Photometric screens identified Arabidopsis peroxisome proteins that impact photosynthesis under dynamic light conditions

Jiying Li; Stefanie Tietz; Jeffrey A. Cruz; Deserah D. Strand; Ye Xu; Jin Chen; David M. Kramer; Jianping Hu

doi:10.1111/tpj.14134

Photometric screens identified Arabidopsis peroxisome proteins that impact photosynthesis under dynamic light conditions

Jiying Li, Stefanie Tietz, Jeffrey A. Cruz, Deserah D. Strand, Ye Xu, Jin Chen, David M. Kramer, Jianping Hu

Internal Medicine

Research output: Contribution to journal › Article › peer-review

15 Scopus citations

Abstract

Plant peroxisomes function collaboratively with other subcellular organelles, such as chloroplasts and mitochondria, in several metabolic processes. To comprehensively investigate the impact of peroxisomal function on photosynthesis, especially under conditions that are more relevant to natural environments, a systematic screen of over 150 Arabidopsis mutants of genes encoding peroxisomal proteins was conducted using the automated Dynamic Environment Photosynthesis Imager (DEPI). Dynamic and high-light (HL) conditions triggered significant photosynthetic defects in a subset of the mutants, including those of photorespiration (PR) and other peroxisomal processes, some of which may also be related to PR. Further analysis of the PR mutants revealed activation of cyclic electron flow (CEF) around photosystem I and higher accumulation of hydrogen peroxide (H ₂ O ₂ ) under HL conditions. We hypothesize that impaired PR disturbs the balance of ATP and NADPH, leading to the accumulation of H ₂ O ₂ that activates CEF to produce ATP to compensate for the imbalance of reducing equivalents. The identification of peroxisomal mutants involved in PR and other peroxisomal functions in the photometric screen will enable further investigation of regulatory links between photosynthesis and PR and interorganellar interaction at the mechanistic level.

Original language	English
Pages (from-to)	460-474
Number of pages	15
Journal	Plant Journal
Volume	97
Issue number	3
DOIs	https://doi.org/10.1111/tpj.14134
State	Published - Feb 1 2019

Bibliographical note

Funding Information:
The authors thank Linda Savage and David Hall for help with DEPI experiments and image processing, Oliver Tessmer for assisting in using OLIVER software, Dr Mio Sato-Cruz and Megan Mulheron for assisting with the Amplex Red assays, Drs Geoffry Davis and Nick Fischer for insightful discussions, Drs Rob Last and Jun Liu for technical assistance and comments on the manuscript, Arabidopsis Biological Resource Center (ABRC) for mutant seeds, Prof. Andreas Weber for the plgg1-1 seeds, and Center for Advanced Algal and Plant Phenotyping (CAAPP) at MSU Plant Research Laboratories for technical support. This work was supported by the Chemical Sciences, Geosciences and Biosciences Division, Office of Basic Energy Sciences, Office of Science, US Department of Energy (DE-FG02-91ER20021) to DMK and JH.

Publisher Copyright:
© 2018 The Authors The Plant Journal © 2018 John Wiley & Sons Ltd

Keywords

cyclic electron flow
dynamic environment photosynthesis imager
dynamic light
hydrogen peroxide
peroxisomes
photorespiration
photosynthesis

ASJC Scopus subject areas

Genetics
Plant Science
Cell Biology

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10.1111/tpj.14134

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title = "Photometric screens identified Arabidopsis peroxisome proteins that impact photosynthesis under dynamic light conditions",

abstract = " Plant peroxisomes function collaboratively with other subcellular organelles, such as chloroplasts and mitochondria, in several metabolic processes. To comprehensively investigate the impact of peroxisomal function on photosynthesis, especially under conditions that are more relevant to natural environments, a systematic screen of over 150 Arabidopsis mutants of genes encoding peroxisomal proteins was conducted using the automated Dynamic Environment Photosynthesis Imager (DEPI). Dynamic and high-light (HL) conditions triggered significant photosynthetic defects in a subset of the mutants, including those of photorespiration (PR) and other peroxisomal processes, some of which may also be related to PR. Further analysis of the PR mutants revealed activation of cyclic electron flow (CEF) around photosystem I and higher accumulation of hydrogen peroxide (H 2 O 2 ) under HL conditions. We hypothesize that impaired PR disturbs the balance of ATP and NADPH, leading to the accumulation of H 2 O 2 that activates CEF to produce ATP to compensate for the imbalance of reducing equivalents. The identification of peroxisomal mutants involved in PR and other peroxisomal functions in the photometric screen will enable further investigation of regulatory links between photosynthesis and PR and interorganellar interaction at the mechanistic level. ",

