Abstract
Comparative genetic mapping has indicated that the grass family (Poaceae) exhibits extensive chromosomal collinearity. In order to investigate microcollinearity in these genomes, several laboratories have begun to undertake comparative DNA sequence analyses of orthologous chromosome segments from various grass species. Five different regions have now been investigated in detail, with four regions sequenced for maize, rice and sorghum, plus two for wheat and one for barley. In all five of these segments, gene rearrangements were observed in at least one of the comparisons. Most of the detected rearrangements are small, involving the inversion, duplication, translocation or deletion of DNA segments that contain only 1-3 genes. Even closely related species, like barley and wheat or maize and sorghum, exhibit approximately 20% alterations in gene content or orientation. These results indicate that thousands of small genetic rearrangements have occurred in several grass lineages since their divergence from common ancestors. These rearrangements have largely been missed by genetic mapping and will both complicate and enrich the use of comparative genetics in the grasses.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bennetzen, J.L. and Freeling, M. 1993. Grasses as a single genetic system: genome composition, collinearity and compatibility. Trends Genet. 9: 259-261.
Bennetzen, J.L. and Freeling, M. 1997. The unified grass genome: synergy in synteny. Genome Res. 7: 301-307.
Blanc, G., Barakat, A., Guyot, R., Cooke, R. and Delseny, M. 2000. Extensive duplication and reshuffling in the Arabidopsis thaliana genome. Plant Cell 12: 1093-1101.
Bonierbale, M.W., Plaisted, R.L. and Tanksley, S.D. 1988. RFLP maps based on a common set of clones reveal modes of chromosomal evolution in potato and tomato. Genetics 120: 1095-1103.
Chen, M., SanMiguel, P. and Bennetzen, J.L. 1998. Sequence organization and conservation in Sh2/A1-homologous regions of sorghum and rice. Genetics 148: 435-443.
Chen, M., SanMiguel, P., Oliveira, A.C., Woo, S-S., Zhang, H., Wing, R.A. and Bennetzen, J.L. 1997. Microcolinearity in the sh2-homologous regions of the maize, rice and sorghum genomes. Proc. Natl. Acad. Sci. USA 94: 3431-3435.
Clark, L.G., Zhang, W. and Wendel, J.F. 1995. A phylogeny of the grass family (Poaceae) based on ndhf sequence data. Syst. Bot. 20: 436-460.
Crepet, W.L. and Feldman, G.D. 1991. The earliest remains of grasses in the fossil record. J. Bot. 78: 1010-1014.
Dubcovsky, J., Ramakrishna, W., SanMiguel, P., Busso, C.S., Yan, L., Shiloff, B.A. and Bennetzen, J.L. 2001. Comparative sequence analysis of colinear barley and rice bacterial artificial chromosomes. Plant Physiol. 125: 1342-1353.
Fatokun, C.A., Menancio-Hautea, D.I., Danesh, D. and Young, N.D. 1992. Evidence for orthologous seed weight genes in cowpea and mungbean based on RFLP mapping. Genetics 132: 841-846.
Gale, M.D. and Devos, K.M. 1998. Plant comparative genetics after 10 years. Science 282: 656-659.
Gaut, B.S. and Doebley, J.F. 1997. DNA sequence evidence for the segmental allotetraploid origin of maize. Proc. Natl. Acad. Sci. USA 88: 2060-2064.
Grant, D., Cregan, P. and Shoemaker, R.C. 2000. Genome organization in dicots. I. Genome duplication in Arabidopsis and synteny between soybean and Arabidopsis. Proc. Natl. Acad. Sci. USA 97: 4168-4173.
Kilian, A., Chen, J., Han, F., Steffenson, B. and Kleinhofs, A. 1997. Towards map-based cloning of the barley stem rust resistance genes Rpg1 and rpg4 using rice as an intergenomic cloning vehicle. Plant Mol. Biol. 35: 187-95.
Kowalski, S.P., Lan, T-H., Feldmann, K.A. and Paterson, A.H. 1994. Comparative mapping of Arabidopsis thaliana and Brassica oleracea chromosomes reveals islands of conserved organization. Genetics 138: 499-510.
