Convergent and/or parallel evolution of RNA-binding proteins in angiosperms after polyploidization
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Date
Authors
Guo, Liangyu
Wang, Shuo
Jiao, Xi
Ye, Xiaoxue
Deng, Deyin
Liu, Hua
Li, Yan
Van de Peer, Yves
Wu, Wenwu
Journal Title
Journal ISSN
Volume Title
Publisher
Wiley
Abstract
Increasing studies suggest that the biased retention of stress-related transcription factors (TFs) after whole-genome duplications (WGDs) could rewire gene transcriptional networks, facilitating plant adaptation to challenging environments. However, the role of posttranscriptional factors (e.g. RNA-binding proteins, RBPs) following WGDs has been largely ignored.
Uncovering thousands of RBPs in 21 representative angiosperm species, we integrate genomic, transcriptomic, regulatomic, and paleotemperature datasets to unravel their evolutionary trajectories and roles in adapting to challenging environments.
We reveal functional enrichments of RBP genes in stress responses and identify their convergent retention across diverse angiosperms from independent WGDs, coinciding with global cooling periods. Numerous RBP duplicates derived from WGDs are then identified as cold-induced. A significant overlap of 29 orthogroups between WGD-derived and cold-induced RBP genes across diverse angiosperms highlights a correlation between WGD and cold stress. Notably, we unveil an orthogroup (Glycine-rich RNA-binding Proteins 7/8, GRP7/8) and relevant TF duplicates (CCA1/LHY, RVE4/8, CBF2/4, etc.), co-retained in different angiosperms post-WGDs. Finally, we illustrate their roles in rewiring circadian and cold-regulatory networks at both transcriptional and posttranscriptional levels during global cooling.
Altogether, we underline the adaptive evolution of RBPs in angiosperms after WGDs during global cooling, improving our understanding of plants surviving periods of environmental turmoil.
Description
DATA AVAILABILITY : The RNA-seq datasets of eight plants (Arabidopsis thaliana, Carya illinoinensis, Glycine max, Populus trichocarpa, Oryza sativa, Phyllostachys edulis, Setaria italica, and Zea mays) under cold stress have been deposited in the NCBI BioProject (Accession: PRJNA767196). The programming code for identifying Pfam domains, classifying duplication modes, calculating Ks, assessing retention differences of RBP genes and other gene families, and drawing relative expression heatmaps was included in Dataset S1.
SUPPLEMENTARY MATERIAL 1 : DATASET S1 Programming code used in this study. FIG. S1 Identification of RBPs in 21 selected angiosperms. FIG. S2 Synonymous substitution (Ks) ranges associated with the well-documented WGD events in the 21 selected angiosperm species. FIG. S3 Overview strategy of cold-responsive RNA-seq experiments and expression profiles of leaf development-related genes before and after cold stress. FIG. S4 Two examples for redefining orthogroups. FIG. S5 Cold-induced TF duplicates were biased retained after R-WGD. FIG. S6 Diverse cold-responsive transcriptome datasets consistently demonstrate the cold-upregulation of R-WGD-derived RBP genes. FIG. S7 Alternative splicing seems to be enriched in genes with longer introns. FIG. S8 Functional enrichments of cold-induced differentially alternatively spliced genes. FIG. S9 GRP7-GRP8 duplicates resulted from β-WGD event (R1-WGD). FIG. S10 GRP7 expression was significantly correlated with the average expression of 433 cold-induced GRP7 targets. FIG. S11 Significant association of 433 cold-induced GRP7 targets with differentially expressed genes in GRP7-overexpressing and loss-of-function plants. FIG. S12 Overlapping and unique genes between 433 cold-induced GRP7 targets and differentially alternatively spliced genes. FIG. S13 Expression profile of the top 30 transcription factors that bind to promoters of cold-induced GRP7 targets. FIG. S14 Negative correlation between RBP gene number and the WGD age. FIG. S15 Cold-induced tandem duplicates mainly generated around global cooling periods.
SUPPLEMENTARY MATERIAL 2 : TABLE S1 Source information of 21 selected angiosperm species. TABLE S2 High-confidence list of RBPs in Arabidopsis. TABLE S3 Gene accessions, protein domains, and duplication modes of RBPs in 21 selected angiosperms. TABLE S4 Statistical summary of duplication modes of RBP genes and non-RBP genes in angiosperm genomes. TABLE S5 Total of 4594 gene families, including 494 gene-rich families, were identified in angiosperm genomes. TABLE S6 Well-documented WGD events and their predicted Ks ranges for collinear pair genes in 21 selected angiosperms. TABLE S7 RBP duplicates retained from different periods of WGDs in 21 selected species. TABLE S8 Expression values of RBP genes in eight cold-treated species. TABLE S9 Cold-induced differentially alternative splicing genes in eight cold-treated species. TABLE S10 Total of 282 RBP orthogroups identified in eight cold-treated species. TABLE S11 Total of 857 GRP7 targets, including 433 cold-induced genes. TABLE S12 One hundred eight cold-induced TFs from a library of 540 TFs with ChIP/DAP-seq data. TABLE S13 Summary of the 433 cold-induced genes bound by the 108 cold-induced TFs. TABLE S14 Retention status of RBP genes and 494 gene-rich families in angiosperms after WGDs. TABLE S15 RNA-seq expression values of leaf development-related genes in eight cold-treated species. TABLE S16 Statistical summary of cold-induced RBPs retained from WGD, TSP, TD, DD, and Singleton. TABLE S17 Details of cold-induced duplicates from WGDs in eight cold-treated species. TABLE S18 Eighteen additional datasets of cold-responsive transcriptomes. TABLE S19 Twenty-nine overlapping RBP orthogroups retained and cold-induced in angiosperms. TABLE S20 Timing of WGD events in producing GRP7/8-containing collinear gene pairs.
