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Estimation of diffusive resistance of bundle sheath cells to CO2 from modeling of C4 photosynthesis

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Abstract

Bundle sheath resistance to diffusion of CO2 (rc) is a critical component of C4 photosynthesis which allows accumulation of inorganic carbon in bundle sheath cells of C4 plants. Several analyses were made to evaluate the magnitude of rc in C4 plants. Experimental data on the O2 inhibition of photosynthesis (Dai et al. (1993) Plant Physiol 103: 83–90; (1995) Plant Physiol 107: 815–825) and rates of photorespiration (de Veau and Burris (1989) Plant Physiol 90: 500–511) in Z. mays at different stages of development were analyzed using mathematical models of C4 photosynthesis. In young and senescing leaves modeled values of rc and the CO2 partial pressure in bundle sheath cells (Cbs) were lower and fractional leakage of CO2 from bundle sheath cells (fL) was higher than in mature leaves. Diffusive resistance of bundle sheath cells of C4 plants was also evaluated by analyzing the response of photosynthetic rates to varying CO2 in Amaranthus edulis in which the C4 cycle was dysfunctional by chemical mutagenesis (Dever et al. (1995) J Exp Bot 46: 1363–1376) and in Sorghum bicolor, Panicum maximum and Panicum miliaceum in which the C4 cycle was chemically inhibited (Brown and Byrd (1993) Plant Physiol 103: 1183–1188). These analyses indicate that in mature leaves of C4 plants the values of rc are substantially lower (ca. 50–200 m2 s mol−1) than previous suggested (ca. 500–1500 m2 s mol−1) for C4 photosynthesis and that there is considerable leakage of CO2 from bundle sheath cells. Nevertheless, rc and Cbs values are sufficiently high in mature leaves to minimize photorespiration in C4 plants under normal levels of CO2.

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Abbreviations

DCDP-:

3,3-dichloro-2-(dihydroxyphosphinoylmethyl)-propenoate

PEPcase-:

phosphoenolpyruvate carboxylase

Rubisco-:

ribulose 1,5-bisphosphate carboxylase/oxygenase

VPD-:

vapor pressure deficit between the leaf and atmosphere. See Table 1 for definitions of other symbols used in the paper

References

  • Berry JA and Farquhar GD (1978) The CO2 concentrating function of C4 photosynthesis: A biochemical model. In: Hall D, Coombs J and Goodwin T (eds) Proceedings of the 4th International Congress on Photosynthesis, pp 119–131 Biochemical Society, London

    Google Scholar 

  • Brown R and Byrd G (1993) Estimation of bundle sheath cell conductance in C4 species and O2 insensitivity of photosynthesis. Plant Physiol 103: 1183–1188

    Google Scholar 

  • Chen D, Coughenour MB, Knapp AK and Owensby CE (1994) Mathematical simulation of C4 grass photosynthesis in ambient and elevated CO2. Ecol Modelling 73: 63–80

    Google Scholar 

  • Chollet R and Ogren WL (1975) Regulation of photorespiration in C3 and C4 species. Bot Rev 41: 137–179

    Google Scholar 

  • Collatz GJ, Ribas-Carbo M and Berry JA (1992) Coupled photosynthesis-stomatal conductance model for leaves of C4 plants. Aust J Plant Physiol 19: 519–538

    Google Scholar 

  • Dai Z, Ku MSB and Edwards GE (1993) C4 photosynthesis. The CO2-concentrating mechanism and photorespiration. Plant Physiol 103: 83–90

    Google Scholar 

  • Dai Z, Ku MSB and Edwards GE (1995) C4 photosynthesis. The effect of leaf development on the CO2-concentrating mechanism and photorespiration in Z. mays. Plant Physiol 107: 815–825

    Google Scholar 

  • Dai Z, Ku MSB and Edwards GE (1996) Oxygen sensitivity of photosynthesis in C3, C4, and C3–C4 intermediate species of Flaveria. Planta 198: 563–571

    Google Scholar 

  • de Veau EJ and Burris JE (1989) Photorespiratory rates in wheat and Z. mays as determined by 18O-labeling. Plant Physiol 90: 500–511

    Google Scholar 

  • Dever LV, Blackwell RD, Fullwood NJ, Lacuesta M, Leegood RC, Onek LA, Pearson M and Lea PJ (1995) The isolation and characterization of mutants of the C4 photosynthetic pathway. J Exp Bot 46: 1363–1376

    Google Scholar 

  • Edwards GE and Walker D (1983) C3, C4: Mechanisms, and Cellular and Environmental Regulation, of Photosynthesis. Blackwell, Oxford, UK

