The HY5-PIF Regulatory Module Coordinates Light and Temperature Control of Photosynthetic Gene Transcription

The ability to interpret daily and seasonal alterations in light and temperature signals is essential for plant survival. This is particularly important during seedling establishment when the phytochrome photoreceptors activate photosynthetic pigment production for photoautotrophic growth. Phytochro...

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Published in	PLoS genetics Vol. 10; no. 6; p. e1004416
Main Authors	Toledo-Ortiz, Gabriela, Johansson, Henrik, Lee, Keun Pyo, Bou-Torrent, Jordi, Stewart, Kelly, Steel, Gavin, Rodríguez-Concepción, Manuel, Halliday, Karen J.
Format	Journal Article
Language	English
Published	United States Public Library of Science 01.06.2014 Public Library of Science (PLoS)
Subjects	Arabidopsis - growth & development Arabidopsis - metabolism Arabidopsis Proteins - biosynthesis Arabidopsis Proteins - genetics Basic Helix-Loop-Helix Transcription Factors - genetics Basic-Leucine Zipper Transcription Factors - genetics Biology and Life Sciences Biosynthesis Carotenoids - biosynthesis Chlorophyll Chlorophyll - biosynthesis Chromophores Circadian rhythm G-Box Binding Factors - genetics Gene expression Gene Expression Regulation, Plant Genetic aspects Genetic transcription Nuclear Proteins - genetics Photoperiod Photoreceptors Photosynthesis Photosynthesis - genetics Physiological aspects Phytochrome Promoter Regions, Genetic Proteins Receptors, Peptide - biosynthesis Seasons Temperature Transcription factors Transcription, Genetic Transcriptional Activation - genetics
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Abstract	The ability to interpret daily and seasonal alterations in light and temperature signals is essential for plant survival. This is particularly important during seedling establishment when the phytochrome photoreceptors activate photosynthetic pigment production for photoautotrophic growth. Phytochromes accomplish this partly through the suppression of phytochrome interacting factors (PIFs), negative regulators of chlorophyll and carotenoid biosynthesis. While the bZIP transcription factor long hypocotyl 5 (HY5), a potent PIF antagonist, promotes photosynthetic pigment accumulation in response to light. Here we demonstrate that by directly targeting a common promoter cis-element (G-box), HY5 and PIFs form a dynamic activation-suppression transcriptional module responsive to light and temperature cues. This antagonistic regulatory module provides a simple, direct mechanism through which environmental change can redirect transcriptional control of genes required for photosynthesis and photoprotection. In the regulation of photopigment biosynthesis genes, HY5 and PIFs do not operate alone, but with the circadian clock. However, sudden changes in light or temperature conditions can trigger changes in HY5 and PIFs abundance that adjust the expression of common target genes to optimise photosynthetic performance and growth.
AbstractList	The ability to interpret daily and seasonal alterations in light and temperature signals is essential for plant survival. This is particularly important during seedling establishment when the phytochrome photoreceptors activate photosynthetic pigment production for photoautotrophic growth. Phytochromes accomplish this partly through the suppression of PHYTOCHROME INTERACTING FACTORS (PIFs), negative regulators of chlorophyll and carotenoid biosynthesis. While the bZIP transcription factor LONG HYPOCOTYL 5 (HY5), a potent PIF antagonist, promotes photosynthetic pigment accumulation in response to light. Here we demonstrate that by directly targeting a common promoter cis-element (G- box), HY5 and PIFs form a dynamic activation-suppression transcriptional module responsive to light and temperature cues. This antagonistic regulatory module provides a simple, direct mechanism through which environmental change can redirect transcriptional control of genes required for photosynthesis and photoprotection. In the regulation of photopigment biosynthesis genes, HY5 and PIFs do not operate alone, but with the circadian clock. However, sudden changes in light or temperature conditions can trigger changes in HY5 and PIFs abundance that adjust the expression of common target genes to optimise photosynthetic performance and growth. The ability to interpret daily and seasonal alterations in light and temperature signals is essential for plant survival. This is particularly important during seedling establishment when the phytochrome photoreceptors activate photosynthetic pigment production for photoautotrophic growth. Phytochromes accomplish this partly through the suppression of PHYTOCHROME INTERACTING FACTORS (PIFs), negative regulators of chlorophyll and carotenoid biosynthesis. While the bZIP transcription factor LONG HYPOCOTYL 5 (HY5), a potent PIF antagonist, promotes photosynthetic pigment accumulation in response to light. Here we demonstrate that by directly targeting a common promoter cis-element (G-box), HY5 and PIFs form a dynamic activation-suppression transcriptional module responsive to light and temperature cues. This antagonistic regulatory module provides a simple, direct mechanism through which environmental change can redirect transcriptional control of genes required for photosynthesis and photoprotection. In the regulation of