SUPPLEMENTARY MATERIAL 1 : DATASET S1 Programming code used in this study. FIG. S1 Identification of RBPs in 21 selected angiosperms. FIG. S2 Synonymous substitution (Ks) ranges associated with the well-documented WGD events in the 21 selected angiosperm species. FIG. S3 Overview strategy of cold-responsive RNA-seq experiments and expression profiles of leaf development-related genes before and after cold stress. FIG. S4 Two examples for redefining orthogroups. FIG. S5 Cold-induced TF duplicates were biased retained after R-WGD. FIG. S6 Diverse cold-responsive transcriptome datasets consistently demonstrate the cold-upregulation of R-WGD-derived RBP genes. FIG. S7 Alternative splicing seems to be enriched in genes with longer introns. FIG. S8 Functional enrichments of cold-induced differentially alternatively spliced genes. FIG. S9 GRP7-GRP8 duplicates resulted from β-WGD event (R1-WGD). FIG. S10 GRP7 expression was significantly correlated with the average expression of 433 cold-induced GRP7 targets. FIG. S11 Significant association of 433 cold-induced GRP7 targets with differentially expressed genes in GRP7-overexpressing and loss-of-function plants. FIG. S12 Overlapping and unique genes between 433 cold-induced GRP7 targets and differentially alternatively spliced genes. FIG. S13 Expression profile of the top 30 transcription factors that bind to promoters of cold-induced GRP7 targets. FIG. S14 Negative correlation between RBP gene number and the WGD age. FIG. S15 Cold-induced tandem duplicates mainly generated around global cooling periods.
SUPPLEMENTARY MATERIAL 2 : TABLE S1 Source information of 21 selected angiosperm species. TABLE S2 High-confidence list of RBPs in Arabidopsis. TABLE S3 Gene accessions, protein domains, and duplication modes of RBPs in 21 selected angiosperms. TABLE S4 Statistical summary of duplication modes of RBP genes and non-RBP genes in angiosperm genomes. TABLE S5 Total of 4594 gene families, including 494 gene-rich families, were identified in angiosperm genomes. TABLE S6 Well-documented WGD events and their predicted Ks ranges for collinear pair genes in 21 selected angiosperms. TABLE S7 RBP duplicates retained from different periods of WGDs in 21 selected species. TABLE S8 Expression values of RBP genes in eight cold-treated species. TABLE S9 Cold-induced differentially alternative splicing genes in eight cold-treated species. TABLE S10 Total of 282 RBP orthogroups identified in eight cold-treated species. TABLE S11 Total of 857 GRP7 targets, including 433 cold-induced genes. TABLE S12 One hundred eight cold-induced TFs from a library of 540 TFs with ChIP/DAP-seq data. TABLE S13 Summary of the 433 cold-induced genes bound by the 108 cold-induced TFs. TABLE S14 Retention status of RBP genes and 494 gene-rich families in angiosperms after WGDs. TABLE S15 RNA-seq expression values of leaf development-related genes in eight cold-treated species. TABLE S16 Statistical summary of cold-induced RBPs retained from WGD, TSP, TD, DD, and Singleton. TABLE S17 Details of cold-induced duplicates from WGDs in eight cold-treated species. TABLE S18 Eighteen additional datasets of cold-responsive transcriptomes. TABLE S19 Twenty-nine overlapping RBP orthogroups retained and cold-induced in angiosperms. TABLE S20 Timing of WGD events in producing GRP7/8-containing collinear gene pairs.
Keywords
Alternative splicing, C-repeat binding factors, Cold stress, Convergent evolution, Global cooling, K-Pg boundary, RNA-binding proteins, Whole-genome duplication (WGD)
Sustainable Development Goals
None
Citation
Guo, L.Y., Wang, S., Jiao, X. et al. 2024, 'Convergent and/or parallel evolution of RNA-binding proteins in angiosperms after polyploidization', New Phytologist, vol. 242, no. 3, pp. 1377-1393, doi : 10.1111/nph.19656.