Plant Respiration

Abstract

Plant respiration is the controlled oxidation of energy‐rich photosynthetic end‐products (i.e. starch and sucrose) via the pathways of glycolysis, the tricarboxylic acid (TCA) cycle and mitochondrial electron transport chain, producing CO2 and adenosine triphosphate (ATP). Respiration also generates low‐molecular‐weight ‘building block’ molecules needed as precursors for biosynthesis and nitrogen assimilation. Although most respiratory enzymes are common to all organisms, there are many features unique to plant respiration including the occurrence of parallel glycolytic pathways in the cytosol and plastid, and alternative ‘bypass’ enzymes in cytosolic glycolysis, and the mitochondrial TCA cycle and electron transport chain. These bypasses include glycolytic enzymes that use pyrophosphate instead of ATP and non‐energy‐conserving routes of mitochondrial electron transport. The resulting flexible nature of plant respiratory metabolism represents an essential adaptation that helps sessile plants acclimatise to the many stresses that they are exposed to in their natural environment. Genetic engineering of respiratory metabolism in transgenic plants is providing an important biotechnological approach for improving crop yields and enhancing sustainable agriculture.

Key Concepts

  • Respiration is represented by the combined reactions of glycolysis, the TCA cycle and the miETC.
  • Plant respiration produces ATP as well as biosynthetic precursors needed for growth and various metabolites needed for stress acclimation.
  • Comparing the organisation and control of metabolism between different organisms provides key insights into the two main themes of biology: namely, evolution and adaptation.
  • Carbohydrates are the dominant respiratory substrate in plants, whereas fatty acids are rarely respired.
  • Plant cytosolic glycolysis is a complex network containing alternative enzymatic reactions that circumvent a classical reaction dependent on ATP, ADP or phosphate as a cosubstrate.
  • Alternative PPi‐dependent cytosolic enzymes confer a considerable bioenergetic benefit that extends the survival time of ATP‐depleted plant cells during abiotic stresses such as anoxia or severe phosphate starvation.
  • PEPC is a tightly regulated enzyme situated at a crucial branch point of plant metabolism that controls anaplerotic replenishment of TCA cycle intermediates withdrawn for biosynthesis and N‐assimilation.
  • The operation of the TCA ‘cycle’ is flexible and changes flux modes to suit the needs of the cell.
  • Plants dynamically alter the efficiency of mitochondrial ATP production by their miETC via use of alternate dehydrogenases and oxidases, and UCP, thereby providing additional metabolic flexibility in an ever‐changing and stressful environment.
  • At the ecosystem level, plant respiration has a profound impact on the CO2 concentration in the atmosphere, and is therefore a key component influencing the global carbon cycle and climate change.
  • Metabolic engineering of plant respiration is providing an important approach to enhancing crop yields, as well as a potential mechanism for mitigating global climate change owing to elevated atmospheric CO2 levels.

Keywords: climate change; compartmentation of metabolism; electron transport chain; glycolysis; TCA cycle; mitochondria; pyrophosphate; metabolic flexibility; metabolons; respiration

