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Theoretical and Applied Genetics

, Volume 109, Issue 3, pp 515–522 | Cite as

Physical mapping and putative candidate gene identification of a quantitative trait locus Ctb1 for cold tolerance at the booting stage of rice

  • K. SaitoEmail author
  • Y. Hayano-Saito
  • W. Maruyama-Funatsuki
  • Y. Sato
  • A. Kato
Original Paper

Abstract

Norin-PL8 is a cold-tolerant variety of rice (Oryza sativa L.) that was developed by introgressing chromosomal segments from a cold-tolerant tropical japonica variety, Silewah, into a template japonica variety, Hokkai241. We previously identified two closely linked quantitative trait loci, Ctb1 and Ctb2, for cold tolerance at the booting stage of Norin-PL8 in the long arm of chromosome 4. We report here the physical mapping of Ctb1 and the identification of the candidate genes. A total of 2,008 segregating individuals were screened for recombination in the Ctb1 region by a PCR-based screening, and a series of near-isogenic lines (NILs) were developed from progenies of recombinants. A comparison of the degrees of cold tolerance of the NILs indicated that Ctb1 is located in the 56-kb region covered by a bacterial artificial chromosome clone, OSJNBa0058 K23, that had been sequenced by the International Rice Genome Sequence Project. We found seven open reading frames (ORFs) in the 56-kb region. Two ORFs encoded receptor-like protein kinases that are possibly involved in signal transduction pathways. Proteins that may be associated with a ubiquitin-proteasome pathway were encoded by three ORFs, two of which encoded F-box proteins and one of which encoded a protein with a BAG domain. The other two ORFs encoded a protein with an OTU domain and an unknown protein. We were also able to show that Ctb1 is likely to be associated with anther length, which is one of major factors in cold tolerance at the booting stage.

Keywords

Quantitative Trait Locus Bacterial Artificial Chromosome Cold Tolerance Spikelet Fertility Japonica Variety 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

We thank the Rice Genome Research Program, Japan for providing RFLP probes and Eriko Fujii for her technical assistance. This work was supported by the Rice Genome Project sponsored by the Ministry of Agriculture, Forestry and Fisheries of Japan.

