Advertisement

Functional & Integrative Genomics

, Volume 9, Issue 1, pp 97–108 | Cite as

The 172-kb genomic DNA region of the O. rufipogon yld1.1 locus: comparative sequence analysis with O. sativa ssp. japonica and O. sativa ssp. indica

  • Beng-Kah Song
  • Ingo Hein
  • Arnis Druka
  • Robbie Waugh
  • David Marshall
  • Kalaivani Nadarajah
  • Soon-Joo Yap
  • Wickneswari Ratnam
Original Paper

Abstract

Common wild rice (Oryza rufipogon) plays an important role by contributing to modern rice breeding. In this paper, we report the sequence and analysis of a 172-kb genomic DNA region of wild rice around the RM5 locus, which is associated with the yield QTL yld1.1. Comparative sequence analysis between orthologous RM5 regions from Oryza sativa ssp. japonica, O. sativa ssp. indica and O. rufipogon revealed a high level of conserved synteny in the content, homology, structure, orientation, and physical distance of all 14 predicted genes. Twelve of the putative genes were supported by matches to proteins with known function, whereas two were predicted by homology to rice and other plant expressed sequence tags or complementary DNAs. The remarkably high level of conservation found in coding, intronic and intergenic regions may indicate high evolutionary selection on the RM5 region. Although our analysis has not defined which gene(s) determine the yld1.1 phenotype, allelic variation and the insertion of transposable elements, among other nucleotide changes, represent potential variation responsible for the yield QTL. However, as suggested previously, two putative receptor-like protein kinase genes remain the key suspects for yld1.1.

Keywords

Oryza rufipogon Yield QTL yld1.1 Comparative sequence analysis Microcolinearity 

Notes

Acknowledgements

We specifically thank Dr. Nils Rostoks and other staff in the Scottish Crop Research Institute, Dundee, Scotland for their help and encouragement. This work is supported by the Malaysian Ministry of Science and Technology, grant number IRPA 01-03-03-0001-BTK/ER/001 and the Scottish Executive Environment and Rural Affairs Department.

Supplementary material

10142_2008_91_MOESM1_ESM.doc (278 kb)
Supplementary Table 1 Annotation comparison between the GenBank, TIGR and reannotation of the RM5 region in japonica genome and O. rufipogon genome (DOC 278 KB).

