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PMID: 21441385 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The mechanistic basis of internal conductance: a theoretical analysis of mesophyll cell photosynthesis and CO2 diffusion.

Plant physiology ·Vol. 156 ·No. 1 ·2011-05-00 ·Pages 90-105

Tholen D, Zhu XG

Abstract

Photosynthesis is limited by the conductance of carbon dioxide (CO(2)) from intercellular spaces to the sites of carboxylation. Although the concept of internal conductance (g(i)) has been known for over 50 years, shortcomings in the theoretical description of this process may have resulted in a limited understanding of the underlying mechanisms. To tackle this issue, we developed a three-dimensional reaction-diffusion model of photosynthesis in a typical C(3) mesophyll cell that includes all major components of the CO(2) diffusion pathway and associated reactions. Using this novel systems model, we systematically and quantitatively examined the mechanisms underlying g(i). Our results identify the resistances of the cell wall and chloroplast envelope as the most significant limitations to photosynthesis. In addition, the concentration of carbonic anhydrase in the stroma may also be limiting for the photosynthetic rate. Our analysis demonstrated that higher levels of photorespiration increase the apparent resistance to CO(2) diffusion, an effect that has thus far been ignored when determining g(i). Finally, we show that outward bicarbonate leakage through the chloroplast envelope could contribute to the observed decrease in g(i) under elevated CO(2). Our analysis suggests that physiological and anatomical features associated with g(i) have been evolutionarily fine-tuned to benefit CO(2) diffusion and photosynthesis. The model presented here provides a novel theoretical framework to further analyze the mechanisms underlying diffusion processes in the mesophyll.

