A novel TF molecular switch-mechanism found in two contrasting ecotypes of a psammophyte, Agriophyllum squarrosum, in regulating transcriptional drought memory

Abstract

Background Prior drought stress may change plants response patterns and subsequently increase their tolerance to the same condition, which can be referred to as “drought memory” and proved essential for plants well-being. However, the mechanism of transcriptional drought memory in psammophytes remains unclear. Agriophyllum squarrosum, a pioneer species on mobile dunes, is widely spread in Northern China’s vast desert areas with outstanding ability of water use efficiency. Here we conducted dehydration-rehydration treatment on A. squarrosum semi-arid land ecotype AEX and arid land ecotype WW to dissect the drought memory mechanism of A. squarrosum, and to determine the discrepancy in drought memory of two contrasting ecotypes that had long adapted to water heterogeneity. Result Physiological traits monitoring unveiled the stronger ability and longer duration in drought memory of WW than that of AEX. A total of 1,642 and 1,339 drought memory genes (DMGs) were identified in ecotype AEX and WW, respectively. Furthermore, shared DMGs among A. squarrosum and the previously studied species depicted that drought memory commonalities in higher plants embraced pathways like primary and secondary metabolisms; while drought memory characteristics in A. squarrosum were mainly related to response to heat, high light intensity, hydrogen peroxide, and dehydration, which might be due to local adaptation to desert circumstances. Heat shock proteins (HSPs) occupied the center of the protein-protein interaction (PPI) network in drought memory transcription factors (TF), thus playing a key regulatory role in A. squarrosum drought memory. Co-expression analysis of drought memory TFs and DMGs uncovered a novel regulating module, whereby pairs of TFs might function as molecular switches in regulating DMG transforming between high and low expression levels, thus promoting drought memory reset. Conclusion Based on the co-expression analysis, protein-protein interaction prediction, and drought memory metabolic network construction, a novel regulatory module of transcriptional drought memory in A. squarrosum was hypothesized here, whereby recurrent drought signal is activated by primary TF switches, then amplified by secondary amplifiers, and thus regulates downstream complicated metabolic networks. The present research provided valuable molecular resources on plants’ stress-resistance basis and shed light on drought memory in A. squarrosum.

Intergenerational and transgenerational effects of drought stress on winter wheat (Triticum aestivum L.)

“…Current research has demonstrated that many environmental conditions may cause epigenetic modifications, including DNA methylation, histone modification, and changes in small non-coding RNAs, which, when passed on, can affect gene activity in the offspring and impact its phenotypes (Ding et al, 2022;Fang et al, 2023;Manh et al, 2023;Tian et al, 2022;Wang et al, 2021). Epigenetic modifications are either mitotically and/or meiotically heritable alterations in gene expression that are independent of primary DNA sequence changes and potentially affect the outcome of a chromosome or locus without changing the underlying DNA (Bird, 2007).…”