ABA-responsive small RNAs contribute to drought stress memory by regulating antioxidant activity and lignification

Abstract

Previously we showed that a single exogenous application of Abscisic acid (ABA) on Arabidopsis in early developmental stages results in enhanced plant biomass and drought tolerance in the adult plants. Here we tested the hypothesis that small RNAs (sRNAs), including micro RNAs (miRNAs) and small interfering RNAs (siRNAs), contribute to the observed ABA effects. We sequenced sRNA populations in Arabidopsis plants that were sprayed with ABA or water at the cotyledonary stage at two time-points, 4 hours and 14 days after spraying. Analyses of the sRNAs revealed that at 4 hours, four miRNA families, miR408, miR398, miR397, and miR393, were significantly down-regulated by the ABA application. These miRNAs are all copper-induced miRNAs, which are known to be involved in the regulation of antioxidant enzymes and lignification metabolic pathways. After 14 days, miR395 and miR169 families were up-regulated, while miR399 and miR827 families were down-regulated in ABA-treated plants. These miRNAs are mostly characterized as regulators of macronutrient uptake. We identified 77 and 30 differentially expressed siRNA loci in the first and second time-points respectively. Interestingly, a majority of these ABA-responsive siRNAs were found to be mainly associated with the non-coding regions of the genome, as well as with genes related to photosynthesis, particularly those encoding light-harvesting complex proteins. In summary, our data suggest that ABA-responsive miRNAs contribute to the positive effects of ABA by increasing plant antioxidant capacity and lignification in the short-term while increasing nutrient uptake in the long term.