MeSH Terms
Carbon Dioxide/metabolism Cell Wall/metabolism Chlorophyll/metabolism Chloroplasts/metabolism Diffusion Light Mesophyll Cells/physiology,radiation effects Models, Biological Oxygen/metabolism Photosynthesis/physiology Plant Leaves/metabolism Plant Stomata/metabolism
Chemicals
Chlorophyll Carbon Dioxide Oxygen
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Tholen Danny
Chinese Academy of Sciences and Max Planck Society Partner Institute for Computational Biology, Key Laboratory of Computational Biology, Shanghai 200031, People's Republic of China.
Zhu Xin-Guang
References (57)
57 references, click to expand
  1. Mesophyll conductance to CO2: current knowledge and future prospects.
    Plant Cell Environ. 2008 May;31(5):602-21 PMID: 17996013
  2. Irradiance and phenotype: comparative eco-development of sun and shade leaves in relation to photosynthetic CO2 diffusion.
    J Exp Bot. 2006;57(2):343-54 PMID: 16356943
  3. Characterization of CO2/carbonic acid mediated proton flux through phosphatidylcholine vesicles as model membranes.
    Biochim Biophys Acta. 1992 Oct 19;1111(1):17-26 PMID: 1327142
  4. Plant Carbonic Anhydrases: II. Preparation and Some Properties of Monocotyledon and Dicotyledon Enzyme Types.
    Plant Physiol. 1972 Aug;50(2):218-23 PMID: 16658145
  5. Stand aside stomata, another actor deserves centre stage: the forgotten role of the internal conductance to CO2 transfer.
    J Exp Bot. 2008;59(7):1475-87 PMID: 17975206
  6. Variation in the k(cat) of Rubisco in C(3) and C(4) plants and some implications for photosynthetic performance at high and low temperature.
    J Exp Bot. 2002 Apr;53(369):609-20 PMID: 11886880
  7. Subcellular distribution of carbonic anhydrase in Solanum tuberosum L. leaves: characterization of two compartment-specific isoforms.
    Planta. 1996;199(1):79-88 PMID: 8680307
  8. Effect of local irradiance on CO(2) transfer conductance of mesophyll in walnut.
    J Exp Bot. 2002 Dec;53(379):2423-30 PMID: 12432034
  9. Facilitated transport of CO(2) across a membrane bearing carbonic anhydrase.
    FEBS Lett. 1970 Apr 16;7(3):223-226 PMID: 11947477
  10. Using tunable diode laser spectroscopy to measure carbon isotope discrimination and mesophyll conductance to CO₂ diffusion dynamically at different CO₂ concentrations.
    Plant Cell Environ. 2011 Apr;34(4):580-91 PMID: 21251018
  11. Plant Carbonic Anhydrases: I. Distribution of Types among Species.
    Plant Physiol. 1972 Aug;50(2):214-7 PMID: 16658144
  12. Potential errors in electron transport rates calculated from chlorophyll fluorescence as revealed by a multilayer leaf model.
    Plant Cell Physiol. 2009 Apr;50(4):698-706 PMID: 19282373
  13. Light and CO2 do not affect the mesophyll conductance to CO2 diffusion in wheat leaves.
    J Exp Bot. 2009;60(8):2291-301 PMID: 19255060
  14. Mesophyll conductance to CO(2) transport estimated by two independent methods: effect of variable CO(2) concentration and abscisic acid.
    J Exp Bot. 2009;60(8):2315-23 PMID: 19433478
  15. Plant carbonic anhydrase. Properties and carbon dioxide hydration kinetics.
    Biochemistry. 1973 Dec 4;12(25):5127-34 PMID: 4210017
  16. The lack of mitochondrial complex I in a CMSII mutant of Nicotiana sylvestris increases photorespiration through an increased internal resistance to CO2 diffusion.
    J Exp Bot. 2006;57(12):3195-207 PMID: 16945981
  17. Overexpression of the barley aquaporin HvPIP2;1 increases internal CO(2) conductance and CO(2) assimilation in the leaves of transgenic rice plants.
    Plant Cell Physiol. 2004 May;45(5):521-9 PMID: 15169933
  18. Variability in mesophyll conductance between barley genotypes, and effects on transpiration efficiency and carbon isotope discrimination.
    Plant Cell Environ. 2010 Jul;33(7):1176-85 PMID: 20199618
  19. Rubisco in planta kcat is regulated in balance with photosynthetic electron transport.
    J Exp Bot. 2009;60(14):4077-88 PMID: 19661266
  20. Kinetics of bicarbonate-chloride exchange across the human red blood cell membrane.
    J Gen Physiol. 1976 Dec;68(6):633-52 PMID: 993774
  21. Rapid variations of mesophyll conductance in response to changes in CO2 concentration around leaves.
    Plant Cell Environ. 2007 Oct;30(10):1284-98 PMID: 17727418
  22. Restrictions to carbon dioxide conductance and photosynthesis in spinach leaves recovering from salt stress
    Plant Physiol. 1999 Mar;119(3):1101-6 PMID: 10069849
  23. Resistances along the CO2 diffusion pathway inside leaves.
    J Exp Bot. 2009;60(8):2235-48 PMID: 19395390
  24. Elevated CO2 induces physiological, biochemical and structural changes in leaves of Arabidopsis thaliana.
    New Phytol. 2006;172(1):92-103 PMID: 16945092
  25. Models of photosynthesis.
    Plant Physiol. 2001 Jan;125(1):42-5 PMID: 11154292
  26. Estimating mesophyll conductance to CO2: methodology, potential errors, and recommendations.
    J Exp Bot. 2009;60(8):2217-34 PMID: 19357431
  27. Molecular cloning and biochemical characterization of carbonic anhydrase from Populus tremula x tremuloides.
    Plant Mol Biol. 1997 Jul;34(4):583-92 PMID: 9247540
