Dataset Information

Fine-Tuning the Expression of Duplicate Genes by Translational Regulation in Arabidopsis and Maize.

ABSTRACT: Plant genomes are extensively shaped by various types of gene duplication. However, in this active area of investigation, the vast majority of studies focus on the sequence and transcription of duplicate genes, leaving open the question of how translational regulation impacts the expression and evolution of duplicate genes. We explored this issue by analyzing the ribo- and mRNA-seq data sets across six tissue types and stress conditions in Arabidopsis thaliana and maize (Zea mays). We dissected the relative contributions of transcriptional and translational regulation to the divergence in the abundance of ribosome footprint (RF) for different types of duplicate genes. We found that the divergence in RF abundance was largely programmed at the transcription level and that translational regulation plays more of a modulatory role. Intriguingly, translational regulation is characterized by its strong directionality, with the divergence in translational efficiency (TE) globally counteracting the divergence in mRNA abundance, indicating partial buffering of the transcriptional divergence between paralogs by translational regulation. Divergence in TE was associated with several sequence features. The faster-evolving copy in a duplicate pair was more likely to show lower RF abundance, which possibly results from relaxed purifying selection compared with its paralog. A considerable proportion of duplicates displayed differential TE across tissue types and stress conditions, most of which were enriched in photosynthesis, energy production, and translation-related processes. Additionally, we constructed a database TDPDG-DB (http://www.plantdupribo.tk), providing an online platform for data exploration. Overall, our study illustrates the roles of translational regulation in fine-tuning duplicate gene expression in plants.

SUBMITTER: Wang S

PROVIDER: S-EPMC6530396 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Fine-Tuning the Expression of Duplicate Genes by Translational Regulation in Arabidopsis and Maize.

Wang Sishuo S Chen Youhua Y

Frontiers in plant science 20190508

Plant genomes are extensively shaped by various types of gene duplication. However, in this active area of investigation, the vast majority of studies focus on the sequence and transcription of duplicate genes, leaving open the question of how translational regulation impacts the expression and evolution of duplicate genes. We explored this issue by analyzing the ribo- and mRNA-seq data sets across six tissue types and stress conditions in Arabidopsis thaliana and maize (Zea mays). ...[more]

PMID: 31156655

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Project description:Dendritic cells (DCs) are the sentinels of the mammalian immune system and they undergo a complex maturation process mediated by activation upon pathogen detection. Recent studies described the analysis of activated DCs by transcriptional profiling, but translation regulation was never taken in account. Therefore, the nature of the mRNAs being translated at various stages of DC activation was determined with the help of translational profiling, which is the sucrose gradient fractionation of polysomal-bound mRNAs combined to microarrays analysis. Total and polysomal-bound mRNA populations were compared in immature (0h) and LPS-stimulated (4h and 16h) human monocyte-derived DCs with the help of Affymetrix microarrays. Biostatistical analysis indicated that 296 mRNA molecules are translationally regulated during DC-activation. The most abundant biological process among the regulated mRNAs was protein biosynthesis, indicating the existence of a negative feedback loop regulating translation. Interestingly, a cluster of 17 ribosomal proteins were part of the regulated mRNAs, indicating that translation may be fine-tuned by particular components of the translational machinery. Our observations highlight the importance of translation regulation during the immune response, and may favour the identification of novel gene clusters or protein networks relevant for immunity. Our study also provides information on the possible absence of correlation between gene expression and real protein production in DCs. To identify translationally regulated mRNA molecules, gene expression derived from the polysome-bound mRNAs was compared by Affymetrix microarrays analysis to the gene expression derived from unfractionated total mRNAs derived from whole-cell lysates, as recently described on several reports (Johannes 1999, Rajasekhar 2003, Bushell 2006, Lü 2006, Parent 2008). Polysomal RNA (P) and total RNA (T) were isolated from MoDCs generated from four different blood donors. Since three timepoints (0h, 4h and 16h) were chosen for each blood donor and RNA type, twenty-four RNA samples were totally analyzed by microarrays.

Project description:Due to the selection pressure imposed by highly variable environmental conditions, stress sensing and regulatory response mechanisms in plants are expected to evolve rapidly. One potential source of innovation in plant stress response mechanisms is gene duplication. In this study, we examined the evolution of stress-regulated gene expression among duplicated genes in the model plant Arabidopsis thaliana. Key to this analysis was reconstructing the putative ancestral stress regulation pattern. By comparing the expression patterns of duplicated genes with the patterns of their ancestors, duplicated genes likely lost and gained stress responses at a rapid rate initially, but the rate is close to zero when the synonymous substitution rate (a proxy for time) is > approximately 0.8. When considering duplicated gene pairs, we found that partitioning of putative ancestral stress responses occurred more frequently compared to cases of parallel retention and loss. Furthermore, the pattern of stress response partitioning was extremely asymmetric. An analysis of putative cis-acting DNA regulatory elements in the promoters of the duplicated stress-regulated genes indicated that the asymmetric partitioning of ancestral stress responses are likely due, at least in part, to differential loss of DNA regulatory elements; the duplicated genes losing most of their stress responses were those that had lost more of the putative cis-acting elements. Finally, duplicate genes that lost most or all of the ancestral responses are more likely to have gained responses to other stresses. Therefore, the retention of duplicates that inherit few or no functions seems to be coupled to neofunctionalization. Taken together, our findings provide new insight into the patterns of evolutionary changes in gene stress responses after duplication and lay the foundation for testing the adaptive significance of stress regulatory changes under highly variable biotic and abiotic environments.

Project description:Gene duplication is a key evolutionary phenomenon, prevalent in all organisms but particularly so in plants, where whole genome duplication (WGD; polyploidy) is a major force in genome evolution. Much effort has been expended in attempting to understand the evolution of duplicate genes, addressing such questions as why some paralog pairs rapidly return to single copy status whereas, in other pairs, both paralogs are retained and may diverge in expression pattern or function. The effect of a gene - its site of expression and thus the initial locus of its function - occurs at the level of a cell comprising a single cell type at a given state of the cell's development. Using Arabidopsis thaliana single cell transcriptomic data we categorized patterns of expression for 11,470 duplicate gene pairs across 36 cell clusters comprising nine cell types and their developmental states. Among these 11,470 pairs, 10,187 (88.8%) had at least one copy expressed in at least one of the 36 cell clusters. Pairs produced by WGD more often had both paralogs expressed in root cells than did pairs produced by small scale duplications. Three quarters of gene pairs expressed in the 36 cell clusters (7,608/10,187) showed extreme expression bias in at least one cluster, including 352 cases of reciprocal bias, a pattern consistent with expression subfunctionalization. More than twice as many pairs showed reciprocal expression bias between cell states than between cell types or between roots and leaves. A group of 33 gene pairs with reciprocal expression bias showed evidence of concerted divergence of gene networks in stele vs. epidermis. Pairs with both paralogs expressed without bias were less likely to have paralogs with divergent mutant phenotypes; such bias-free pairs showed evidence of preservation by maintenance of dosage balance. Overall, we found considerable evidence of shifts in gene expression following duplication, including in >80% of pairs encoding 7,653 genes expressed ubiquitously in all root cell types and states for which we inferred the polarity of change.

Dataset Information

Fine-Tuning the Expression of Duplicate Genes by Translational Regulation in Arabidopsis and Maize.

Publications

Fine-Tuning the Expression of Duplicate Genes by Translational Regulation in <i>Arabidopsis</i> and Maize.

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