    Google Scholar 

  • Edwards GE Nakamoto H, Burnell JN and Hatch MD (1985) Pyruvate, Pi dikinase and NADP-malate dehydrogenase in C4 photosynthesis: Properties and mechanism of light/dark regulation. Ann Rev Plant Physiol 36: 255–286

    Google Scholar 

  • Evans JR, Sharkey TD, Berry JA and Farquhar GD (1986) Carbon isotope discrimination measured concurrently with gas-exchange to investigate CO2 diffusion in leaves of higher plants. Aust J Plant Physiol 13: 281–292

    Google Scholar 

  • Farquhar GD (1983) On the nature of carbon isotope discrimination in C4 species. Aust J Plant Physiol 10: 205–226

    Google Scholar 

  • Farquhar GD, von Caemmerer S and Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149: 78–90

    Google Scholar 

  • Furbank R, Jenkins C and Hatch M (1989) CO2 concentrating mechanism of C4 photosynthesis. Permeability of isolated bundle sheath cells to inorganic carbon. Plant Physiol 91: 1364–1371

    Google Scholar 

  • Furbank R and Hatch MD (1987) Mechanism of C4 photosynthesis. The size and composition of the inorganic carbon pool in bundle sheath cells, Plant Physiol 85: 958–964

    Google Scholar 

  • Hatch MD (1971) The C4 pathway of photosynthesis: evidence for an intermediate pool of carbon dioxide and the identity of the donor C4 acid. Biochem J 125: 425–432

    Google Scholar 

  • Hatch MD, Agostino A and Jenkins CLD (1995) Measurement of the leakage of CO2 from bundle-sheath cells of leaves during C4 photosynthesis. Plant Physiol 108: 173–181

    Google Scholar 

  • Henderson SA, von Caemmerer S and Farquhar GD (1992) Shortterm measurements of carbon isotope discrimination in several C4 species. Aust J Plant Physiol 19: 263–285

    Google Scholar 

  • Hesketh J (1967) Enhancement of photosynthetic CO2 assimilation in the absence of oxygen, as dependent upon species and temperature. Planta 76: 371–374

    Google Scholar 

  • Jenkins CLD (1989) Effects of the phosphoenolpyruvate carboxylase inhibitor 3,3-dichloro-2-(dihydroxyphosphinoylmethyl) propenoate on photosynthesis. C4 selectivity and studies on C4 photosynthesis. Plant Physiol 89: 1231–1237

    Google Scholar 

  • Jenkins CD, Furbank R and Hatch M (1989a) Mechanism of C4 photosynthesis. A model describing the inorganic carbon pool in bundle sheath cells. Plant Physiol 91: 1372–1381

    Google Scholar 

  • Jenkins C, Furbank R and Hatch M (1989b) Inorganic carbon diffusion between C4 mesophyll and bundle sheath cells. Direct bundle sheath CO2 assimilation in intact leaves in the presence of an inhibitor of the C4 pathway. Plant Physiol 91: 1356–1363

    Google Scholar 

  • Jordan DB and Ogren WL (1984) The CO2/O2 specificity or ribulose 1,5-bisphosphate carboxylase/oxygenase. Dependence on ribulose bisphosphate concentration, pH and temperature. Planta 161: 308–313

    Google Scholar 

  • Long SP (1991) Modification of the response of photosynthetic productivity to rising temperature by atmospheric CO2 concentrations: Has its importance been underestimated? Plant Cell Environ 14: 729–739

    Google Scholar 

  • Pfeffer M and Peisker M (1995) In vivo Km for CO2 (Kp) of phospho-enolpyruvate carboxylase (PEPC) and mesophyll CO2 transport resistance (rm) in leaves of Zea mays L. In: P Mathis (ed) Photosynthesis: From Light to Biosphere V, pp 547–550. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Sage RF and Sharkey TD (1987) The effect of temperature on the occurrence of O2 and CO2 insensitive photosynthesis in field grown plants. Plant Physiol 84: 658–664

    Google Scholar 

  • Usuda H, Ku MSB and Edwards GE (1984) Rates of photosynthesis relative to activity of photosynthetic enzymes, chlorophyll, and soluble protein content among ten C4 species. Aust J Plant Physiol 11: 509–518

    Google Scholar 

  • Woodrow IE and Berry JA (1988) Enzymatic regulation of photosynthetic CO2 fixation in C3 plants. Ann Rev Plant Physiol Plant Mol Biol 39: 533–594

    Google Scholar 

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He, D., Edwards, G.E. Estimation of diffusive resistance of bundle sheath cells to CO2 from modeling of C4 photosynthesis. Photosynth Res 49, 195–208 (1996). https://doi.org/10.1007/BF00034781

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