Respiration and Carbon Assimilate Use

Respiration is the primary process linking the assimilation of C and energy during photosynthesis with their use in growth, maintenance, transport, and nutrient acquisition. Respiration generates usable energy, reductant, and in­ termediates (C skeletons) from an array of substrates and releases CO2 and heat as bypro ducts (Beevers, 1961). James (1971) wrote, "nothing in [living] cells happens without the support of their respiration." Thus, crop growth and productivity are functions of respiration as well as of photosynthesis and morphogenesis, with up to one-half of the C assimilated by crops in pho­ tosynthesis (less photorespiration) subsequently "lost" as respiratory CO2 (Table 9A-l). Because respiration is a large component of a crop's C balance, it is important to understand how the rate of respiration is controlled, how respiration is related to growth (are the two coupled?), and whether respira­ tion in crops is operating as efficiently as its biochemistry allows. In this chapter, the pathways of respiration, the stoichiometries of respiratory substrate consumption and end-product generation, and the meta­ bolic controls of respiration are outlined. The growth and maintenance model of respiration and physiological controls of respiration rate also are reviewed. Measured respiration rates are compared to rates predicted from analyses of the underlying biochemistry. The difference between these rates is an in­ dication of the gains that might be made in crop growth as a result of using respiratory rate and efficiency as breeding program selection criteria. The coordinated activities of glycolysis, the oxidative pentose phosphate ­ (OPP) network, the tricarboxylic acid (TCA) cycle, the respiratory chain, oxidative phosphorylation, and associated metabolism makeup respiration (Beevers, 1961; Douce, 1985). Respiratory reactions do not operate in isola­ tion from the rest of metabolism; many other pathways branch from and converge on respiration, as befits a process central to the whole of metabolism. The starting point (i.e., initial substrate) of plant respiration is variable. In a photosynthetically active cell, triose-P leaving chloroplasts can enter glycolysis and the OPP network in the cytosol directly. In germinat-

[1]  H. Mooney,et al.  Estimation of tissue construction cost from heat of combustion and organic nitrogen content , 1987 .

[2]  D. Davies Physiological Aspects of Protein Turnover , 1982 .

[3]  David T. Clarkson,et al.  Factors Affecting Mineral Nutrient Acquisition by Plants , 1985 .

[4]  A. Hanson,et al.  Betaine Synthesis and Accumulation in Barley During Field Water‐Stress1 , 1982 .

[5]  K. Brouwer,et al.  Alternative Path Mediated ATP Synthesis in Roots of Pisum sativum upon Nitrogen Supply. , 1986, Plant physiology.

[6]  O. Jardetzky,et al.  Measurement of mitochondrial ATPase activity in maize root tips by saturation transfer p nuclear magnetic resonance. , 1984, Plant physiology.

[7]  B. Meeuse Thermogenic Respiration in Aroids , 1975 .

[8]  J. Mahon Root and nodule respiration in relation to acetylene reduction in intact nodulated peas. , 1977, Plant physiology.

[9]  K. J. Mccree Carbon Balance as a function of Plant Size in Sorghum Plants 1 , 1983 .

[10]  R. Huffaker Proteolytic activity during senescence of plants. , 1990, The New phytologist.

[11]  J. Thornley,et al.  Respiration, Growth and Maintenance in Plants , 1970, Nature.

[12]  I. Dry,et al.  Partial Purification and Characterization of Complex I, NADH:Ubiquinone Reductase, from the Inner Membrane of Beetroot Mitochondria. , 1992, Plant physiology.

[13]  H. H. Laar,et al.  Products, requirements and efficiency of biosynthesis: a quantitative approach. , 1974, Journal of theoretical biology.

[14]  R. B. Austin,et al.  The Fate of the Dry Matter, Carbohydrates and 14C Lost from the Leaves and Stems of Wheat during Grain Filling , 1977 .

[15]  J. Yamaguchi Respiration and the growth efficiency in relation to crop productivity , 1978 .

[16]  H. Lambers Respiration in Intact Plants and Tissues: Its Regulation and Dependence on Environmental Factors, Metabolism and Invaded Organisms , 1985 .

[17]  D. Wilson,et al.  Effect of Selection for Dark Respiration Rate of Mature Leaves on Crop Yields of Lolium perenne cv. S23 , 1982 .

[18]  D. Wilson Response to Selection for Dark Respiration Rate of Mature Leaves in Lolium perenne and its Effects on Growth of Young Plants and Simulated Swards , 1982 .

[19]  K. Mccree,et al.  An equation for the rate of respiration of white clover grown under controlled conditions. , 1970 .

[20]  K. Wohl,et al.  THE ENERGY CHANGES ASSOCIATED WITH PLANT RESPIRATION , 1942 .

