Phytochrome-dependent coordinate control of distinct aspects of nuclear and plastid gene expression during anterograde signaling and photomorphogenesis
Abstract
Light perception by photoreceptors impacts plastid transcription, development, and differentiation. This photoreceptor-dependent activity suggests a mechanism for photoregulation of gene expression in the nucleus and plastid that serves to coordinate expression of critical genes of these two organelles. This coordinate expression is required for proper stoichiometric accumulation of components needed for assembly of plastids, photosynthetic light-harvesting complexes and components such as phytochromes. Chloroplast-targeted sigma factors, which function together with the plastid-encoded RNA polymerase to regulate expression of plastid-encoded genes, and nuclear-encoded plastid development factors, such as GLK1 and GLK2, are targets of phytochrome regulation. Such phytochrome-dependent functions are hypothesized to allow light-dependent regulation, and feasibly tuning, of plastid components and function in response to changes in the external environment, which directly affects photosynthesis and the potential for light-induced damage. When the size and protein composition of the light-harvesting complexes are not tuned to the external environment, imbalances in electron transport can impact the cellular redox state and cause cellular damage. We show that phytochromes specifically regulate the expression of multiple factors that function to modulate plastid transcription and, thus, provide a paradigm for coordinate expression of the nuclear and plastid genomes in response to changes in external light conditions. Asmore »
- Authors:
-
- Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
- Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory; Michigan State Univ., East Lansing, MI (United States). Dept. of Biochemistry and Molecular Biology
- Publication Date:
- Research Org.:
- Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1602772
- Grant/Contract Number:
- FG02-91ER20021
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Plant Science
- Additional Journal Information:
- Journal Volume: 5; Journal ID: ISSN 1664-462X
- Publisher:
- Frontiers Research Foundation
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Oh, Sookyung, and Montgomery, Beronda L. Phytochrome-dependent coordinate control of distinct aspects of nuclear and plastid gene expression during anterograde signaling and photomorphogenesis. United States: N. p., 2014.
Web. doi:10.3389/fpls.2014.00171.
Oh, Sookyung, & Montgomery, Beronda L. Phytochrome-dependent coordinate control of distinct aspects of nuclear and plastid gene expression during anterograde signaling and photomorphogenesis. United States. https://doi.org/10.3389/fpls.2014.00171
Oh, Sookyung, and Montgomery, Beronda L. Wed .
"Phytochrome-dependent coordinate control of distinct aspects of nuclear and plastid gene expression during anterograde signaling and photomorphogenesis". United States. https://doi.org/10.3389/fpls.2014.00171. https://www.osti.gov/servlets/purl/1602772.
@article{osti_1602772,
title = {Phytochrome-dependent coordinate control of distinct aspects of nuclear and plastid gene expression during anterograde signaling and photomorphogenesis},
author = {Oh, Sookyung and Montgomery, Beronda L.},
abstractNote = {Light perception by photoreceptors impacts plastid transcription, development, and differentiation. This photoreceptor-dependent activity suggests a mechanism for photoregulation of gene expression in the nucleus and plastid that serves to coordinate expression of critical genes of these two organelles. This coordinate expression is required for proper stoichiometric accumulation of components needed for assembly of plastids, photosynthetic light-harvesting complexes and components such as phytochromes. Chloroplast-targeted sigma factors, which function together with the plastid-encoded RNA polymerase to regulate expression of plastid-encoded genes, and nuclear-encoded plastid development factors, such as GLK1 and GLK2, are targets of phytochrome regulation. Such phytochrome-dependent functions are hypothesized to allow light-dependent regulation, and feasibly tuning, of plastid components and function in response to changes in the external environment, which directly affects photosynthesis and the potential for light-induced