Physiological functions of malate shuttles in plants and algae

doi:10.1016/j.tplants.2021.11.007

Trends in Plant Science

Volume 27, Issue 5, May 2022, Pages 488-501

https://doi.org/10.1016/j.tplants.2021.11.007 Get rights and content

Highlights

The malate shuttle, as a valve for photosynthetic electron dissipation, has been proposed for >50 years, but only recently has this function been clearly demonstrated.
The plastidial NAD-MDH is essential for embryogenesis and chloroplast development. This role is not due to its enzymatic activity but rather to its ability to stabilize a large AAA-ATPase complex at the inner envelope. The plNAD-MDH is therefore a moonlighting protein.
The malate shuttle connects fatty acid biosynthesis in the chloroplast to mitochondrial reactive oxygen species (ROS) production and to programmed cell death in plants.
The malate shuttle connects fatty acid catabolism in the peroxisome to photosynthesis and chloroplast metabolism in algae.
Expression of malate shuttle components is responsive to CO₂ levels. The latest results indicate its critical role in plant photorespiration and points to a possible role in the algal CO₂-concentrating mechanism.

Subcellular compartmentalization confers evolutionary advantage to eukaryotic cells but entails the need for efficient interorganelle communication. Malate functions as redox carrier and metabolic intermediate. It can be shuttled across membranes through translocators. The interconversion of malate and oxaloacetate mediated by malate dehydrogenases requires oxidation/reduction of NAD(P)H/NAD(P)⁺; therefore, malate trafficking serves to transport reducing equivalents and this is termed the ‘malate shuttle’. Although the term 'malate shuttle' was coined more than 50 years ago, novel functions are still emerging. This review highlights recent findings on the functions of malate shuttles in photorespiration, fatty acid β-oxidation, interorganelle signaling and its putative role in CO₂-concentrating mechanisms. We compare and contrast knowledge in plants and algae, thereby providing an evolutionary perspective on redox trafficking in photosynthetic eukaryotes.

Section snippets

Malate as a major cellular redox carrier

Eukaryotic cells are compartmentalized, and distinct subcellular organelles house specific subsets of metabolic reactions that are physically separated from each other by biological membranes. Exchange of information and energy between compartments, mostly mediated by metabolites, is indispensable to achieve whole-cell homeostasis and ensure optimal growth [1,2]. While some of these exchanges occur through passive diffusion, most of them are mediated by transporters [3]. Understanding the

Malate shuttle as a valve for photosynthetic electron dissipation

During the linear electron flow (LEF) of photosynthesis, light energy is converted by two photosystems (PSII and PSI) into chemical energy in the form of NADPH and ATP, which are subsequently used to drive metabolic reactions, particularly CO₂ fixation by RuBisCo and its conversion into triose phosphates through the Calvin–Benson–Bassham (CBB) cycle [13]. However, the LEF is known to produce an insufficient amount of ATP (as compared to NADPH) than that required for optimal CO₂ photoreduction,

The role of the malate shuttle in plant photorespiration

Photorespiration, initiated by the oxygenation reaction of RuBisCo, is inevitable in an oxygen-containing atmosphere. The rate of photorespiration is reduced in land plants performing C4 photosynthesis and in algae having a CCM [27]. Photorespiration consists of multiple metabolic reactions distributed over four subcellular compartments: chloroplast, cytosol, peroxisome, and mitochondrion, and it therefore requires intimate interorganelle communication. Photorespiratory reactions have a strong

A putative role of the malate shuttle in the algal CCM

To cope with the low CO₂-to-O₂ ratio, unlike plants where photorespiration plays a significant role, microalgae frequently use a CCM. The algal biophysical CCM is an energetic mechanism that pumps and sequestrates atmospheric CO₂ into the pyrenoid close to the active site of RuBisCo, key to the proliferation of algae in their natural habitat where the CO₂ level could be extremely low [27]. In the past 10 years, enzymes (carbonic anhydrases), transcription factors (CCM1), and also several

The malate shuttle mediates interorganelle signaling through ROS

Intercompartmental exchange of signals is key for cellular homeostasis and the acclimation of photosynthetic organisms in fluctuating environments [47]. ROS signaling has been considered a powerful system for the regulation of gene expression, leading to a cascade of physiological adjustments, such as induction of programmed cell death (PCD) [48,49]. ROS can be generated in four major subcellular compartments, that is, chloroplast, peroxisome, mitochondria, and cytosol. ROS are produced when O₂

