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

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...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 107; no. 25; pp. 11626 - 11631
Main Authors Toledo-Ortiz, Gabriela, Huq, Enamul, Rodríguez-Concepción, Manuel, Quail, Peter H.
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 22.06.2010
National Acad Sciences
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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 (PlF1) and other transcription factors of the phytochrome-interacting factor (PlF) 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 PlF1 directly binds to the promoter of the PSY gene, and that this binding results in repression of PSY expression. Light-triggered degradation of PlFs 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 PlF1 and other PlFs in transducing light signals to regulate PSY gene expression and carotenoid accumulation during daily cycles of light and dark in mature plants.
AbstractList 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.
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.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.
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.
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 (PlF1) and other transcription factors of the phytochrome-interacting factor (PlF) 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 PlF1 directly binds to the promoter of the PSY gene, and that this binding results in repression of PSY expression. Light-triggered degradation of PlFs 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 PlF1 and other PlFs in transducing light signals to regulate PSY gene expression and carotenoid accumulation during daily cycles of light and dark in mature plants.
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. [PUBLICATION ABSTRACT]
Author Rodríguez-Concepción, Manuel
Huq, Enamul
Quail, Peter H.
Toledo-Ortiz, Gabriela
Author_xml – sequence: 1
  givenname: Gabriela
  surname: Toledo-Ortiz
  fullname: Toledo-Ortiz, Gabriela
– sequence: 2
  givenname: Enamul
  surname: Huq
  fullname: Huq, Enamul
– sequence: 3
  givenname: Manuel
  surname: Rodríguez-Concepción
  fullname: Rodríguez-Concepción, Manuel
– sequence: 4
  givenname: Peter H.
  surname: Quail
  fullname: Quail, Peter H.
BackLink https://www.ncbi.nlm.nih.gov/pubmed/20534526$$D View this record in MEDLINE/PubMed
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Author contributions: G.T.-O. and M.R.-C. designed research; G.T.-O. performed research; E.H. contributed new reagents/analytic tools; G.T.-O., E.H., and M.R.-C. analyzed data; and G.T.-O. and M.R.-C. wrote the paper.
Edited* by Peter H. Quail, University of California, Albany, CA, and approved May 14, 2010 (received for review December 15, 2009)
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SSID ssj0009580
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Snippet 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...
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Publisher
StartPage 11626
SubjectTerms Alkyl and Aryl Transferases - biosynthesis
Alkyl and Aryl Transferases - genetics
Amino Acid Motifs
Arabidopsis - genetics
Arabidopsis Proteins - genetics
Arabidopsis Proteins - metabolism
Arabidopsis Proteins - physiology
Basic Helix-Loop-Helix Transcription Factors - genetics
Basic Helix-Loop-Helix Transcription Factors - physiology
Biological Sciences
Biosynthesis
carbon
Carotenoids
Carotenoids - metabolism
Chlorophyll
Chlorophyll - chemistry
Chlorophyll - genetics
Chlorophylls
chloroplasts
energy
etiolation
Flowers & plants
Gene expression
Gene expression regulation
Gene Expression Regulation, Enzymologic
Gene Expression Regulation, Plant
Genes
Geranylgeranyl-Diphosphate Geranylgeranyltransferase
Light
mature plants
Models, Biological
phytochrome
Phytochrome - metabolism
phytoene synthase
Pigments
Plant cells
Plants
Promoter regions
Promoter Regions, Genetic
Proteins
Seedlings
Seedlings - metabolism
Signal transduction
solar radiation
transcription factors
Transcription, Genetic
Title Direct regulation of phytoene synthase gene expression and carotenoid biosynthesis by phytochrome-interacting factors
URI https://www.jstor.org/stable/20724118
http://www.pnas.org/content/107/25/11626.abstract
https://www.ncbi.nlm.nih.gov/pubmed/20534526
https://www.proquest.com/docview/521205599
https://www.proquest.com/docview/1825411997
https://www.proquest.com/docview/733401089
https://pubmed.ncbi.nlm.nih.gov/PMC2895139
Volume 107
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