References

  1. Abe F, Saito K, Miura K, Toriyama K (2002) A single nucleotide polymorphism in the alternative oxidase gene among rice varieties differing in low temperature tolerance. FEBS Lett 527:181–185CrossRefPubMedGoogle Scholar
  2. Akagi H, Yokozeki Y, Inagaki A, Fujimura T (1996) Microsatellite DNA markers for rice chromosomes. Theor Appl Genet 93:1071–1077CrossRefGoogle Scholar
  3. Andaya VC, Mackill DJ (2003) QTLs conferring cold tolerance at the booting stage of rice using recombinant inbred lines from a japonica × indica cross. Theor Appl Genet 106:1084–1090PubMedGoogle Scholar
  4. Andrade MA, González-Guzmán M, Serrano R, Rodríguez PL (2001) A combination of the F-box motif and kelch repeats defines a large Arabidopsis family of F-box proteins. Plant Mol Biol 46:603–614CrossRefPubMedGoogle Scholar
  5. Bariknarová K, Takayama S, Homma S, Baker K, Cabezas E, Hoyt DW, Li Z, Satterthwait AC, Ely KR (2002) BAG4/SODD protein contains a short BAG domain. J Biol Chem 277:31172–31178CrossRefPubMedGoogle Scholar
  6. Bedinger P (1992) The remarkable biology of pollen. Plant Cell 4:879–887PubMedGoogle Scholar
  7. Dieterle M, Zhou YC, Schafer E, Funk M, Kretsch T (2001) EID1, an F-box protein involved in phytochrome A-specific light signaling. Genes Dev 15:939–944PubMedGoogle Scholar
  8. Dwyer KG, Kandasamy MK, Mahosky DI, Acciai J, Kudish BI, Miller JE, Nasrallah ME, Nasrallah JB (1994) A superfamily of S locus-related sequences in Arabidopsis: diverse structures and expression patterns. Plant Cell 6:1829–1843CrossRefPubMedGoogle Scholar
  9. Evans PC, Smith TC, Lai MJ, Williams MG, Burke DF, Heyninck K, Kreike MM, Beyaert R, Blundell TL, Kilshew PJ (2003) A novel type of deubiquitinating enzyme. J Biol Chem 278:23180–23186CrossRefPubMedGoogle Scholar
  10. Futsuhara Y, Toriyama K (1964) Studies on the testing methods of cold resistance in rice. Jpn J Breed 14:166–172Google Scholar
  11. Harushima Y, Yano M, Shomura A, Sato M, Shimano T, Kuboki Y, Yamamoto T, Lin SY, Antonio BA, Parco A, Kajiya H, Huang N, Yamamoto K, Nagamura Y, Kurata N, Khush GS, Sasaki T (1998) A high-density rice genetic linkage map with 2275 markers using a single F2 population. Genetics 148:479–494PubMedGoogle Scholar
  12. Ito N (1978) Male sterility caused by cooling treatment at the young microspore stage in rice plants. XVI. Changes in carbohydrates, nitrogenous and phosphorous compounds in rice anthers after cooling treatment. Jpn J Crop Sci 47:318–323Google Scholar
  13. Kawaguchi K, Shibuya N, Ishii T (1996) A novel tetrasaccharide, with a structure similar to the terminal sequence of an arabinogalactan-protein, accumulates in rice anthers in a stage-specific manner. Plant J 9:777–785CrossRefPubMedGoogle Scholar
  14. Kiyosue T, Wada M (2000) LKP1 (LOV kelch protein 1): a factor involved in the regulation of flowering time in Arabidopsis. Plant J 23:807–815PubMedGoogle Scholar
  15. Klimyuk VI, Carroll BJ, Thomas CM, Jones JDG (1993) Alkali treatment for rapid preparation of plant material for reliable PCR analysis. Plant J 3:493–494PubMedGoogle Scholar
  16. Kurata N, Nagamura Y, Yamamoto K, Harushima Y, Sue N, Wu J, Antonio BA, Shomura A, Shimizu T, Lin SY, Inoue T, Fukuda A, Shimao Y, Kuboki Y, Toyama T, Miyamoto Y, Kirihara T, Hayasaka K, Miyano A, Monna L, Zhong HS, Tamura Y, Wang ZX, Momma T, Umehara Y, Yano M, Sasaki T, Minobe Y (1994) A 300 kilobase interval genetic map of rice including 883 expressed sequences. Nat Genet 8:365–372PubMedGoogle Scholar
  17. Kuroda H, Takahashi N, Shimada H, Seki M, Shinozaki K, Matsui M (2002) Classification and expression analysis of Arabidopsis F-box-containing protein genes. Plant Cell Physiol 43:1073–1085CrossRefPubMedGoogle Scholar
  18. Li HB, Wang J, Liu AM, Liu KD, Zhang Q, Zou JS (1997) Genetic basis of low-temperature-sensitive sterility in indica-japonica hybrids of rice as determined by RFLP analysis. Theor Appl Genet 95:1092–1097Google Scholar
  19. Li HY, Gray JE (1997) Pollination-enhanced expression of a receptor-like protein kinase related gene in tobacco styles. Plant Mol Biol 33:653–665CrossRefPubMedGoogle Scholar
  20. Lüders J, Demand J, Höhfeld J (2000) The ubiquitin-related BAG-1 provides a link between molecular chaperones Hsc70/Hsp70 and the proteasome. J Biol Chem 275:4613–4617CrossRefPubMedGoogle Scholar
  21. Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325PubMedGoogle Scholar
  22. Nelson DC, Lasswell J, Rogg LE, Cohen MA, Bartel B (2000) FKF1, a clock-controlled gene that regulates the transition to flowering in Arabidopsis. Cell 101:331–340PubMedGoogle Scholar
  23. Nishiyama I (1976) Male sterility caused by cooling treatment at the young microspore stage in rice plants XIII. Ultrastructure of tapetal hypertrophy without primary wall. Proc Crop Sci Soc Jpn 45:270–278Google Scholar
  24. Nishiyama I (1983) Male sterility caused by cooling treatment at the young microspore stage in rice plants XXVI. The number of ripened pollen grains and the difference in susceptibility to coolness among spikelets on the panicle. Jpn J Crop Sci Soc 52:307–313Google Scholar