The malate shuttle connects fatty acid catabolism to chloroplast metabolism

Fatty acid β-oxidation, photorespiration, and the glyoxylate cycle occur either totally or partially in the peroxisome, making it a third subcellular compartment involved in energy metabolism after the chloroplast and the mitochondrion [62., 63., 64.]. In addition, peroxisomes house reactions that produce H₂O₂. Fatty acid degradation and glyoxylate cycle generate the reducing equivalents NADH inside the peroxisome, whereas photorespiration consumes it. Therefore, CO₂ availability, by modulating

Concluding remarks and future perspectives

Because variations in environmental parameters may differentially affect the different cellular functions involved in the bioenergetics of photosynthetic cells, which are located in different subcellular compartments, plants and algae have evolved efficient trafficking of reducing equivalents between subcellular compartments to maintain redox homeostasis. Among these mechanisms, the 'malate shuttle' enables efficient transport of reducing equivalents between chloroplasts, cytosol, mitochondria,

Acknowledgments

O.D. thanks The French Atomic Energy and Alternative Energy Commission (CEA) for a PhD scholarship. G.P. and Y.L.-B. thank the continuous financial support of CEA (LD-power, CO2Storage). F.K. and A.P.M.W. acknowledge funding by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) – Project-ID 267205415 – CRC 1208 and under Germany’s Excellence Strategy EXC-2048/1, Project ID 390686111.

Declaration of interests

No interests were declared.

Glossary

CO₂-concentrating mechanism (CCM): CCM, as the name implies, is a process of concentrating CO₂ to the active site of RuBisCo, the major protein of the carbon photoreduction cycle (i.e., often called Calvin–Benson–Bassham cycle). It is therefore considered a mechanism to reduce the rate of photorespiration. Depending on species, CCM could refer to the dicarboxylic acid cycle in C4 plants, CAM-based CCM in CAM plants, carboxysome based-CCM in cyanobacteria, and the biophysical CCM occurring in

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Moreover, NADH cannot cross the peroxisomal membrane; the known NAD transporters import NAD+ only in exchange with AMP or ADP (Palmieri et al., 2009; van Roermund et al., 2016). Therefore, a web of redox shuttles, including those already mentioned, provides the balance of NAD+ and NADH between the different cellular compartments (Reumann et al., 1994; Dao et al., 2021). This explanation is obvious and widely accepted, but cannot explain all relevant experimental observations.
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This article is a review and update particularly on the enzyme components of plant photorespiration and their catalytic mechanisms, on the interaction of photorespiration with other metabolism and on its impact on the evolution of photosynthesis. This focus was chosen because a better knowledge of the enzymes involved and how they are embedded in overall plant metabolism can facilitate the targeted use of the now highly advanced methods of metabolic network modelling and flux analysis. Understanding photorespiration more than before as a process that enables, rather than reduces, plant photosynthesis, will help develop rational strategies for crop improvement.

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Trends in Plant Science

ReviewPhysiological functions of malate shuttles in plants and algae

Highlights

Section snippets

Malate as a major cellular redox carrier

Malate shuttle as a valve for photosynthetic electron dissipation

The role of the malate shuttle in plant photorespiration

A putative role of the malate shuttle in the algal CCM

The malate shuttle mediates interorganelle signaling through ROS

The malate shuttle connects fatty acid catabolism to chloroplast metabolism

Concluding remarks and future perspectives

Acknowledgments

Declaration of interests

Glossary

Trends Plant Sci.

Biochim. Biophys. Acta (Biomembranes)

Algal Res.

J. Biol. Chem.

J. Biol. Chem.

Trends Plant Sci.

Cell

Curr. Opin. Plant Biol.

J. Biotechnol.

Cell

Free Radic. Biol. Med.

Trends Plant Sci.

Prog. Lipid Res.

Arch. Biochem. Biophys.

J. Plant Physiol.

J. Biol. Chem.

Front. Plant Sci.

Connecting the plastid: transporters of the plastid envelope and their role in linking plastidial with cytosolic metabolism

Annu. Rev. Plant Biol.

