Abstract
Our knowledge of recombination rates and patterns in plants is far from being comprehensive. However, compelling evidence indicates a central role for recombination, through its influences on mutation and selection, in the evolution of plant genomes. Furthermore, recombination seems to be generally higher and more variable in plants than in animals, which could be one of the primary reasons for differences in genome lability between these two kingdoms. Much additional study of recombination in plants is needed to investigate these ideas further.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$189.00 per year
only $15.75 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Gaut, B. S. Evolutionary dynamics of grass genomes. New Phytol. 154, 15–28 (2002).
Bennett, M. D. & Smith, J. B. Nuclear DNA amounts in angiosperms. Phil. Trans. R. Soc. Lond. B Biol. Sci. 334, 309–345 (1991).
Adams, K. L. & Wendel, J. F. Polyploidy and genome evolution in plants. Curr. Opin. Plant Biol. 8, 135–141 (2005).
Cui, L. et al. Widespread genome duplications throughout the history of flowering plants. Genome Res. 16, 738–749 (2006).
Blanc, G., Hokamp, K. & Wolfe, K. H. A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome. Genome Res. 13, 137–144 (2003).
Vision, T. J., Brown, D. G. & Tanksley, S. D. The origins of genomic duplications in Arabidopsis. Science 290, 2114–2117 (2000).
Bennetzen, J. L., Ma, J. & Devos, K. M. Mechanisms of recent genome size variation in flowering plants. Ann. Bot. 95, 127–132 (2005).
Schuermann, D., Molinier, J., Fritsch, O. & Hohn, B. The dual nature of homologous recombination in plants. Trends Genet. 21, 172–181 (2005).
Jelesko, J. G., Carter, K., Thompson, W., Kinoshita, Y. & Gruissem, W. Meiotic recombination between paralogous RBCSB genes on sister chromatids of Arabidopsis thaliana. Genetics 166, 947–957 (2004).
Zhang, L. & Gaut, B. S. Does recombination shape the distribution and evolution of tandemly arrayed genes (TAGs) in the Arabidopsis thaliana genome? Genome Res. 13, 2533–2540 (2003).
Yandeau-Nelson, M. D., Xia, Y., Li, J., Neuffer, M. G. & Schnable, P. Unequal sister chromatid and homolog recombination at a tandem duplication of the a1 locus in maize. Genetics 173, 2211–2226 (2006).
Molinier, J., Stamm, M. E. & Hohn, B. SNM-dependent recombinational repair of oxidatively induced DNA damage in Arabidopsis thaliana. EMBO Rep. 5, 994–999 (2004).
Egli, D., Hafen, E. & Schaffner, W. An efficient method to generate chromosomal rearrangements by targeted DNA double-strand breaks in Drosophila melanogaster. Genome Res. 14, 1382–1393 (2004).
Lysak, M. A. et al. Mechanisms of chromosome number reduction in Arabidopsis thaliana and related Brassicaceae species. Proc. Natl Acad. Sci. USA 103, 5224–5229 (2006).
Ziolkowski, P. A., Blanc, G. & Sadowski, J. Structural divergence of chromosomal segments that arose from successive duplication events in the Arabidopsis genome. Nucleic Acids Res. 31, 1339–1350 (2003).
Lockton, S. & Gaut, B. S. Plant conserved non-coding sequences and paralogue evolution. Trends Genet. 21, 60–65 (2005).
Pearson, C. E., Edamura, K. N. & Cleary, J. D. Repeat instability: mechanisms of dynamic mutations. Nature Rev. Genet. 6, 729–742 (2005).
Lercher, M. J. & Hurst, L. D. Can mutation or fixation biases explain the allele frequency distribution of human single nucleotide polymorphisms (SNPs)? Gene 300, 53–58 (2002).
Hellmann, I., Ebersberger, I., Ptak, S. E., Paabo, S. & Przeworski, M. A neutral explanation for the correlation of diversity with recombination rates in humans. Am. J. Hum. Genet. 72, 1527–1535 (2003).
Rattray, A. J. & Strathern, J. N. Error-prone DNA polymerases: when making a mistake is the only way to get ahead. Annu. Rev. Genet. 37, 31–66 (2003).
Spencer, C. C. A. et al. The influence of recombination on human genetic diversity. PLoS Genet. 2, e148 (2006).
