The chloroplast can act as an environmental sensor, communicating with the cell during biogenesis and operation to change the expression of thousands of proteins. This process, termed retrograde signaling, regulates expression in response to developmental cues and stresses that affect photosynthesis and yield. Recent advances have identified many signals and pathways-including carotenoid derivatives, isoprenes, phosphoadenosines, tetrapyrroles, and heme, together with reactive oxygen species and proteins-that build a communication network to regulate gene expression, RNA turnover, and splicing. However, retrograde signaling pathways have been viewed largely as a means of bilateral communication between organelles and nuclei, ignoring their potential to interact with hormone signaling and the cell as a whole to regulate plant form and function. Here, we discuss new findings on the processes by which organelle communication is initiated, transmitted, and perceived, not only to regulate chloroplastic processes but also to intersect with cellular signaling and alter physiological responses.

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...

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