Sensing and signaling of oxidative stress in chloroplasts by inactivation of the SAL1 phosphoadenosine phosphatase

Abstract

Intracellular signaling during oxidative stress is complex, with organelle-to-nucleus retrograde communication pathways ill-defined or incomplete. Here we identify the 3′-phosphoadenosine 5′-phosphate (PAP) phosphatase SAL1 as a previously unidentified and conserved oxidative stress sensor in plant chloroplasts. Arabidopsis thaliana SAL1 (AtSAL1) senses changes in photosynthetic redox poise, hydrogen peroxide, and superoxide concentrations in chloroplasts via redox regulatory mechanisms. AtSAL1 phosphatase activity is suppressed by dimerization, intramolecular disulfide formation, and glutathionylation, allowing accumulation of its substrate, PAP, a chloroplast stress retrograde signal that regulates expression of plastid redox associated nuclear genes (PRANGs). This redox regulation of SAL1 for activation of chloroplast signaling is conserved in the plant kingdom, and the plant protein has evolved enhanced redox sensitivity compared with its yeast ortholog. Our results indicate that in addition to sulfur metabolism, SAL1 orthologs have evolved secondary functions in oxidative stress sensing in the plant kingdom. There is also a shift from reducing to more oxidizing states in the redox poise of plastoquinone (PQ) and other stromal redox couples such as glutathione (GSH/GSSG). All of these changes are associated with adjustment of photosystem stoichiometry and chloroplastic metabolic enzymes by chloroplast-resident kinases (2) and redox-sensitive thioredoxins (TRXs) (3), respectively, as well as activation of signaling pathways for the induction of common and unique sets of nuclear genes (4, 5).The nuclear transcriptional response to stress in chloroplasts is mediated by chemical signals emanating from the chloroplasts to the nucleus in a process called retrograde signaling (6). There are at least seven distinct retrograde signaling pathways responding to changes in chloroplastic ROS and redox state (7), including betacyclocitral for PSII-1 O 2 responses (8) and the PAP-XRN pathway which alters expression of 25% of the HL-associated transcriptome, many of which are ROS and redox associated (9). The unique gene sets which expression are induced by PSI ROS and changes in chloroplast redox poise are collectively referred to herein as plastid redox associated nuclear genes (PRANGs) (7); they include key and common stress marker genes such as ASCORBATE PEROXIDASE 2 (APX2) (10, 11) and ZAT10 (12) critical for acclimation. The nuclear regulators of PRANGs and the subsequent chloroplasttargeted stress responses, including induction of chloroplast antioxidant and redox regulation enzymes such as redoxin proteins, have been extensively elucidated for the different retrograde pathways (7,12). Despite these advances, however, in all of the PRANG retrograde signaling pathways no chloroplastic sensor(s) of ROS and redox state has been conclusively identified (7). For instance, a previously hypothesized sensor kinase for the PQ redox state (2) has recently been reascribed to facilitate H 2 O 2 production rather than redox sensi...

A chloroplast retrograde signal, 3’-phosphoadenosine 5’-phosphate, acts as a secondary messenger in abscisic acid signaling in stomatal closure and germination

“…Oxidative stress during drought alters chloroplast redox poise to induce a 30-fold PAP accumulation via redox regulation of SAL1 (Estavillo et al, 2011; Chan et al, 2016b). PAP accumulation could activate its downstream signaling through XRNs to transcriptionally up-regulate multiple ABA/Ca 2+ signaling proteins that are normally lowly expressed, and this includes four CDPKs that can activate SLAC1 in oocytes.…”

Plant immunity in signal integration between biotic and abiotic stress responses

“…Conversely, phytopathogenic bacteria, including Pseudomonas syringae pv tomato DC3000 (Pst), target photosynthetic electron transport at photosystem II to inhibit CO 2 assimilation and ROS production in an ABA-dependent manner (Rodr ıguez-Herva et al, de Torres Zabala et al, 2015). Under high light or drought, perturbations in the Calvin cycle generate ROS and chloroplast-nucleus retrograde signals such as methylerythritol cyclodiphosphate (MEcPP; Xiao et al, 2012) and 3 0 -phosphoadenosine-5 0 -phosphate (PAP), a by-product of sulfur metabolism (Chan et al, 2016). Oxidation-mediated inactivation of SAL1 phosphoadenosine phosphatase generates PAP to confer drought tolerance (Chan et al, 2016).…”

Ubiquitin-Proteasome Dependent Regulation of the GOLDEN2-LIKE 1 Transcription Factor in Response to Plastid Signals

“…In contrast, operational control enables plastids to regulate the expression of nuclear genes in response to environmental cues, enabling plants to optimize photosynthetic performance. To date, several molecules, including reactive oxygen species (Karpinski et al, 1999;Wagner et al, 2004), methylerythritol cyclodiphosphate (Xiao et al, 2012), and 39-phosphoadenosine-59-P (Estavillo et al, 2011;Chan et al, 2016), have been shown to participate in operational control.…”