Skip to main content
Log in

Temperature-sensitive splicing is an important molecular regulation mechanism of thermosensitive genic male sterility in rice

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

Abstract

Photoperiod and temperature-sensitive genetic male sterility (PGMS and TGMS) plants have a number of desirable characteristics for hybrid production. Two-line hybrids developed using the PGMS/TGMS system now account for a large proportion of rice production in China. In this paper, we summarize recent advances on molecular regulation mechanisms and genetics of PGMS/TGMS in rice. We suggest that temperature-sensitive splicing, an important posttranscriptional regulatory mechanism in modulating gene expression and eventually development and differentiation, is also an important molecular regulation mechanism of TGMS in rice. We review those factors involved in temperature-sensitive splicing like cis splice site, snRNA, trans pre-mRNA splicing protein and SR proteins, and delineate that splicing could be regulated by a complex cell signaling pathway. These might shed light on other unknown molecular PGMS/TGMS mechanisms.

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

  1. Ma H. Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol, 2005, 56: 393–434

    Article  Google Scholar 

  2. Shi M S. The discovery and preliminary studies of the photoperiodsensitive recessive male sterile rice (Oryza sativa L. ssp. japonica) (in Chinese). Sci Agric Sin, 1985, 2: 44–48

    Google Scholar 

  3. Zhang Z G. The influence of photoperiod on pollen fertility change of Hubei photoperiod-sensitive genic male sterile rice (in Chinese). Chin J Rice Sci, 1987, 1: 137–143

    Google Scholar 

  4. Yuan L P, Peng J M. Hybrid Rice and World Food Security (in Chinese). Beijing: China Science and Technology Press, 2005

    Google Scholar 

  5. Zhang Q F, Shen B Z, Dai X K, et al. Using bulked extremes and recessive class to map genes for photoperiod-sensitive genic male sterility in rice. Proc Natl Acad Sci USA, 1994, 91: 8675–8679

    Article  Google Scholar 

  6. Mei M H, Dai X K, Xu C G, et al. Mapping and genetic analysis of the genes for photoperiod-sensitive genic sterility in rice using the original mutant Nongken 58S. Crop Sci, 1999, 39: 1711–1715

    Article  Google Scholar 

  7. Mei M H, Chen L, Zhang Z H, et al. Pms3 is the locus causing the original photoperiod-sensitive genic male sterility mutation of Nongken 58S. Sci China Ser C-Life Sci, 1999, 42: 316–322

    Google Scholar 

  8. Lu Q, Li X H, Guo D, et al. Localization of pms3, a gene for photo period sensitive genic male sterility, to a 28.4-kb DNA fragment. Mol Genet Genomics, 2005, 273: 507–511

    Article  Google Scholar 

  9. Liu N, Shan Y, Wang F P, et al. Identification of an 85-kb DNA fragment containing pms1, a locus for photoperiod-sensitive genic male sterility in rice. Mol Genet Genomics, 2001, 266: 271–275

    Article  Google Scholar 

  10. Yu J S, Fan Y R, Liu N, et al. Rapid genome evolution in Pms1 region of rice revealed by comparative sequence analysis. Chinese Sci Bull, 2007, 52: 912–921

    Article  Google Scholar 

  11. Peng H F, Zhang Z F, Wu B, et al. Molecular mapping of two reverse photoperiod-sensitive genic male sterility genes (rpms1 and rpms2) in rice (Oryza sativa L.). Theor Appl Genet, 2008, 118: 77–83

    Article  Google Scholar 

  12. Wang B, Xu W W, Wang J Z, et al. Tagging and mapping the thermo-sensitive genic male-sterile gene in rice with molecular markers. Theor Appl Genet, 1995, 91: 1111–1114

    Google Scholar 

  13. Jia J H, Zhang D S, Li C Y, et al. Molecular mapping of the reverse thermo-sensitive genic male-sterile gene (rtms1) in rice. Theor Appl Genet, 2001, 103: 607–612

