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. 2003 Jun;164(2):673–683. doi: 10.1093/genetics/164.2.673

A large rearrangement involving genes and low-copy DNA interrupts the microcollinearity between rice and barley at the Rph7 locus.

S Brunner 1, B Keller 1, C Feuillet 1
PMCID: PMC1462599  PMID: 12807788

Abstract

Grass genomes differ greatly in chromosome number, ploidy level, and size. Despite these differences, very good conservation of the marker order (collinearity) was found at the genetic map level between the different grass genomes. Collinearity is particularly good between rice chromosome 1 and the group 3 chromosomes in the Triticeae. We have used this collinearity to saturate the leaf rust resistance locus Rph7 on chromosome 3HS in barley with ESTs originating from rice chromosome 1S. Chromosome walking allowed the establishment of a contig of 212 kb spanning the Rph7 resistance gene. Sequencing of the contig showed an average gene density of one gene/20 kb with islands of higher density. Comparison with the orthologous rice sequence revealed the complete conservation of five members of the HGA gene family whereas intergenic regions differ greatly in size and composition. In rice, the five genes are closely associated whereas in barley intergenic regions are >38-fold larger. The size difference is due mainly to the presence of six additional genes as well as noncoding low-copy sequences. Our data suggest that a major rearrangement occurred in this region since the Triticeae and rice lineage diverged.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997 Sep 1;25(17):3389–3402. doi: 10.1093/nar/25.17.3389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bennetzen J. L. Comparative sequence analysis of plant nuclear genomes:m microcolinearity and its many exceptions. Plant Cell. 2000 Jul;12(7):1021–1029. doi: 10.1105/tpc.12.7.1021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bennetzen J. L. Transposable element contributions to plant gene and genome evolution. Plant Mol Biol. 2000 Jan;42(1):251–269. [PubMed] [Google Scholar]
  4. Bennetzen Jeffrey L. Mechanisms and rates of genome expansion and contraction in flowering plants. Genetica. 2002 May;115(1):29–36. doi: 10.1023/a:1016015913350. [DOI] [PubMed] [Google Scholar]
  5. Bennetzen Jeffrey L., Ramakrishna Wusirika. Numerous small rearrangements of gene content, order and orientation differentiate grass genomes. Plant Mol Biol. 2002 Mar-Apr;48(5-6):821–827. doi: 10.1023/a:1014841515249. [DOI] [PubMed] [Google Scholar]
  6. Chen M., SanMiguel P., Bennetzen J. L. Sequence organization and conservation in sh2/a1-homologous regions of sorghum and rice. Genetics. 1998 Jan;148(1):435–443. doi: 10.1093/genetics/148.1.435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chen M., SanMiguel P., de Oliveira A. C., Woo S. S., Zhang H., Wing R. A., Bennetzen J. L. Microcolinearity in sh2-homologous regions of the maize, rice, and sorghum genomes. Proc Natl Acad Sci U S A. 1997 Apr 1;94(7):3431–3435. doi: 10.1073/pnas.94.7.3431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Devos Katrien M., Brown James K. M., Bennetzen Jeffrey L. Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res. 2002 Jul;12(7):1075–1079. doi: 10.1101/gr.132102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dobbs DA, Vanhessche KP, Brazi E, Rautenstrauch V, V, Lenoir JY, Genêt JP, Wiles J, Bergens SH. Industrial Synthesis of (+)-cis-Methyl Dihydrojasmonate by Enantioselective Catalytic Hydrogenation; Identification of the Precatalyst. Angew Chem Int Ed Engl. 2000 Jun 2;39(11):1992–1995. doi: 10.1002/1521-3773(20000602)39:11<1992::aid-anie1992>3.0.co;2-w. [DOI] [PubMed] [Google Scholar]
  10. Druka A., Kudrna D., Han F., Kilian A., Steffenson B., Frisch D., Tomkins J., Wing R., Kleinhofs A. Physical mapping of the barley stem rust resistance gene rpg4. Mol Gen Genet. 2000 Oct;264(3):283–290. doi: 10.1007/s004380000320. [DOI] [PubMed] [Google Scholar]
