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

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.

Oryza CLIMtools: A Genome-Environment Association Resource Reveals Adaptive Roles for Heterotrimeric G Proteins in the Regulation of Rice Agronomic Traits

“…Of particular note, we also provide riboSNitch predictions, which indicate the likelihood that a variant alters RNA structure, which is a mechanism for differential post-transcriptional regulation (Halvorsen et al, 2010). As shown by our analyses in Arabidopsis (Ferrero-Serrano et al, 2022), riboSNitches are a fruitful topic for investigation.…”

Diverse patterns of secondary structure across genes and transposable elements are associated with siRNA production and epigenetic fate

“…Overall, our results show that stable secondary structures -as inferred from low MFEscorrelates positively with siRNA abundance and may be shaped by a trade-off between functional requirements and the potential disruptive effects of self-priming. We hope this work sparks further exploration of the roles of secondary structure in plant genome evolution, including the population genetics of mutations in regions of secondary structure (Ferrero-Serrano et al, 2022), their roles in the stress response (Zhu et al, 2018), and comparative analyses of secondary structure characteristics between species.…”

RNA biology takes root in plant systems

“…Assmann also presented work highlighting the relationship between structure-altering single-nucleotide polymorphisms (SNPs) (riboSNitches) and climatic factors in Arabidopsis. The ZINC RIBBON 3 (ZR3) transcript is an example of a riboSNitch possessing a G to A SNP that alters its secondary structure (Ferrero-Serrano et al, 2022).…”

“…Assmann also presented work highlighting the relationship between structure‐altering single‐nucleotide polymorphisms (SNPs) (riboSNitches) and climatic factors in Arabidopsis. The ZINC RIBBON 3 ( ZR3 ) transcript is an example of a riboSNitch possessing a G to A SNP that alters its secondary structure (Ferrero‐Serrano et al, 2022). It was found that there was a correlation between the frequency of this SNP for ZR3 and the plants' geographical location away from the coast; plants further inland that experienced a wider range of fluctuating temperatures contained a higher percentage of the G to A variant than those growing near the coast.…”