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

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.

Integrated metabolomics and transcriptomics insights on flavonoid biosynthesis of a medicinal functional forage, Agriophyllum squarrosum (L.), based on a common garden trial covering six ecotypes.

Agriophyllum squarrosum (L.) Moq., well known as sandrice, is an important wild forage in sandy areas and a promising edible and medicinal resource plant with great domestication potential. Previous studies showed flavonoids are one of the most abundant medicinal ingredients in sandrice, whereby isorhamnetin and isorhamnetin-3-glycoside were the top two flavonols with multiple health benefits. However, the molecular regulatory mechanisms of flavonoids in sandrice remain largely unclear. Based on a common garden trial, in this study, an integrated transcriptomic and flavonoids-targeted metabolomic analysis was performed on the vegetative and reproductive periods of six sandrice ecotypes, whose original habitats covered a variety of environmental factor gradients. Multiple linear stepwise regression analysis unveiled that flavonoid accumulation in sandrice was positively correlated with temperature and UVB and negatively affected by precipitation and sunshine duration, respectively. Weighted co-expression network analysis (WGCNA) indicated the bHLH and MYB transcription factor (TF) families might play key roles in sandrice flavonoid biosynthesis regulation. A total of 22,778 differentially expressed genes (DEGs) were identified between ecotype DL and ecotype AEX, the two extremes in most environmental factors, whereby 85 DEGs could be related to known flavonoid biosynthesis pathway. A sandrice flavonoid biosynthesis network embracing the detected 23 flavonoids in this research was constructed. Gene families Plant flavonoid O-methyltransferase (AsPFOMT) and UDP-glucuronosyltransferase (AsUGT78D2) were identified and characterized on the transcriptional level and believed to be synthases of isorhamnetin and isorhamnetin-3-glycoside in sandrice, respectively. A trade-off between biosynthesis of rutin and isorhamnetin was found in the DL ecotype, which might be due to the metabolic flux redirection when facing environmental changes. This research provides valuable information for understanding flavonoid biosynthesis in sandrice at the molecular level and laid the foundation for precise development and utilization of this functional resource forage.

Corrigendum: Integrated metabolomics and transcriptomics insights on flavonoid biosynthesis of a medicinal functional forage, Agriophyllum squarrosum (L.), based on a common garden trial covering six ecotypes.

[This corrects the article DOI: 10.3389/fpls.2022.985572.].