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The genetic and molecular basis of cytoplasmic male sterility and fertility restoration in rice

  • Special Topic/Review/Developmental Genetics
  • Published:
Chinese Science Bulletin

Abstract

Cytoplasmic male sterility (CMS) is a maternally inherited characteristic found in many (>150) plant species. CMS/restoration systems are useful tools for hybrid seed production, and are ideal models for study of the interactions between nuclear and mitochondrial genomes. CMS/restoration systems in rice have been widely used for hybrid seed production, greatly contributing to the food supply. This article reviews the progress of the studies on the genetic and molecular basis of cytoplasmic male sterility and fertility restoration in rice.

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References

  1. Chase C, Babay-Laughnan S. Cytoplasmic male sterility and fertility restoration by nuclear genes. In: Daniell H, Chase C, eds. Molecular Biology and Biotechnology of Plant Organelles. Dordrecht: Kluwer Academic Publishers, 2004. 593–622

    Chapter  Google Scholar 

  2. Hanson M R, Bentolila S. Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell, 2004, 16: S154–S169

    Article  Google Scholar 

  3. Schnable P S, Wise R P. The molecular basis of cytoplasmic male sterility and fertility restoration. Trends Plant Sci, 1998, 3: 175–180

    Article  Google Scholar 

  4. Dewey R E, Timothy D H, Levings C S III. A mitochondrial protein associated with cytoplasmic male sterility in the T cytoplasm of maize. Proc Natl Acad Sci USA, 1987, 84: 5374–5378

    Article  Google Scholar 

  5. Dewey R E, Siedow J N, Timothy D H, et al. A 13-kilodalton maize mitochondrial protein in E. coli confers sensitivity to Bipolaris maydis toxin. Science, 1988, 239: 293–295

    Article  Google Scholar 

  6. Hack E, Lin C, Yang H, et al. T-URF 13 protein from mitochondria of Texas male-sterile maize (Zea mays L.): Its purification and submitochondrial localization, and immunogold labeling in anther tapetum during microsporogenesis. Plant Physiol, 1991, 95: 861–870

    Article  Google Scholar 

  7. Wise R P, Fliss A E, Pring D R, et al. urf13-T of T cytoplasm maize mitochondria encodes a 13-kD polypeptide. Plant Mol Biol, 1987, 9: 121–126

    Article  Google Scholar 

  8. Boeshore M L, Hanson M R, Izhar S. A variant mitochondrial DNA arrangement specific to Petunia stable sterile somatic hybrids. Plant Mol Biol, 1985, 4: 125–132

    Article  Google Scholar 

  9. Nivison H T, Sutton C A, Wilson R K, et al. Sequencing, processing, and localization of the petunia CMS-associated mitochondrial protein. Plant J, 1994, 5: 613–623

    Article  Google Scholar 

  10. Bonhomme S, Budar F, Lancelin D, et al. Sequence and transcript analysis of the Nco2.5 Ogura-specific fragment correlated with cytoplasmic male sterility in Brassica cybrids. Mol Gen Genet, 1992, 235: 340–348

    Article  Google Scholar 

  11. Grelon M, Budar F, Bonhomme S, et al. Ogura cytoplasmic male-sterility (CMS)-associated orf138 is translated into a mitochondrial membrane polypeptide in male-sterile Brassica cybrids. Mol Gen Genet, 1994, 243: 540–547

    Article  Google Scholar 

  12. Singh M, Brown G G. Suppression of cytoplasmic male sterility by nuclear genes alters expression of a novel mitochondrial gene region. Plant Cell, 1991, 3: 1349–1362

    Article  Google Scholar 

  13. Singh M, Hamel N, Menassa X, et al. Nuclear genes associated with a single brassica CMS restorer locus influence transcripts of three different mitochondrial gene regions. Genetics, 1996, 143: 505–516

