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MBE Advance Access published online on January 12, 2009
Molecular Biology and Evolution, doi:10.1093/molbev/msn300
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© The Author 2009. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Research Article

Complex rearrangements lead to novel chimeric gene fusion polymorphisms at the Arabidopsis thaliana MAF2-5 flowering time gene cluster

Ana L. Caicedo1,*, Cristina Richards2, Ian M. Ehrenreich2,3 and Michael D. Purugganan2

1 Biology Department, 221 Morrill Science Center, University of Massachusetts, Amherst, MA 01003
2 Center for Genomics and Systems Biology, Department of Biology, 100 Washington Square East, New York University, New York, NY 10003
3 Department of Genetics, North Carolina State University, Raleigh, NC 27695

* Corresponding author: Ana L. Caicedo, Biology Department, University of Massachusetts, Amherst, MA 01003; Email: caicedo{at}bio.umass.edu, Tel. (413) 545 0975.

Received for publication August 7, 2008. Revision received December 3, 2008. Accepted for publication December 22, 2008.

Tandem gene clusters of multigene families are rearrangement hotspots, and may be a major source of novel gene formation. Here we report on a molecular population genetic analysis of the MAF2-5 gene cluster of the model plant species, Arabidopsis thaliana. The MAF2-5 genes are a MADS-box multigene family cluster spanning ~24 kilo base pairs on chromosome 5. We find heterogeneous evolutionary dynamics among these genes, all of which are closely related to the floral repressor, FLC, and are believed to play a role in the control of flowering time in A. thaliana. Low levels of nonsynonymous single nucleotide polymorphism (SNPs) observed for MAF4 and MAF5 suggest purifying selection and conservation of function. In contrast, high levels of nonsynonymous SNPs, indels, and rearrangements are observed for MAF2 and MAF3, including novel gene fusions that persist as a moderate-frequency polymorphism in A. thaliana. These fused genes, involving MAF2 and portions of MAF3, are expressed, resulting in the production of chimeric, alternatively spliced transcripts of MAF2. Association studies support a correlation between the described MAF2-MAF3 gene rearrangements and flowering time variation in the species. The finding that complex rearrangements within gene clusters, such as those observed for MAF2, might play a role in the generation of ecologically important phenotypic variation, emphasize the need for emerging high throughput genotyping and sequencing techniques to correctly reconstruct gene chimeras and other complex polymorphisms.

Key Words: alternative splicing • gene origin • gene fusion • MADS-box • quantitative trait loci


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