Photosynthetica 2007, 45(1):75-84 | DOI: 10.1007/s11099-007-0012-6

Differential inhibition of photosynthesis under drought stress in Flaveria species with different degrees of development of the C4 syndrome

M. C. Dias1, W. Brüggemann1,*
1 Department of Botany, J.W. Goethe University, Frankfurt am Main, Germany

The effect of drought stress (DS) on photosynthesis and photosynthesis-related enzyme activities was investigated in F. pringlei (C3), F. floridana (C3-C4), F. brownii (C4-like), and F. trinervia (C4) species. Stomatal closure was observed in all species, probably being the main cause for the decline in photosynthesis in the C3 species under ambient conditions. In vitro ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBPCO) and stromal fructose 1,6-bisphosphatase (sFBP) activities were sufficient to interpret the net photosynthetic rates (P N), but, from the decreases in P N values under high CO2 (C a = 700 µmol mol- 1) it is concluded that a decrease in the in vivo rate of the RuBPCO reaction may be an additional limiting factor under DS in the C3 species. The observed decline in the photosynthesis capacity of the C3-C4 species is suggested to be associated both to in vivo decreases of RuBPCO activity and of the RuBP regeneration rate. The decline of the maximum P N observed in the C4-like species under DS was probably attributed to a decrease in maximum RuBPCO activity and/or to decrease of enzyme substrate (RuBP or PEP) regeneration rates. In the C4 species, the decline of both in vivo photosynthesis and photosynthetic capacity could be due to in vivo inhibition of the phosphoenolpyruvate carboxylase (PEPC) by a twofold increase of the malate concentration observed in mesophyll cell extracts from DS plants.

Additional key words: bundle sheath cells; C3, C4 metabolism; CO2 compensation concentration; malic enzyme; NADP-malate dehydrogenase; phosphoenolpyruvate carboxylase; pyruvate-orthophosphate dikinase; RuBP; RuBPCO; stromal fructose 1,6-bisphosphatase; water potential

Received: January 2, 2006; Accepted: June 16, 2006; Published: March 1, 2007  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Dias, M.C., & Brüggemann, W. (2007). Differential inhibition of photosynthesis under drought stress in Flaveria species with different degrees of development of the C4 syndrome. Photosynthetica, 45(1), 75-84. doi: 10.1007/s11099-007-0012-6
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Berkowitz, G.A.: Water and salt stress.-In: Raghavendra, A.S. (ed.): Photosynthesis. A Comprehensive Treatise. Pp. 226-237. Cambridge University Press, Cambridge 1998.
    2. Berkowitz, G.A., Chen, C., Gibbs, M.: Stromal acidification mediates in vivo water stress inhibition of nonstomatal-controlled photosynthesis.-Plant Physiol. 72: 1123-1126, 1983. Go to original source...
    3. Beyel, V., Brüggemann, W.: Differential inhibition of photosynthesis during pre-flowering drought stress in Sorghum bicolor genotyps with different senescence traits.-Physiol. Plant. 124: 249-259, 2005. Go to original source...
    4. Bläsing, O., Ernst, K.P., Streubel, M., Westhooff, P., Svensson, P.: The non-photosynthetic phosphoenolpyruvate carboxylases of the C4 dicot Flaveria trinervia - implications for the evolution of C4 photosynthesis.-Planta 215: 448-456, 2002. Go to original source...
    5. Boyer, J.S., Wong, S.C., Farquhar, G.D.: CO2 and water vapor exchange across leaf cuticle (epidermis) at various water potentials.-Plant Physiol. 114: 185-191, 1997. Go to original source...
    6. Brüggemann, W., Dauborn, B., Klaucke, S., Linger, P., Maas-Kantel, K., Wenner, A.: Chilling sensitivity of photosynthesis: Ecophysiological studies in two Lycopersicon species of different chilling tolerance.-Acta Physiol. Plant. 17: 113-122, 1995. Go to original source...
    7. Brüggemann, W., Klaucke, S., Maas-Kantel, K.: Long-term chilling of young tomato plants under low light. V. Kinetic and molecular properties of two key enzymes of the Calvin cycle in Lycopersicon esculentum Mill. and L. peruvianum Mill.-Planta 194: 160-168, 1994. Go to original source...
    8. Caemmerer, S. von, Farquhar, G.D.: Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves.-Planta 153: 376-387, 1981. Go to original source...
    9. Caemmerer, S. von, Furbank, R.T.: Modelling C4 photosynthesis.-In: Sage, R.F., Monson, R.K. (ed.): C4 Plant Biology. Pp. 173-211. Academic Press, San Diego 1999. Go to original source...
