N-glycosylation of SnRK2s controls NADPH maintenance in peroxisomes during prolonged ABA signalling

Abstract Unfavourable conditions threaten the survival and agricultural yield of plants and are often maintained in the long term, such as drought season and high salinity field. The phytohormone ABA plays key roles in the regulation of plant stress adaptation and is often sustained at high level for long periods of time1-3. Much is known about ABA signal perception and activation/sensitization in the early signalling stage4-6. However, the molecular mechanism underlying desensitization of ABA signalling largely unknown. Here, we revealed that, in the endoplasmic reticulum (ER)-Golgi network, SnRK2.2/2.3, the key regulators of ABA signalling, are unexpectedly N-glycosylated, which promotes their gradual redistribution from the nucleus to the peroxisomes in Arabidopsis roots, leading to a desensitization of the transcriptional response in the nucleus during prolonged ABA signalling. On the peroxisomal membrane, SnRK2s directly interact with glucose-6-phosphate (G6P)/phosphate translocator 1 (GPT1) to maintain NADPH homeostasis through increased activity of the peroxisomal oxidative pentose phosphate pathway (OPPP). The resulting maintenance in NADPH is required for modulation of hydrogen peroxide (H2O2) accumulation, relieving ABA-induced root growth inhibition. The subcellular dynamics of SnRK2s achieved by N-glycosylation seems to reflect a switch to control ABA responses from transcriptional regulation in the nucleus to metabolic control in the peroxisomes to help plants adapt to long-term environmental stress.