  25. Oka H, Morishima H (1967) Variations in the breeding systems of a wild rice, Oryza perennis. Evolution 21:249–258Google Scholar
  26. Patton EE, Willems AR, Tyers M (1998) Combinatorial control in ubiquitin-dependent proteolysis: don’t Skp the F-box hypothesis. Trends Genet 14:236–248PubMedGoogle Scholar
  27. Rueggar M, Dewey E, Gray WM, Hobbie L, Tumer J, Estelle M (1998) The TIR1 protein of Arabidopsis functions in auxin response and is related to human SKP2 and yeast grr1p. Genes Dev 12:198–207PubMedGoogle Scholar
  28. Saito A, Yano M, Kishimoto N, Nakagahra M, Yoshimura A, Saito K, Kuhara S, Ukai Y, Kawase M, Nagamine T, Yoshimura S, Ideta O, Ohsawa R, Hayano Y, Iwata N, Sugiura M (1991) Linkage map of restriction fragment length polymorphism loci in rice. Jpn J Breed 41:665–670Google Scholar
  29. Saito K, Miura K, Nagano K, Hayano-Saito Y, Saito A, Araki H, Kato A (1995) Chromosomal location of quantitative trait loci for cool tolerance at the booting stage in rice variety ‘Norin-PL8’. Breed Sci 45:337–340Google Scholar
  30. Saito K, Miura K, Nagano K, Hayano-Saito Y, Araki H, Kato A (2001) Identification of two closely linked quantitative trait loci for cold tolerance on chromosome 4 of rice and their association with anther length. Theor Appl Genet 103:862–868CrossRefGoogle Scholar
  31. Samach A, Klenz JE, Kohalmi SE, Risseeuw E, Haughn GW, Crosby WL (1999) The UNUSUAL FLORAL ORGANS gene of Arabidopsis thaliana is an F-box protein required for normal patterning and growth in the floral meristem. Plant J 20:433–445CrossRefPubMedGoogle Scholar
  32. Satake T, Hayase H (1970) Male sterility caused by cooling treatment at the young microspore stage in rice plants. V. Estimation of pollen developmental stage and the most sensitive stage to coolness. Proc Crop Sci Soc Jpn 39:468–473Google Scholar
  33. Satake T, Toriyama K (1979) Two extremely cool-tolerance varieties. Int Rice Res Newsl 4(2):9–10Google Scholar
  34. Sheoran IS, Saini HS (1996) Drought-induced male sterility in rice: changes in carbohydrate levels and enzyme activities associated with the inhibition of starch accumulation in pollen. Sex Plant Reprod 9:161–169CrossRefGoogle Scholar
  35. Somers DE, Schultz TF, Milnamow M, Kay SA (2000) ZEITLUPE encodes a novel clock-associated PAS protein from Arabidopsis. Cell 101:319–329PubMedGoogle Scholar
  36. Sondermann H, Scheufler C, Schneider C, Höhfeld H, Hartl F-U, Moarefi I (2001) Functional evolution of Hsp70 nucleotide exchange factors. Science 291:1553–1557CrossRefPubMedGoogle Scholar
  37. Sung DY, Guy CL (2003) Physiological and molecular assessment of altered expression of Hsc70-1 in Arabidopsis. Evidence for pleiotropic consequences. Plant Physiol 132:979–987CrossRefPubMedGoogle Scholar
  38. Suzuki S (1981) Cold tolerance in rice plants with special reference to the floral characters. I. Varietal differences in anther and stigma lengths and the effects of planting densities on these characters. Jpn J Breed 31:57–64Google Scholar
  39. Suzuki S (1982) Cold tolerance in rice plants with special reference to the floral characters. II. Relations between floral characters and the degree of cold tolerance in segregating generations. Jpn J Breed 32:9–16Google Scholar
  40. Takeuchi Y, Hayasaka H, Chiba B, Tanaka I, Shimano T, Yamagishi M, Nagano K, Sasaki T, Yano M (2001) Mapping quantitative trait loci controlling cool-temperature tolerance at booting stage in temperate japonica rice. Breed Sci 51:191–197Google Scholar
  41. Tanno H, Xiong J, Dai L, Ye C (1999) Some characteristics of cool weather-tolerant rice varieties in Yunnan Province, China. Jpn J Crop Sci 68:508–514Google Scholar
  42. Temnykh S, Park WD, Ayres N, Cartinhour S, Hauck N, Lipovich L, Cho YG, Ishii T, McCouch SR (2000) Mapping and genome organization of microsatellite sequences in rice (Oryza sativa L.). Theor Appl Genet 100:697–712Google Scholar
  43. Townsend PA, Cutress RI, Sharp A, Brimmell M, Packham G (2003) BAG-1: a multifunctional regulator of cell growth and survival. Biochim Biophys Acta 1603:83–98CrossRefPubMedGoogle Scholar
  44. Walker JC (1993) Receptor-like protein kinase genes of Arabidopsis. Plant J 3:451–456PubMedGoogle Scholar
  45. Walker JC, Zhang R (1990) Relationship of a putative receptor protein kinase from maize to the S-locus glycoproteins of Brassica. Nature 345:743–746CrossRefPubMedGoogle Scholar
  46. Xie DX, Feys BF, James S, Nieto-Rostro M, Turner JG (1998) COI1: An Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280:1091–094PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • K. Saito
    • 1
    Email author
  • Y. Hayano-Saito
    • 1
  • W. Maruyama-Funatsuki
    • 1
  • Y. Sato
    • 1
  • A. Kato
    • 1
  1. 1.National Agricultural Research Center for Hokkaido RegionSapporoJapan

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