    Google Scholar 

  14. Jean M, Brown G G, Landry B S. Genetics mapping of nuclear fertility restorer genes ofr the `Polima’ cytoplasmic male sterility in canola (Brassica napus L.) using DNA markers. Theor Appl Genet, 1997, 95: 321–328

    Article  Google Scholar 

  15. Akagi H, Sakamoto M, Shinjyo C, et al. A unique sequence located downstream from the rice mitochondrial apt6 may cause male sterility. Curr Genet, 1994, 25: 52–58

    Article  Google Scholar 

  16. Wang Z, Zou Y, Li X, et al. 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, 2006, 18: 676–687

    Article  Google Scholar 

  17. Yi P, Wang L, Sun Q, et al. Discovery of mitochondrial chimeric-gene associated with cytoplasmic male sterility of HL-rice. Chinese Sci Bull, 2002, 47: 744–747

    Article  Google Scholar 

  18. Liu F, Cui X C, Hrner H T, et al. Mitochondrial Aldehyde dehydrogenase activity is required for male fertility in maize. Plant Cell, 2001, 13: 1063–1078

    Article  Google Scholar 

  19. Small I D, Peeters N. The PPR motif—a TPR-related motif prevalent in plant organellar proteins. Trends Biochem Sci, 2000, 25: 46–47

    Article  Google Scholar 

  20. Lurin C, Andres C, Aubourg S, et al. Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell, 2004, 16: 2089–2103

    Article  Google Scholar 

  21. Schmitz-Linneweber C, Williams-Carrier R, Barkan A. RNA immunoprecipitation and microarray analysis show a chloroplast pentatricopeptide repeat protein to be associated with the 5□ region of mRNAs whose translation it activates. Plant Cell, 2005, 17: 2791–2804

    Article  Google Scholar 

  22. Shinjyo C. Cytoplasmic genetic male sterility in cultivated rice, Oryza sativa L. II. The inheritance of male sterility. Jpn J Genet, 1969, 44: 149–156

    Article  Google Scholar 

  23. Lin S C, Yuan L P. Hybrid rice breeding in China. Innovative approaches to rice breeding. In: IRRI ed. IRRI, Manila, Philippines, 1980. 35–51

    Google Scholar 

  24. Rao Y S. Cytohistology of cytoplasmic male sterile lines in hybrid rice. In: Smith W H, Bostian L R, Cervantes E, eds. Hybrid Rice. IRRI, Manila, Philippines, 1988. 115–128

    Google Scholar 

  25. Zhu Y. Biology of the Male Sterility in Rice (in Chinese). Wuhan, China: Wuhan University Press, 2000

    Google Scholar 

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

    Article  Google Scholar 

  27. Cheng S, Zhuang J, Fan Y, et al. Progress in Research and Development on Hybrid Rice: A super-domesticate in China. Ann Bot, 2007, 100: 959–966

    Article  Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

  30. Yuan L P. The execution and theory of developing hybrid rice. Chin Agric Sci, 1977, 1: 27–31

    Google Scholar 

  31. Yao F, Xu C, Yu S, et al. Mapping and genetic analysis of two fertility restorer loci in wild abortive cytoplasmic male sterility system of rice. Euphytica, 1997, 98: 183–187

    Article  Google Scholar 

  32. Zhang G, Bharaji T, Lu Y, et al. Mapping of the Rf-3 nuclear fertility restoring gene for WA cytoplasmic male sterility in rice using RAPD and RFLP markers. Theor Appl Genet, 1997, 94: 27–33

    Article  Google Scholar 

  33. Zhang Q Y, Liu Y G, Mei M T. Molecular mapping of the fertility restorer gene Rf4 for WA cytoplasmic male sterility. Acta Genet Sin, 2002, 29: 1001–1004

    Google Scholar 

  34. Kazama T, Nakamura T, Watanabe M, et al. Suppression mechanism of mitochondrial ORF79 accumulation by Rf1 protein in BT-type cytoplasmic male sterile rice. Plant J, 2008, 55: 619–628