photopigment biosynthesis genes, HY5 and PIFs do not operate alone, but with the circadian clock. However, sudden changes in light or temperature conditions can trigger changes in HY5 and PIFs abundance that adjust the expression of common target genes to optimise photosynthetic performance and growth. The ability to interpret daily and seasonal alterations in light and temperature signals is essential for plant survival. This is particularly important during seedling establishment when the phytochrome photoreceptors activate photosynthetic pigment production for photoautotrophic growth. Phytochromes accomplish this partly through the suppression of PHYTOCHROME INTERACTING FACTORS (PIFs), negative regulators of chlorophyll and carotenoid biosynthesis. While the bZIP transcription factor LONG HYPOCOTYL 5 (HY5), a potent PIF antagonist, promotes photosynthetic pigment accumulation in response to light. Here we demonstrate that by directly targeting a common promoter cis -element (G-box), HY5 and PIFs form a dynamic activation-suppression transcriptional module responsive to light and temperature cues. This antagonistic regulatory module provides a simple, direct mechanism through which environmental change can redirect transcriptional control of genes required for photosynthesis and photoprotection. In the regulation of photopigment biosynthesis genes, HY5 and PIFs do not operate alone, but with the circadian clock. However, sudden changes in light or temperature conditions can trigger changes in HY5 and PIFs abundance that adjust the expression of common target genes to optimise photosynthetic performance and growth. Plants, as sessile and photosynthetic organisms, have to constantly adjust their growth and development in response to the environment. While light and temperature are recognized as the most prominent environmental factors modulating plant photosynthetic metabolism, how the seasonal and daily adjustments are achieved is not understood. Global climate alterations will bring together the combination of light and temperature changes and will require an understanding of signal convergence. If we are to mitigate the impact of variable weather patterns on agriculture, it is critical to advance our understanding of the basis of plant responses to environmental variations. In our study we show that the antagonistic activity of key plant transcription factors involved in phytochrome red light photoreceptors signaling (PIFs and HY5) optimize photosynthetic pigment production in response to environmental cues. These light and temperature responsive transcription factors operate in cooperation with the circadian clock to regulate photosynthetic pigment production through a common gene promoter element. The ability to interpret daily and seasonal alterations in light and temperature signals is essential for plant survival. This is particularly important during seedling establishment when the phytochrome photoreceptors activate photosynthetic pigment production for photoautotrophic growth. Phytochromes accomplish this partly through the suppression of phytochrome interacting factors (PIFs), negative regulators of chlorophyll and carotenoid biosynthesis. While the bZIP transcription factor long hypocotyl 5 (HY5), a potent PIF antagonist, promotes photosynthetic pigment accumulation in response to light. Here we demonstrate that by directly targeting a common promoter cis-element (G-box), HY5 and PIFs form a dynamic activation-suppression transcriptional module responsive to light and temperature cues. This antagonistic regulatory module provides a simple, direct mechanism through which environmental change can redirect transcriptional control of genes required for photosynthesis and photoprotection. In the regulation of photopigment biosynthesis genes, HY5 and PIFs do not operate alone, but with the circadian clock. However, sudden changes in light or temperature conditions can trigger changes in HY5 and PIFs abundance that adjust the expression of common target genes to optimise photosynthetic performance and growth.The ability to interpret daily and seasonal alterations in light and temperature signals is essential for plant survival. This is particularly important during seedling establishment when the phytochrome photoreceptors activate photosynthetic pigment production for photoautotrophic growth. Phytochromes accomplish this partly through the suppression of phytochrome interacting factors (PIFs), negative regulators of chlorophyll and carotenoid biosynthesis. While the bZIP transcription factor long hypocotyl 5 (HY5), a potent PIF antagonist, promotes photosynthetic pigment accumulation in response to light. Here we demonstrate that by directly targeting a common promoter cis-element (G-box), HY5 and PIFs form a dynamic activation-suppression transcriptional module responsive to light and temperature cues. This antagonistic regulatory module provides a simple, direct mechanism through which environmental change can redirect transcriptional control of genes required for photosynthesis and photoprotection. In the regulation of photopigment biosynthesis genes, HY5 and PIFs do not operate alone, but with the circadian clock. However, sudden changes in light or temperature conditions can trigger changes in HY5 and PIFs abundance that adjust the expression of common target genes to optimise photosynthetic performance and growth.