Betancourt, A. J. & Presgraves, D. C. Linkage limits the power of natural selection in Drosophila. Proc. Natl Acad. Sci. USA 99, 13616–13620 (2002).
Ometto, L., Glinka, S., De Lorenzo, D. & Stephan, W. Inferring the effects of demography and selection on Drosophila melanogaster populations from a chromosome-wide scan of DNA variation. Mol. Biol. Evol. 22, 2119–2130 (2005).
Tenaillon, M. I. et al. Patterns of diversity and recombination along chromosome 1 of maize (Zea mays ssp. mays L.). Genetics 162, 1401–1413 (2002).
Wright, S. I. et al. Testing for effects of recombination on nucleotide diversity in natural populations of Arabidopsis lyrata. Genetics 174, 1421–1430 (2006).
Fisher, R. A. The Genetical Theory of Natural Selection (Oxford Univ. Press, Oxford, 1930).
Hill, W. G. & Robertson, A. The effect of linkage on limits to artificial selection. Genet. Res. 8, 269–294. (1966).
Felsenstein, J. The evolutionary advantage of recombination. Genetics 78, 737–756 (1974).
Jensen-Seaman, M. I. et al. Comparative recombination rates in the rat, mouse, and human genomes. Genome Res. 14, 528–538 (2004).
Anderson, L. K., Hooker, K. D. & Stack, S. M. The distribution of early recombination nodules on zygotene bivalents from plants. Genetics 159, 1259–1269 (2001).
Kim, J. S. et al. Comprehensive molecular cytogenetic analysis of sorghum genome architecture: distribution of euchromatin, heterochromatin, genes and recombination in comparison to rice. Genetics 171, 1963–1976 (2005).
Wang, Y. et al. euchromatin and pericentromeric heterochromatin: comparative composition in the tomato genome. Genetics 172, 22529–22540 (2006).
Tanksley, S. D. et al. High density molecular linkage maps of the tomato and potato genomes. Genetics 132, 1141–1160 (1992).
Buckler, E. S. T. et al. Meiotic drive of chromosomal knobs reshaped the maize genome. Genetics 153, 415–426 (1999).
Yan, H. et al. Transcription and histone modifications in the recombination-free region spanning a rice centromere. Plant Cell 17, 3227–3238 (2005).
Drouaud, J. et al. Variation in crossing-over rates across chromosome 4 of Arabidopsis thaliana reveals the presence of meiotic recombination 'hot spots'. Genome Res. 16, 106–114 (2006).
Wu, J. Z. et al. Physical maps and recombination frequency of six rice chromosomes. Plant J. 36, 720–730 (2003).
See, D. R. et al. Gene evolution at the ends of wheat chromosomes. Proc. Natl Acad. Sci. USA 103, 4162–4167 (2006).
Khrustaleva, L. I., de Melo, P. E., van Heusden, A. W. & Kik, C. The integration of recombination and physical maps in a large-genome monocot using haploid genome analysis in a trihybrid allium population. Genetics 169, 1673–1685 (2005).
Schnable, P. S., Hsia, A. P. & Nikolau, B. J. Genetic recombination in plants. Curr. Opin. Plant Biol. 1, 123–129 (1998).
Fu, H., Zheng, Z. & Dooner, H. K. Recombination rates between adjacent genic and retrotransposon regions in maize vary by 2 orders of magnitude. Proc. Natl Acad. Sci. USA 99, 1082–1087 (2002).
Yao, H. et al. Molecular characterization of meiotic recombination across the 140-kb multigenic a1–sh2 interval of maize. Proc. Natl Acad. Sci. USA 99, 6157–6162 (2002).
Ma, J. & Bennetzen, J. L. Recombination, rearrangement, reshuffling, and divergence in a centromeric region of rice. Proc. Natl Acad. Sci. USA 103, 383–388 (2006).
Matsuo, M., Ito, Y., Yamauchi, R. & Obokata, J. The rice nuclear genome continuously integrates, shuffles, and eliminates the chloroplast genome to cause chloroplast-nuclear DNA flux. Plant Cell 17, 665–675 (2005).
Lin, X. et al. Sequence and analysis of chromosome 2 of the plant Arabidopsis thaliana. Nature 402, 761–768 (1999).
Bowers, J. E. et al. Comparative physical mapping links conservation of microsynteny to chromosome structure and recombination in grasses. Proc. Natl Acad. Sci. USA 102, 13206–13211 (2005).
