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

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 kbp 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 (SNP) observed for MAF4 and MAF5 suggest purifying selection and conservation of function. In contrast, high levels of nonsynonymous SNPs, insertion-deletion, 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.