    Article  Google Scholar 

  14. Yamaguchi Y, Ikeda R, Hirasawa H, et al. Linkage analysis of the thermo-sensitive genic male sterility gene Tms2 in rice (Oryza sativa L.). Breed Sci, 1997, 47: 371–377

    Google Scholar 

  15. Lopez M T, Toojinda T, Vanavichit A, et al. Microsatellite markers flanking the tms2 gene facilitated tropical TGMS rice line development. Crop Sci, 2003, 43: 2267–2271

    Google Scholar 

  16. Pitnjam K, Chakhonkaen S, Toojinda T, et al. Identification of a deletion in tms2 and development of gene-based markers for selection. Planta, 2008, 228: 813–822

    Article  Google Scholar 

  17. Subudhi P K, Borkakati R K, Virmani S S, et al. Molecular mapping of a thermosensitive genetic male-sterility gene in rice using bulked segregant analysis. Genome, 1997, 40: 188–194

    Article  Google Scholar 

  18. Wang Y G, Xing Q H, Deng Q Y, et al. Fine mapping of the rice thermo-sensitive genic male-sterile gene tms5. Theor Appl Genet, 2003, 107: 917–921

    Article  Google Scholar 

  19. Yang Q K, Liang C Y, Zhuang W, et al. Characterization and identification of the candidate gene of rice thermo-sensitive genic male sterile gene tms5 by mapping. Planta, 2007, 225: 321–330

    Article  Google Scholar 

  20. Dong N V, Subudhi P K, Luong P N, et al. Molecular mapping of a rice gene conditioning thermosensitive genic male sterility using AFLP, RFLP and SSR techniques. Theor Appl Genet, 2000, 100: 727–734

    Article  Google Scholar 

  21. Reddy O, Siddiq E, Ali N, et al. Genetic analysis of temperature-sensitive male sterility in rice. Theor Appl Genet, 2000, 100: 794–801

    Article  Google Scholar 

  22. Wang C H, Zhang P, Ma Z R, et al. Development of a genetic marker linked to a new thermo-sensitive male sterile gene in rice (Oryza sativa L.). Euphytica, 2004, 140: 217–222

    Article  Google Scholar 

  23. Lee D S, Chen L J, Suh H S. Genetic characterization and fine mapping of a novel thermo-sensitive genic male-sterile gene tms6 in rice (Oryza sativa L.). Theor Appl Genet, 2005, 111: 1271–1277

    Article  Google Scholar 

  24. Koh H J, Heu M H. Agronomic characteristics of a mutant for genic male sterility-chalky endosperm and its utilization on F1 hybrid breeding system in rice. Korean J Crop Sci, 1995, 40: 684–696

    Google Scholar 

  25. Koh H J, Son Y H, Heu M H, et al. Molecular mapping of a new genic male-sterility gene causing chalky endosperm in rice (Oryza sativa L.). Euphytica, 1999, 106: 57–62

    Article  Google Scholar 

  26. Woo M O, Ham T H, Ji H S, et al. Inactivation of the UGPase1 gene causes genic male sterility and endosperm chalkiness in rice (Oryza sativa L.). Plant J, 2008, 54: 190–204

    Article  Google Scholar 

  27. Chen R Z, Zhao X, Shao Z, et al. Rice UDP-glucose pyrophosphorylase1 is essential for pollen callose deposition and its cosuppression results in a new type of thermosensitive genic male sterility. Plant Cell, 2007, 19: 847–861

    Article  Google Scholar 

  28. Christensen A H, Sharrock R A, Quail P H. Maize polyubiquitin genes: Structure, thermal perturbation of expression and transcript splicing, and promoter activity following transfer to protoplasts by electroporation. Plant Mol Biol, 1992, 18: 675–689

    Article  Google Scholar 

  29. Bowman J L, Smyth D R, Meyerowitz E M. Genes directing flower development in Arabidopsis. Plant Cell, 1989, 1: 37–52

    Article  Google Scholar 

  30. Zachgo S, Silva E A, Motte P, et al. Functional analysis of the Antirrhinum floral homeotic DEFICIENS gene in vivo and in vitro by using a temperature-sensitive mutant. Development, 1995, 121: 2861–2875

