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Plants, as sessile organisms, gained the ability to sense and respond to biotic and abiotic stressors to survive severe changes in their environments. The change in our climate comes with extreme dry periods but also episodes of flooding. The latter stress condition causes anaerobiosis-triggered cytosolic acidosis and impairs plant function. The molecular mechanism that enables plant cells to sense acidity and convey this signal via membrane depolarization was previously unknown. Here, we show that acidosis-induced anion efflux from Arabidopsis (Arabidopsis thaliana) roots is dependent on the S-type anion channel AtSLAH3. Heterologous expression of SLAH3 in Xenopus oocytes revealed that the anion channel is directly activated by a small, physiological drop in cytosolic pH. Acidosis-triggered activation of SLAH3 is mediated by protonation of histidine 330 and 454. Super-resolution microscopy analysis showed that the increase in cellular proton concentration switches SLAH3 from an electrically silent channel dimer into its active monomeric form. Our results show that, upon acidification, protons directly switch SLAH3 to its open configuration, bypassing kinase-dependent activation. Moreover, under flooding conditions, the stress response of Arabidopsis wild-type (WT) plants was significantly higher compared to SLAH3 loss-of-function mutants. Our genetic evidence of SLAH3 pH sensor function may guide the development of crop varieties with improved stress tolerance.

Plants synthesize a plethora of defense compounds crucial for their survival in a challenging and changing environment. Transport processes are important for shaping the distribution pattern of defense compounds, albeit focus hitherto has been mostly on their biosynthetic pathways. A recent identification of two glucosinolate transporters represents a breakthrough in our understanding of glucosinolate transport in Arabidopsis and has advanced knowledge in transport of defense compounds. In this review, we discuss the role of the glucosinolate transporters in establishing dynamic glucosinolate distribution patterns and source-sink relations. We focus on lessons learned from glucosinolate transport that may apply to transport of other defense compounds and discuss future avenues in the emerging field of defense compound transport.