Abstract
Comparative RFLP mapping has revealed extensive conservation of marker order in different grass genomes. However, microcolinearity studies at the sequence level have shown rapid genome evolution and many exceptions to colinearity. Most of these studies have focused on a limited size of genomic fragment and the extent of microcolinearity over large distances or across entire genomes remains poorly characterized in grasses. Here, we have investigated the microcolinearity between the rice genome and a total of 1,500 kb from physical BAC contigs on wheat chromosome 1AS. Using ESTs mapped in wheat chromosome bins as an additional source of physical data, we have identified 27 conserved orthologous sequences between wheat chromosome 1AS and a region of 1,210 kb located on rice chromosome 5S. Our results extend the orthology described earlier between wheat chromosome group 1S and rice chromosome 5S. Microcolinearity was found to be frequently disrupted by rearrangements which must have occurred after the divergence of wheat and rice. At the Lr10 orthologous loci, microrearrangements were due to the insertion of mobile elements, but also originated from gene movement, amplification, deletion and inversion. These mechanisms of genome evolution are at the origin of the mosaic conservation observed between the orthologous regions. Finally, in silico mapping of wheat genes identified an intragenomic colinearity between fragments from rice chromosome 1L and 5S, suggesting an ancestral segmental duplication in rice.
Similar content being viewed by others
References
Ahn S, Anderson JA, Sorrells ME, Tanksley SD (1993) Homoeologous relationships of rice, wheat and maize chromosomes. Mol Gen Genet 241:483–490
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Arumuganathan K, Earle ED (1991) Nuclear DNA content of some important plant species. Plant Mol Biol Rep 9:208–218
Bennetzen JL, Ramakrishna W (2002) Numerous small rearrangements of gene content, order and orientation differentiate grass genomes. Plant Mol Biol 48:821–827
Blanc G, Barakat A, Guyot R, Cooke R, Delseny M (2000) Extensive duplication and reshuffling in the Arabidopsis genome. Plant Cell 12:1093–1101
Brunner S, Keller B, Feuillet C (2003) A large rearrangement involving genes and low-copy DNA interrupts the microcolinearity between rice and barley at the Rph7 locus. Genetics 164:673–683
Cenci A, Chantret N, Kong X, Gu Y, Anderson OD, Fahima T, Distelfeld A, Dubcovsky J (2003) Construction and characterization of a half million clone BAC library of durum wheat (Triticum turgidum ssp. durum). Theor Appl Genet 107:931–939
Chen M, SanMiguel P, de Oliveira AC, Woo SS, Zhang H, Wing RA, Bennetzen JL (1997) Microcolinearity in sh2-homologous regions of the maize, rice, and sorghum genomes. Proc Natl Acad Sci USA 94:3431–3435
Chen M, SanMiguel P, Bennetzen JL (1998) Sequence organization and conservation in sh2/a1-homologous regions of sorghum and rice. Genetics 148:435–443
Dubcovsky J, Luo M, Dvorak J (1995) Differentiation between homoeologous chromosomes 1A of wheat and 1Am of Triticum monococcum and its recognition by the wheat Ph1 locus. Proc Natl Acad Sci USA 92:6645–6649
Dubcovsky J, Ramakrishna W, SanMiguel PJ, Busso CS, Yan L, Shiloff BA, Bennetzen JL (2001) Comparative sequence analysis of colinear barley and rice bacterial artificial chromosomes. Plant Physiol 125:1342–1353
Endo TR, Gill BS (1996) The deletion stocks of common wheat. J Hered 87:295–307
Feuillet C, Keller B (1999) High gene density is conserved at syntenic loci of small and large grass genomes. Proc Natl Acad Sci USA 96:8265–8270
Feuillet C, Keller B (2002) Comparative genomics in the grass family: molecular characterization of grass genome structure and evolution. Ann Bot (Lond) 89:3–10
Gale MD, Devos KM (1998) Comparative genetics in the grasses. Proc Natl Acad Sci USA 95:1971–1974
Gallego F, Feuillet C, Messmer M, Penger A, Graner A, Yano M, Sasaki T, Keller B (1998) Comparative mapping of the two wheat leaf rust resistance loci Lr1 and Lr10 in rice and barley. Genome 41:328–336
Gaut BS (2002) Evolutionary dynamics of grass genomes. New Phytol 154:15–28
Gill KS, Gill BS, Endo TR, Taylor T (1996) Identification and high-density mapping of gene-rich regions in chromosome group 1 of wheat. Genetics 144:1883–1891
Goff SA, Ricke D, Lan TH, Presting G, Wang R et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296:92–100
Keller B, Feuillet C (2000) Colinearity and gene density in grass genomes. Trends Plant Sci 5:246–251
Kishimoto N, Higi H, Abe K, Arai S, Saito A, Higo K (1994) Identification of the duplicated segments in rice chromosome 1 and 5 by linkage analysis of cDNA markers of known functions. Theor Appl Genet 88:722–726
Klein PE, Klein RR, Vrebalov J, Mullet JE (2003) Sequence-based alignment of sorghum chromosome 3 and rice chromosome 1 reveals extensive conservation of gene order and one major chromosomal rearrangement. Plant J 34:605–621