[21]  T. Rees The Organization of Glycolysis and the Oxidative Pentose Phosphate Pathway in Plants , 1985 .

[22]  D. Graham Effects of Light on “Dark” Respiration , 1980 .

[23]  D. Wilson Variation in leaf respiration in relation to growth and photosynthesis of Lolium , 1975 .

[24]  S. S. Sung,et al.  A reassessment of glycolysis and gluconeogenesis in higher plants , 1988 .

[25]  M. R. Thorpe,et al.  Further Evidence of Apoplastic Unloading into the Stem of Bean: Identification of the Phloem Buffering Pool , 1984 .

[26]  I. Dry,et al.  Regulation of Mitochondrial Respiration , 1987 .

[27]  P. Nobel,et al.  Growth respiration, maintenance respiration and structural-carbon costs for roots of three desert succulents , 1992 .

[28]  E. H. Roberts,et al.  Carbon and nitrogen nutrition of nodulated roots of grain legumes , 1981 .

[29]  F. D. Vries,et al.  The cost of maintenance processes in plant cells , 1975 .

[30]  J. T. Madison,et al.  Turnover of Storage Protein in Seeds of Soya Bean and Pea , 1981 .

[31]  A. L. Christy,et al.  Carbohydrate translocation in sugar beet petioles in relation to petiolar respiration and adenosine 5'-triphosphate. , 1972, Plant physiology.

[32]  A. Galston Plant Physiology , 1967, Nature.

[33]  D A Day,et al.  Regulation of alternative pathway activity in plant mitochondria: nonlinear relationship between electron flux and the redox poise of the quinone pool. , 1989, Archives of biochemistry and biophysics.

[34]  N. L. Crapo,et al.  METABOLIC PRIORITIES WITH RESPECT TO GROWTH AND MINERAL UPTAKE IN ROOTS OF HORDEUM, TRITICUM AND LYCOPERSICON , 1981 .

[35]  J. Thornley,et al.  Energy Requirements for Assimilate Translocation from Mature Tomato Leaves , 1978 .

[36]  I. Dry,et al.  The Tricarboxylic Acid Cycle in Plant Mitochondria: Its Operation and Regulation , 1985 .

[37]  S. Pirt The maintenance energy of bacteria in growing cultures , 1965, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[38]  J. Amthor,et al.  Higher Plant Respiration and Its Relationships to Photosynthesis , 1995 .

[39]  R. K. Scott,et al.  Barley and its Environment. III. Carbon Budget of the Stand , 1975 .

[40]  A. Hawkins Protein Turnover: A Functional Appraisal , 1991 .

[41]  D. N. Baker,et al.  Simulation of Growth and Yield in Cotton: Respiration and the Carbon Balance 1 , 1971 .

[42]  P. Rich,et al.  Organization of the Respiratory Chain and Oxidative Phosphorylation , 1985 .

[43]  J. Farrar,et al.  Control of barley root respiration , 1990 .

[44]  J. Amthor Plant respiratory responses to the environment and their effects on the carbon balance , 1994 .

[45]  M. Osaki,et al.  Growth and behavior of photosynthesized 14C in various crops in relation to productivity , 1983 .

[46]  H. Gawrońska,et al.  Partitioning of Photoassimilates by Four Potato Clones 1 , 1984 .

[47]  H. Lambers,et al.  Regulation of Respiration in the Leaves and Roots of Two Lolium perenne Populations with Contrasting Mature Leaf Respiration Rates and Crop Yields. , 1985, Plant physiology.

[48]  S. Huber Biochemical Mechanism for Regulation of Sucrose Accumulation in Leaves during Photosynthesis. , 1989, Plant physiology.

[49]  J. Hesketh,et al.  Photosynthesis Under Field Conditions. IV. Light Studies with Individual Corn Leaves 1 , 1962 .

[50]  M. Stitt,et al.  Regulation of glycolysis in heterotrophic cell suspension cultures of Chenopodium rubrum in response to proton fluxes at the plasmalemma , 1991 .

[51]  C. Roumet,et al.  Why and how to estimate the cost of symbiotic N2 fixation? A progressive approach based on the use of 14C and l5N isotopes , 1989 .

[52]  A. Moore,et al.  Role of nonohmicity in the regulation of electron transport in plant mitochondria. , 1989, Plant physiology.

[53]  B. Strain,et al.  Root restriction as a factor in photosynthetic acclimation of cotton seedlings grown in elevated carbon dioxide. , 1991, Plant physiology.

[54]  Estimated Drainage of Carbon from the Tricarboxylic Acid Cycle for Protein Synthesis in Suspension Cultures of Paul's Scarlet Rose Cells. , 1976, Plant physiology.

[55]  M. Monsi,et al.  Physiological and Ecological Analyses of Shade Tolerance of Plants , 1961 .

