Diverse selective modes among orthologs/paralogs of the chalcone synthase (Chs) gene family of Arabidopsis thaliana and its relative A. halleri ssp. gemmifera

As a model system, Arabidopsis thaliana and its wild relatives have played an important role in the study of genomics and evolution in plants. In this study, we examined the genetic diversity of the chalcone synthase (Chs) gene, which encodes a key enzyme of the flavonoid pathway and is located on chromosome five, as well as two Chs-like genes on the first and fourth chromosomes of Arabidopsis. The objectives of the study are to determine if natural selection operates differentially on the paralogs of the Chs gene family in A. thaliana and Arabidopsis halleri ssp. gemmifera. The mode of selection was inferred from Tajima’s D values from noncoding and coding regions, as well as from the ratio of nonsynonymous to synonymous substitutions. Both McDonald–Kreitman and HKA tests revealed the effects of selection on the allelic distribution, except for the chromosome 1 paralog in ssp. gemmifera. The Chs gene on chromosome 5 was under purifying selection in both species. Significant, negative Tajima’s D values at synonymous sites and positive Fay and Wu’s H values within coding region, plus reduced genetic variability in introns, indicated effects of background selection in shaping the evolution of this gene region in A. thaliana. The Chs paralog on chromosome 1 was under positive selection in A. thaliana, while interspecific introgression and balancing selection determined the fates of the paralog and resulted in high heterogeneity in ssp. gemmifera. Local adaptation differentiated populations of Japan and China at the locus. In contrast, the other Chs-paralog of chromosome 4 was shaped by purifying selection in A. thaliana, while under positive selection in ssp. gemmifera, as indicated by dn/ds > 1. Moreover, these contrasting patterns of selection have likely resulted in functional divergence in Arabidopsis, as indicated by radical amino acid substitutions at the chalcone synthase/stilbene synthase motif of the Chs genes. Unlike previous studies of the evolutionary history of A. thaliana, the high levels of genetic diversity in most gene regions of Chs paralogs and nonsignificant Tajima’s D in the intron sequences of the Chs gene family in A. thaliana did not reflect the effects of a recent demographic expansion.