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The Effects of Gene Duplication Modes on the Evolution of Regulatory Divergence in Wild and Cultivated Soybean.

ABSTRACT: Regulatory changes include divergence in both cis-elements and trans-factors, which play roles in organismal evolution. Whole genome duplications (WGD) followed by diploidization are a recurrent feature in the evolutionary history of angiosperms. Prior studies have shown that duplicated genes have different evolutionary fates due to variable selection constraints and results in genomic compositions with hallmarks of paleopolyploidy. The recent sequential WGDs and post-WGD evolution in the common ancestor of cultivated soybean (Glycine max) and wild soybean (Glycine soja), together with other models of gene duplication, have resulted in a highly duplicated genome. In this study, we investigated the transcriptional changes in G. soja and G. max. We identified a sizable proportion of interspecific differentially expressed genes (DEGs) and found parental expression level dominance of G. max in their F1 hybrids. By classifying genes into different regulatory divergence types, we found the trans-regulatory changes played a predominant role in transcriptional divergence between wild and cultivated soybean. The same gene ontology (GO) and protein family (Pfam) terms were found to be over-represented in DEGs and genes of cis-only between JY47 and GS, suggesting the substantial contribution of cis-regulatory divergences to the evolution of wild and cultivated soybeans. By further dissecting genes into five different duplication modes, we found genes in different duplication modes tend to accumulate different types of regulatory differences. A relatively higher proportion of cis-only regulatory divergences was detected in singleton, dispersed, proximal, and tandem duplicates than WGD duplicates and genome-wide level, which is in line with the prediction of gene balance hypothesis for the differential fates of duplicated genes post-WGD. The numbers of cis-only and trans-only regulated genes were similar for singletons, whereas there were more genes of trans-only than cis-only in the rest duplication types, especially in WGD in which there were two times more trans-only genes than that in cis-only type. Tandem duplicates showed the highest proportion of trans-only genes probably due to some special features of this class. In summary, our results demonstrate that genes in different duplication modes have different fates in transcriptional evolution underpinned by cis- or trans-regulatory divergences in soybean and likely in other paleopolyploid higher organisms.

SUBMITTER: Zhao N

PROVIDER: S-EPMC7753205 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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The Effects of Gene Duplication Modes on the Evolution of Regulatory Divergence in Wild and Cultivated Soybean.

Zhao Na N Ding Xiaoyang X Lian Taotao T Wang Meng M Tong Yan Y Liang Di D An Qi Q Sun Siwen S Jackson Scott A SA Liu Bao B Xu Chunming C

Frontiers in genetics 20201208

Regulatory changes include divergence in both <i>cis</i>-elements and <i>trans</i>-factors, which play roles in organismal evolution. Whole genome duplications (WGD) followed by diploidization are a recurrent feature in the evolutionary history of angiosperms. Prior studies have shown that duplicated genes have different evolutionary fates due to variable selection constraints and results in genomic compositions with hallmarks of paleopolyploidy. The recent sequential WGDs and post-WGD evolution ...[more]

PMID: 33363574

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Project description:BackgroundCarbon and nitrogen metabolism need to be highly regulated to achieve cell acclimation to changing environmental conditions. The understanding of physio-biochemical responses of crops to salinity stress could help to stabilize their performance and yield. In this study we have analyzed the roles of photosynthesis, ion physiology and nitrate assimilation toward saline/alkaline stress acclimation in wild and cultivated soybean seedlings.MethodsGrowth and photosynthetic parameters, ion concentrations and the activity of enzymes involved in nitrogen assimilation were determined in seedlings of one wild and one cultivated soybean accession subjected to saline or alkaline stresses.ResultsBoth saline and alkaline stresses had a negative impact on the growth and metabolism of both wild and cultivated soybean.The growth, photosynthesis, and gas exchange parameters showed a significant decrease in response to increasing salt concentration. Additionally, a significant increase in root Na+ and Cl- concentration was observed. However, photosynthetic performance and ion regulation were higher in wild than in cultivated soybean under saline and alkaline stresses. Nitrate reductase (NR) and the glutamine synthetase/glutamate synthase (GS/GOGAT) cycle showed a significant decrease in leaves of both genotypes. The reduction in the GS/GOGAT cycle was accompanied by high aminating glutamate dehydrogenase (NADH-glutamate dehydrogenase) activity, indicating the assimilation of high levels of NH4 +. A significant increase in the activities of aminating and deaminating enzymes, including glutamate dehydrogenase (GDH), alanine aminotransferase (AlaAT) and aspartate aminotransferase (AspAT), was observed, probably due to the high glutamate demand and maintenance of the Krebs cycle to correct the C: N status.ConclusionsCultivated soybean was much more stress sensitive than was the wild soybean. The decrease in growth, photosynthesis, ion regulation and nitrogen assimilation enzymes was greater in cultivated soybean than in wild soybean. The impact of alkaline stress was more pronounced than that of saline stress. Wild soybean regulated the physiological mechanisms of photosynthesis and nitrate assimilation more effectively than did cultivated soybean. The present findings provide a theoretical basis with which to screen and utilize wild and cultivated soybean germplasm for breeding new stress-tolerant soybean.

Dataset Information

The Effects of Gene Duplication Modes on the Evolution of Regulatory Divergence in Wild and Cultivated Soybean.

Publications

The Effects of Gene Duplication Modes on the Evolution of Regulatory Divergence in Wild and Cultivated Soybean.

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