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Optimization of photosynthesis by multiple metabolic pathways involving interorganelle interactions: resource sharing and ROS maintenance as the bases

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Abstract

The bioenergetic processes of photosynthesis and respiration are mutually beneficial. Their interaction extends to photorespiration, which is linked to optimize photosynthesis. The interplay of these three pathways is facilitated by two major phenomena: sharing of energy/metabolite resources and maintenance of optimal levels of reactive oxygen species (ROS). The resource sharing among different compartments of plant cells is based on the production/utilization of reducing equivalents (NADPH, NADH) and ATP as well as on the metabolite exchange. The responsibility of generating the cellular requirements of ATP and NAD(P)H is mostly by the chloroplasts and mitochondria. In turn, besides the chloroplasts, the mitochondria, cytosol and peroxisomes are common sinks for reduced equivalents. Transporters located in membranes ensure the coordinated movement of metabolites across the cellular compartments. The present review emphasizes the beneficial interactions among photosynthesis, dark respiration and photorespiration, in relation to metabolism of C, N and S. Since the bioenergetic reactions tend to generate ROS, the cells modulate chloroplast and mitochondrial reactions, so as to ensure that the ROS levels do not rise to toxic levels. The patterns of minimization of ROS production and scavenging of excess ROS in intracellular compartments are highlighted. Some of the emerging developments are pointed out, such as model plants, orientation/movement of organelles and metabolomics.

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Abbreviations

2-OG:

2-Oxoglutarate

3-PGA:

3-Phosphoglycerate

AOX:

Alternative oxidase

APX:

Ascorbate peroxidase

ASC:

Ascorbate

AT:

Adenylate transporter

BPGA:

Bisphosphoglycerate

CAT:

Catalase

CET:

Cyclic electron transport

DHAP:

Dihydroxyacetone phosphate

DiT1/2:

Plastidic 2-oxoglutarate-malate transporter/plastidic glutamate-malate transporter

DTC:

Dicarboxylate/tricarboxylate carrier

Fd:

Ferredoxin

FNR:

Fd-NADP+ reductase

GABA:

γ-Aminobutyric acid

GAP:

Glyceraldehyde 3-phosphate

GDC:

Glycine decarboxylase

GO:

Glycolate oxidase

GOGAT:

Glutamine:oxoglutarate aminotransferase

GPx:

Glutathione peroxidase

GS:

Glutamine synthetase

GSH:

Glutathione

MET:

Mitochondrial electron transport

NiR:

Nitrite reductase

NiTr:

Nitrate transporter

NR:

Nitrate reductase

OAA:

Oxaloacetate

PC:

Plastocyanin

PEP:

Phosphoenolpyruvate

PLGG1:

Plastidic glycolate glycerate transporter

PQ:

Plastoquinone

PrxR:

Peroxiredoxins

PyrT:

Pyruvate transporter

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

TPT:

Triose phosphate/phosphate translocator

XO:

Xanthine oxidase

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Acknowledgments

The study is supported by a J.C. Bose National Fellowship (No. SR/S2/JCB-06/2006) to A.S.R, from the Department of Science and Technology, India; Council of Scientific and Industrial Research (New Delhi)—Research Associateship to B. S. and University Grants Commission-Junior Research Fellowship to V. A. We also thank DBT-CREBB, DST-FIST and UGC-SAP-CAS, for support to Department/School.

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  1. Department of Plant Sciences, School of Life Sciences, University of Hyderabad, Hyderabad, 500046, India

    Bobba Sunil, Sai K. Talla, Vetcha Aswani & Agepati S. Raghavendra

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  1. Bobba Sunil
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Correspondence to Agepati S. Raghavendra.

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Sunil, B., Talla, S.K., Aswani, V. et al. Optimization of photosynthesis by multiple metabolic pathways involving interorganelle interactions: resource sharing and ROS maintenance as the bases. Photosynth Res 117, 61–71 (2013). https://doi.org/10.1007/s11120-013-9889-z

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