Previously, it has been shown that Arabidopsis thaliana leaves exposed to high light accumulate hydrogen peroxide (H2O2) in bundle sheath cell (BSC) chloroplasts as part of a retrograde signaling network that induces ASCORBATE PEROXIDASE2 (APX2). Abscisic acid (ABA) signaling has been postulated to be involved in this network. To investigate the proposed role of ABA, a combination of physiological, pharmacological, bioinformatic, and molecular genetic approaches was used. ABA biosynthesis is initiated in vascular parenchyma and activates a signaling network in neighboring BSCs. This signaling network includes the Gα subunit of the heterotrimeric G protein complex, the OPEN STOMATA1 protein kinase, and extracellular H2O2, which together coordinate with a redox-retrograde signal from BSC chloroplasts to activate APX2 expression. High light–responsive genes expressed in other leaf tissues are subject to a coordination of chloroplast retrograde signaling and transcellular signaling activated by ABA synthesized in vascular cells. ABA is necessary for the successful adjustment of the leaf to repeated episodes of high light. This process involves maintenance of photochemical quenching, which is required for dissipation of excess excitation energy.

The rapid induction of the bundle sheath cell (BSC)-specific expression of ASCORBATE PEROXIDASE2 ( APX2 ) in high light (HL)-exposed leaves of Arabidopsis thaliana is, in part, regulated by the hormone abscisic acid (ABA) produced by vascular parenchyma cells. In this study, we provide more details of the ABA signalling that regulates APX2 expression and consider its importance in the photosynthetic responses of BSCs and whole leaves. This was done using a combination of analyses of gene expression and chlorophyll a fluorescence of both leaves and individual BSCs and mesophyll cells. The regulation of APX2 expression occurs by the combination of the protein kinase SnRK2.6 (OST1):protein phosphatase 2C ABI2 and a Gα (GPA1)-regulated signalling pathway. The use of an ost1-1/gpa1-4 mutant established that these signalling pathways are distinct but interact to regulate APX2 . In HL-exposed leaves, BSC chloroplasts were more susceptible to photoinhibition than those of mesophyll cells. The activity of the ABA-signalling network determined the degree of susceptibility of BSCs to photoinhibition by influencing non-photochemical quenching. By contrast, in HL-exposed whole leaves, ABA signalling did not have any major influence on their transcriptomes nor on their susceptibility to photoinhibition, except where guard cell responses were observed.