Peterson-Burch, B. D., Nettleton, D. & Voytas, D. F. Genomic neighborhoods for Arabidopsis retrotransposons: a role for targeted integration in the distribution of the Metaviridae. Genome Biol. 5, R78 (2004).
Wright, S. I., Agrawal, N. & Bureau, T. E. Effects of recombination rate and gene density on transposable element distributions in Arabidopsis thaliana. Genome Res. 13, 1897–1903 (2003).
Rizzon, C. et al. Patterns of selection against transposons inferred from the distribution of Tc1, Tc3 and Tc5 insertions in the mut-7 line of the nematode Caenorhabditis elegans. Genetics 165, 1127–1135 (2003).
Anderson, L. K., Lai, A., Stack, S. M., Rizzon, C. & Gaut, B. S. Uneven distribution of expressed sequence tag loci on maize pachytene chromosomes. Genome Res. 16, 115–122 (2006).
International Rice Genome Sequencing Project. The map-based sequence of the rice genome. Nature 436, 793–800 (2005).
Dvorak, J., Yang, Z. L., You, F. M. & Luo, M. C. Deletion polymorphism in wheat chromosome regions with contrasting recombination rates. Genetics 168, 1665–1675 (2004).
Initiative, A. G. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796–815 (2000).
Mizuno, H. et al. Sequencing and characterization of telomere and subtelomere regions on rice chromosomes 1S, 2S, 2L, 6L, 7S, 7L and 8S. Plant J. 46, 206–217 (2006).
Yao, H. & Schnable, P. S. Cis-effects on meiotic recombination across distinct a1–sh2 intervals in a common zea genetic background. Genetics 170, 1929–1944 (2005).
Mezard, C. Meiotic recombination hotspots in plants. Biochem. Soc. Trans. 34, 531–534 (2006).
Anderson, L. K. & Stack, S. M. Recombination nodules in plants. Cytogenet. Genome Res. 109, 198–204 (2005).
Rizzon, C., Ponger, L. & Gaut, B. S. Striking similarities in the genomic distribution of tandemly arrayed genes in Arabidopsis and rice. PLoS Comp. Bio. 1 Sep 2006 (doi:10.1371/journal.pcbi.0020115).
Akhunov, E. D. et al. The organization and rate of evolution of wheat genomes are correlated with recombination rates along chromosome arms. Genome Res. 13, 753–763 (2003).
Thomas, J. H. Analysis of homologous gene clusters in Caenorhabditis elegans reveals striking regional cluster domains. Genetics 172, 127–143 (2006).
Dvorak, J. & Akhunov, E. D. Tempos of gene locus deletions and duplications and their relationship to recombination rate during diploid and polyploid evolution in the aegilops-triticum alliance. Genetics 171, 323–332 (2005).
Hall, A. E., Kettler, G. C. & Preuss, D. Dynamic evolution at pericentromeres. Genome Research 16, 355–364 (2006).
Akhunov, E. D. et al. Synteny perturbations between wheat homoeologous chromosomes caused by locus duplications and deletions correlate with recombination rates. Proc. Natl Acad. Sci. USA 100, 10836–10841 (2003).
Hurst, L. D., Pal, C. & Lercher, M. J. The evolutionary dynamics of eukaryotic gene order. Nature Rev. Genet. 5, 299–310 (2004).
Sorrells, M. E. et al. Comparative DNA sequence analysis of wheat and rice genomes. Genome Res. 13, 1818–1827 (2003).
Rice Chromosomes 11 and 12 Sequencing Consortia. The sequence of rice chromosomes 11 and 12, rich in disease resistance genes and recent gene duplications. BMC Biol. 3, 20 (2005).
Olmo, E. Quantitative variations in the nuclear DNA and phylogenesis of the Amphibia Caryologia. 26, 43–68 (1973).
Gregory, T. R. Animal Genome Size Database [onlline], (2005).
Murphy, W. J., Stanyon, R. & O'Brien, S. J. Evolution of mammalian genome organization inferred from comparative gene mapping. Genome Biol. 2, R1–R8 (2001).
Molinier, J., Ries, G., Zipfel, C. & Hohn, B. Transgeneration memory of stress in plants. Nature 442, 1046–1049 (2006).
Singh, N. D., Arndt, P. F. & Petrov, D. A. Genomic heterogeneity of background substitutional patterns in Drosophila melanogaster. Genetics 169, 709–722 (2005).