References

  1. Ahn S, Tanksley SD (1993) Comparative linkage maps of the rice and maize genomes. Proc Natl Acad Sci U S A 90:7980–7984PubMedCrossRefGoogle Scholar
  2. Ankeny RA (2003) Sequencing the genome from nematode to human: changing methods, changing science. Endeavour 27:87–92PubMedCrossRefGoogle Scholar
  3. Armstead IP, Turner LB, Farrell M, Skøt L, Gomez P, Montoya T, Donnison IS, King IP, Humphreys MO (2004) Synteny between a major heading-date QTL in perennial ryegrass (Lolium perenne L.) and the Hd3 heading-date locus in rice. Theor Appl Genet 108:822–828PubMedCrossRefGoogle Scholar
  4. Bautista NS, Shimadzutsu K, Teranishi T, Takamatsu S, Kobayashi N, Uchida N, Kamijima O, Ishii T (2000) Rice wild QTL analysis. 4. QTL analysis for several agronomic characters using BC2 population between Oryza rufipogon and O. sativa IR36. Breeding Res 2:132Google Scholar
  5. Bautista NS, Solis R, Kamijima O, Ishii T (2001) RAPD, RFLP and SSLP analyses of phylogenetic relationships between cultivated and wild species of rice. Genes Genet Syst 76:71–79PubMedCrossRefGoogle Scholar
  6. Bennetzen JL (2000) Comparative sequence analysis of plant nuclear genomes: microcolinearity and its many exceptions. Plant Cell 12:1021–1029PubMedCrossRefGoogle Scholar
  7. Bennetzen JL, Coleman C, Liu R, Ma J, Ramakrishna W (2004) Consistent over-estimation of gene number in complex plant genomes. Curr Opin Plant Biol 7:732–736PubMedCrossRefGoogle Scholar
  8. Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27:573–580PubMedCrossRefGoogle Scholar
  9. Burge C, Karlin S (1997) Prediction of complete gene structures in human genomic DNA. J Mol Biol 268:78–94PubMedCrossRefGoogle Scholar
  10. Caldwell KS, Langridge P, Powell W (2004) Comparative sequence analysis of the region harboring the hardness locus in barley and its colinear region in rice. Plant Physiol 136:3177–3190PubMedCrossRefGoogle Scholar
  11. Chang TT (1976) The origin, evolution, cultivation, dissemination and diversification of Asian and African rices. Euphytica 25:425–441CrossRefGoogle Scholar
  12. Cheema KK, Bains NS, Mangat GS, Das A, Vikal Y, Brar DS, Khush GS, Singh K (2008) Development of high yielding IR64 × Oryza rufipogon (GriV.) introgression lines and identification of introgressed alien chromosome segments using SSR markers. Euphytica 160:401–409CrossRefGoogle Scholar
  13. Chen E, Schlessinger D, Kere J (1993) Ordered shotgun sequencing, a strategy for integrated mapping and sequencing of YAC clones. Genomics 17:651–656PubMedCrossRefGoogle Scholar
  14. Cheng C, Motohashi R, Tsuchimoto S, Fukuta Y, Ohtsubo H, Ohtsubo E (2003) Polyphyletic origin of cultivated rice: based on the interspersion pattern of SINEs. Mol Biol Evol 20:67–75PubMedCrossRefGoogle Scholar
  15. Cho YC, Suh JP, Choi IS, Hong HC, Beak MK, Kang KH, Kim YG, Ahn SN, Choi HC, Hwang HG, Moon HP (2003) QTLs analysis of yield and its related traits in wild rice relative Oryza rufipogon. Treatises Crop Res Korea 4:19–29Google Scholar
  16. Devos KM (2005) Updating the ‘Crop Circle’. Curr Opin Plant Biol 8:155–162PubMedCrossRefGoogle Scholar
  17. Devos KM, Gale MD (2000) Genome relationships: the grass model in current research. Plant Cell 12:637–646PubMedCrossRefGoogle Scholar
  18. Dubcovsky J, Ramakrishna W, SanMiguel P, Busso CS, Yan L, Shiloff BA, Bennetzen JL (2001) Comparative sequence analysis of collinear barley and rice bacterial artificial chromosomes. Plant Physiol 125:1342–1353PubMedCrossRefGoogle Scholar
  19. El-Assal S, Alonso-Blanco C, Peeters AJ, Raz V, Koornneef M (2001) A QTL for flowering time in Arabidopsis reveals a novel allele of CRY2. Nat Genet 29:435–440CrossRefGoogle Scholar
  20. Engler F, Soderlund C (2002) Software for physical maps. In: Dunham I (ed) Genomic mapping and sequencing. Horizon Press, Genome Technology Series, Norfolk, UK, pp 201–236Google Scholar
  21. Feuillet C, Keller B (2002) Comparative genomics in the grass family: molecular characterization of grass genome structure and evolution. Ann Bot 89:3–10PubMedCrossRefGoogle Scholar
  22. Gale MD, Devos KM (1998) Comparative genetics in the grasses. Proc Natl Acad Sci U S A 95:1971–1974PubMedCrossRefGoogle Scholar