    Google Scholar 

  31. Sablowski R W, Meyerowitz E M. Temperature-sensitive splicing in the floral homeotic mutant apetala3-1. Plant Cell, 1998, 10: 1453–1463

    Article  Google Scholar 

  32. Yi Y, Jack T. An intragenic suppressor of the Arabidopsis floral organ identity mutant apetala3-1 functions by suppressing defects in splicing. Plant Cell, 1998, 10: 1465–1477

    Article  Google Scholar 

  33. Majercak J, Sidote D, Hardin P E, et al. How a circadian clock adapts to seasonal decreases in temperature and day length. Neuron, 1999, 24: 219–230

    Article  Google Scholar 

  34. Colot H V, Loros J J, Dunlap J. Temperature-modulated alternative splicing and promoter use in the circadian clock gene frequency. Mol Biol Cell, 2005, 16: 5563–5571

    Article  Google Scholar 

  35. Diernfellner A C R, Schafmeier T, Merrow M W, et al. Molecular mechanism of temperature-sensing by the circadian clock of Neurospora crassa. Genes Dev, 2005, 19: 1968–1973

    Article  Google Scholar 

  36. Majercak J, Chen W F, Edery I. Splicing of the period gene 3′-terminal intron is regulated by light, circadian clock factors, and phospholipase C. Mol Cell Biol, 2004, 24: 3359–3372

    Article  Google Scholar 

  37. Collins B H, Rosato E, Kyriacou C P. Seasonal behavior in Drosophila melanogaster requires the photoreceptors, the circadian clock, and phospholipase C. Proc Natl Acad Sci USA, 2004, 101: 1945–1950

    Article  Google Scholar 

  38. Chen W F, Low K H, Lim C, et al. Thermosensitive splicing of a clock gene and seasonal adaptation. Cold Spring Harb Symp Quant Biol, 2007, 72: 599–606

    Article  Google Scholar 

  39. Brunner M, Schafmeier T. Transcriptional and post-transcriptional regulation of the circadian clock of cyanobacteria and Neurospora. Genes Dev, 2006, 20: 1061–1074

    Article  Google Scholar 

  40. Reddy A S N. Alternative splicing of pre-messenger RNAs in plants in the genomic era. Annu Rev Plant Biol, 2007, 58: 267–294

    Article  Google Scholar 

  41. Rappsilber J, Ryder U, Lamond A I, et al. Large scale proteomic analysis of the human spliceosome. Genome Res, 2002, 12: 1231–1245

    Article  Google Scholar 

  42. Zhou Z, Licklider L J, Gygi S P, et al. Comprehensive analysis of the human spliceosome. Nature, 2002, 419: 182–185

    Article  Google Scholar 

  43. Chen Y I G, Moore R E, Ge H Y, et al. Proteomic analysis of in vivo-assembled pre-mRNA splicing complexes expands the catalog of participating factors. Nucleic Acids Res, 2007, 35: 3928–3944

    Article  Google Scholar 

  44. Lin R J, Lustig A, Abelson J. Splicing of yeast nuclear pre-mRNA in vitro requires a functional 40S spliceosome and several extrinsic factors. Genes Dev, 1987, 1: 7–18

    Article  Google Scholar 

  45. Grainger R J, Beggs J D. Prp8 protein: At the heart of the spliceosome. RNA, 2005, 11: 533–557

    Article  Google Scholar 

  46. Schwer B, Guthrie C. A conformational rearrangement in the spliceosome is dependent on PRP16 and ATP hydrolysis. EMBO J, 1992, 11: 5033–5039

    Google Scholar 

  47. Wang Y, Wagner J D O, Guthrie C. The DEAH-box splicing factor Prp16 unwinds RNA duplexes in vitro. Curr Biol, 1998, 8: 441–451

