Skip to main content
SpringerLink
Log in
Book cover

C4 Photosynthesis and Related CO2 Concentrating Mechanisms pp 63–80Cite as

Chapter 5 Single-Cell C4 Photosynthesis in Aquatic Plants

  • Chapter
  • First Online:

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 32))

Summary

In water with low free [CO2] a common strategy of submersed plants is to use HCO −3 , but some ­species utilize a C4 photosynthetic system that surprisingly lacks the Kranz dual-cell compartmentation of most terrestrial C4 plants. Instead, the C4 and C3 cycles are in the same cell, with phosphoenolpyruvate ­carboxylase (PEPC) and ribulose bisphosphate carboxylase–oxygenase (rubisco) sequestered in the cytosol and chloroplasts, respectively. Malate decarboxylation by NADP malic enzyme (NADP-ME) in the chloroplasts produces a chloroplastic CO2 concentrating mechanism (CCM). It occurs in the ­submersed monocots Hydrilla verticillata and Egeria densa (Hydrocharitaceae), and in these species it is facultative because low [CO2] induces a metabolic shift in the leaves from C3 to single-cell C4 photosynthesis. ­Submersed leaves of other species also perform single-cell C4 photosynthesis, including Sagittaria ­subulata (Alismataceae), the grasses Orcuttia californica and O. viscida (Poaceae), and the sedge ­Eleocharis acicularis. A marine macroalga (Udotea flabellum, Chlorophyta) and a diatom (Thalassiosira weissflogii) likewise show evidence of its occurrence, so it is not restricted to higher plants. The change from C3 to C4 photosynthetic gas exchange and pulse-chase characteristics is well documented in Hydrilla, along with enzyme kinetics and localization; high internal [CO2], and improved growth. ­Multiple isoforms of PEPC, NADP-ME and pyruvate orthophosphate dikinase (PPDK) exist in Hydrilla and Egeria, but specific forms, including hvpepc4, hvme1 and hvppdk1are up-regulated in the C4 leaves of Hydrilla and encode proteins with C4 photosynthetic characteristics. Interestingly, the photosynthetic hvpepc4 differs from its terrestrial C4 counterparts in lacking a “C4-signature” serine near the carboxy terminus. The C3 leaf must maximize CO2 conductance to rubisco, but as the C4 system is induced, ­chloroplast conductance is probably minimized to reduce leakage from the CCM. Further study of the facultative system of Hydrilla could determine if down-regulation of chloroplast-envelope aquaporins is involved in reducing CO2 conductance. Hydrilla and Egeria are in the ancient Hydrocharitaceae ­family, and can give insights into early C4 photosynthesis, which likely originated in water prior to its advent on land.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Abbreviations

AA:

Aminotransferase;

Ala:

Alanine;

Asp:

Aspartate;

BN-PAGE:

Blue native polyacrylamide gel electrophoresis;

CAM:

Crassulacean acid metabolism;

CA:

Carbonic anhydrase;

CCM:

CO2 concentrating mechanism;

Γ:

-CO2 compensation point;

DW:

Dry weight;

FW:

Fresh weight;

Glc:

Glucose;

MDH:

Malate dehydrogenase;

NADP-ME:

NADP malic enzyme;

NAD-ME:

NAD malic enzyme;

OAA:

Oxaloacetate;

PEP:

Phosphoenolpyruvate;

PEPC:

Phosphoenolpyruvate carboxylase;

PEPCK:

Phosphoenolpyruvate carboxykinase;

PNUE:

Photosynthetic nitrogen use efficiency;

PPDK:

Pyruvate orthophosphate dikinase;

PS II:

Photosystem II;

RT-PCR:

Real-time polymerase chain reaction;

Rubisco:

Ribulose bisphosphate carboxylase–­oxygenase;

Ser:

Serine;

WUE:

Water use efficiency

References

  • Andrews TJ, Johnson HS, Slack CR and Hatch MD (1971) Malic enzyme and aminotransferases in relation to 3-phosphoglycerate formation in plants with the C4-dicarboxylic acid pathway of photosynthesis. Phytochemistry 10: 2005–2013

    Article  CAS  Google Scholar 

  • Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Nicholas H, Putnam NH, Zhou S, Allen AE, Apt KE et al (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306: 79–86

    Article  PubMed  CAS  Google Scholar 

  • Ascencio J and Bowes G (1983) Phosphoenolpyruvate carboxylase in Hydrilla plants with varying CO2 compensation points. Photosynth Res 4: 151–170

    CAS  Google Scholar 

  • Berry JA, Downton JS and Tregunna EB (1970) The photosynthetic carbon metabolism of Zea mays and Gomphrena globosa: the location of the CO2 fixation and the carboxyl transfer reactions. Can J Bot 48: 777–786

