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MBE Advance Access published online on January 22, 2004

Molecular Biology and Evolution, doi:10.1093/molbev/msh059
Molecular Biology and Evolution © Society for Molecular Biology and Evolution 2004; all rights reserved
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Accepted November 18, 2003
© 2004 Society for Molecular Biology and Evolution

Original Articles

Rapid Evolution of a Pollen-Specific Oleosin-Like Gene Family from Arabidopsis Thaliana and Closely Related Species

Manja Schein 1, Ziheng Yang 2, Thomas Mitchell-Olds 1, and Karl J. Schmid 1*

1 Department of Genetics and Evolution, Max-Planck-Institute of Chemical Ecology, Jena, Germany
2 Department of Biology, University College London, London, UK

* To whom correspondence should be addressed. E-mail: schmid{at}ice.mpg.de.


   Abstract

It has been shown in a variety of species that genes expressed in reproductive tissues evolve rapidly, which often appears to be the result of positive Darwinian selection. We investigated the evolution of a family of seven pollen-specific oleosin-like proteins (or oleopollenins) in Arabidopsis thaliana and two closely related species. More than 30 kb of a genomic region that harbors the complete, tandemly repeated oleopollenin cluster were sequenced from Arabidopsis lyrata ssp. lyrata and Boechera drummondii. A phylogenetic analysis of the complete gene cluster from these three species and from Brassica oleracea confirmed its rapid evolution due to gene duplication and gene loss events, numerous amino acid substitutions and insertions/deletions in the coding sequence. Independent duplications were inferred in the lineages leading to Arabidopsis and to Brassica, and gene loss in the lineage leading to B. drummondii. Comparisons of the ratio of nonsynonymous (dN) and synonymous (dS) divergence revealed that the oleopollenins are among the most rapidly evolving proteins currently known from Arabidopsis and that they may evolve under positive Darwinian selection. RT-PCR analysis demonstrated the expression of oleopollenins in flowers of the outcrossing A. lyrata, the selfing B. drummondii, and the apomictic Boechera holboellii, suggesting that oleopollenins play an important role in species with different breeding systems. These results are consistent with a putative function in species recognition, but further analyses of protein function and sequence variation in species with different breeding systems are necessary to reveal the underlying causes for the rapid evolution of oleopollenins.

Key Words: Oleopollenin, reproductive protein, positive selection, comparative genomics, Arabidopsis, speciation


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