  23. Glaszmann JC (1987) Isozymes and classification of Asian rice varieties. Theor Appl Genet 74:21–30CrossRefGoogle Scholar
  24. Goff SA, Ricke D, Lan TH et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296:92–100PubMedCrossRefGoogle Scholar
  25. Gu YQ, Coleman-Derr D, Kong XY, Anderson OD (2004) Rapid genome evolution revealed by comparative sequence analysis of orthologous regions from four triticeae genomes. Plant Physiol 135:459–470PubMedCrossRefGoogle Scholar
  26. Hackauf B, Wehling P (2005) Approaching the self-incompatibility locus Z in rye (Secale cereale L.) via comparative genetics. Theor Appl Genet 110:832–845PubMedCrossRefGoogle Scholar
  27. Han B, Xue Y (2003) Genome-wide intraspecific DNA sequence variations in rice. Curr Opin Plant Biol 6:134–138PubMedCrossRefGoogle Scholar
  28. He G, Luo X, Tian F, Li K, Zhu Z, Su W, Qian X, Fu Y, Wang X, Sun C, Yang J (2006) Haplotype variation in structure and expression of a gene cluster associated with a quantitative trait locus for improved yield in rice. Genome Res 16:618–626PubMedCrossRefGoogle Scholar
  29. Ishii T, Terachi T, Tsunewaki K (1988) Restriction endonuclease analysis of chloroplast DNA from A-genome diploid species of rice. Jpn J Genet 63:523–536CrossRefGoogle Scholar
  30. Ishii T, Xu Y, McCouch SR (2001) Nuclear- and chloroplast-microsatellite variation in A-genome species of rice. Genome 44:658–666PubMedCrossRefGoogle Scholar
  31. Jabbari K, Cruveiller S, Clay O, Le Saux J, Bernardi G (2004) The new genes of rice: a closer look. Trends Plant Sci 9:281–285PubMedCrossRefGoogle Scholar
  32. Jurka J (1997) Repbase Update Genetic Information Research Institute (on-line). http://www.girinst.org/Repbase_Update.html (8 Aug 2005)
  33. Keller B, Feuillet C (2000) Colinearity and gene density in grass genomes. Trends Plant Sci 5:246–251PubMedCrossRefGoogle Scholar
  34. Kellogg EA, Bennetzen JR (2004) The evolution of nuclear genome structure in seed plants. Am J Bot 91:1709–1725CrossRefGoogle Scholar
  35. Khush GS (1997) Origin, dispersal, cultivation and variation of rice. Plant Mol Biol 35:25–34, 153Google Scholar
  36. Kikuchi S, Satoh K, Nagata T, et al. (2003) Collection, mapping, and annotation of over 28,000 cDNA clones from japonica rice. Science 301:376–379PubMedCrossRefGoogle Scholar
  37. Li J, Thomson M, McCouch SR (2004) Fine mapping of a grain-weight quantitative trait locus in the pericentromeric region of rice chromosome 3. Genetics 168:2187–2195PubMedCrossRefGoogle Scholar
  38. Li L, Strahwald J, Hofferbert HR, Lübeck J, Tacke E, Junghans H, Wunder J, Gebhardt C (2005) DNA variation at the invertase locus invGE/GF is associated with tuber quality traits in populations of potato breeding clones. Genetics 170:813–821PubMedCrossRefGoogle Scholar
  39. Liang F, Deng Q, Wang Y, Xiong Y, Jin D, Li J, Wang B (2004) Molecular marker-assisted selection for yield-enhancing genes in the progeny of “9311×O. rufipogon” using SSR. Euphytica 139:159–165CrossRefGoogle Scholar
  40. Lin H, Liang ZW, Sasaki T, Yano M (2003) Fine mapping and characterization of quantitative trait loci Hd4 and Hd5 controlling heading date in rice. Breed Sci 53:51–59CrossRefGoogle Scholar
  41. Lukashin AV, Borodovsky M (1998) GeneMark.hmm: new solutions for gene finding. Nucleic Acids Res 26:1107–1115PubMedCrossRefGoogle Scholar
  42. Ma J, Bennetzen JL (2004) Rapid recent growth and divergence of rice nuclear genomes. P Natl Acad Sci U S A 101:12404–12410CrossRefGoogle Scholar
  43. Ma J, SanMiguel P, Lai J, Messing J, Bennetzen JL (2005) DNA Rearrangement in orthologous Orp regions of the maize, rice and sorghum genomes. Genetics 170:1209–1220PubMedCrossRefGoogle Scholar
  44. McCouch SR, Sweeney M, Li J, Jiang H, Thomson M, Septiningsih E, Edwards J, Moncada P, Xiao J, Garris A, Tai T, Martinez C, Tohme J, Sugiono M, McClung A, Yuan LP, Ahn SN (2007) Through the genetic bottleneck: O. rufipogon as a source of trait-enhancing alleles for O. sativa. Euphytica 154:317–339CrossRefGoogle Scholar
  45. Menéndez CM, Ritter E, Schäfer-Pregl R, Walkemeier B, Kalde A, Salamini F, Gebhardt C (2002) Cold sweetening in diploid potato: mapping quantitative trait loci and candidate genes. Genetics 162:1423–1434PubMedGoogle Scholar