damage. When the size and protein composition of the light-harvesting complexes are not tuned to the external environment, imbalances in electron transport can impact the cellular redox state and cause cellular damage. We show that phytochromes specifically regulate the expression of multiple factors that function to modulate plastid transcription and, thus, provide a paradigm for coordinate expression of the nuclear and plastid genomes in response to changes in external light conditions. As phytochromes respond to changes in the prevalent wavelengths of light and light intensity, we propose that specific phytochrome-dependent molecular mechanisms are used during light-dependent signaling between the nucleus and chloroplast during photomorphogenesis to coordinate chloroplast development with plant developmental stage and the external environment.},
doi = {10.3389/fpls.2014.00171},
journal = {Frontiers in Plant Science},
number = ,
volume = 5,
place = {United States},
year = {Wed Apr 30 00:00:00 EDT 2014},
month = {Wed Apr 30 00:00:00 EDT 2014}
}
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Works referenced in this record:
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PIF1 directly and indirectly regulates chlorophyll biosynthesis to optimize the greening process in Arabidopsis
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Phytochrome-induced SIG2 expression contributes to photoregulation of phytochrome signalling and photomorphogenesis in Arabidopsis thaliana
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Downstream effectors of light- and phytochrome-dependent regulation of hypocotyl elongation in Arabidopsis thaliana
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Cryptochrome 1, Cryptochrome 2, and Phytochrome A Co-Activate the Chloroplast psbD Blue Light–Responsive Promoter
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Blue light specific and differential expression of a plastid σ factor, Sig5 in Arabidopsis thaliana
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Detection of Spatial-Specific Phytochrome Responses Using Targeted Expression of Biliverdin Reductase in Arabidopsis
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GLK Transcription Factors Coordinate Expression of the Photosynthetic Apparatus in Arabidopsis
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- The Plant Cell, Vol. 21, Issue 4
Response of Etioplasts in situ and in Isolated Suspensions to Pre-Illumination with Various Combinations of red, Far-Red and blue Light
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Eukaryotic-type plastid nucleoid protein pTAC3 is essential for transcription by the bacterial-type plastid RNA polymerase
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Recent advances in the study of chloroplast gene expression and its evolution
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Different Roles for Phytochrome in Etiolated and Green Plants Deduced from Characterization of Arabidopsis thaliana Mutants
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Cryptochrome 1, Cryptochrome 2, and Phytochrome A Co-Activate the Chloroplast psbD Blue Light-Responsive Promoter
journal, December 2001
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- The Plant Cell, Vol. 13, Issue 12
PRDA1, a Novel Chloroplast Nucleoid Protein, is Required for Early Chloroplast Development and is Involved in the Regulation of Plastid Gene Expression in Arabidopsis
journal, February 2014
- Qiao, J.; Li, J.; Chu, W.
- Plant and Cell Physiology, Vol. 55, Issue 2
Downstream effectors of light- and phytochrome-dependent regulation of hypocotyl elongation in Arabidopsis thaliana
journal, March 2013
- Oh, Sookyung; Warnasooriya, Sankalpi N.; Montgomery, Beronda L.
- Plant Molecular Biology, Vol. 81, Issue 6
Nuclear-encoded chloroplast RNA polymerase sigma factor SIG2 activates chloroplast-encoded phycobilisome genes in a red alga, Cyanidioschyzon merolae
journal, September 2013
- Fujii, Gaku; Imamura, Sousuke; Hanaoka, Mitsumasa
- FEBS Letters, Vol. 587, Issue 20
Biogenesis and homeostasis of chloroplasts and other plastids
journal, November 2013
- Jarvis, Paul; López-Juez, Enrique
- Nature Reviews Molecular Cell Biology, Vol. 14, Issue 12
GLK gene pairs regulate chloroplast development in diverse plant species
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- Fitter, David W.; Martin, David J.; Copley, Martin J.