keywords = "cyclic electron flow, dynamic environment photosynthesis imager, dynamic light, hydrogen peroxide, peroxisomes, photorespiration, photosynthesis",

author = "Jiying Li and Stefanie Tietz and Cruz, {Jeffrey A.} and Strand, {Deserah D.} and Ye Xu and Jin Chen and Kramer, {David M.} and Jianping Hu",

note = "Funding Information: The authors thank Linda Savage and David Hall for help with DEPI experiments and image processing, Oliver Tessmer for assisting in using OLIVER software, Dr Mio Sato-Cruz and Megan Mulheron for assisting with the Amplex Red assays, Drs Geoffry Davis and Nick Fischer for insightful discussions, Drs Rob Last and Jun Liu for technical assistance and comments on the manuscript, Arabidopsis Biological Resource Center (ABRC) for mutant seeds, Prof. Andreas Weber for the plgg1-1 seeds, and Center for Advanced Algal and Plant Phenotyping (CAAPP) at MSU Plant Research Laboratories for technical support. This work was supported by the Chemical Sciences, Geosciences and Biosciences Division, Office of Basic Energy Sciences, Office of Science, US Department of Energy (DE-FG02-91ER20021) to DMK and JH. Publisher Copyright: {\textcopyright} 2018 The Authors The Plant Journal {\textcopyright} 2018 John Wiley & Sons Ltd",

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AU - Li, Jiying

AU - Tietz, Stefanie

AU - Cruz, Jeffrey A.

AU - Strand, Deserah D.

AU - Xu, Ye

AU - Chen, Jin

AU - Kramer, David M.

AU - Hu, Jianping

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N2 - Plant peroxisomes function collaboratively with other subcellular organelles, such as chloroplasts and mitochondria, in several metabolic processes. To comprehensively investigate the impact of peroxisomal function on photosynthesis, especially under conditions that are more relevant to natural environments, a systematic screen of over 150 Arabidopsis mutants of genes encoding peroxisomal proteins was conducted using the automated Dynamic Environment Photosynthesis Imager (DEPI). Dynamic and high-light (HL) conditions triggered significant photosynthetic defects in a subset of the mutants, including those of photorespiration (PR) and other peroxisomal processes, some of which may also be related to PR. Further analysis of the PR mutants revealed activation of cyclic electron flow (CEF) around photosystem I and higher accumulation of hydrogen peroxide (H 2 O 2 ) under HL conditions. We hypothesize that impaired PR disturbs the balance of ATP and NADPH, leading to the accumulation of H 2 O 2 that activates CEF to produce ATP to compensate for the imbalance of reducing equivalents. The identification of peroxisomal mutants involved in PR and other peroxisomal functions in the photometric screen will enable further investigation of regulatory links between photosynthesis and PR and interorganellar interaction at the mechanistic level.

AB - Plant peroxisomes function collaboratively with other subcellular organelles, such as chloroplasts and mitochondria, in several metabolic processes. To comprehensively investigate the impact of peroxisomal function on photosynthesis, especially under conditions that are more relevant to natural environments, a systematic screen of over 150 Arabidopsis mutants of genes encoding peroxisomal proteins was conducted using the automated Dynamic Environment Photosynthesis Imager (DEPI). Dynamic and high-light (HL) conditions triggered significant photosynthetic defects in a subset of the mutants, including those of photorespiration (PR) and other peroxisomal processes, some of which may also be related to PR. Further analysis of the PR mutants revealed activation of cyclic electron flow (CEF) around photosystem I and higher accumulation of hydrogen peroxide (H 2 O 2 ) under HL conditions. We hypothesize that impaired PR disturbs the balance of ATP and NADPH, leading to the accumulation of H 2 O 2 that activates CEF to produce ATP to compensate for the imbalance of reducing equivalents. The identification of peroxisomal mutants involved in PR and other peroxisomal functions in the photometric screen will enable further investigation of regulatory links between photosynthesis and PR and interorganellar interaction at the mechanistic level.

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Photometric screens identified Arabidopsis peroxisome proteins that impact photosynthesis under dynamic light conditions

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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