  11. Dubcovsky J., Ramakrishna W., SanMiguel P. J., Busso C. S., Yan L., Shiloff B. A., Bennetzen J. L. Comparative sequence analysis of colinear barley and rice bacterial artificial chromosomes. Plant Physiol. 2001 Mar;125(3):1342–1353. doi: 10.1104/pp.125.3.1342. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Faris J. D., Haen K. M., Gill B. S. Saturation mapping of a gene-rich recombination hot spot region in wheat. Genetics. 2000 Feb;154(2):823–835. doi: 10.1093/genetics/154.2.823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Feuillet C., Keller B. High gene density is conserved at syntenic loci of small and large grass genomes. Proc Natl Acad Sci U S A. 1999 Jul 6;96(14):8265–8270. doi: 10.1073/pnas.96.14.8265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Feuillet Catherine, Keller Beat. Comparative genomics in the grass family: molecular characterization of grass genome structure and evolution. Ann Bot. 2002 Jan;89(1):3–10. doi: 10.1093/aob/mcf008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gale M. D., Devos K. M. Comparative genetics in the grasses. Proc Natl Acad Sci U S A. 1998 Mar 3;95(5):1971–1974. doi: 10.1073/pnas.95.5.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Goff Stephen A., Ricke Darrell, Lan Tien-Hung, Presting Gernot, Wang Ronglin, Dunn Molly, Glazebrook Jane, Sessions Allen, Oeller Paul, Varma Hemant. A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science. 2002 Apr 5;296(5565):92–100. doi: 10.1126/science.1068275. [DOI] [PubMed] [Google Scholar]
  17. Han F, Kilian A, Chen JP, Kudrna D, Steffenson B, Yamamoto K, Matsumoto T, Sasaki T, Kleinhofs A. Sequence analysis of a rice BAC covering the syntenous barley Rpg1 region. Genome. 1999 Dec;42(6):1071–1076. doi: 10.1139/g99-060. [DOI] [PubMed] [Google Scholar]
  18. He Z. H., Dong H. T., Dong J. X., Li D. B., Ronald P. C. The rice Rim2 transcript accumulates in response to Magnaporthe grisea and its predicted protein product shares similarity with TNP2-like proteins encoded by CACTA transposons. Mol Gen Genet. 2000 Sep;264(1-2):2–10. doi: 10.1007/s004380000278. [DOI] [PubMed] [Google Scholar]
  19. Hulbert S. H., Webb C. A., Smith S. M., Sun Q. Resistance gene complexes: evolution and utilization. Annu Rev Phytopathol. 2001;39:285–312. doi: 10.1146/annurev.phyto.39.1.285. [DOI] [PubMed] [Google Scholar]
  20. Kilian A., Chen J., Han F., Steffenson B., Kleinhofs A. Towards map-based cloning of the barley stem rust resistance genes Rpg1 and rpg4 using rice as an intergenomic cloning vehicle. Plant Mol Biol. 1997 Sep;35(1-2):187–195. [PubMed] [Google Scholar]
  21. Koprek T., McElroy D., Louwerse J., Williams-Carrier R., Lemaux P. G. An efficient method for dispersing Ds elements in the barley genome as a tool for determining gene function. Plant J. 2000 Oct;24(2):253–263. doi: 10.1046/j.1365-313x.2000.00865.x. [DOI] [PubMed] [Google Scholar]
  22. Künzel G., Korzun L., Meister A. Cytologically integrated physical restriction fragment length polymorphism maps for the barley genome based on translocation breakpoints. Genetics. 2000 Jan;154(1):397–412. doi: 10.1093/genetics/154.1.397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Moore G., Devos K. M., Wang Z., Gale M. D. Cereal genome evolution. Grasses, line up and form a circle. Curr Biol. 1995 Jul 1;5(7):737–739. doi: 10.1016/s0960-9822(95)00148-5. [DOI] [PubMed] [Google Scholar]
  24. Nacken W. K., Piotrowiak R., Saedler H., Sommer H. The transposable element Tam1 from Antirrhinum majus shows structural homology to the maize transposon En/Spm and has no sequence specificity of insertion. Mol Gen Genet. 1991 Aug;228(1-2):201–208. doi: 10.1007/BF00282466. [DOI] [PubMed] [Google Scholar]
  25. Panstruga R., Büschges R., Piffanelli P., Schulze-Lefert P. A contiguous 60 kb genomic stretch from barley reveals molecular evidence for gene islands in a monocot genome. Nucleic Acids Res. 1998 Feb 15;26(4):1056–1062. doi: 10.1093/nar/26.4.1056. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. SanMiguel P., Tikhonov A., Jin Y. K., Motchoulskaia N., Zakharov D., Melake-Berhan A., Springer P. S., Edwards K. J., Lee M., Avramova Z. Nested retrotransposons in the intergenic regions of the maize genome. Science. 1996 Nov 1;274(5288):765–768. doi: 10.1126/science.274.5288.765. [DOI] [PubMed] [Google Scholar]
  27. SanMiguel Phillip J., Ramakrishna Wusirika, Bennetzen Jeffrey L., Busso Carlos S., Dubcovsky Jorge. Transposable elements, genes and recombination in a 215-kb contig from wheat chromosome 5A(m). Funct Integr Genomics. 2002 Apr 12;2(1-2):70–80. doi: 10.1007/s10142-002-0056-4. [DOI] [PubMed] [Google Scholar]