  28. Temperature response of mesophyll conductance. Implications for the determination of Rubisco enzyme kinetics and for limitations to photosynthesis in vivo.
    Plant Physiol. 2002 Dec;130(4):1992-8 PMID: 12481082
  29. Effects of internal conductance on the temperature dependence of the photosynthetic rate in spinach leaves from contrasting growth temperatures.
    Plant Cell Physiol. 2006 Aug;47(8):1069-80 PMID: 16816408
  30. Carbon Dioxide Diffusion inside Leaves.
    Plant Physiol. 1996 Feb;110(2):339-346 PMID: 12226185
  31. Low carbon dioxide permeability of the apical epithelial membrane of guinea-pig colon.
    J Physiol. 2005 Aug 15;567(Pt 1):253-65 PMID: 15932894
  32. Leaf functional anatomy in relation to photosynthesis.
    Plant Physiol. 2011 Jan;155(1):108-16 PMID: 21075960
  33. Accumulation of bicarbonate in intact chloroplasts following a pH gradient.
    Biochim Biophys Acta. 1972 Dec 14;283(3):430-41 PMID: 4630890
  34. Dynamics, structure, and function are coupled in the mitochondrial matrix.
    Proc Natl Acad Sci U S A. 1991 Sep 15;88(18):8057-61 PMID: 1896451
  35. Using combined measurements of gas exchange and chlorophyll fluorescence to estimate parameters of a biochemical C photosynthesis model: a critical appraisal and a new integrated approach applied to leaves in a wheat (Triticum aestivum) canopy.
    Plant Cell Environ. 2009 May;32(5):448-64 PMID: 19183300
  36. Nonequilibrium facilitated transport of carbon dioxide in bicarbonate and bovine albumin solutions.
    Ann Biomed Eng. 1986;14(6):493-511 PMID: 3103500
  37. Diffusion of carbon dioxide through lipid bilayer membranes: effects of carbonic anhydrase, bicarbonate, and unstirred layers.
    J Gen Physiol. 1977 Jun;69(6):779-94 PMID: 408462
  38. Intercellular Diffusion Limits to CO(2) Uptake in Leaves : Studies in Air and Helox.
    Plant Physiol. 1990 Nov;94(3):1024-32 PMID: 16667792
  39. Characteristics of light-dependent inorganic carbon uptake by isolated spinach chloroplasts.
    Plant Physiol. 1984 Apr;74(4):962-6 PMID: 16663542
  40. Measurement of cytosolic, mitochondrial, and Golgi pH in single living cells with green fluorescent proteins.
    Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):6803-8 PMID: 9618493
  41. Function of Nicotiana tabacum aquaporins as chloroplast gas pores challenges the concept of membrane CO2 permeability.
    Plant Cell. 2008 Mar;20(3):648-57 PMID: 18349152
  42. 110 years of the Meyer-Overton rule: predicting membrane permeability of gases and other small compounds.
    Chemphyschem. 2009 Jul 13;10(9-10):1405-14 PMID: 19514034
  43. Diffusion coefficients of CO2 molecule and bicarbonate ion in hemoglobin solution measured by fluorescence technique.
    Jpn J Physiol. 1983;33(4):619-34 PMID: 6417383
  44. Plant carbonic anhydrase. Properties and bicarbonate dehydration kinetics.
    Biochemistry. 1978 Mar 21;17(6):1119-25 PMID: 415758
  45. Tobacco aquaporin NtAQP1 is involved in mesophyll conductance to CO2 in vivo.
    Plant J. 2006 Nov;48(3):427-39 PMID: 17010114
  46. Theoretical Considerations when Estimating the Mesophyll Conductance to CO(2) Flux by Analysis of the Response of Photosynthesis to CO(2).
    Plant Physiol. 1992 Apr;98(4):1429-36 PMID: 16668811
  47. Internal conductance to CO(2) diffusion and C(18)OO discrimination in C(3) leaves.
    Plant Physiol. 2000 May;123(1):201-14 PMID: 10806237
  48. Estimation of Mesophyll Conductance to CO(2) Flux by Three Different Methods.
    Plant Physiol. 1992 Apr;98(4):1437-43 PMID: 16668812
  49. Soil water deficits decrease the internal conductance to CO2 transfer but atmospheric water deficits do not.
    J Exp Bot. 2008;59(2):327-34 PMID: 18238801
  50. Influence of leaf dry mass per area, CO2, and irradiance on mesophyll conductance in sclerophylls.
    J Exp Bot. 2009;60(8):2303-14 PMID: 19286919
  51. A model of carbon dioxide assimilation in Chlamydomonas reinhardii.
    Planta. 1985 Jun;164(3):308-20 PMID: 24249600
  52. Improving photosynthetic efficiency for greater yield.
    Annu Rev Plant Biol. 2010;61:235-61 PMID: 20192734
  53. A biochemical model of photosynthetic CO2 assimilation in leaves of C 3 species.
    Planta. 1980 Jun;149(1):78-90 PMID: 24306196
  54. The chloroplast avoidance response decreases internal conductance to CO2 diffusion in Arabidopsis thaliana leaves.
    Plant Cell Environ. 2008 Nov;31(11):1688-700 PMID: 18721264
  55. The diffusion of carbon dioxide in erythrocytes and hemoglobin solutions.
    Pflugers Arch. 1971;324(3):249-66 PMID: 5102608
  56. Carbon metabolism enzymes and photosynthesis in transgenic tobacco (Nicotiana tabacum L.) having excess phytochrome.
    Planta. 1991 Oct;185(3):287-96 PMID: 24186408
  57. Active protein transport through plastid tubules: velocity quantified by fluorescence correlation spectroscopy.
    J Cell Sci. 2000 Nov;113 ( Pt 22):3921-30 PMID: 11058079
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
1532-2548
Published
2011-05-00
Epub
2011-00-25
Pages
90-105
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC3091052
Subset
IM
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