[56]  M. Steer Plasma Membrane Turnover in Plant Cells , 1988 .

[57]  4 – The Regulation of Glycolysis and the Pentose Phosphate Pathway , 1987 .

[58]  M. Robson The Growth and Carbon Economy of Selection Lines of Lolium perenne cv. S23 with Differing Rates of Dark Respiration 1. Grown as Simulated Swards During a Regrowth Period , 1982 .

[59]  I. R. Johnson Plant respiration in relation to growth, maintenance, ion uptake and nitrogen assimilation , 1990 .

[60]  H. D. Cooper,et al.  Metabolism and translocation of nitrogen in two Lolium perenne populations with contrasting rates of mature leaf respiration and yield , 1988 .

[61]  T. Rees Assessment of the Contributions of Metabolic Pathways to Plant Respiration , 1980 .

[62]  R. Douce,et al.  THE UNIQUENESS OF PLANT MITOCHONDRIA , 1989 .

[63]  T. Bouma,et al.  Energy cost of protein turnover: theorectical calculation and experimental estimation from regression of respiration on protein concentration of fulle-grown leaves , 1992 .

[64]  T. Rees,et al.  1 – Hexose Phosphate Metabolism by Nonphotosynthetic Tissues of Higher Plants , 1988 .

[65]  P. Srere,et al.  Complexes of sequential metabolic enzymes. , 1987, Annual review of biochemistry.

[66]  L. A. Hunt,et al.  GENOTYPIC DIFFERENCES IN DARK RESPIRATION OF MATURE LEAVES IN WINTER WHEAT (Triticum aestivum L.) , 1988 .

[67]  H. H. Laar,et al.  Substrate utilization in germinating seeds , 1977 .

[68]  J. Palmer,et al.  Measurements of Proton Pumping in Arum maculatum Mitochondria. , 1988, Plant physiology.

[69]  A. Herold REGULATION OF PHOTOSYNTHESIS BY SINK ACTIVITY–THE MISSING LINK , 1980 .

[70]  I. Bingham,et al.  Activity and capacity of respiratory pathways in barley roots deprived of inorganic nutrients , 1989 .

[71]  I. Dry,et al.  Regulation of Alternative Pathway Activity in Plant Mitochondria : Deviations from Q-Pool Behavior during Oxidation of NADH and Quinols. , 1991, Plant physiology.

[72]  H. Berge,et al.  Simulation of Ecophysiological Processes of Growth in Several Annual Crops , 1989 .

[73]  R. Grange,et al.  Carbon partitioning and export from mature cotton leaves. , 1991, Plant physiology.

[74]  J. Raven The Quantitative Role of ‘Dark’ Respiratory Processes in Heterotrophic and Photolithotrophic Plant Growth , 1976 .

[75]  I. R. Johnson,et al.  Plant and Crop Modelling: A Mathematical Approach to Plant and Crop Physiology , 1990 .

[76]  A. Tanaka,et al.  The growth efficiency in relation to the growth of the rice plant , 1968 .

[77]  J. Pate,et al.  1 – Energetics and Biological Costs of Nitrogen Assimilation , 1990 .

[78]  A. James,et al.  The kinetics of NADH oxidation by complex I of isolated plant mitochondria , 1990 .

[79]  H. Beevers Respiration in plants and its regulation , 1970 .

[80]  H. Beevers Respiratory metabolism in plants , 1961 .

[81]  C. Foyer FEEDBACK INHIBITION OF PHOTOSYNTHESIS THROUGH SOURCE-SINK REGULATION IN LEAVES , 1988 .

[82]  T. Larue,et al.  Root respiration associated with nitrate assimilation by cowpea. , 1986, Plant physiology.

[83]  C. Brady,et al.  Respiration and protein synthesis in nongrowing cultured pear fruit cells in response to ethylene and modified atmospheres: a model system for fruits postharvest. , 1988, Plant physiology.

[84]  R. Loomis,et al.  Calculation of growth yield, growth respiration and heat content of grain sorghum from elemental and proximal analyses , 1988 .

[85]  J. Palmer,et al.  The Oxidation of NADH by Plant Mitochondria , 1985 .

[86]  T. Goodwin,et al.  Introduction to plant biochemistry , 1972 .

[87]  J. Palmer THE ORGANIZATION AND REGULATION OF ELECTRON TRANSPORT IN PLANT MITOCHONDRIA , 1976 .

[88]  H. Beevers Conceptual developments in metabolic control, 1924-1974. , 1974, Plant physiology.

[89]  R. Douce Mitochondria in higher plants , 1985 .

[90]  P. Ruckenbauer Photosynthetic and translocation pattern in contrasting winter wheat varieties , 1975 .