    10. Casati, P., Fresco, A., Andreo, C., Drincovich, M.F.: An intermediate form of NADP-malic enzyme from the C3-C4 intermediate species Flaveria floridana.-Plant Sci. 147: 101-109, 1999. Go to original source...
    11. Castrillo, M., Fernandez, D., Calcagno, A.M., Trujillo, I., Guenni, L.: Responses of ribulose-1,5-bisphosphate carboxylase, protein content, and stomatal conductance to water deficit in maize, tomato, and bean.-Photosynthetica 39: 221-226, 2001. Go to original source...
    12. Chastain, C., Chollet, R.: Interspecific variation in assimilation of 14CO2 into C4 acids by leaves of C3, C4 and C3-C4 intermediate Flaveria species near the CO2 compensation concentration.-Planta 179: 81-88, 1989. Go to original source...
    13. Chaves, M.M.: Effects of water deficits on carbon assimilation.-J. exp. Bot. 42: 1-16, 1991. Go to original source...
    14. Cheng, S.-H., Moore, B.D., Edwards, G.E., Ku, M.S.B.: Photosynthesis in Flaveria brownii, a C4-like species. Leaf anatomy, characteristics of CO2 exchange, compartmentation of photosynthetic enzymes, and metabolism of 14CO2.-Plant Physiol. 87: 867-873, 1988. Go to original source...
    15. Chollet, R., Vidal, J., O'Leary, M.H.: Phosphoenolpyruvate carboxylase: A ubiquitous, highly regulated enzyme in plants.-Annu. Rev. Plant Physiol. Plant mol. Biol. 47: 273-298, 1996. Go to original source...
    16. Cornic, G.: Drought stress inhibits photosynthesis by decreasing stomatal aperture - not by affecting ATP synthesis.-Trends Plant Sci. 5: 187-188, 2000. Go to original source...
    17. Correia, M.J., Rodrigues, M.L., Osório, M.L., Chaves, M.M.: Effects of growth temperature on the response of lupin stomata to drought and abscisic acid.-Aust. J. Plant Physiol. 26: 549-559, 1999. Go to original source...
    18. Du, Y.C., Kawamitsu, Y., Nose, A., Hiyane, S., Murayama, S., Wasano, K., Uchida, Y.: Effects of water stress on carbon exchange rate and activities of photosynthetic enzymes in leaves of sugarcane (Saccharum sp.).-Aust. J. Plant Physiol. 23: 719-726, 1996. Go to original source...
    19. Du, Y.-C., Nose, A., Wasano, K., Uchida, Y.: Responses to water stress of enzyme activities and metabolite levels in relation to sucrose and starch synthesis, the Calvin cycle and the C4 pathway in sugarcane (Saccharum sp.) leaves.-Aust. J. Plant Physiol. 25: 253-260, 1998. Go to original source...
    20. Edwards, G.E., Furbank, R.T., Hatch, M.D., Osmond, C.B.: What does it take to be C4? Lessons from the evolution of C4 photosynthesis.-Plant Physiol. 125: 46-49, 2001. Go to original source...
    21. Ehleringer, J.R., Sage, R.F., Flanagan, L.B., Pearcy, R.W.: Climate change and the evolution of C4 photosynthesis.-Trends Ecol. Evolut. 6: 95-99, 1991. Go to original source...
    22. Escalona, J.M., Flexas, J., Medrano, H.: Stomatal and non-stomatal limitations of photosynthesis under water stress in field-grown grapevines.-Aust. J. Plant Physiol. 26: 421-433, 1999. Go to original source...
    23. Flexas, J., Medrano, H.: Drought-inhibition of photosynthesis in C3 plants: Stomatal and non-stomatal limitations revisited.-Ann. Bot. 89: 183-189, 2002. Go to original source...
    24. Gregory, J.M., Mitchell, J.F.B., Brady, A.J.: Summer drought in northern midlaltitudes in a time-dependent CO2 climate experiment.-J. Climate 10: 662-686, 1997. Go to original source...
    25. Hatch, M.D.: The C4-pathway of photosynthesis. Evidence for an intermediate pool of carbon dioxide and the identity of the donor C4-dicarboxylic acid.-Biochem. J. 125: 425-432, 1971. Go to original source...
    26. Holaday, A.S., Lee, K.W., Chollet, R.: C3-C4 intermediate species in the genus Flaveria: leaf anatomy, ultrastructure, and the effect of O2 on the CO2 compensation concentration.-Planta 160: 25-32, 1984. Go to original source...
    27. Hunt, S., Smith, A.M., Woolhouse, H.W.: Evidence for a light-dependent system for reassimilation of photorespiratory CO2, which does not include a C4 cycle, in the C3-C4 intermediate species Moricandia arvensis.-Planta 171: 227-234, 1987. Go to original source...
