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

Department of Agronomy, Purdue University, West Lafayette, Indiana 47907, USA.
The Plant Cell (Impact Factor: 9.34). 02/2012; 24(1):21-32. DOI: 10.1105/tpc.111.092759
Source: PubMed


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.

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    • "These regions may have become LR relatively recently and ohnolog elimination has not yet been completed or they may not be fully within the LR-PC region. We define the LR-PC region as a continuous region with at least 20-fold lower average recombination rate than the genomic average and none of the soybean regions fulfil that criterion, with reduced recombination ratios of between 4-fold and 13-fold (Du et al., 2012). "

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    • "The ratio of MIRNA singletons to MIRNA duplicates is ;1.06:1, significantly higher than the ratio (0.48:1) of the PEG singletons to PEG duplicates generated by the same WGD event (P < 0.01, x 2 test). Further comparison of genomic regions harboring these MIRNAs with respective putative duplicated regions generated by the recent WGD (Schmutz et al., 2010; Du et al., 2012) identified 39 MIRNA sequences that are homoeologous to 39 of the 234 singletons defined above (Supplemental Data Set 4). Of these 39 homoeologs, 30 contains point mutations and two contain small insertions/ deletions (indels) in the mature miRNA regions compared with their duplicates, and the remaining seven were more diverged from their duplicates. "
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    ABSTRACT: The evolutionary dynamics of duplicated protein-encoding genes (PEGs) is well documented. However, the evolutionary patterns and consequences of duplicated MIRNAs and the potential influence on the evolution of their PEG targets are poorly understood. Here, we demonstrate the evolution of plant MIRNAs subsequent to a recent whole-genome duplication. Overall, the retention of MIRNA duplicates was correlated to the retention of adjacent PEG duplicates, and the retained MIRNA duplicates exhibited a higher level of interspecific preservation of orthologs than singletons, suggesting that the retention of MIRNA duplicates is related to their functional constraints and local genomic stability. Nevertheless, duplication status, rather than local genic collinearity, was the primary determinant of levels of nucleotide divergence of MIRNAs. In addition, the retention of duplicated MIRNAs appears to be associated with the retention of their corresponding duplicated PEG targets. Furthermore, we characterized the evolutionary novelty of a legume-specific microRNA (miRNA) family, which resulted from rounds of genomic duplication, and consequent dynamic evolution of its NB-LRR targets, an important gene family with primary roles in plant-pathogen interactions. Together, these observations depict evolutionary patterns and novelty of MIRNAs in the context of genomic duplication and evolutionary interplay between MIRNAs and their PEG targets mediated by miRNAs. © 2015 American Society of Plant Biologists. All rights reserved.
    Full-text · Article · Mar 2015 · The Plant Cell
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    • "The protein sequences of the individual PEBP family members from Arabidopsis were used as queries against the soybean genome (Schmutz et al., 2010). Duplicated gene pairs of PEBP members were identified based on previous whole-genome analyses of duplicated regions and genes (Schmutz et al., 2010; Du et al., 2012). Phylogenetic analysis was performed following a previously reported method (Jiao et al., 2011). "
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    ABSTRACT: Gene duplication provides resources for novel gene functions. Identification of the amino acids responsible for functional conservation and divergence of duplicated genes will strengthen our understanding of their evolutionary course. Here, we conducted a systemic functional investigation of phosphatidylethanolamine binding proteins (PEBPs) in soybean (Glycine max) and Arabidopsis thaliana. Our results demonstrated that after the ancestral duplication, the lineage of the common ancestor of the FLOWERING LOCUS T (FT) and TERMINAL FLOWER1 (TFL1) subfamilies functionally diverged from the MOTHER OF FT AND TFL1 (MFT) subfamily to activate flowering and repress flowering, respectively. They also underwent further specialization after subsequent duplications. Although the functional divergence increased with duplication age, we observed rapid functional divergence for a few pairs of young duplicates in soybean. Association analysis between amino acids and functional variations identified critical amino acid residues that led to functional differences in PEBP members. Using transgenic analysis, we validated a subset of these differences. We report clear experimental evidence for the functional evolution of the PEBPs in the MFT, FT, and TFL1 subfamilies, which predate the origin of angiosperms. Our results highlight the role of amino acid divergence in driving evolutionary novelty after duplication. © 2015 American Society of Plant Biologists. All rights reserved.
    Full-text · Article · Feb 2015 · The Plant Cell
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