Experimental demonstration and pan-structurome prediction of climate-associated riboSNitches in arabidopsis

Authors: FERRORO-SERRANO, ANGEL - Pennsylvania State University; SYLVIA, MEGAN - Pennsylvania State University; FORSTMEIER, PETER - Pennsylvania State University; OLSON, ANDREW - Cold Spring Harbor Laboratory; Ware, Doreen; BEVILACQUA, PHILIP - Pennsylvania State University; ASSMANN, SARAH - Pennsylvania State University

Submitted to: Genome Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/20/2022
Publication Date: 4/19/2022
Citation: Ferroro-Serrano, A., Sylvia, M.M., Forstmeier, P.C., Olson, A.J., Ware, D., Bevilacqua, P.C., Assmann, S.M. 2022. Experimental demonstration and pan-structurome prediction of climate-associated riboSNitches in arabidopsis. Genome Biology. 23:101. https://doi.org/10.1186/s13059-022-02656-4.
DOI: https://doi.org/10.1186/s13059-022-02656-4

Interpretive Summary: Genetic variation happens at random, but some variants contribute to the fitness of an organism and are more likely to be passed on to offspring and spread throughout a population. In plants, this is one mechanism of adaptation to the environment. A single nucleotide change in the genome may have no discernible effect, or it could modify a protein-DNA binding site involved in regulating gene expression, change the splicing of a messenger RNA (mRNA) during transcription, or alter a protein translation. This study focuses on variants that change the way an mRNA is folded and whether they are climate associated adaptations. Two such riboSNitches were experimentally validated following data analyses to identify genetic variations among 879 varieties of Arabidopsis thaliana associated with 434 climate descriptors. The results were made accessible to scientists through the CLIMtools websites hosted at gramene.org.

Technical Abstract: Background Genome-wide association studies (GWAS) aim to correlate phenotypic changes with genotypic variation. Upon transcription, single nucleotide variants (SNVs) may alter mRNA structure, with potential impacts on transcript stability, macromolecular interactions, and translation. However, plant genomes have not been assessed for the presence of these structure-altering polymorphisms or “riboSNitches.” Results We experimentally demonstrate the presence of riboSNitches in transcripts of two Arabidopsis genes, ZINC RIBBON 3 (ZR3) and COTTON GOLGI-RELATED 3 (CGR3), which are associated with continentality and temperature variation in the natural environment. These riboSNitches are also associated with differences in the abundance of their respective transcripts, implying a role in regulating the gene's expression in adaptation to local climate conditions. We then computationally predict riboSNitches transcriptome-wide in mRNAs of 879 naturally inbred Arabidopsis accessions. We characterize correlations between SNPs/riboSNitches in these accessions and 434 climate descriptors of their local environments, suggesting a role of these variants in local adaptation. We integrate this information in CLIMtools V2.0 and provide a new web resource, T-CLIM, that reveals associations between transcript abundance variation and local environmental variation. Conclusion We functionally validate two plant riboSNitches and, for the first time, demonstrate riboSNitch conditionality dependent on temperature, coining the term “conditional riboSNitch.” We provide the first pan-genome-wide prediction of riboSNitches in plants. We expand our previous CLIMtools web resource with riboSNitch information and with 1868 additional Arabidopsis genomes and 269 additional climate conditions, which will greatly facilitate in silico studies of natural genetic variation, its phenotypic consequences, and its role in local adaptation.