    Article  Google Scholar 

  48. Raghunathan P L, Guthrie C. RNA unwinding in U4/U6 snRNPs requires ATP hydrolysis and the DEIH-box splicing factor Brr2. Curr Biol, 1998, 8: 847–855

    Article  Google Scholar 

  49. Kim S H, Lin R J. Spliceosome activation by PRP2 ATPase prior to the first transesterification reaction of pre-mRNA splicing. Mol Cell Biol, 1996, 16: 6810–6819

    Google Scholar 

  50. Wagner J D, Jankowsky E, Company M, et al. The DEAH-box protein PRP22 is an ATPase that mediates ATP-dependent mRNA release from the spliceosome and unwinds RNA duplexes. EMBO J. 1998, 17: 2926–2937

    Article  Google Scholar 

  51. Arenas J E, Abelson J N. Prp43: An RNA helicase-like factor involved in spliceosome disassembly. Proc Natl Acad Sci USA, 1997, 94: 11798–11802

    Article  Google Scholar 

  52. Blanton S, Srinivasan A, Rymond B C. PRP38 encodes a yeast protein required for pre-mrna splicing and maintenance of stable U6 small nuclear RNA levels. Mol Cell Biol, 1992, 12: 3939–3947

    Google Scholar 

  53. Chan S P, Kao D I, Tsai W Y, et al. The Prp19p-associated complex in spliceosome activation. Science, 2003, 302: 279–282

    Article  Google Scholar 

  54. Crotti L B, Bacikova D, Horowitz D S. The Prp18 protein stabilizes the interaction of both exons with the U5 snRNA during the second step of pre-mRNA splicing. Genes Dev, 2007, 21: 1204–1216

    Article  Google Scholar 

  55. Valadkhan S. The spliceosome: Caught in a web of shifting interactions. Curr Opin Struct Biol, 2007, 17: 310–315

    Article  Google Scholar 

  56. Madhani H D, Bordonne R, Guthrie C. Multiple roles for U6 snRNA in the splicing pathway. Genes Dev, 1990, 4: 2264–2277

    Article  Google Scholar 

  57. Alvarez C J, Romfo C M, Vanhoy R W, et al. Mutational analysis of U1 function in Schizosaccharomyces pombe: Pre-mRNAs differ in the extent and nature of their requirements for this snRNA in vivo. RNA, 1996, 2: 404–418

    Google Scholar 

  58. Maddock J R, Roy J, Woolford J L J. Six novel genes necessary for pre-mRNA splicing in Saccharomyces cerevisiae. Nucleic Acids Res, 1996, 24: 1037–1044

    Article  Google Scholar 

  59. Xiao S H, Manley J L. Phosphorylation of the ASF/SF2 RS domain affects both protein-protein and protein-RNA interactions and is necessary for splicing. Genes Dev, 1997, 11: 334–344

    Article  Google Scholar 

  60. Xiao S H, Manley J L. Phosphorylation-dephosphorylation differentially affects activities of splicing factor ASF/SF2. EMBO J, 1998, 17: 6359–6367

    Article  Google Scholar 

  61. Gui J F, Lane W S, Fu X D. A serine kinase regulates intracellular localization of splicing factors in the cell cycle. Nature, 1994, 369: 678–682

    Article  Google Scholar 

  62. Colwill K, Pawson T, Andrews B, et al. The Clk/Sty protein kinase phosphorylates SR splicing factors and regulates their intranuclear distribution. EMBO J, 1996, 15: 265–275

    Google Scholar 

  63. Misteli T, Spector D L. Serine/threonine phosphatase 1 modulates the subnuclear distribution of pre-mRNA splicing factors. Mol Biol Cell, 1996, 7: 1559–1572

    Google Scholar 

  64. Misteli T. RNA splicing: what has phosphorylation got to do with it? Curr Biol, 1999, 9: 198–200

    Article  Google Scholar 

  65. Shi Y, Reddy B, Manley J L. PP1/PP2A phosphatases are required for the second step of pre-mRNA splicing and target specific snRNP proteins. Mol Cell, 2006, 23: 819–829

