MBE Advance Access published online on September 6, 2007
Molecular Biology and Evolution, doi:10.1093/molbev/msm184
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Research Article |
The Monosaccharide Transporter Gene Family in Arabidopsis and Rice: A History of Duplications, Adaptive Evolution and Functional Divergence
Department of Biological Sciences, Idaho State University, Pocatello, ID
1 Corresponding Author, Dept. of Biological Sciences, Campus Box 8007, Idaho State University, Pocatello, ID 83209-8007, johndeb2{at}isu.edu
Received for publication May 16, 2007. Revision received August 9, 2007. Accepted for publication August 13, 2007.
Current hypotheses of gene duplicate divergence propose that surviving members of a gene duplicate pair may evolve, under conditions of purifying or nearly neutral selection, in one of two ways: With new function arising in one duplicate while the other retains original function (neofunctionalization) or partitioning of the original function between the two paralogs (subfunctionalization). More recent studies propose that subfunctionalization followed by neofunctionalization (subneofunctionalization) explains the divergence of many duplicate genes. In this analysis, we evaluate these hypotheses in the context of the large monosaccharide transporter (MST) gene families in Arabidopsis and rice. MSTs have an ancient origin, predating plants, and have evolved in the seed plant lineage to comprise seven subfamilies. In Arabidopsis, 53 putative MST genes have been identified, with one subfamily greatly expanded by tandem gene duplications. We searched the rice genome for members of the MST gene family and compared them to the MST gene family in Arabidopsis to determine subfamily expansion patterns and estimate gene duplicate divergence times. We tested hypotheses of gene duplicate divergence in 24 paralog pairs by comparing protein sequence divergence rates, estimating positive selection on codon sites, and analyzing tissue expression patterns. Results reveal the MST gene family to be significantly larger (65) in rice with two subfamilies greatly expanded by tandem duplications. Gene duplicate divergence time estimates indicate that early diversification of most subfamilies occurred in the Proterozoic (2500-540 MY) and that expansion of large subfamilies continued through the Cenozoic (65-0 MY). Two thirds of paralog pairs show statistically symmetric rates of sequence evolution, most consistent with the subfunctionalization model, with half of those showing evidence for positive selection in one or both genes. Among eight paralog pairs showing asymmetric divergence rates, most consistent with the neofunctionalization model, nearly half show evidence of positive selection. Positive selection does not appear in any duplicate pairs younger than 
34 MY. Our data suggest that the neofunctionalization, subfunctionalization and subneofunctionalization models describe different outcomes along a continuum of divergence resulting from initial conditions of relaxed constraint after duplication.
Key Words: Gene duplicate divergence • molecular clock • adaptive evolution • monosaccharide transporter • Arabdiopsis thaliana • Oryza sativa