  28. Sandhu Devinder, Gill Kulvinder S. Structural and functional organization of the '1S0.8 gene-rich region' in the Triticeae. Plant Mol Biol. 2002 Mar-Apr;48(5-6):791–804. doi: 10.1023/a:1014876409166. [DOI] [PubMed] [Google Scholar]
  29. Smilde W. D., Haluskova J., Sasaki T., Graner A. New evidence for the synteny of rice chromosome 1 and barley chromosome 3H from rice expressed sequence tags. Genome. 2001 Jun;44(3):361–367. [PubMed] [Google Scholar]
  30. Stein N., Feuillet C., Wicker T., Schlagenhauf E., Keller B. Subgenome chromosome walking in wheat: a 450-kb physical contig in Triticum monococcum L. spans the Lr10 resistance locus in hexaploid wheat (Triticum aestivum L.). Proc Natl Acad Sci U S A. 2000 Nov 21;97(24):13436–13441. doi: 10.1073/pnas.230361597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Takai R., Hasegawa K., Kaku H., Shibuya N., Minami E. Isolation and analysis of expression mechanisms of a rice gene, EL5, which shows structural similarity to ATL family from Arabidopsis, in response to N-acetylchitooligosaccharide elicitor. Plant Sci. 2001 Mar;160(4):577–583. doi: 10.1016/s0168-9452(00)00390-3. [DOI] [PubMed] [Google Scholar]
  32. Takai Ryota, Matsuda Noriyuki, Nakano Akihiko, Hasegawa Koji, Akimoto Chiharu, Shibuya Naoto, Minami Eiichi. EL5, a rice N-acetylchitooligosaccharide elicitor-responsive RING-H2 finger protein, is a ubiquitin ligase which functions in vitro in co-operation with an elicitor-responsive ubiquitin-conjugating enzyme, OsUBC5b. Plant J. 2002 May;30(4):447–455. doi: 10.1046/j.1365-313x.2002.01299.x. [DOI] [PubMed] [Google Scholar]
  33. Tarchini R., Biddle P., Wineland R., Tingey S., Rafalski A. The complete sequence of 340 kb of DNA around the rice Adh1-adh2 region reveals interrupted colinearity with maize chromosome 4. Plant Cell. 2000 Mar;12(3):381–391. doi: 10.1105/tpc.12.3.381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997 Dec 15;25(24):4876–4882. doi: 10.1093/nar/25.24.4876. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Tikhonov A. P., SanMiguel P. J., Nakajima Y., Gorenstein N. M., Bennetzen J. L., Avramova Z. Colinearity and its exceptions in orthologous adh regions of maize and sorghum. Proc Natl Acad Sci U S A. 1999 Jun 22;96(13):7409–7414. doi: 10.1073/pnas.96.13.7409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Vision T. J., Brown D. G., Tanksley S. D. The origins of genomic duplications in Arabidopsis. Science. 2000 Dec 15;290(5499):2114–2117. doi: 10.1126/science.290.5499.2114. [DOI] [PubMed] [Google Scholar]
  37. Wei F., Gobelman-Werner K., Morroll S. M., Kurth J., Mao L., Wing R., Leister D., Schulze-Lefert P., Wise R. P. The Mla (powdery mildew) resistance cluster is associated with three NBS-LRR gene families and suppressed recombination within a 240-kb DNA interval on chromosome 5S (1HS) of barley. Genetics. 1999 Dec;153(4):1929–1948. doi: 10.1093/genetics/153.4.1929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Wei Fusheng, Wing Rod A., Wise Roger P. Genome dynamics and evolution of the Mla (powdery mildew) resistance locus in barley. Plant Cell. 2002 Aug;14(8):1903–1917. doi: 10.1105/tpc.002238. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Wicker T., Stein N., Albar L., Feuillet C., Schlagenhauf E., Keller B. Analysis of a contiguous 211 kb sequence in diploid wheat (Triticum monococcum L.) reveals multiple mechanisms of genome evolution. Plant J. 2001 May;26(3):307–316. doi: 10.1046/j.1365-313x.2001.01028.x. [DOI] [PubMed] [Google Scholar]
  40. Wolfe K. H., Gouy M., Yang Y. W., Sharp P. M., Li W. H. Date of the monocot-dicot divergence estimated from chloroplast DNA sequence data. Proc Natl Acad Sci U S A. 1989 Aug;86(16):6201–6205. doi: 10.1073/pnas.86.16.6201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Woo S. S., Jiang J., Gill B. S., Paterson A. H., Wing R. A. Construction and characterization of a bacterial artificial chromosome library of Sorghum bicolor. Nucleic Acids Res. 1994 Nov 25;22(23):4922–4931. doi: 10.1093/nar/22.23.4922. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Yu Jun, Hu Songnian, Wang Jun, Wong Gane Ka-Shu, Li Songgang, Liu Bin, Deng Yajun, Dai Li, Zhou Yan, Zhang Xiuqing. A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science. 2002 Apr 5;296(5565):79–92. doi: 10.1126/science.1068037. [DOI] [PubMed] [Google Scholar]

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