Can prolonged exposure to low VPD disturb the ABA signalling in stomatal guard cells?

Abstract

The response of stomata to many environmental factors is well documented. Multiple signalling pathways for abscisic acid (ABA)-induced stomatal closure have been proposed over the last decades. However, it seems that exposure of a leaf for a long time (several days) to some environmental conditions generates a sort of memory in the guard cells that results in the loss of suitable responses of the stomata to closing stimuli, such as desiccation and ABA. In this review paper we discuss changes in the normal pattern of signal transduction that could account for disruption of guard cell signalling after long-term exposure to some environmental conditions, with special emphasis on long-term low vapour pressure deficit (VPD).

Keywords: Abscisic acid; calcium; environmental factors; guard cell signalling pathway; hydrogen peroxide; nitric oxide; secondary messengers; stomata; vapour pressure deficit..

Fig. 1.

Schematic overview of the perception of ABA in stomatal guard cells. In conditions which favour ABA production (right), such as high VPD ❶, the produced ABA accumulates in the apoplast. Through the function of importers (AtABCG22&40), its level increases in the guard cell symplast. By binding of ABA to its receptor PYR/PYL/RCAR, it is able to block ABI1&2/PP2C activity; as a result, SnRK2/OST1 protein kinase will be activated. Also production of PA through PLDα1 will be increased, inhibiting ABI1/PP2C activity even more. Consequently, SnRK2/OST1 will stimulate SLAC1 as well as inhibit KAT1; as a result, stomatal closure will take place. On the other hand in the conditions which do not favour ABA production (left), such as low VPD ❷, the rest of the ABA will be catabolized by CYP707A1 inside the guard cells and by CYP707A3 outside the guard cells; in this situation, PYR/PYL/RCAR is unable to block ABI1&2/PP2C activity. As a result, ABI1/PP2C will inactivate SnRK2/OST1 protein kinase; therefore, the ion channels such as KAT1 continue to import K⁺ which causes stomata to remain open. Red bars show blockage effects in the presence of ABA. Blue bars show blockage effects in the absence of ABA. Arrows indicate positive effects.

Fig. 2.

Schematic of the cross-talk of secondary messengers in stomatal guard cells. Under the conditions which lead to a high transpiration rate (right), such as high VPD, Ca²⁺ and ABA will accumulate in the guard cell apoplast. In the case of ABA ❶, after increasing its concentration in the guard cell symplast, it leads to activation of NADPH oxidases, AtrbohD and AtrbohF, through PA-activated GPA1. As a result, the level of H₂O₂ increases which leads to: (i) NO production; (ii) MAPK activation; and (iii) I_Ca channel activation via GCA2. Consequently, stomatal closure takes place through the regulation of ion channels. When Ca²⁺ accumulate in the guard cell apoplast ❶, its concentration will increase in the guard cell symplast via the I_Ca channel; also CAS activation will result in [Ca²⁺]_cyt transients and H₂O₂ accumulation which cause activation of MAPK as well as CDPK. In addition, extracellular calmodulin (CaM) can activate the signalling pathways leading to H₂O₂ and NO generation. As a result, export of anions via SLAC1 will be accelerated and import of K⁺ via KAT1 will be inhibited; therefore, the membrane potential depolarizes and stomatal closure occurs. On the other hand, under conditions which lead to a lower transpiration rate (left), such as low VPD ❷, the concentration of ABA and Ca²⁺ will be low in the apoplast and symplast of the guard cells, which leads to activation of PP2C/ABI2 via the inhibitory effect of PP2Cs/ABI1 on SnRK2/OST1. ABI2 can prevent H₂O₂ signal transduction; consequently, the downstream components will not be activated and stomata remain open. Red bars show blockage effect under high apoplastic and symplastic ABA and Ca²⁺ concentrations. Blue bars show blockage effect under low apoplastic and symplastic ABA and Ca²⁺ concentrations. Arrows indicate positive effects.