Chen L, Wu H, Su D, Chen Y, Guo J, Luo D, Long Y, Zhong Y, Liu YG (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  Google Scholar 

  • Yashitola J, Sundaram RM, Biradar SK, Thirumurugan T, Vishnupriya MR, Rajeshwari R, Viraktamath BC, Sarma NP, Sonti RV (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

    CAS  Google Scholar 

  • Zhang QY, Liu YG, Zhang GQ, Mei MT (2002) Molecular mapping of the fertility restorer gene Rf4 for WA cytoplasmic male sterility in rice. Acta Genet Sin 29:1001–1004

    PubMed  Google Scholar 

Download references

Acknowledgments

The work was partly funded under the NAAS-TATA Fellowship scheme awarded to the corresponding author by the National Academy of Agricultural Sciences, New Delhi. Part of the research work carried out by the first and the third authors for their M.Sc. degrees is included. Funding support to the first and the third authors in the form of fellowship by the Indian Agricultural Research Institute (IARI) and research facilities provided by the Project Director, National Research Centre on Plant Biotechnology, New Delhi are duly acknowledged.

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Authors and Affiliations

  1. National Research Centre on Plant Biotechnology, Indian Agricultural Research Institute, New Delhi, 110012, India

    Umakanta Ngangkham, Swarup K. Parida, Sandip De, K. Anand Raj Kumar, Nagendra K. Singh & Trilochan Mohapatra

  2. Division of Genetics, Indian Agricultural Research Institute, New Delhi, 110012, India

    Ashok K. Singh

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  1. Umakanta Ngangkham
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  2. Swarup K. Parida
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  3. Sandip De
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  4. K. Anand Raj Kumar
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  5. Ashok K. Singh
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  6. Nagendra K. Singh
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  7. Trilochan Mohapatra
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Correspondence to Trilochan Mohapatra.

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The authors Umakanta Ngangkham, Swarup K. Parida, Sandip De and K. Anand Raj Kumar have contributed equally to the work.

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Ngangkham, U., Parida, S.K., De, S. et al. Genic markers for wild abortive (WA) cytoplasm based male sterility and its fertility restoration in rice. Mol Breeding 26, 275–292 (2010). https://doi.org/10.1007/s11032-010-9397-1

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  • DOI: https://doi.org/10.1007/s11032-010-9397-1

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