Pericentromeric Effects Shape the Patterns of Divergence, Retention, and Expression of Duplicated Genes in the Paleopolyploid Soybean  

Abstract

The evolutionary forces that govern the divergence and retention of duplicated genes in polyploids are poorly understood. In this study, we first investigated the rates of nonsynonymous substitution (Ka) and the rates of synonymous substitution (Ks) for a nearly complete set of genes in the paleopolyploid soybean (Glycine max) by comparing the orthologs between soybean and its progenitor species Glycine soja and 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. It is theorized that deleterious mutations can easily accumulate in recombination-suppressed regions, because of Hill-Robertson effects. Intriguingly, the genes in pericentromeric regions-the cold spots for meiotic recombination in soybean-showed significantly lower Ka and higher levels of expression than their homoeologs in chromosomal arms. This asymmetric evolution of two members of individual whole genome duplication (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-Wide Characterization of Nonreference Transposons Reveals Evolutionary Propensities of Transposons in Soybean

“…We found that the densities of nonreference LTR-RTs (either gypsy or copia subclasses) detected in either the G. soja or the G. max subpopulations in pericentromeric regions were significantly higher than in chromosomal arms (Table 4), consistent with the distribution pattern of the accumulated LTR-RTs in these two types of chromatin environments in the reference genome (Du et al, 2012;Table 4, Figure 3). By contrast, the densities of the nonreference DNA TEs in both the G. max and G. soja subpopulations did not show significant differences between pericentromeric regions and chromosomal arms, although the accumulated DNA TEs were significantly enriched in pericentromeric regions compared with chromosomal arms of the reference genome (Du et al, 2012; Further comparisons between the pericentromeric regions and chromosomal arms of the 20 chromosomes revealed positive correlations between the nonreference LTR-RTs (either gypsy or copia subclasses) in either the G. max or G. soja subpopulations and the accumulated LTR-RT contents and negative correlations between the nonreference DNA TEs in either the G. max or G. soja subpopulations and the accumulated DNA TE contents (Table 5).…”

“…By contrast, the densities of the nonreference DNA TEs in both the G. max and G. soja subpopulations did not show significant differences between pericentromeric regions and chromosomal arms, although the accumulated DNA TEs were significantly enriched in pericentromeric regions compared with chromosomal arms of the reference genome (Du et al, 2012; Further comparisons between the pericentromeric regions and chromosomal arms of the 20 chromosomes revealed positive correlations between the nonreference LTR-RTs (either gypsy or copia subclasses) in either the G. max or G. soja subpopulations and the accumulated LTR-RT contents and negative correlations between the nonreference DNA TEs in either the G. max or G. soja subpopulations and the accumulated DNA TE contents (Table 5). By contrast, negative correlations of nonreference LTR-RTs (either gypsy or copia subclasses) in either the G. max or G. soja subpopulations with gene densities and positive correlations of nonreference DNA TEs with gene densities were detected (Table 5).…”

“…This distinction was much clearer when unmappable insertions were included in the comparison between the two classes of nonreference TEs (see Supplemental Figure 6 online). Because the proportions of TEs, genes, and unclassified sequences vary significantly between pericentromeric regions and chromosomal arms (Table 4; Du et al, 2012), the relative abundance of the nonreference LTR-RT and DNA TE insertions in these three categories of DNA components also differ substantially ( Figure 5). It is notable that, in chromosomal arms, the relative abundance of nonreference LTR-RTs in genic sequences (17.7%) was even higher than that of nonreference DNA TEs in genic regions (9.2%) ( Figure 5), suggesting that the insertional biases of either LTR-RTs or DNA TEs vary between these two distinct chromatin environments.…”

Evolutionary Patterns and Coevolutionary Consequences of MIRNA Genes and MicroRNA Targets Triggered by Multiple Mechanisms of Genomic Duplications in Soybean

“…Despite the widespread acceptance of these evolutionary models, with empirical examples for each (Assis and Bachtrog, 2013), more and more studies suggest that rewiring of the regulatory networks following WGD might have had a significant impact on the evolutionary consequences of duplicated genes rather than functional divergence of duplicated proteins (De Smet and Van de Peer, 2012). This proposition seems to be well supported by the observation that the majority of duplicated genes exhibit distinct patterns of expression between the two members of each pair, as revealed by genome-wide profiling of plant transcriptomes across different tissues and development stages (Danilevskaya et al, 2003;Du et al, 2012;Roulin et al, 2012).…”

“…Based on the newly annotated set of PEGs in the soybean reference genome (version 1.1, www.soybase.org) and reanalysis of the duplicated genomic blocks retained after the recent WGD event (Schmutz et al, 2010;Du et al, 2012), 16,996 singletons and 17,627 PEG pairs that correspond to 35,254 duplicates were defined (Supplemental Data Set 3). As per the assumption that a singleton is the product of deletion of one of two members of a duplicated gene pair (Schmutz et al, 2010), it is estimated that, maximally, 16,996 PEGs were eliminated after the recent soybean WGD event (Supplemental Data Set 3), suggesting rapid fragmentation of the duplicated genomes.…”