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Direct regulation of phytoene synthase gene expression and carotenoid biosynthesis by phytochrome-interacting factors.

ABSTRACT: Carotenoids are key for plants to optimize carbon fixing using the energy of sunlight. They contribute to light harvesting but also channel energy away from chlorophylls to protect the photosynthetic apparatus from excess light. Phytochrome-mediated light signals are major cues regulating carotenoid biosynthesis in plants, but we still lack fundamental knowledge on the components of this signaling pathway. Here we show that phytochrome-interacting factor 1 (PIF1) and other transcription factors of the phytochrome-interacting factor (PIF) family down-regulate the accumulation of carotenoids by specifically repressing the gene encoding phytoene synthase (PSY), the main rate-determining enzyme of the pathway. Both in vitro and in vivo evidence demonstrate that PIF1 directly binds to the promoter of the PSY gene, and that this binding results in repression of PSY expression. Light-triggered degradation of PIFs after interaction with photoactivated phytochromes during deetiolation results in a rapid derepression of PSY gene expression and a burst in the production of carotenoids in coordination with chlorophyll biosynthesis and chloroplast development for an optimal transition to photosynthetic metabolism. Our results also suggest a role for PIF1 and other PIFs in transducing light signals to regulate PSY gene expression and carotenoid accumulation during daily cycles of light and dark in mature plants.

SUBMITTER: Toledo-Ortiz G

PROVIDER: S-EPMC2895139 | biostudies-literature | 2010 Jun

REPOSITORIES: biostudies-literature

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Direct regulation of phytoene synthase gene expression and carotenoid biosynthesis by phytochrome-interacting factors.

Toledo-Ortiz Gabriela G Huq Enamul E Rodríguez-Concepción Manuel M

Proceedings of the National Academy of Sciences of the United States of America 20100607 25

Carotenoids are key for plants to optimize carbon fixing using the energy of sunlight. They contribute to light harvesting but also channel energy away from chlorophylls to protect the photosynthetic apparatus from excess light. Phytochrome-mediated light signals are major cues regulating carotenoid biosynthesis in plants, but we still lack fundamental knowledge on the components of this signaling pathway. Here we show that phytochrome-interacting factor 1 (PIF1) and other transcription factors ...[more]

PMID: 20534526

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Project description:BACKGROUND:Euglena gracilis, a unicellular phytoflagellate within Euglenida, has attracted much attention as a potential feedstock for renewable energy production. In outdoor open-pond cultivation for biofuel production, excess direct sunlight can inhibit photosynthesis in this alga and decrease its productivity. Carotenoids play important roles in light harvesting during photosynthesis and offer photoprotection for certain non-photosynthetic and photosynthetic organisms including cyanobacteria, algae, and higher plants. Although, Euglenida contains ?-carotene and xanthophylls (such as zeaxanthin, diatoxanthin, diadinoxanthin and 9'-cis neoxanthin), the pathway of carotenoid biosynthesis has not been elucidated. RESULTS:To clarify the carotenoid biosynthetic pathway in E. gracilis, we searched for the putative E. gracilis geranylgeranyl pyrophosphate (GGPP) synthase gene (crtE) and phytoene synthase gene (crtB) by tblastn searches from RNA-seq data and obtained their cDNAs. Complementation experiments in Escherichia coli with carotenoid biosynthetic genes of Pantoea ananatis showed that E. gracilis crtE (EgcrtE) and EgcrtB cDNAs encode GGPP synthase and phytoene synthase, respectively. Phylogenetic analyses indicated that the predicted proteins of EgcrtE and EgcrtB belong to a clade distinct from a group of GGPP synthase and phytoene synthase proteins, respectively, of algae and higher plants. In addition, we investigated the effects of light stress on the expression of crtE and crtB in E. gracilis. Continuous illumination at 460 or 920 ?mol m(-2) s(-1) at 25 °C decreased the E. gracilis cell concentration by 28-40 % and 13-91 %, respectively, relative to the control light intensity (55 ?mol m(-2) s(-1)). When grown under continuous light at 920 ?mol m(-2) s(-1), the algal cells turned reddish-orange and showed a 1.3-fold increase in the crtB expression. In contrast, EgcrtE expression was not significantly affected by the light-stress treatments examined. CONCLUSIONS:We identified genes encoding CrtE and CrtB in E. gracilis and found that their protein products catalyze the early steps of carotenoid biosynthesis. Further, we found that the response of the carotenoid biosynthetic pathway to light stress in E. gracilis is controlled, at least in part, by the level of crtB transcription. This is the first functional analysis of crtE and crtB in Euglena.

Dataset Information

Direct regulation of phytoene synthase gene expression and carotenoid biosynthesis by phytochrome-interacting factors.

Publications

Direct regulation of phytoene synthase gene expression and carotenoid biosynthesis by phytochrome-interacting factors.

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