Kurata N, Moore G, Nagamura Y, Foote T, Yano M, Minobe Y, Gale M (1994) Conservation of genome structure between rice and wheat. Bio-Technology 12:276–278
Leister D, Kurth J, Laurie DA, Yano M, Sasaki T, Devos K, Graner A, Schulze-Lefert P (1998) Rapid reorganization of resistance gene homologues in cereal genomes. Proc Natl Acad Sci USA 95:370–375
Lijavetzky D, Muzzi G, Wicker T, Keller B, Wing R, Dubcovsky J (1999) Construction and characterization of a bacterial artificial chromosome (BAC) library for the A genome of wheat. Genome 42:1176–1182
Ma Z, Weining S, Sharp PJ, Liu C (2000) Non-gridded library: a new approach for BAC (bacterial artificial chromosome) exploitation in hexaploid wheat (Triticum aestivum). Nucleic Acids Res 28:E106
Moullet O, Zhang HB, Lagudah ES (1999) Construction and characterization of a large DNA insert library from the D genome of wheat. Theor Appl Genet 99:305–313
Qi L, Echalier B, Friebe B, Gill BS (2003) Molecular characterization of a set of wheat deletion stocks for use in chromosome bin mapping of ESTs. Funct Integr Genom 3:39–55
Rice P, Longden I, Bleasby A (2000) EMBOSS: The European Molecular Biology Open Software Suite. Trends Genetics 16:276–277
Sandhu D, Gill KS (2002) Structural and functional organization of the “1S0.8 gene-rich region” in the Triticeae. Plant Mol Biol 48:791–804
Sandhu D, Champoux JA, Bondareva SN, Gill KS (2001) Identification and physical localization of useful genes and markers to a major gene-rich region on wheat group 1S chromosomes. Genetics 157:1735–1747
SanMiguel PJ, Ramakrishna W, Bennetzen JL, Busso CS, Dubcovsky J (2002) Transposable elements, genes and recombination in a 215-kb contig from wheat chromosome 5Am. Funct Integr Genom 2:70–80
Sasaki T, Matsumoto T, Yamamoto K, Sakata K et al (2002) The genome sequence and structure of rice chromosome 1. Nature 420:312–316
Sears ER (1966) Nullisomic-tetrasomic combinations in hexaploid wheat. In: Riley R, Lewis KR (eds) Chromosome manipulations and plant genetics. Oliver and Boyd, Edinburgh, pp 29–45
Song R, Llaca V, Messing J (2002) Mosaic organization of orthologous sequences in grass genomes. Genome Res 12:1549–1555
Sonnhammer EL, Durbin R (1995) A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis. Gene 167:GC1–GC10
Sorrells ME, La Rota M, Bermudez-Kandianis CE, Greene RA et al (2003) Comparative DNA sequence analysis of wheat and rice genomes. Genome Res 13:1818–1827
Stein N, Feuillet C, Wicker T, Schlagenhauf E, Keller B (2000) 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 USA 97:13436–13441
Tarchini R, Biddle P, Wineland R, Tingey S, Rafalski A (2000) The complete sequence of 340 kb of DNA around the rice Adh1-adh2 region reveals interrupted colinearity with maize chromosome 4. Plant Cell 12:381–391
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 USA 96:7409–7414
Van Deynze AE, Dubcovsky J, Gill, KS, Nelson JC, Sorrells ME, Dvorak J, Gill BS, Lagudah ES, McCouch SR, Appels R (1995a) Molecular-genetic maps of group 1 chromosomes of Triticeae species and their relations to chromosomes in rice and oat. Genome 38:45–59
Van Deynze AE, Nelson JC, Yglesias ES, Harrington SE, Braga DP, McCouch SR, Sorrells ME (1995b) Comparative mapping in grasses. Wheat relationships. Mol Gen Genet 248:744–754
Wicker T, Stein N, Albar L, Feuillet C, Schlagenhauf E, Keller B (2001) Analysis of a contiguous 211 kb sequence in diploid wheat (Triticum monococcum L.) reveals multiple mechanisms of genome evolution. Plant J 26:307–316
Wicker T, Yahiaoui N, Guyot R, Schlagenhauf E, Liu ZD, Dubcovsky J, Keller B (2003) Rapid genome divergence at orthologous low molecular weight glutenin loci of the A and Am genomes of wheat. Plant Cell 15:1186–1197
Wolfe KH, Gouy M, Yang YW, Sharp PM, Li WH (1989) Date of the monocot-dicot divergence estimated from chloroplast DNA sequence data. Proc Natl Acad Sci USA 86:6201–6205
Wu J, Kurata N, Tanoue H, Shimokawa T, Umehara Y, Yano M, Sasaki T (1998) Physical mapping of duplicated genomic regions of two chromosome ends in rice. Genetics 150:1595–1603
Yu J, Hu S, Wang J, Wong GK, Li S et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296:79–92
Acknowledgements
The authors thank Gerhard Herren for excellent technical assistance. This work was supported by a grant from the Swiss National Science Foundation (no. 3100-065114).
Author information
Authors and Affiliations
Corresponding author
Electronic Supplementary Material
Rights and permissions
About this article
Cite this article
Guyot, R., Yahiaoui, N., Feuillet, C. et al. In silico comparative analysis reveals a mosaic conservation of genes within a novel colinear region in wheat chromosome 1AS and rice chromosome 5S. Funct Integr Genomics 4, 47–58 (2004). https://doi.org/10.1007/s10142-004-0103-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10142-004-0103-4