Acetate-mediated novel survival strategy against drought in plants

Abstract

Water deficit caused by global climate changes seriously endangers the survival of organisms and crop productivity, and increases environmental deterioration. Plants' resistance to drought involves global reprogramming of transcription, cellular metabolism, hormone signalling and chromatin modification. However, how these regulatory responses are coordinated via the various pathways, and the underlying mechanisms, are largely unknown. Herein, we report an essential drought-responsive network in which plants trigger a dynamic metabolic flux conversion from glycolysis into acetate synthesis to stimulate the jasmonate (JA) signalling pathway to confer drought tolerance. In Arabidopsis, the ON/OFF switching of this whole network is directly dependent on histone deacetylase HDA6. In addition, exogenous acetic acid promotes de novo JA synthesis and enrichment of histone H4 acetylation, which influences the priming of the JA signalling pathway for plant drought tolerance. This novel acetate function is evolutionarily conserved as a survival strategy against environmental changes in plants. Furthermore, the external application of acetic acid successfully enhanced the drought tolerance in Arabidopsis, rapeseed, maize, rice and wheat plants. Our findings highlight a radically new survival strategy that exploits an epigenetic switch of metabolic flux conversion and hormone signalling by which plants adapt to drought.

Plant Desiccation Tolerance and its Regulation in the Foliage of Resurrection “Flowering-Plant” Species

“…In Arabidopsis plants, drought stimulated the synthesis of acetic acid, while 10-20 mM acetic acid applied to the roots lowered the pH of xylem sap and ultimately promoted the drought resistance of the plants. A similar promotion of drought resistance was found in plants of maize, rice, rapeseed and wheat [96].…”

“…Strigolactones and the recently-reported messenger agents, acetate [96] and CLE25 peptide [97] have yet to be examined as possible root-to-shoot signals in the induction of desiccation tolerance: CLE25 synthesized in droughted Arabidopsis roots is transmitted in the vascular system to leaves where it acts with BARELY ANY MERISTEM (BAM) receptors to influence ABA-synthesis and thereby produces closure of stomata [97]. In Arabidopsis plants, drought stimulated the synthesis of acetic acid, while 10-20 mM acetic acid applied to the roots lowered the pH of xylem sap and ultimately promoted the drought resistance of the plants.…”

Comparative metabolomics analysis reveals different metabolic responses to drought in tolerant and susceptible poplar species

“…Additionally, a novel survival strategy against drought showed that exogenous acetate can promote JA signaling and histone H4 acetylation enrichment to enhance plant drought tolerance, and the acetate‐induced drought tolerance is evolutionarily conserved in both monocots and dicots (Kim et al , ). In P. simonii and P. deltoides cv.…”

“…Ascorbate plays a role in maize tolerance to drought, and the foliar application of ascorbate can alleviate the adverse effects of drought stress (Noman et al ). In A. thaliana , α‐tocopherol can move easily within lipid membranes because of its adequate fluidity, and it eliminates ROS free radicals to prevent lipid peroxidation (Kim et al , ). The carotenoids, β‐carotene and zeaxanthin, are not only essential for photosynthesis and photoprotection, but they are also precursors to phytohormones, such as ABA and strigolactone, which are potent antioxidants and free radical scavengers (Cazzonelli , Mibei et al ).…”

Excess light priming in Arabidopsis thaliana genotypes with altered DNA methylomes

“…It has also been reported that the activity of the HSFA2 transcription factor can result in H3K4me2 and H3K4me3 changes, in response to recurring heat stress, to convey transcriptional priming (Lämke et al 2016). Additionally, HDA6-mediated histone H4 de-acetylation has been linked to prime jasmonic acid signalling leading to enhanced drought tolerance (Kim et al 2017). These various examples highlight the importance of chromatin variation in facilitating of plant stress priming.…”