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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.
Highlights
One of the most prominent genomic differences between plants and other eukaryotes is the prevalence of duplicate genes in plant genomes (Panchy et al, 2016)
Translational regulation could act in two ways for duplicate genes, either in the same direction as transcriptional regulation to amplify the mRNA abundance divergence, or in the opposite direction to buffer the expression divergence established at the transcriptional level
Defined as the amount of ribosome footprint (RF) normalized to underlying mRNA abundance (Ingolia et al, 2009), translational efficiency (TE) is widely used as an indicator of the propensity of mRNA to undergo translation
Summary
One of the most prominent genomic differences between plants and other eukaryotes is the prevalence of duplicate genes in plant genomes (Panchy et al, 2016). One duplicate copy might evolve novel expression patterns or functions (neofunctionalization) (Ohno, 1970; Hughes et al, 2014) Counterbalancing these ideas is the gene dosage hypothesis, where both paralogs are subjected to constraints on dosage balance and show high conservation in sequence and expression (Edger and Pires, 2009; Conant et al, 2014). These evolutionary scenarios are not mutually exclusive [e.g., constraints on gene dosage may provide long enough time for duplicates to diverge in function (Force et al, 1999; Conant et al, 2014; Vaattovaara et al, 2019)], but their relative contributions remain to be explored in depth
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