ARS | Publication request: Pericentromeric effects shape the patterns of divergence, retention, and expression of duplicated genes in the Paleopolyploid Soybean

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: December 20, 2011
Publication Date: January 6, 2012
Citation: Du, J., Tian, Z., Sui, Y., Zhao, M., Song, Q., Cannon, S.B., Cregan, P.B., Ma, J. 2012. Pericentromeric effects shape the patterns of divergence, retention, and expression of duplicated genes in the Paleopolyploid Soybean. The Plant Cell. 24(1):21-32.

Interpretive Summary: Plant evolution differs from animal evolution in several key ways. Many plants can self-fertilize, and this self-fertilization allows plants to occasionally undergo a doubling of all of their chromosomes. The chromosomal doubling may either result from a single plant's chromosomes dividing too many times, or from two different varieties or closely-related species combining their chromosomes and then producing viable offspring through self-fertilization. This chromosomal doubling, or "polyploidy", seems to have occurred in the history of most plants. In soybean, it occurred about 10 million years ago, and also about 60 million years ago. This study examines how soybean's duplicated genes changed and evolved in soybean over those 10 million years. Genes near the chromosome centers changed more slowly than near the chromosome arms, but genes near the chromosome centers are also more active in plant cells (are often more highly "expressed", and potentially produce more proteins). These results are relevant to plant breeders because the genes in the chromosome centers are especially difficult to work with (the chromosome centers from two different soybean varieties can't be easily combined to give new plant varieties). This study shows, however, that the genes near the chromosome centers may still be very important in determining the characteristics of a soybean variety.

Technical Abstract: Sequence divergence and fractionation of duplicated genes following whole genome duplication (WGD) are important processes in the course of polyploid genome evolution. However, the evolutionary forces that govern the divergence and retention of WGD-derived genes are poorly understood. In this study, we first investigated the rates of non-synonymous substitution (Ka) and the rates of synonymous substitution (Ks) for a nearly complete set of genes in the palaeopolyploid soybean by comparing the orthologs between soybean (Glycine max) and its progenitor species Glycine soja. We then compared the patterns of gene divergence and expression between pericentromeric regions and chromosomal arms in different gene categories. Our results reveal strong associations between duplication status and Ka and gene expression levels, and overall low Ks and low levels of gene expression in pericentromeric regions – which account for only 6.9% of recombination of the whole genome. It is theorized that deleterious mutations can easily accumulate in recombination-suppressed regions because of Hill-Robertson effects. Intriguingly, the genes in pericentromeric regions showed significantly lower Ka and higher levels of expression than their homoeologs in chromosomal arms. This asymmetric evolution of two members of individual WGD-derived gene pairs, echoing the biased accumulation of singletons in pericentromeric regions, suggests that distinct genomic features between the two distinct chromatin types are important determinants shaping the patterns of divergence and retention of WGD-derived genes. Genome reshuffling after the WGD event appears to be the major cause for restructuring of homologous regions, including transitions from chromosomal arms to pericentromeric regions or vice versa.