Charlesworth, D. & Wright, S. I. Breeding systems and genome evolution. Curr. Opin. Genet. Dev. 11, 685–690 (2001).
Cutter, A. D. & Payseur, B. A. Selection at linked sites in the partial selfer Caenorhabditis elegans. Mol. Biol. Evol. 20, 665–673 (2003).
Coop, G. & Przeworski, M. An evolutionary view of human recombination. Nature Rev. Genet. 5 Dec 2006 (doi:10.1038/nrg1947).
Myers, S., Bottolo, L., Freeman, C., McVean, G. & Donnelly, P. A fine-scale map of recombination rates and hotspots across the human genome. Science 310, 321–324 (2005).
Plagnol, V., Padhukasahasram, B., Wall, J. D., Marjoram, P. & Nordborg, M. relative influences of crossing over and gene conversion on the pattern of linkage disequilibrium in Arabidopsis thaliana. Genetics 172, 2441–2448 (2006).
Qi, L. L. et al. A chromosome bin map of 16,000 expressed sequence tag loci and distribution of genes among the three genomes of polyploid wheat. Genetics 168, 701–712 (2004).
Anderson, L. K. et al. High-resolution crossover maps for each bivalent of Zea mays using recombination nodules. Genetics 165, 849–865 (2003).
Sherman, J. D. & Stack, S. M. Two-dimensional spreads of synaptonemal complexes from Solanaceous plants: high-resolution recombination nodule map for tomato (Lycopersicon esculentum). Genetics 141, 683–708 (1995).
Stephan, W. & Langley, C. H. DNA polymorphism in lycopersicon and crossing-over per physical length. Genetics 150, 1585–1593 (1998).
Fransz, P. F. et al. Integrated cytogenetic map of chromosome arm 4S of A. thaliana: structural organization of heterochromatic knob and centromere region. Cell 100, 367–376 (2000).
Feltus, F. A. et al. An SNP resource for rice genetics and breeding based on subspecies indica and japonica genome alignments. Genome Res. 14, 1812–1819 (2004).
Acknowledgements
The work on recombination and genome evolution in the Gaut, Anderson and Dvorak laboratories are funded by the US National Science Foundation. S.I.W. is funded by the Alfred P. Sloan Foundation and the Canadian National Science and Engineering Research Council.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Glossary
- Fluorescence in situ hybridization
-
A technique that is used to label specific sequences on chromosomes with fluorescent molecules.
- Heterochromatic knobs
-
Cytologically visible regions of highly condensed chromatin that are distinct from pericentromeric regions.
- Microsatellite instability
-
A change in the number of repeats of microsatellites.
- Paracentric inversion
-
A structural chromosome alteration that results from breakage, inversion and reinsertion of a fragment of a chromosomal arm.
- Pericentric inversion
-
A structural alteration to a chromosome that results from breakage, inversion and reinsertion of a fragment that spans the centromere.
- Polyploid
-
Having three or more sets of homologous chromosomes (for example, tetraploid organisms have four sets of chromosomes).
- Synapsis
-
Formation of a synaptonemal complex between homologous chromosomes during prophase I of meiosis. Pairing is a more general term that refers to homologous associations in somatic as well as meiotic nuclei.
Rights and permissions
About this article
Cite this article
Gaut, B., Wright, S., Rizzon, C. et al. Recombination: an underappreciated factor in the evolution of plant genomes. Nat Rev Genet 8, 77–84 (2007). https://doi.org/10.1038/nrg1970
Issue Date:
DOI: https://doi.org/10.1038/nrg1970
This article is cited by
-
Evolution of a plant sex chromosome driven by expanding pericentromeric recombination suppression
Scientific Reports (2024)
-
Transcriptomic insights into shared responses to Fusarium crown rot infection and drought stresses in bread wheat (Triticum aestivum L.)
Theoretical and Applied Genetics (2024)
-
Telomere and subtelomere high polymorphism might contribute to the specificity of homologous recognition and pairing during meiosis in barley in the context of breeding
BMC Genomics (2023)
-
Linkage mapping combined with GWAS revealed the genetic structural relationship and candidate genes of maize flowering time-related traits
BMC Plant Biology (2022)
-
Phylogenomics of the genus Glycine sheds light on polyploid evolution and life-strategy transition
Nature Plants (2022)