    Article  Google Scholar 

  66. Huang Y, Steitz J A. Splicing factors SRp20 and 9G8 promote the nucleocytoplasmic export of mRNA. Mol Cell, 2001, 7: 899–905

    Article  Google Scholar 

  67. Lemaire R, Prasad J, Kashima T, et al. Stability of a PKCI-1-related mRNA is controlled by the splicing factor ASF/SF2: A novel function for SR proteins. Genes Dev, 2002, 16: 594–607

    Article  Google Scholar 

  68. Sanford J R, Gray N K, Beckmann K, et al. A novel role for shuttling SR proteins in mRNA translation. Genes Dev, 2004, 18: 755–768

    Article  Google Scholar 

  69. Graveley B R. Sorting out the complexity of SR protein functions. RNA, 2000, 6: 1197–1211

    Article  Google Scholar 

  70. Iida K, Go M. Survey of conserved alternative splicing events of mRNAs encoding SR proteins in land plants. Mol Biol Evol, 2006, 23: 1085–1094

    Article  Google Scholar 

  71. Isshiki M, Tsumoto A, Shimamoto K. The serine/arginine-rich protein family in rice plays important roles in constitutive and alternative splicing of pre-mRNA. Plant Cell, 2006, 18: 146–158

    Article  Google Scholar 

  72. Reddy A S N. Plant serine/arginine-rich proteins and their role in pre-mRNA splicing. Trends Plant Sci, 2004, 9: 541–547

    Article  Google Scholar 

  73. Hopf N, Plesofsky-Vig N, Brambl R. The heat shock response of pollen and other tissues of maize. Plant Mol Biol, 1992, 19: 623–630

    Article  Google Scholar 

  74. Larkin P D, Park W D. Transcript accumulation and utilization of alternate and nonconsensus splice sites in rice granule-bound starch synthase are temperature-sensitive and controlled by a single-nucleotide polymorphism. Plant Mol Biol, 1999, 40: 719–727

    Article  Google Scholar 

  75. Palusa S G, Ali G S, Reddy A S N. Alternative splicing of premRNAs of Arabidopsis serine/arginine-rich proteins: regulation by hormones and stresses. Plant J, 2007, 49: 1091–1107

    Article  Google Scholar 

  76. Yost H J, Petersen R B, Lindquist S. RNA metabolism: Strategies for regulation in the heat shock response. Trends Genet, 1990, 6: 223–227

    Article  Google Scholar 

  77. Shin C, Manley J L. The SR protein SRp38 represses splicing in M phase cells. Cell, 2002, 111: 407–417

    Article  Google Scholar 

  78. Shin C, Feng Y, Manley J L. Dephosphorylated SRp38 acts as a splicing repressor in response to heat shock. Nature, 2002, 427: 553–558

    Article  Google Scholar 

  79. Shi Y S, Manley J L. A complex signaling pathway regulates SRp38 phosphorylation and pre-mRNA splicing in response to heat shock. Mol Cell, 2007, 28: 79–90

    Article  Google Scholar 

  80. Feng Y, Chen M, Manley J L. Phosphorylation switches the general splicing repressor SRp38 to a sequence-specific activator. Nat Struct Mol Biol, 2008, 15: 1040–1048

    Article  Google Scholar 

  81. Jiang S Y, Cai M, Ramachandran S. ORYZA SATIVA MYOSIN XI B controls pollen development by photoperiod-sensitive protein localizations. Dev Biol, 2007, 304: 579–592

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to GuangCun He.

Additional information

Supported by the National Key Basic Research and Development Program of China (Grant No. 2007CB108705) and the National Natural Science Foundation of China (Grant No. 30700448)

About this article

Cite this article

Chen, R., Pan, Y., Wang, Y. et al. Temperature-sensitive splicing is an important molecular regulation mechanism of thermosensitive genic male sterility in rice. Chin. Sci. Bull. 54, 2354–2362 (2009). https://doi.org/10.1007/s11434-009-0349-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11434-009-0349-2

Keywords

Navigation