  46. Moncada P, Martinez CP, Borrero J, Chatel M, Gauch H Jr, Guimaraes E, Tohme J, McCouch SR (2001) Quantitative trait loci for yield and yield components in an Oryza sativa × Oryza rufipogon BC2F2 population evaluated in an upland environment. Theor Appl Genet 102:41–52CrossRefGoogle Scholar
  47. Moore G, Devos K, Wang Z, Gale M (1995) Grasses, line up and form a circle. Curr Biol 5:737–739PubMedCrossRefGoogle Scholar
  48. Nakamura I, Urairong H, Kameya N, Fukuta V, Chitrakon S, Sato YI (1998) Six different plastid subtypes were found in O. sativaO. rufipogon complex. Rice Genet Newsl 15:80–82Google Scholar
  49. Nguyen BD, Brar DS, Bui BC, Nguyen TV, Pham LN, Nguyen HT (2003) Identification and mapping of the QTL for aluminum tolerance introgressed from the new source, Oryza rufipogon Griff, into indica rice (Oryza sativa L.). Theor Appl Genet 106:583–593PubMedGoogle Scholar
  50. Oka HI (1974) Experimental studies on the origin of cultivated rice. Genetics 78:475–486PubMedGoogle Scholar
  51. Park YJ, Dixit A, Yoo JW, Bennetzen J (2004) Further evidence of microcolinearity between barley and rice genomes at two orthologous regions. Mol Cells 17:492–502PubMedGoogle Scholar
  52. Ramakrishna W, Dubcovsky J, Park YJ, Busso C, Emberton J et al (2002) Different types and rates of genome evolution detected by comparative sequence analysis of orthologous segments from four cereal genomes. Genetics 162:1389–1400PubMedGoogle Scholar
  53. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B (2000) Artemis: sequence visualisation and annotation. Bioinformatics 16:944–945PubMedCrossRefGoogle Scholar
  54. Sakata, K, Nagasaki, H, Idonuma, A, Waki, K, Kise, M, Sasaki, T (1999) A computer program for prediction of gene domain on rice genome sequence. The 2nd Georgia Tech International Conference on Bioinformatics, Abstracts p.78, Nov. 1999Google Scholar
  55. Sakata K, Nagamura Y, Numa H, Antoniol BA, Nagasaki H, Idonumal A, Watanabe W, Shimizu Y, Horiuchi I, Matsumoto T, Sasaki T, Higo K (2002) RiceGAAS: an annotation system and database for rice genome sequence. Nucleic Acids Res 30:98–102PubMedCrossRefGoogle Scholar
  56. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  57. Second G (1982) Origin of the genetic diversity of cultivated rice (Oryza ssp.): study of the polymorphism scored at 40 isozyme loci. Jpn J Genet 57:25–57CrossRefGoogle Scholar
  58. Septiningsih EM, Prasetiyono J, Lubis E, Tai TH, Tjubaryat T, Moeljopawiro S, McCouch SR (2003a) Identification of quantitative trait loci for yield and yield components in an advanced backcross population derived from the Oryza sativa variety IR64 and the wild relative O. rufipogon. Theor Appl Genet 107:1419–1432PubMedCrossRefGoogle Scholar
  59. Septiningsih EM, Trijatmiko KR, Moeljopawiro S, McCouch SR (2003b) Identification of quantitative trait loci for grain quality in an advance backcross population derived from the Oryza sativa variety IR64 and the wild relative O. rufipogon. Theor Appl Genet 107:1433–1411PubMedCrossRefGoogle Scholar
  60. Smit AF, Riggs AD (1996) Tiggers and DNA transposon fossils in the human genome. P Natl Acad Sci U S A 93:1443–1448CrossRefGoogle Scholar
  61. Song R, Llaca V, Messing J (2002) Mosaic organization of orthologous sequences in grass genome. Genome Res 12:1549–1555PubMedCrossRefGoogle Scholar
  62. Song BK, Nadarajah K, Romanov MN, Ratnam W (2005) Cross-species bacterial artificial chromosome (BAC) library screening via overgo-based hybridization and BAC-contig mapping of a yield enhancement quantitative trait locus (QTL) yld1.1 in the Malaysian wild rice Oryza rufipogon. Cell Mol Biol Lett 10:425–437PubMedGoogle Scholar
  63. Sonnhammer ELL, Durbin R (1995) A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis. Gene 167:GC1–GC10PubMedCrossRefGoogle Scholar
  64. Swigoňová Z, Bennetzen JL, Messing J (2005) Structure and evolution of the r/b chromosomal regions in rice maize and sorghum. Genetics 169:891–906PubMedCrossRefGoogle Scholar
  65. 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 100:697–712CrossRefGoogle Scholar
  66. Thomson MJ, Tai TH, McClung AM, Lai XH, Hinga ME, Lobos KB, Xu Y, Martinez CP, McCouch SR (2003) Mapping quantitative trait loci for yield, yield components and morphological traits in an advanced backcross population between Oryza rufipogon and the Oryza sativa cultivar Jefferson. Theor Appl Genet 107:479–493PubMedCrossRefGoogle Scholar