    Article  Google Scholar 

  35. Kadowaki K, Suzaki T, Kazama S. A chimeric gene containing the 5□ portion of atp6 is associated with cytoplasmic male-sterility of rice. Mol Gen Genet, 1990, 224: 10–16

    Article  Google Scholar 

  36. Iwabuchi M, Kyozuka J, Shimamoto K. Processing followed by complete editing of an altered mitochondrial apt6 RNA restores fertility of cytoplasmic male sterile rice. EMBO J, 1993, 12: 1437–1446

    Google Scholar 

  37. He S, Abad A, Gelvin S B. A cytoplasmic male sterility-associated mitochondrial protein causes pollen disruption in transgenic tobacco. Proc Natl Acad Sci USA, 1996, 93: 11763–11768

    Article  Google Scholar 

  38. Sarria R, Lyznik A, Vallejos C E, Mackenzie S A. A cytoplasmic male sterility-associated mitochondrial peptide in common bean is post-translationally regulated. Plant Cell, 1998, 10: 1217–1228

    Article  Google Scholar 

  39. Duan S H, Li S Q, Li Y S, et al. Distribution and SNPs of the rice CMS-related gene in AA-genome of Oryza species. Hereditas, 2007, 29: 455–461

    Google Scholar 

  40. Liu Z, Xu H, Guo J X, Liu Y G. Structural and expressional variations of the mitochondrial genome conferring the WA type of CMS in rice. J Integr Plant Biol, 2007, 49: 908–914

    Article  Google Scholar 

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

    Article  Google Scholar 

  42. Akagi H, Nakamura A, Yokozeki-Misono Y, et al. 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, 2004, 108: 1449–1457

    Article  Google Scholar 

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

    Article  Google Scholar 

  44. Bentolila S, Alfonso A, Hanson, M. A pentatricopeptide repeat-containing gene restores fertility to male-sterile plants. Proc Natl Acad Sci USA, 2002, 99: 10887–10892

    Article  Google Scholar 

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

    Article  Google Scholar 

  46. Ikeda T M, Gray M W. Characterization of a DNA-binding protein implicated in transcription in wheat mitochondria. Mol Cell Biol, 1999, 19: 8113–8122

    Google Scholar 

  47. Lahmy S, Barneche F, Derancourt J, et al. A chloroplastic RNA-binding protein is a new member of the PPR family. FEBS Lett, 2000, 480: 255–260

    Article  Google Scholar 

  48. Nakamura T, Meierhoff K, Westhoff P, et al. RNA-binding properties of HC152, an Arabidopsis PPR protein involved in the processing of chloroplast RNA. Eur J Biochem, 2003, 270: 4070–4081

    Article  Google Scholar 

  49. Uyttewaal M, Arnal N, Quadrado M, et al. Characterization of Raphanus sativus pentatricopeptide repeat proteins encoded by the fertility restorer locus for Ogura cytoplasmic male sterility. Plant Cell, 2008, 20: 3331–3345

    Article  Google Scholar 

  50. Zubko M K. Mitochondrial tuning fork in nuclear homeotic functions. Trends Plant Sci, 2004, 9: 61–64

    Article  Google Scholar 

  51. Fujii S, Toriyama K. DCW11, down-regulated gene 11 in CW-type cytoplasmic male sterile rice, encoding mitochondrial protein phosphatase 2c is related to cytoplasmic male sterility. Plant Cell Physiol, 2008, 49: 633–640

    Article  Google Scholar 

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Correspondence to YaoGuang Liu.

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Guo, J., Liu, Y. The genetic and molecular basis of cytoplasmic male sterility and fertility restoration in rice. Chin. Sci. Bull. 54, 2404–2409 (2009). https://doi.org/10.1007/s11434-009-0322-0

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  • DOI: https://doi.org/10.1007/s11434-009-0322-0

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