    28. Kaiser, W.M.: Correlation between changes in photosynthetic activity and changes in total protoplast volume in leaf tissue from hygro-, meso-and xerophytes under osmotic stress.-Planta 154: 538-545, 1982. Go to original source...
    29. Kanechi, M., Uchida, N., Yasuda, T., Yamaguchi, T.: Non-stomatal inhibition associated with inactivation of Rubisco in dehydrated coffee leaves under unshaded and shaded conditions.-Plant Cell Physiol. 37: 455-460, 1996. Go to original source...
    30. Kicheva, M.I., Tsonev, T.D., Popova, L.P.: Stomatal and non-stomatal limitations to photosynthesis in two wheat cultivars subjected to water stress.-Photosynthetica 30: 107-116, 1994.
    31. Ku, M.S.B., Wu, J., Dai, Z., Scott, R.A., Chu, C., Edwards, G.E.: Photosynthetic and photorespiratory characteristics of Flaveria species.-Plant Physiol. 96: 518-528, 1991. Go to original source...
    32. Laemmli, U.K.: Cleavage of structural proteins during the assembly of the head of bacteriophage T4.-Nature 227: 680-685, 1970. Go to original source...
    33. Lal, A., Ku, M.S.B., Edwards, G.E.: Analysis of inhibition of photosynthesis due to water stress in the C3 species Hordeum vulgare and Vicia faba: Electron transport, CO2 fixation and carboxylation activity.-Photosynth. Res. 49: 57-69, 1996. Go to original source...
    34. Lawlor, D.W.: Limitation to photosynthesis in water-stressed leaves: Stomata vs. metabolism and the role of ATP.-Ann. Bot. 89: 871-885, 2002. Go to original source...
    35. Leegood, R.C.: The intercellular compartmentation of metabolites in leaves of Zea mays L.-Planta 164: 163-171, 1985. Go to original source...
    36. Leegood, R.C., Walker, R.P.: Regulation of the C4 pathway.-In: Sage, R.F., Monson, R.K. (ed.): C4 Plant Biology. Pp. 89-131. Academic Press, San Diego 1999. Go to original source...
    37. Lilley, R.Mc.C., Walker, D.A.: An improved spectrophotometric assay for ribulosebisphosphate carboxylase.-Biochim. biophys. Acta 358: 226-229, 1974. Go to original source...
    38. Lowry, O.H., Passoneau, J.V.: A Flexible System of Enzymatic Analysis.-Academic Press, London 1972. Go to original source...
    39. Mansfield, T.A., Hetherington, A.M., Atkinson, C.J.: Some current aspects of stomatal physiology.-Annu. Rev. Plant Physiol. Plant mol. Biol. 41: 55-75, 1990. Go to original source...
    40. Maroco, P.M., Rodrigues, M.L., Lopes, C., Chaves, M.M.: Limitations to leaf photosynthesis in field-grown grapevine under drought - metabolic and modelling approaches.-Funct. Plant Biol. 29: 451-459, 2002. Go to original source...
    41. Medrano, H., Parry, M.A.J., Socías, X., Lawlor, D.W.: Long term water stress inactivates Rubisco in subterranean clover.-Ann. appl. Biol. 131: 491-501, 1997. Go to original source...
    42. Monson, R.K.: The relative contributions of reduced photorespiration, and improved water-and nitrogen-use efficiencies, to the advantages of C3-C4 intermediate photosynthesis in Flaveria.-Oecologia 80: 215-221, 1989. Go to original source...
    43. Monson, R.K., Moore, B.d.: On the significance of C3-C4 intermediate photosynthesis to the evolution of C4 photosynthesis.-Plant Cell Environ. 12: 689-699, 1989. Go to original source...
    44. Monson, R.K., Moore, B.d., Ku, M.S.B., Edwards, G.E.: Cofunction of C3-and C4-photosynthetic pathways in C3, C4 and C3-C4 intermediate Flaveria species.-Planta 168: 493-502, 1986. Go to original source...
    45. Monson, R.K., Schuster, W.S., Ku, M.S.B.: Photosynthesis in Flaveria brownii A.M. Powell. A C4-like C3-C4 intermediate.-Plant Physiol. 85: 1063-1067, 1987. Go to original source...
    46. Nimmo, G.A., Nimmo, H.G., Hamilton, I.D., Fewson, C.A., Wilkins, M.B.: Purification of the phosphorylated night form and dephosphorylated day form of phosphoenolpyruvate carboxylase from Bryophyllum fedtschenkoi.-Biochem. J. 239: 213-220, 1986. Go to original source...
    47. Panković, D., Sakač, Z., Kevreąan, S., Plesničar, M.: Acclimation to long-term water deficit in the leaves of two sunflower hybrids: photosynthesis, electron transport and carbon metabolism.-J. exp. Bot. 50: 127-138, 1999. Go to original source...