  67. Tikhonov AP, SanMiguel PJ, Nakajima Y, Gorenstein NM, Bennetzen JL, Avramova Z (1999) Colinearity and its exceptions in orthologous adh regions of maize and sorghum. Proc Natl Acad Sci U S A 96:7409–7414PubMedCrossRefGoogle Scholar
  68. Turner A, Beales J, Faure S, Dunford RP, Laurie DA (2005) The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310:1031–1034PubMedCrossRefGoogle Scholar
  69. Utami DW, Moeljopawiro S, Septiningsih EM, Aswidinnoor H, Sujiprihati S (2001) Introgression of blast resistance characters from the wild rice Oryza rufipogon into IR64 variety. (in Indonesian). J Biotek Pertan 6:51–58Google Scholar
  70. Vignols F, Lund G, Pammi S, Tremousaygue D, Grellet F, Kader CJ, Puigdomenech P, Delseny M (1994) Characterization of a rice gene coding for a lipid transfer protein. Gene 142:265–270PubMedCrossRefGoogle Scholar
  71. Vitte C, Panaud O (2003) Formation of solo-LTRs through unequal homologous recombination counterbalances amplifications of LTR retrotransposons in rice Oryza sativa L. Mol Biol Evol 20:528–540PubMedCrossRefGoogle Scholar
  72. Vitte C, Ishii T, Lamy F, Brar D, Panaud O (2004) Genomic paleontology provides evidence for two distinct origins of Asian rice (Oryza sativa L.). Mol Genet Genomics 272:504–511PubMedCrossRefGoogle Scholar
  73. Wang Q, Dooner HK (2006) Remarkable variation in maize genome structure inferred from haplotype diversity at the bz locus. Proc Natl Acad Sci U S A 103:17644–17649PubMedCrossRefGoogle Scholar
  74. Wissuwa M, Yano M, Ae N (1998) Mapping of QTLs for phosphorus-deficiency tolerance in rice (Oryza sativa L.). Theor Appl Genet 97:777–783CrossRefGoogle Scholar
  75. Wissuwa M, Wegner J, Ae N, Yano M (2002) Substitution mapping of Pup1: a major QTL increasing phosphorus uptake of rice from a phosphorus-deficient soil. Theor Appl Genet 105:890–897PubMedCrossRefGoogle Scholar
  76. Xiao J, Li J, Grandillo S, Ahn SN, Yuan L, Tanksley SD, McCouch SR (1998) Identification of trait-improving quantitative trait loci alleles from a wild rice relative, Oryza rufipogon. Genetics 150:899–909PubMedGoogle Scholar
  77. Xie X, Jin F, Song MH, Suh JP, Hwang HG, Kim YG, McCouch SR, Ahn SN (2008) Fine mapping of a yield-enhancing QTL cluster associated with transgressive variation in an Oryza sativa × O. rufipogon cross. Theor Appl Genet 116:613–622PubMedCrossRefGoogle Scholar
  78. Yamamoto T, Kuboki Y, Lin SY, Sasaki T, Yano M (1998) Fine mapping of quantitative trait loci Hd-1, Hd-2 and Hd-3 controlling heading date of rice as single Mendelian factors. Theor Appl Genet 97:37–44CrossRefGoogle Scholar
  79. Yano M, Harushima Y, Kurata N, Nagamura Y, Minobe Y, Sasaki T (1997) Identification of quantitative trait loci controlling heading date in rice using a high-density linkage map. Theor Appl Genet 95:1025–1032CrossRefGoogle Scholar
  80. You FM, Luo MC (2003) GenoProfiler User’s Manual. http://wheat.pw.usda.gov/PhysicalMapping/tools/genoprofiler/manual. Cited 19 Jan 2005
  81. Yu J, Hu S, Wang J, Wong GK, Li S, Liu B, Deng Y, Dai L, Zhou Y, Zhang X et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296:79–92PubMedCrossRefGoogle Scholar
  82. Yu J, Wang J, Lin W et al (2005) The Genomes of Oryza sativa: a history of duplications. PLoS Biol 3:266–281CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Beng-Kah Song
    • 1
    • 4
  • Ingo Hein
    • 2
  • Arnis Druka
    • 2
  • Robbie Waugh
    • 2
  • David Marshall
    • 2
  • Kalaivani Nadarajah
    • 3
  • Soon-Joo Yap
    • 5
  • Wickneswari Ratnam
    • 1
  1. 1.School of Environmental and Natural Resource Sciences, Faculty of Science and TechnologyUniversiti Kebangsaan MalaysiaBangiMalaysia
  2. 2.Genome Dynamics ProgramScottish Crop Research InstituteDundeeUK
  3. 3.School of BioScience and Biotechnology, Faculty of Science and TechnologyUniversiti Kebangsaan MalaysiaBangiMalaysia
  4. 4.School of Arts and SciencesMonash University, Sunway CampusBandar SunwayMalaysia
  5. 5.Malaysia Genome Institute, UKM-MTDC Smart Technology CentreUniversiti Kebangsaan Malaysia (UKM)BangiMalaysia

Personalised recommendations