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Photosynthetic gene expression in higher plants

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Abstract

Within the chloroplasts of higher plants and algae, photosynthesis converts light into biological energy, fueling the assimilation of atmospheric carbon dioxide into biologically useful molecules. Two major steps, photosynthetic electron transport and the Calvin-Benson cycle, require many gene products encoded from chloroplast as well as nuclear genomes. The expression of genes in both cellular compartments is highly dynamic and influenced by a diverse range of factors. Light is the primary environmental determinant of photosynthetic gene expression. Working through photoreceptors such as phytochrome, light regulates photosynthetic genes at transcriptional and posttranscriptional levels. Other processes that affect photosynthetic gene expression include photosynthetic activity, development, and biotic and abiotic stress. Anterograde (from nucleus to chloroplast) and retrograde (from chloroplast to nucleus) signaling insures the highly coordinated expression of the many photosynthetic genes between these different compartments. Anterograde signaling incorporates nuclear-encoded transcriptional and posttranscriptional regulators, such as sigma factors and RNA-binding proteins, respectively. Retrograde signaling utilizes photosynthetic processes such as photosynthetic electron transport and redox signaling to influence the expression of photosynthetic genes in the nucleus. The basic C3 photosynthetic pathway serves as the default form used by most of the plant species on earth. High temperature and water stress associated with arid environments have led to the development of specialized C4 and CAM photosynthesis, which evolved as modifications of the basic default expression program. The goal of this article is to explain and summarize the many gene expression and regulatory processes that work together to support photosynthetic function in plants.

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Abbreviations

BS:

Bundle sheath

CAM:

Crassulacean acid metabolism

CES:

Control by epistasy of synthesis

GTF:

General transcription factor

iLRE:

Internal light responsive element

Lhcb/CabII:

Light-harvesting chlorophyll a/b-binding genes

LRE:

Light response element

LSU:

Large subunit of Rubisco

M:

Mesophyll

NEP:

Nuclear-encoded plastid RNA polymerase

PEP:

Plastid-encoded plastid RNA polymerase

PEPCase:

Phosphoenolpyruvate carboxylase

PET:

Photosynthetic electron transport

3-PGA:

3-Phosphoglycerate

PhANG:

Photosynthesis-associated nuclear gene

PHD:

Plant homeodomain

PolII:

RNA polymerase II

PPDK:

Pyruvate orthophosphate dikinase

ppGpp:

Guanosine-3′,5′-(bis)pyrophosphate

PPR:

Pentatricopeptide repeat

PQ:

Plastoquinone

PSI(II):

Photosystem I(II)

RCA:

Rubisco activase

RNAP:

RNA polymerase

ROGE:

Regulator of organelle gene expression

ROS:

Reactive oxygen species

Rubisco:

Ribulose-1,5-bisphosphate carboxylase/oxygenase

RuBP:

Ribulose bisphosphate

RSH:

RelA/SpoT homologue

SMD:

Stress-induced mRNA decay

SSU:

Small subunit of Rubisco

TPR:

Tetratricopeptide repeat

TT:

Tic and toc translocon

UCR:

Unique-conserved region

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Acknowledgements

Photosynthesis research in the Berry lab has been supported by grants from the US Department of Agriculture and the National Science Foundation. We thank Jim Stamos for preparing the illustrations and tables, and Alan Siegel for assistance with the confocal microscopy. The confocal microscope used for fluorescent imaging was purchased through an NSF Major Research Instrumentation (MRI) grant. We also thank two exceptional reviewers and the guest editor for careful, thoughtful evaluation of this article, as well as their excellent advice and recommendations.

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Berry, J.O., Yerramsetty, P., Zielinski, A.M. et al. Photosynthetic gene expression in higher plants. Photosynth Res 117, 91–120 (2013). https://doi.org/10.1007/s11120-013-9880-8

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