Divergence in expression between duplicated genes in Arabidopsis.

New genes may arise through tandem duplication, dispersed small-scale duplication, and polyploidy, and patterns of divergence between duplicated genes may vary among these classes. We have examined patterns of gene expression and coding sequence divergence between duplicated genes in Arabidopsis thaliana. Due to the simultaneous origin of polyploidy-derived gene pairs, we can compare covariation in the rates of expression divergence and sequence divergence within this group. Among tandem and dispersed duplicates, much of the divergence in expression profile appears to occur at or shortly after duplication. Contrary to findings from other eukaryotic systems, there is little relationship between expression divergence and synonymous substitutions, whereas there is a strong positive relationship between expression divergence and nonsynonymous substitutions. Because this pattern is pronounced among the polyploidy-derived pairs, we infer that the strength of purifying selection acting on protein sequence and expression pattern is correlated. The polyploidy-derived pairs are somewhat atypical in that they have broader expression patterns and are expressed at higher levels, suggesting differences among polyploidy- and nonpolyploidy-derived duplicates in the types of genes that revert to single copy. Finally, within many of the duplicated pairs, 1 gene is expressed at a higher level across all assayed conditions, which suggests that the subfunctionalization model for duplicate gene preservation provides, at best, only a partial explanation for the patterns of expression divergence between duplicated genes.

Ganko EW ，Meyers BC ，Vision TJ 《MOLECULAR BIOLOGY AND EVOLUTION》

Extensive divergence in alternative splicing patterns after gene and genome duplication during the evolutionary history of Arabidopsis.

Gene duplication at various scales, from single gene duplication to whole-genome (WG) duplication, has occurred throughout eukaryotic evolution and contributed greatly to the large number of duplicated genes in the genomes of many eukaryotes. Previous studies have shown divergence in expression patterns of many duplicated genes at various evolutionary time scales and cases of gain of a new function or expression pattern by one duplicate or partitioning of functions or expression patterns between duplicates. Alternative splicing (AS) is a fundamental aspect of the expression of many genes that can increase gene product diversity and affect gene regulation. However, the evolution of AS patterns of genes duplicated by polyploidy, as well as in a sizable number of duplicated gene pairs in plants, has not been examined. Here, we have characterized conservation and divergence in AS patterns in genes duplicated by a polyploidy event during the evolutionary history of Arabidopsis thaliana. We used reverse transcription-polymerase chain reaction to assay 104 WG duplicates in six organ types and in plants grown under three abiotic stress treatments to detect organ- and stress-specific patterns of AS. Differences in splicing patterns in one or more organs, or under stress conditions, were found between the genes in a large majority of the duplicated pairs. In a few cases, AS patterns were the same between duplicates only under one or more abiotic stress treatments and not under normal growing conditions or vice versa. We also examined AS in 42 tandem duplicates and we found patterns of AS roughly comparable with the genes duplicated by polyploidy. The alternatively spliced forms in some of the genes created premature stop codons that would result in missing or partial functional domains if the transcripts are translated, which could affect gene function and cause functional divergence between duplicates. Our results indicate that AS patterns have diverged considerably after gene and genome duplication during the evolutionary history of the Arabidopsis lineage, sometimes in an organ- or stress-specific manner. AS divergence between duplicated genes may have contributed to gene functional evolution and led to preservation of some duplicated genes.

Zhang PG ，Huang SZ ，Pin AL ，Adams KL ... -  《-》

Molecular population genetics of redundant floral-regulatory genes in Arabidopsis thaliana.

Functional redundancy between duplicated genes is predicted to be transitory, as one gene either loses its function or gains a new function, or both genes accrue degenerative, yet complimentary mutations. Yet there are many examples where functional redundancy has been maintained between gene duplicates. To determine whether selection is acting on functionally redundant gene duplicates, we performed molecular evolution and population genetic analyses between two pairs of functionally redundant MADS-box genes from the model plant Arabidopsis thaliana: SEPALLATA1 (SEP1) and SEPALLATA2 (SEP2), involved in floral organ identity, and SHATTERPROOF1 (SHP1) and SHATTERPROOF2 (SHP2), involved in seed shattering. We found evidence for purifying selection acting to constrain functional divergence between paralogous genes. The protein evolution of both pairs of duplicate genes is functionally constrained, as evidenced by Ka/Ks ratios of 0.16 between paralogs. This functional constraint is stronger in the highly conserved DNA-binding and protein-binding MIK region than in the C-terminal region. We also assayed the evolutionary forces acting between orthologs of the SEP and SHP genes in A. thaliana and the closely related species, Arabidopsis lyrata. Heterogeneity analyses of the polymorphism-to-divergence ratio indicate selective sweeps have occurred within the transcriptional unit of SHP1 and the promoter of SHP2 in the A. thaliana lineage. Similar analyses identified a significant reduction in polymorphism within the SEP1 locus, spanning the 3' region of intron 1 to exon 3, that may represent an intragenic sweep within the SEP1 locus. We discuss whether the evolutionary forces acting on SEP1 and SEP2 versus SHP1 and SHP2 vary according to their position in the floral developmental pathway, as found with other floral-regulatory genes.

Moore RC ，Grant SR ，Purugganan MD 《MOLECULAR BIOLOGY AND EVOLUTION》

Transcriptional divergence of the duplicated oxidative stress-responsive genes in the Arabidopsis genome.

Previous studies have indicated that Arabidopsis thaliana experienced a genome-wide duplication event shortly before its divergence from Brassica followed by extensive chromosomal rearrangements and deletions. While a large number of the duplicated genes have significantly diverged or lost their sister genes, we found 4222 pairs that are still highly conserved, and as a result had similar functional assignments during the annotation of the genome sequence. Using whole-genome DNA microarrays, we identified 906 duplicated gene pairs in which at least one member exhibited a significant response to oxidative stress. Among these, only 117 pairs were up- or down-regulated in both pairs and many of these exhibited dissimilar patterns of expression. Examination of the expression patterns of PAL1 and PAL2, ACD1 and ACD2, genes coding for two Hsp20s, various P450s, and electron transfer flavoproteins suggests Arabidopsis evolved a number of distinct oxidative stress response mechanisms using similar gene sets following the duplication of its genome.

Stanley Kim H ，Yu Y ，Snesrud EC ，Moy LP ，Linford LD ，Haas BJ ，Nierman WC ，Quackenbush J ... -  《PLANT JOURNAL》

The monosaccharide transporter gene family in Arabidopsis and rice: a history of duplications, adaptive evolution, and functional divergence.

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 [NF]) or partitioning of the original function between the 2 paralogs (subfunctionalization [SF]). More recent studies propose that SF followed by NF (subneofunctionalization [SNF]) 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 7 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 with 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 2 subfamilies greatly expanded by tandem duplications. Gene duplicate divergence time estimates indicate that early diversification of most subfamilies occurred in the Proterozoic (2500-540 Myr) and that expansion of large subfamilies continued through the Cenozoic (65-0 Myr). Two-thirds of paralog pairs show statistically symmetric rates of sequence evolution, most consistent with the SF model, with half of those showing evidence for positive selection in one or both genes. Among 8 paralog pairs showing asymmetric divergence rates, most consistent with the NF model, nearly half show evidence of positive selection. Positive selection does not appear in any duplicate pairs younger than approximately 34 Myr. Our data suggest that the NF, SF, and SNF models describe different outcomes along a continuum of divergence resulting from initial conditions of relaxed constraint after duplication.

Johnson DA ，Thomas MA 《MOLECULAR BIOLOGY AND EVOLUTION》