Figure 1. Simplified overview of the pathways of respiratory carbon metabolism in plants highlighting the existence of interconnected glycolytic pathways in the plastid and the cytosol. Several major metabolic demands require carbon flux through parts the respiratory pathway and are indicated as dashed boxes. The two terminal metabolites of cytosolic glycolysis, malate and pyruvate, are respiratory substrates for the mitochondria, but are also substrates for the formation of 2‐oxoglutarate (2‐OG) required for the assimilation of nitrogen into amino acids (i.e. NH4+ is assimilated into glutamate). The pathway of carbon flux through the tricarboxylic acid (TCA) cycle in support of NH4+ assimilation is shown in grey, and the (cyclic) TCA cycle flux supporting NADH production is shown in black. Plastids from some species do not contain all the glycolytic isozymes necessary for conversion of triose‐phosphates to PEP as denoted by the ‘?’. Dashed lines indicate metabolite transport processes.
Figure 2. (a) Pyrophosphate hydrolysis, like ATP hydrolysis, is an exergonic reaction having a highly negative standard free energy change (ΔGo′). (b) A model highlighting alternative pathways of cytosolic glycolysis that are believed to facilitate plant acclimation to stressful environments. Key components of this model are the unique role played by PPi‐dependent cytosolic bypass enzymes (UDP‐glucose pyrophosphorylase, PPi‐PFK and PPDK) and accompanying reactions as shown in bold. The tonoplast proton‐pumping PPi‐dependent pyrophosphatase (H+‐PPiase) also contributes to ATP conservation under stress. The alternative malic enzyme dependent route of pyruvate production from PEP is shown in grey. Enzymes that catalyse the numbered reactions are as follows: 1, hexokinase; 2, fructokinase; 3, nucleoside diphosphate kinase; 5, phosphoglucose mutase; 6, phosphoglucose isomerase; 7, NAD‐dependent glyceraldehyde‐3‐phosphate dehydrogenase (phosphorylating); 8, NADP‐dependent glyceraldehyde‐3‐phosphate dehydrogenase (nonphosphorylating) and 9, 3‐phosphoglycerate kinase. Abbreviations are as described in the text or as follows: DHAP, dihydroxyacetone‐phosphate; Fru‐1‐P; fructose‐1‐phosphate; Fru‐1,6‐P2; fructose‐1,6‐biphosphate; Fru‐2,6‐P2; fructose‐2,6‐biphosphate; G3P, glyceraldehyde‐3‐phosphate; Glc‐1‐P; glucose‐1‐phosphate and Glc‐6‐P; glucose‐6‐phosphate.
Figure 3. Metabolite effectors act as allosteric activators or inhibitors of key glycolytic enzymes. This simplified model illustrates the central role of phosphoenolpyruvate (PEP) in providing a ‘bottom‐up’ glycolytic control whereby PEP feedback inhibits both ATP‐PFK and PPi‐PFK. The metabolism of PEP by cytosolic pyruvate kinase (PKc) and PEPC is tightly controlled by allosteric effectors, mainly from downstream metabolism, including their reciprocal control by aspartate. Furthermore, the potent glycolytic regulator fructose‐2,6‐biphosphate (Fru‐2,6‐P2) activates PPi‐PFK but does not affect ATP‐PFK. The synthesis of Fru‐2,6‐P2 is in turn controlled by allosteric effectors, of which PEP and other glycolytic intermediates are inhibitors. Dotted arrows with a circled plus and minus sign indicate enzyme activation and inhibition, respectively, by allosteric effectors. Abbreviations are as defined in the legend for Figure.
Figure 4. The pathway of the TCA cycle in plants. Pyruvate is oxidised to CO2 and acetyl‐CoA (AcSCoA), which is then condensed with oxaloacetate to produce citrate. The citrate is further oxidised through the cycle, ultimately yielding two further molecules of CO2 and regenerating the oxaloacetate acceptor. During this process, reducing power is transferred to carriers, primarily NAD+, and one ADP is converted into ATP by the succinyl–CoA ligase reaction. NAD+ is reduced to NADH by the pyruvate dehydrogenase complex, isocitrate dehydrogenase, the 2‐oxoglutarate dehydrogenase complex, malate dehydrogenase and malic enzyme. In addition, NADP+ is converted to NADPH by a specific isozyme of isocitrate dehydrogenase. For clarity, enzyme cofactors have been omitted. Abbreviation: Asp, aspartate.
Figure 5. Organisation of electron transport processes occurring within the inner membrane of plant mitochondria. This illustration provides details of the ‘energy‐conserving’ cytochrome pathway (electrons flow to complex IV), which generates the proton motive force for ATP synthesis by ATP synthase, and the ‘non‐energy‐conserving’ alternative pathway (electrons pass directly to O2 via the alternative oxidase). Complex I oxidises NADH and complex II (succinate dehydrogenase of the TCA cycle) oxidises succinate via FADH2. Alternate, complex I bypassing NAD(P)H dehydrogenases exist on the external (NDext) and internal (NDint) side of the inner membrane. Uncoupling protein (UCP) allows dissipation of proton motive force without ATP synthesis. Abbreviations: UQ, ubiquinone; Cyt C, cytochrome C.
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Further Reading

Bar‐Even‐A FA , Noor E and Milo R (2012) Rethinking glycolysis: on the biochemical logic of metabolic pathways. Nature Chemical Biology 8: 509–517.

Fernie AR , Carrari F and Sweetlove LJ (2004) Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport chain. Current Opinion in Plant Biology 7: 254–261.

Millar AH , Whelan J , Soole KL and Day DA (2011) Organization and regulation of mitochondrial respiration in plants. Annual Review of Plant Biology 62: 79–104.

Millar AH , Siedow JN and Day DA (2015) Respiration and photorespiration. In: Buchanan BB , Gruissem W and Jones RL (eds) Biochemistry and Molecular Biology of Plants, 2nd edn, pp. 610–655. Somerset, NJ: Wiley.

Plaxton WC (2010) Metabolic flexibility helps plants survive stress. A Web‐essay for a web‐site (http://6e.plantphys.net/essay12.01.html) that supplements Chapter 12 (Respiration and Lipid Metabolism). In: Taiz L , Zeiger E , Möller IM and Murphy A (eds) Plant Physiology and Development. Sunderland, MA: Sinauer Associates, Inc.

Rasmusson AG , Geisler DA and Moller IM (2007) The multiplicity of dehydrogenases in the electron transport chain of plant mitochondria. Mitochondrion 8: 47–60.

Sweetlove LJ , Fait A , Nunes‐Nesi A , Williams T and Fernie AR (2008) The mitochondrion: An integration point of cellular metabolism and signalling. Critical Reviews in Plant Sciences 26: 17–43.

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O'Leary, Brendan M, and Plaxton, William C(Apr 2016) Plant Respiration. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001301.pub3]