Abstract
The aquatic angiosperm Hydrilla verticillata lacks Kranz anatomy, but has an inducible, C4-based, CO2 concentrating mechanism (CCM) that concentrates CO2 in the chloroplasts. Both C3 and C4 Hydrilla leaves showed light-dependent pH polarity that was suppressed by high dissolved inorganic carbon (DIC). At low DIC (0.25 mol m−3), pH values in the unstirred water layer on the abaxial and adaxial sides of the leaf were 4.2 and10.3, respectively. Abaxial apoplastic acidification served as a CO2 flux mechanism (CFM), making HCO3 − available for photosynthesis by conversion to CO2. DIC at 10 mol m−3 completely suppressed acidification and alkalization. The data, along with previous results, indicated that inhibition was specific to DIC, and not a buffer effect. Acidification and alkalization did not necessarily show 1:1 stoichiometry; their kinetics for the apolar induction phase differed, and alkalization was less inhibited by 2.5 mol m−3 DIC. At low irradiance (50 μmol photons m−2 s−1), where CCM activity in C4 leaves is minimized, both leaf types had similar DIC inhibition of pH polarity. However, as irradiance increased, DIC inhibition of C3 leaves decreased. In C4 leaves the CFM and CCM seemed to compete for photosynthetic ATP and/or reducing power. The CFM may require less, as at low irradiance it still operated maximally, if [DIC] was low. Iodoacetamide (IA), which inhibits CO2 fixation in Hydrilla, also suppressed acidification and alkalization, especially in C4 leaves. IA does not inhibit the C4 CCM, which suggests that the CFM and CCM can operate independently. It has been hypothesized that irradiance and DIC regulate pH polarity by altering the chloroplastic [DIC], which effects the chloroplast redox state and subsequently redox regulation of a plasma-membrane H+-ATPase. The results lend partial support to a down-regulatory role for high chloroplastic [DIC], but do not exclude other sites of DIC action. IA inhibition of pH polarity seems inconsistent with the chloroplast NADPH/NADP+ ratio being the redox transducer. The possibility that malate and oxaloacetate shuttling plays a role in CFM regulation requires further investigation.
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Bowes G and Salvucci ME (1984) Hydrilla: inducible C-4type photosynthesis without Kranz anatomy. In: Sybesma C (ed) Advances in Photosynthesis Research, pp 829–832. Martinus Nijhoff/Dr W Junk Publishers, The Hague
Bowes G and Salvucci ME (1989) Plasticity in the photosynthetic carbon metabolism of submersed aquatic macrophytes. Aquat Bot 34: 233–266
Elzenga JTM and Prins HBA (1987) Light induced polarity of redox reactions in leaves of Elodea canadensis Michx. Plant Physiol 85: 239–242
Elzenga JTM and Prins HBA (1989a) Light-induced polar pH changes in leaves of Elodea canadensis. I. Effects of carbon concentration and light intensity. Plant Physiol 91: 62–67
Elzenga JTM and Prins HBA (1989b) Light-induced polar pH changes in leaves of Elodea canadensis. II. Effects of ferricyanide: evidence for modulation of polar pH changes by the redox state of the cytoplasm. Plant Physiol 91: 68–72
Elzenga JTM and Prins HBA (1990) ATPase activity and redox reactions in polar leaves of the submerged macrophyte Elodea Canadensis. In: Walker NA (ed) Proceedings of the 7th International Workshop on Plant Membrane Transport, pp 327–331
Elzenga JTM, Staal M and Prins HBA (1989) ATPase activity of isolated plasmalemma vesicles of leaves of Elodea as affected by thiol reagents and NADH/NAD ratio. Physiol Plant 76: 379–385
Jahnke LS, Eighmy TT and Fagerberg WR (1991) Studies of Elodea nuttallii grown under photorespiratory conditions. I. Photosynthetic characteristics. Plant Cell Environ 14: 147–156
