siRNA-guided DNA-methylation at a sucrose transporter gene potentially contributes to climatic plant adaptation

Climatic adaptation of plants involves the adjustment of carbon transport to achieve an optimal balance between carbon assimilation and carbon utilization. This study describes a potential molecular mechanism of this adjustment by investigating the climate-dependent regulation of SUCROSE TRANSPORTER 2 (SUC2) in the model plant Arabidopsis thaliana. SUC2 is responsible for loading photosynthetically-produced sucrose into the leaf vascular system. Its protein and mRNA abundance in A. thaliana natural accessions were found to correlate with leaf sucrose export and summer temperature. Exploration of methylome data and epigenome editing experiments suggested that epigenetic marks on SUC2's exon 2 contributed to the climate-dependent expression of SUC2. Two siRNAs were identified as mediators of SUC2 methylations and their respective origins localized to the SUC5 and SUC8 genes. The analysis of plants with reduced or enhanced SUC5 or SUC8 transcriptional activity corroborated the link to SUC2 methylation. Besides illustrating a novel regulatory strategy of carbon export from leaves, our results establish exon methylation mediated by gene-derived siRNAs as yet another potential mechanism for plant adaptation.