Ku, H-M., Vision, T., Liu, J. and Tanksley, S.D. 2000. Comparing sequenced segments of the tomato and Arabidopsis genomes: Large scale duplication followed by selective gene loss creates a network of synteny. Proc. Natl. Acad. Sci. USA 97: 9121-9126.
Lagercrantz, U. 1998. Comparative mapping between Arabidopsis thaliana and Brassica nigra indicates that Brassica genomes have evolved through extensive genome replication accompanied by chromosome fusions and frequent rearrangements. Genetics 150: 1217-1228.
Lagercrantz, U., Putterill, J., Coupland, G. and Lydiate, D. 1996. Comparative mapping in Arabidopsis and Brassica: fine scale genome colinearity and congruence of genes controlling flowering time. Plant J. 9: 13-20.
Llaca, V. and Messing, J. 1998. Amplicons of maize zein genes are conserved within genic but expanded and constricted in intergenic regions. Plant J. 15: 211-20.
Moore, G., Devos, K.M., Wang, Z. and Gale, M.D. 1995. Cereal genome evolution-grasses, line up and form a circle. Curr. Biol. 5: 737-739.
O'Neill, C. and Bancroft, I. 2000. Comparative physical mapping of segments of the genome of Brassica oleracea var alboglabra that are homoeologous to sequenced regions of the chromosomes 4 and 5 of Arabidopsis thaliana. Plant J. 23: 233-243.
Paterson, A.H., Lin, Y.R Li, Z.K., Schertz, K.F., Doebley, J.F., Pinson, S.R.M., Liu, S.C., Stansel, J.W. and Irvine, J.E. 1995. Convergent domestication of cereal crops by independent mutations at corresponding genetic loci. Science 269: 1714-1718.
Peng, J.R., Richards, D.E., Hartley, N.M., Murphy, G.P., Devos, K.M., Flintham, J.E., Beales, J., Fish, L-J., Worland, A.J., Pelica, F. et al. 1999. 'Green revolution' genes encode mutant gibberellin response modulators. Nature 400: 256-261.
SanMiguel, P., Tikhonov, A., Jin, Y-K., Motchoulskaia, N., Zakharov, D., Melake Berhan, A., Springer, P.S., Edwards, K.J., Avramova, Z. and Bennetzen, J.L. 1996. Nested retrotransposons in the intergenic regions of the maize genome. Science 274: 765-768.
Sonnhammer, E.L.L. and Durbin, R. 1995. A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis. Gene 167: 1-10.
Tanksley, S.D., Bernatzky, R., Lapitan, N.L. and Prince, J.P. 1988. Conservation of gene repertoire but not gene order in pepper and tomato. Proc. Natl. Acad. Sci. USA 85: 6419-6423.
Tarchini, R., Biddle, P., Wineland, R., Tingey, S. and 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, A.P., SanMiguel, P.J., Nakajima, Y., Gorenstein, N.M., Bennetzen, J.L. and Avramova, Z. 1999. Colinearity and its exceptions in orthologous adh regions of maize and sorghum. Proc. Natl. Acad. Sci. USA 96: 7409-7414.
Weeden, N.D., Muehlbauer, F.J. and Ladizinsky, G. 1992. Extensive conservation of linkage relationships between pea and lentil genetic maps. J. Hered. 83: 123-129.
Wolfe, K.H., Gouy, M., Yang, Y-H., Sharp, P.M. and Li,W-H. 1989. Date of the monocot-dicot divergence estimated from chloroplast sequence data. Proc. Natl. Acad. Sci. USA 86: 6201-6205.
Xu, X., Hsia, A-P., Zhang, L., Nikolau, B.J. and Schnable, P.S. 1995. Meiotic recombination break points resolve at high rates at the 5' end of a maize coding sequence. Plant Cell 7: 2151-2161.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Bennetzen, J.L., Ramakrishna, W. Numerous small rearrangements of gene content, order and orientation differentiate grass genomes. Plant Mol Biol 48, 821–827 (2002). https://doi.org/10.1023/A:1014841515249
Issue Date:
DOI: https://doi.org/10.1023/A:1014841515249