- The Plant Journal, Vol. 31, Issue 6
Blue light-induced transcription of plastid-encoded psbD gene is mediated by a nuclear-encoded transcription initiation factor, AtSig5
journal, February 2004
- Tsunoyama, Y.; Ishizaki, Y.; Morikawa, K.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 9
The phytochrome-interacting transcription factor, PIF3, acts early, selectively, and positively in light-induced chloroplast development
journal, October 2004
- Monte, E.; Tepperman, J. M.; Al-Sady, B.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 46
PIF1 directly and indirectly regulates chlorophyll biosynthesis to optimize the greening process in Arabidopsis
journal, June 2008
- Moon, J.; Zhu, L.; Shen, H.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 27
PIF3 is a repressor of chloroplast development
journal, April 2009
- Stephenson, P. G.; Fankhauser, C.; Terry, M. J.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 18
Plastid gene expression and plant development require a plastidic protein of the mitochondrial transcription termination factor family
journal, April 2011
- Babiychuk, E.; Vandepoele, K.; Wissing, J.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 16
Eukaryotic-type plastid nucleoid protein pTAC3 is essential for transcription by the bacterial-type plastid RNA polymerase
journal, April 2012
- Yagi, Y.; Ishizaki, Y.; Nakahira, Y.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 19
Leaf-specifically expressed genes for polypeptides destined for chloroplasts with domains of 70 factors of bacterial RNA polymerases in Arabidopsis thaliana
journal, December 1997
- Isono, K.; Shimizu, M.; Yoshimoto, K.
- Proceedings of the National Academy of Sciences, Vol. 94, Issue 26
The Phytochromes, a Family of Red/Far-red Absorbing Photoreceptors
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- Fankhauser, Christian
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The tetratricopeptide repeat-containing protein slow green1 is required for chloroplast development in Arabidopsis
journal, January 2014
- Hu, Zhihong; Xu, Fan; Guan, Liping
- Journal of Experimental Botany, Vol. 65, Issue 4
Plastidic RNA polymerase factors in Arabidopsis
journal, January 1999
- Kanamaru, K.; Fujiwara, M.; Seki, M.
- Plant and Cell Physiology, Vol. 40, Issue 8
An Arabidopsis Sigma Factor (SIG2)-Dependent Expression of Plastid-Encoded tRNAs in Chloroplasts
journal, October 2001
- Kanamaru, Kengo; Nagashima, Akitomo; Fujiwara, Makoto
- Plant and Cell Physiology, Vol. 42, Issue 10
PRDA1, a Novel Chloroplast Nucleoid Protein, is Required for Early Chloroplast Development and is Involved in the Regulation of Plastid Gene Expression in Arabidopsis
journal, November 2013
- Qiao, Jiangwei; Li, Jun; Chu, Wen
- Plant and Cell Physiology, Vol. 54, Issue 12
Phytochrome A and Phytochrome B Have Overlapping but Distinct Functions in Arabidopsis Development
journal, April 1994
- Reed, J. W.; Nagatani, A.; Elich, T. D.
- Plant Physiology, Vol. 104, Issue 4
The Pentratricopeptide Repeat Protein DELAYED GREENING1 Is Involved in the Regulation of Early Chloroplast Development and Chloroplast Gene Expression in Arabidopsis
journal, April 2008
- Chi, Wei; Ma, Jinfang; Zhang, Dongyuan
- Plant Physiology, Vol. 147, Issue 2
Detection of Spatial-Specific Phytochrome Responses Using Targeted Expression of Biliverdin Reductase in Arabidopsis
journal, October 2008
- Warnasooriya, Sankalpi N.; Montgomery, Beronda L.
- Plant Physiology, Vol. 149, Issue 1
Genetic Dissection of Chloroplast Biogenesis and Development: An Overview
journal, February 2011
- Pogson, Barry J.; Albrecht, Verónica
- Plant Physiology, Vol. 155, Issue 4
Modification of Distinct Aspects of Photomorphogenesis via Targeted Expression of Mammalian Biliverdin Reductase in Transgenic Arabidopsis Plants
journal, October 1999
- Montgomery, Beronda L.; Yeh, Kuo-Chen; Crepeau, Marc W.
- Plant Physiology, Vol. 121, Issue 2
Cryptochrome 1, Cryptochrome 2, and Phytochrome A Co-Activate the Chloroplast psbD Blue Light–Responsive Promoter
journal, December 2001
- Thum, Karen E.; Kim, Minkyun; Christopher, David A.
