Carotenoids are mostly C40 terpenoids, a class of hydrocarbons that participate in various biological processes in plants, such as photosynthesis, photomorphogenesis, photoprotection, and development. Carotenoids also serve as precursors for two plant hormones and a diverse set of apocarotenoids. They are colorants and critical components of the human diet as antioxidants and provitamin A. In this review, we summarize current knowledge of the genes and enzymes involved in carotenoid metabolism and describe recent progress in understanding the regulatory mechanisms underlying carotenoid accumulation. The importance of the specific location of carotenoid enzyme metabolons and plastid types as well as of carotenoid-derived signals is discussed.

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...

In addition to acting as photoprotective compounds, carotenoids also serve as precursors in the biosynthesis of several phytohormones and proposed regulatory signals. Here, we report a signaling process derived from carotenoids that regulates early chloroplast and leaf development. Biosynthesis of the signal depends on z-carotene desaturase activity encoded by the z-CAROTENE DESATURASE (ZDS)/CHLOROPLAST BIOGENESIS5 (CLB5) gene in Arabidopsis thaliana. Unlike other carotenoiddeficient plants, zds/clb5 mutant alleles display profound alterations in leaf morphology and cellular differentiation as well as altered expression of many plastid-and nucleus-encoded genes. The leaf developmental phenotypes and gene expression alterations of zds/clb5/spc1/pde181 plants are rescued by inhibitors or mutations of phytoene desaturase, demonstrating that phytofluene and/or z-carotene are substrates for an unidentified signaling molecule. Our work further demonstrates that this signal is an apocarotenoid whose synthesis requires the activity of the carotenoid cleavage dioxygenase CCD4.