Audience	Academic
Author	Rodríguez-Concepción, Manuel Johansson, Henrik Stewart, Kelly Bou-Torrent, Jordi Halliday, Karen J. Steel, Gavin Toledo-Ortiz, Gabriela Lee, Keun Pyo
AuthorAffiliation	1 Institute of Structural and Molecular Biology, SynthSys, University of Edinburgh, Edinburgh, United Kingdom 3 Centre for Research in Agricultural Genomics (CRAG) CSIC-IRTA-UAB-UB, Campus UAB Bellaterra, Barcelona, Spain Peking University, China 2 Plant Physiology, Justus Liebig University, Senckernbergstr, Giessen, Germany
AuthorAffiliation_xml	– name: 1 Institute of Structural and Molecular Biology, SynthSys, University of Edinburgh, Edinburgh, United Kingdom – name: 2 Plant Physiology, Justus Liebig University, Senckernbergstr, Giessen, Germany – name: 3 Centre for Research in Agricultural Genomics (CRAG) CSIC-IRTA-UAB-UB, Campus UAB Bellaterra, Barcelona, Spain – name: Peking University, China
Author_xml	– sequence: 1 givenname: Gabriela surname: Toledo-Ortiz fullname: Toledo-Ortiz, Gabriela – sequence: 2 givenname: Henrik surname: Johansson fullname: Johansson, Henrik – sequence: 3 givenname: Keun Pyo surname: Lee fullname: Lee, Keun Pyo – sequence: 4 givenname: Jordi surname: Bou-Torrent fullname: Bou-Torrent, Jordi – sequence: 5 givenname: Kelly surname: Stewart fullname: Stewart, Kelly – sequence: 6 givenname: Gavin surname: Steel fullname: Steel, Gavin – sequence: 7 givenname: Manuel surname: Rodríguez-Concepción fullname: Rodríguez-Concepción, Manuel – sequence: 8 givenname: Karen J. surname: Halliday fullname: Halliday, Karen J.
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/24922306$$D View this record in MEDLINE/PubMed
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Conceived and designed the experiments: GTO HJ MRC KJH. Performed the experiments: GTO HJ KPL JBT KS GS. Analyzed the data: GTO HJ MRC KJH. Contributed reagents/materials/analysis tools: GTO HJ KPL JBT KS GS. Wrote the paper: GTO HJ MRC KJH. The authors have declared that no competing interests exist.
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Snippet	The ability to interpret daily and seasonal alterations in light and temperature signals is essential for plant survival. This is particularly important during... The ability to interpret daily and seasonal alterations in light and temperature signals is essential for plant survival. This is particularly important...
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SubjectTerms	Arabidopsis - growth & development Arabidopsis - metabolism Arabidopsis Proteins - biosynthesis Arabidopsis Proteins - genetics Basic Helix-Loop-Helix Transcription Factors - genetics Basic-Leucine Zipper Transcription Factors - genetics Biology and Life Sciences Biosynthesis Carotenoids - biosynthesis Chlorophyll Chlorophyll - biosynthesis Chromophores Circadian rhythm G-Box Binding Factors - genetics Gene expression Gene Expression Regulation, Plant Genetic aspects Genetic transcription Nuclear Proteins - genetics Photoperiod Photoreceptors Photosynthesis Photosynthesis - genetics Physiological aspects Phytochrome Promoter Regions, Genetic Proteins Receptors, Peptide - biosynthesis Seasons Temperature Transcription factors Transcription, Genetic Transcriptional Activation - genetics
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Title	The HY5-PIF Regulatory Module Coordinates Light and Temperature Control of Photosynthetic Gene Transcription
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