The High Light Response inArabidopsisInvolves ABA Signaling between Vascular and Bundle Sheath Cells

Abstract

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.

Oxidative Stress: Antagonistic Signaling for Acclimation or Cell Death?

“…The ABA secreted from vascular parenchyma interacts with BSCs and induces the antioxidant gene ASCORBATE PEROXIDASE2 (APX2), which is expressed only in this tissue. An extant ABA biosynthetic capacity is required for successful physiological adjustment to repeated episodes of increased light (Galvez-Valdivieso et al, 2009). The ABA-mediated control of APX2 expression occurs via two antagonistic pathways.…”

“…The ABA-mediated control of APX2 expression occurs via two antagonistic pathways. Positive control is achieved by signaling involving OPEN STOMATA1 (OST1) protein kinase and the ABA-INSENSITIVE1 (ABI1) and ABI2 protein phosphatase 2Cs (Fryer et al, 2003;Galvez-Valdivieso et al, 2009;Galvez-Valdivieso and Mullineaux, 2010). Negative regulation of APX2 expression occurs via the Ga subunit, GPA1, of the heterotrimeric G protein complex (Galvez-Valdivieso et al, 2009;Galvez-Valdivieso and Mullineaux, 2010).…”

“…In bundle sheath cells (BSCs) of leaves exposed to a moderate increase in light intensity and low humidity, ABA signaling is suggested to interact with a chloroplast-sourced H 2 O 2 signal to drive the induction of high-light, ABA-responsive genes (Galvez-Valdivieso et al, 2009). Within 30 min of exposure to high light at ambient or lower humidity, ABA biosynthesis is activated in vascular parenchyma cells triggered by a transient lowering of leaf water potential, which is caused by a rapid increase in transpiration.…”

Molecular components of stress-responsive plastid retrograde signaling networks and their involvement in ammonium stress

“…These results also suggest ABA signaling is not the sole downstream component in AMOS1/EGY1-dependent plastid retrograde signaling during ammonium stress. Similarly, ABA signaling has also been found to be involved in the H 2 O 2 -dependent plastid signal that activates high-light responsive gene expression in leaves 43 and to be recruited by an 1 O 2 -dependent plastid signal during late embryogenesis where it affects plastid differentiation by reactivating relevant nuclear-encoded genes. 44 Therefore, interactions between plastid retrograde signaling and ABA signaling may be a common occurrence during stress responses.…”

“…31 A similar role of ABA signaling in a plastid ROS retrograde regulatory pathway has been documented under high-light stress. 43 Second, other candidates for the AMOS1/EGY1-dependent ammonium-induced plastid retrograde signal are plausible, if the H 2 O 2 defective response in guard cell chloroplasts is merely a secondary outcome of impaired chloroplast functionality in the amos1 mutant. Very recently, the plastid metabolite methylerythritol cyclodiphosphate (MEcPP), a precursor in isoprenoid synthesis in the methylerythritol phosphate (MEP) pathway, has been identified as a novel retrograde signal involved in the regulation of the expression of nuclear stress-responsive genes under high-light and wounding stresses.…”