- The Plant Cell, Vol. 13, Issue 12
Plastid Signals Remodel Light Signaling Networks and Are Essential for Efficient Chloroplast Biogenesis in Arabidopsis
journal, December 2007
- Ruckle, Michael E.; DeMarco, Stephanie M.; Larkin, Robert M.
- The Plant Cell, Vol. 19, Issue 12
GLK Transcription Factors Coordinate Expression of the Photosynthetic Apparatus in Arabidopsis
journal, April 2009
- Waters, Mark T.; Wang, Peng; Korkaric, Muris
- The Plant Cell, Vol. 21, Issue 4
GLK transcription factors regulate chloroplast development in a cell-autonomous manner
journal, November 2008
- Waters, Mark T.; Moylan, Elizabeth C.; Langdale, Jane A.
- The Plant Journal, Vol. 56, Issue 3
Response of Etioplasts in situ and in Isolated Suspensions to Pre-Illumination with Various Combinations of red, Far-Red and blue Light
journal, January 1973
- Wellburn, Florence A. M.; Wellburn, A. R.
- New Phytologist, Vol. 72, Issue 1
Sigma factor-mediated plastid retrograde signals control nuclear gene expression
journal, November 2012
- Woodson, Jesse D.; Perez-Ruiz, Juan M.; Schmitz, Robert J.
- The Plant Journal, Vol. 73, Issue 1
Recent advances in the study of chloroplast gene expression and its evolution
journal, January 2014
- Yagi, Yusuke; Shiina, Takashi
- Frontiers in Plant Science, Vol. 5
Works referencing / citing this record:
Nuclear‐encoded sigma factor 6 ( SIG 6) is involved in the block of greening response in Arabidopsis thaliana
journal, January 2020
- Alameldin, Hussien F.; Oh, Sookyung; Hernandez, Alexandra P.
- American Journal of Botany, Vol. 107, Issue 2
Mesophyll-specific phytochromes impact chlorophyll light-harvesting complexes (LHCs) and non-photochemical quenching
journal, April 2019
- Oh, Sookyung; Montgomery, Beronda L.
- Plant Signaling & Behavior, Vol. 14, Issue 7
Phytochrome B regulates resource allocation in Brassica rapa
journal, March 2018
- Arsovski, Andrej A.; Zemke, Joseph E.; Haagen, Benjamin D.
- Journal of Experimental Botany, Vol. 69, Issue 11
Fruit-localized phytochromes regulate plastid biogenesis, starch synthesis, and carotenoid metabolism in tomato
journal, April 2018
- Ernesto Bianchetti, Ricardo; Silvestre Lira, Bruno; Santos Monteiro, Scarlet
- Journal of Experimental Botany, Vol. 69, Issue 15
Mesophyll-specific phytochromes impact chlorophyll light-harvesting complexes (LHCs) and non-photochemical quenching
text, January 2019
- Oh, Sookyung; Montgomery, Beronda L.
- Figshare
Mesophyll-specific phytochromes impact chlorophyll light-harvesting complexes (LHCs) and non-photochemical quenching
text, January 2019
- Oh, Sookyung; Montgomery, Beronda L.
- Taylor & Francis
Transcriptome and phenotyping analyses support a role for chloroplast sigma factor 2 in red-light-dependent regulation of growth, stress, and photosynthesis
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ATHB17 enhances stress tolerance by coordinating photosynthesis associated nuclear gene and ATSIG5 expression in response to abiotic stress
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Phytochrome B regulates resource allocation in Brassica rapa
journal, March 2018
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Fruit-localized phytochromes regulate plastid biogenesis, starch synthesis, and carotenoid metabolism in tomato
journal, April 2018
- Ernesto Bianchetti, Ricardo; Silvestre Lira, Bruno; Santos Monteiro, Scarlet
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Spatiotemporal Phytochrome Signaling during Photomorphogenesis: From Physiology to Molecular Mechanisms and Back
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