Madsen TV and Sand-Jensen K (1991) Photosynthetic carbon assimilation in aquatic macrophytes. Aquat Bot 41: 5–40
Madsen TV and Baattrup-Pedersen A (1995) Regulation of growth and photosynthetic performance in Elodea canadensis in response to inorganic nitrogen. Functional Ecol 9: 239–247
Magnin NC, Cooley BA, Reiskind JB and Bowes G (1997) Regulation and localization of key enzymes during the induction of Kranz-less, C4-type photosynthesis in Hydrilla verticillata. Plant Physiol 115: 1681–1689
Miedema H and Prins HBA (1992) Coupling of proton fluxes in the polar leaves of Potamogeton lucens. J Exp Bot 43: 907–914
Miedema H and Prins HBA (1993) Simulation of the light induced oscillations of the membrane potential in Potamogeton leaf cells. J Membr Biol 133: 107–117
Ogawa T, Omata T, Miyano A and Inoue Y (1985) Photosynthetic reactions involved in the CO2-concentrating mechanism in the cyanobacterium Anacystis nidulans. In: Lucas WJ and Berry JA (eds) Inorganic Carbon Uptake by Aquatic Photosynthetic Organisms, pp 287–304. Waverly Press, Baltimore
Prins HBA and Elzenga JTM (1989) Bicarbonate utilization: Function and mechanism. Aquat Bot 34: 59–83
Prins HBA, Snel JFH, Zanstra PE and Helder RJ (1982) The mechanism of bicarbonate assimilation by the polar leaves of Potamogeton and Elodea. CO2 concentrations at the leaf surface. Plant Cell Environ 5: 207–214
Reiskind JB, Berg RH, Salvucci ME and Bowes G (1989) Immunogold localization of primary carboxylases in leaves of aquatic and a C3–C4 intermediate species. Plant Sci 61: 43–52
Reiskind JB, Madsen TV, Van Ginkel LC and Bowes G (1997) Evidence that inducible C4-type photosynthesis is a chloroplastic CO2-concentrating mechanism in Hydrilla, a submersed monocot. Plant Cell Environ 20: 211–220
Salvucci ME (1983) Mechanisms for reducing photorespiration in submersed aquatic angiosperms. PhD Dissertation, University of Florida, Gainesville, 117 pp
Salvucci ME and Bowes G (1981) Induction of reduced photorespiratory activity in submersed and amphibious aquatic macrophytes. Plant Physiol 67: 335–340
Spencer W, Teeri J and Wetzel RG (1994) Acclimation of photosynthetic phenotype to environmental heterogeneity. Ecology 75: 301–314
Smith FA and Walker NA (1980) Photosynthesis by aquatic plants: Effects of unstirred layers in relation to assimilation of CO2 and HCO- 3 and to isotopic discrimination. New Phytol. 86: 245–259
Van TK, Haller WT and Bowes G (1976) Comparison of the photosynthetic characteristics of three submersed aquatic plants. Plant Physiol 58: 761–768
Van Ginkel LC and Prins HBA (1998) Bicarbonate utilization and pH polarity. The response of photosynthetic electron transport to carbon limitation in Potamogeton lucens L. leaves. Can J Bot 76: 1018–1024
Van Ginkel LC, Schütz I and Prins HBA (1996) Rubisco, PEP Carboxylase and the pH polar reaction: Their role in photosynthetic bicarbonate utilization in Elodea canadensis. In: Mathis P (ed) Photosynthesis: From Light to Biosphere, Vol 5, pp 599–602. Kluwer Academic Publishers, Dordrecht, The Netherlands
Van Ginkel LC, Schütz I and Prins HBA (2000) Elodea canadensis under N and CO2 limitation: adaptive changes in Rubisco and PEPCase activity in a bicarbonate user. Phyton 40: 133–143
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van Ginkel, L.C., Bowes, G., Reiskind, J.B. et al. A CO2-Flux Mechanism Operating via pH-Polarity in Hydrilla Verticillata Leaves With C3 and C4 Photosynthesis. Photosynthesis Research 68, 81–88 (2001). https://doi.org/10.1023/A:1011838215424
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DOI: https://doi.org/10.1023/A:1011838215424