The roles of organic acids in C4 photosynthesis

Front. Plant Sci.

Mechanistic understanding of photorespiration paves the way to a new green revolution

New Phytol.

The peroxisomal NAD carrier from Arabidopsis imports NAD in exchange with AMP1[OPEN]

Plant Physiol.

Inter-organelle NAD metabolism underpinning light responsive NADP dynamics in plants

Front. Plant Sci.

Malate valves: old shuttles with new perspectives

Plant Biol. (Stuttg)

The importance of energy balance in improving photosynthetic productivity

Plant Physiol.

Alternative electron pathways of photosynthesis drive the algal CO2 concentrating mechanism

bioRxiv

Light stress and photoprotection in Chlamydomonas reinhardtii

Plant J.

Subcellular energetics and carbon storage in Chlamydomonas

Cells

Putative role of the malate valve enzyme NADP–malate dehydrogenase in H2O2 signalling in Arabidopsis

Philos. Trans. R. Soc. B Biol. Sci.

Multiple strategies to prevent oxidative stress in Arabidopsis plants lacking the malate valve enzyme NADP-malate dehydrogenase

J. Exp. Bot.

Redox regulation of NADP-malate dehydrogenase is vital for land plants under fluctuating light environment

PNAS

The chloroplastic 2-oxoglutarate/malate transporter has dual function as the malate valve and in carbon/nitrogen metabolism

Plant J.

NADP-malate dehydrogenase from unicellular green alga Chlamydomonas reinhardtii. A first step toward redox regulation?

Plant Physiol.

Combined increases in mitochondrial cooperation and oxygen photoreduction compensate for deficiency in cyclic electron flow in Chlamydomonas reinhardtii

Plant Cell

Interorganelle communication: peroxisomal malate dehydrogenase2 connects lipid catabolism to photosynthesis through redox coupling in Chlamydomonas

Plant Cell

The CO2 concentrating mechanism and photosynthetic carbon assimilation in limiting CO2: how Chlamydomonas works against the gradient

Plant J.

Adaptation of tobacco plants to elevated CO2: influence of leaf age on changes in physiology, redox states and NADP-malate dehydrogenase activity

J. Exp. Bot.

Was low CO2 a driving force of C4 evolution: Arabidopsis responses to long-term low CO2 stress

J. Exp. Bot.

Impairment of the photorespiratory pathway accelerates photoinhibition of photosystem ii by suppression of repair but not acceleration of damage processes in Arabidopsis

Plant Physiol.

The Arabidopsis mutant dct is deficient in the plastidic glutamate/malate translocator DiT2

Plant J.

Identifying and characterizing plastidic 2-oxoglutarate/malate and dicarboxylate transporters in Arabidopsis thaliana

Plant Cell Physiol.

Reduced mitochondrial malate dehydrogenase activity has a strong effect on photorespiratory metabolism as revealed by 13C labelling

J. Exp. Bot.

Carbon dioxide enrichment inhibits nitrate assimilation in wheat and arabidopsis

Review
Physiological functions of malate shuttles in plants and algae

Alternative electron pathways of photosynthesis drive the algal CO₂ concentrating mechanism

Putative role of the malate valve enzyme NADP–malate dehydrogenase in H₂O₂ signalling in Arabidopsis

The CO₂ concentrating mechanism and photosynthetic carbon assimilation in limiting CO₂: how Chlamydomonas works against the gradient

Adaptation of tobacco plants to elevated CO₂: influence of leaf age on changes in physiology, redox states and NADP-malate dehydrogenase activity

Was low CO₂ a driving force of C4 evolution: Arabidopsis responses to long-term low CO₂ stress

Peroxisomal malate dehydrogenase is not essential for photorespiration in arabidopsis but its absence causes an increase in the stoichiometry of photorespiratory CO₂ release

Knockdown of limiting-CO₂-induced gene HLA3 decreases HCO₃⁻ transport and photosynthetic Ci affinity in Chlamydomonas reinhardtii

Acclimation to very low CO₂: contribution of limiting CO₂ inducible proteins, LCIB and LCIA, to inorganic carbon uptake in Chlamydomonas reinhardtii

Thylakoid localized bestrophin-like proteins are essential for the CO₂ concentrating mechanism of Chlamydomonas reinhardtii