    48. Prakash, K.R., Rao, V.S.: The altered activities of carbonic anhydrase, phosphoenol pyruvate-carboxylase and ribulose-bisphosphate carboxylase due to water-stress and after its relief.-J. environ. Biol. 1: 39-42, 1996.
    49. Premachandra, G.S., Hahn, D.T., Joly, R.J.: Leaf water relations and gas exchange in two grain Sorghum genotypes differing in their pre-and post-flowering drought tolerance.-J. Plant Physiol. 143: 96-101, 1994. Go to original source...
    50. Reed, J.E., Chollet, R.: Immunofluorescent localization of phosphoenolpyruvate carboxylase and ribulose 1,5-bisphosphate carboxylase/oxygenase proteins in leaves of C3, C4 and C3-C4 intermediate Flaveria species.-Planta 165: 439-445, 1985. Go to original source...
    51. Rogers, A., Ellsworth, D.S., Humphries, S.W.: Possible explanation of the disparity between the in vitro and in vivo measurements of Rubisco activity: a study in loblolly pine grown in elevated pCO2.-J. exp. Bot. 52: 1555-1561, 2001. Go to original source...
    52. Sage, R.F., Coleman, J.R.: Effects of low atmospheric CO2 on plants: more than a thing of the past.-Trends Plant Sci. 6: 18-24, 2001. Go to original source...
    53. Sawada, S., Sakamoto, T., Sato, M., Kasai, M., Usuda, H.: Photosynthesis with single-rooted Amaranthus leaves. II. Regulation of ribulose-1,5-bisphosphate carboxylase, phosphoenolpyruvate carboxylase, NAD-malic enzyme and NAD-malate dehydrogenase and coordination between PCR and C4 photosynthetic metabolism in response to changes in the source-sink balance.-Plant Cell Physiol. 43: 1293-1301, 2002. Go to original source...
    54. Sharkey, T.D., Seemann, J.R.: Mild water stress effects on carbon-reduction-cycle intermediates, ribulose bisphosphate carboxylase activity, and spatial homogeneity of photosynthesis in intact leaves.-Plant Physiol. 89: 1060-1065, 1989. Go to original source...
    55. Scholander, P.F.: Sap pressure in vascular plants.-Science 148: 339-346, 1965. Go to original source...
    56. Stitt, M., Heldt, H.W.: Generation and maintenance of concentration gradients between the mesophyll and bundle sheath in maize leaves.-Biochim. biophys. Acta 808: 400-414, 1985. Go to original source...
    57. Terashima, I.: Anatomy of non-uniform leaf photosynthesis.-Photosynth. Res. 31: 195-212, 1992. Go to original source...
    58. Terashima, I., Wong, S.-C., Osmond, C.B., Farquhar, G.D.: Characterisation of non-uniform photosynthesis induced by abscisic acid in leaves having different mesophyll anatomies.-Plant Cell Physiol. 29: 385-394, 1988.
    59. Vassey, T.L., Sharkey, T.D.: Mild water stress of Phaseolus vulgaris plants leads to reduced starch synthesis and extractable sucrose phosphate synthase activity.-Plant Physiol. 89: 1066-1070, 1989. Go to original source...
    60. Vidal, J., Chollet, R.: Regulatory phosphorylation of C4 PEP carboxylase.-Trends Plant Sci. 2: 230-241, 1997. Go to original source...
    61. Wand, S.J.E., Midgley, G.F., Jones, M.H., Curtis, P.S.: Responses of wild C4 and C3 grass (Poaceae) species to elevated atmospheric CO2 concentrations: a meta-analytic test of current theories and perceptions.-Global Change Biol. 5: 723-741, 1999. Go to original source...
    62. Ward, J.K., Tissue, D.T., Thomas, R.B., Strain, R.B.: Comparative responses of model C3 and C4 plants to drought in low and elevated CO2.-Global Change Biol. 5: 857-867, 1999. Go to original source...
    63. Wedding, R.T., Black, M.K., Meyer, C.R.: Inhibition of phosphoenolpyruvate carboxylase by malate.-Plant Physiol. 92: 456-461, 1990. Go to original source...
    64. Yin, Z.-H., Heber, U., Raghavendra, A.S.: Light-induced pH changes in leaves of C4 plants. Comparison of cytosolic alkalization and vacuolar acidification with that of C3 plants.-Planta 189: 267-277, 1993. Go to original source...
    65. Yu, G., Wang, Q., Zhuang, J.: Modelling the water use efficiency of soybean and maize plants under environmental stresses: application of a synthetic model of photosynthesis-transpiration based on stomatal behavior.-J. Plant Physiol. 161: 303-318, 2004. Go to original source...

    Return to the content