The trafficking protein SYP121 of Arabidopsis connects programmed stomatal closure and K plus channel activity with vegetative growth

The vesicle-trafficking protein SYP121 (SYR1/PEN1) was originally identified in association with ion channel control at the plasma membrane of stomatal guard cells, although stomata of the Arabidopsis syp121 loss-of-function mutant close normally in ABA and high Ca2+. We have now uncovered a set of stomatal phenotypes in the syp121 mutant that reduce CO2 assimilation, slow vegetative growth and increase water use efficiency in the whole plant, conditional upon high light intensities and low relative humidity. Stomatal opening and the rise in stomatal transpiration of the mutant was delayed in the light and following Ca2+-evoked closure, consistent with a constitutive form of so-called programmed stomatal closure. Delayed reopening was observed in the syp121, but not in the syp122 mutant lacking the homologous gene product; the delay was rescued by complementation with wild-type SYP121 and was phenocopied in wild-type plants in the presence of the vesicle-trafficking inhibitor Brefeldin A. K+ channel current that normally mediates K+ uptake for stomatal opening was suppressed in the syp121 mutant and, following closure, its recovery was slowed compared to guard cells of wild-type plants. Evoked stomatal closure was accompanied by internalisation of GFP-tagged KAT1 K+ channels in both wild-type and syp121 mutant guard cells, but their subsequently recycling was slowed in the mutant. Our findings indicate that SYP121 facilitates stomatal reopening and they suggest that K+ channel traffic and recycling to the plasma membrane underpins the stress memory phenomenon of programmed closure in stomata. Additionally, they underline the significance of vesicle traffic for whole-plant water use and biomass production, tying SYP121 function to guard cell membrane transport and stomatal control.