    Article  CAS  Google Scholar 

  • Björkman O, Pearcy RW and Nobs MA (1970) Photosynthetic characteristics. Carnegie Inst Wash YB 69: 640–648

    Google Scholar 

  • Blackburn RD, Weldon LW, Yeo RR and Taylor TM (1969) Identification and distribution of certain similar-appearing submersed aquatic weeds in Florida. Hyacinth Contr J 8: 17–21

    Google Scholar 

  • Bläsing OE, Westhoff P and Svensson P (2000) Evolution of C4 phosphoenolpyruvate carboxylase in Flaveria, a conserved serine residue in the carboxyl terminal part of the enzyme is a major determinant for C4 specific characteristics. J Biol Chem 275: 27917–27923

    PubMed  Google Scholar 

  • Bose JC (1924) The Physiology of Photosynthesis. Longmans, Green & Co, London

    Google Scholar 

  • Bowes G, Ogren WL and Hageman RH (1971) Phosphoglycolate production catalyzed by ribulose diphosphate ­carboxylase. Biochem Biophys Res Commun 45: 716–722

    Article  PubMed  CAS  Google Scholar 

  • Bowes G and Ogren WL (1972) Oxygen inhibition and other properties of soybean ribulose-l, 5-diphosphate carboxylase. J Biol Chem 247: 2171–2176

    PubMed  CAS  Google Scholar 

  • Bowes G, Holaday AS, Van TK and Haller WT (1978) ­Photosynthetic and photorespiratory carbon metabolism in aquatic plants. In: Hall DO, Coombs J and Goodwin TW (eds) Photosynthesis 77. Proceedings of the Fourth International Congress on Photosynthesis, pp 289–298. The Biochemical Society, London

    Google Scholar 

  • Bowes G and Salvucci ME (1984) Hydrilla: Inducible C4-type photosynthesis without Kranz anatomy. In: Sybesma C (ed) Advances in Photosynthesis Research, Vol III, pp 829–832. Martinus Nijhoff/Dr. W Junk Publishers, The Hague

    Google Scholar 

  • Bowes G and Salvucci ME (1989) Plasticity in the photosynthetic carbon metabolism of submersed aquatic macrophytes. Aquat Bot 34: 233–266

    Article  CAS  Google Scholar 

  • Bowes G, Rao SK, Estavillo GM and Reiskind JB (2002) C4 mechanisms in aquatic angiosperms: comparisons with terrestrial C4 systems. Funct Plant Biol 29: 379–392

    Article  CAS  Google Scholar 

  • Bowes G, Rao SK, Reiskind JB, Estavillo GM and Rao VS (2007) Hydrilla: retrofitting a C3 leaf with a single-cell C4 NADP-ME system. In: Sheehy JE, Mitchell PL and Hardy B (eds) Charting New Pathways to C4 rice, pp 275–296. International Rice Research Institute, Los Baños, Philippines

    Google Scholar 

  • Boynton JE, Nobs MA, Björkman O and Pearcy RW (1970) Leaf anatomy and ultrastructure. Carnegie Inst Wash YB 69: 629–632

    Google Scholar 

  • Bremer K (2000) Early Cretaceous lineages of monocot flowering plants. Proc Natl Acad Sci USA 97: 4704–4711

    Article  Google Scholar 

  • Brown RH and Bouton JH (1993) Physiology and genetics of interspecific hybrids between photosynthetic types. Annu Rev Plant Physiol Plant Mol Biol 44: 435–456

    Article  Google Scholar 

  • Brown JMA, Dromgoole FI, Towsey MW and Browse J (1974) Photosynthesis and photorespiration in aquatic macrophytes. In: Bieleski RL, Ferguson AR and Cresswell MM (eds) Mechanisms of Regulation of Plant Growth, pp 243–249. The Royal Society of New Zealand, Wellington

    Google Scholar 

  • Browse JA, Dromgoole FI and Brown JMA (1977) Photosynthesis in the aquatic macrophyte Egeria densa. I. 14CO2 fixation at natural CO2 concentrations. Aust J Plant Physiol 4: 169–176

    Article  CAS  Google Scholar 

  • Browse JA, Brown JMA and Dromgoole FI (1979a) Photosynthesis in the aquatic macrophyte Egeria densa. II. Effects of inorganic carbon conditions on 14CO2 fixation. Aust J Plant Physiol 6: 1–9

    Article  CAS  Google Scholar 

  • Browse JA, Dromgoole FI and Brown JMA (1979b) Photosynthesis in the aquatic macrophyte Egeria densa. III. Gas exchange studies. Aust J Plant Physiol 6: 499–512

    Article  CAS  Google Scholar 

  • Browse JA, Brown JMA and Dromgoole FI (1980) Malate synthesis and metabolism during photosynthesis in Egeria densa. Aquat Bot 8: 295–305

    Article  CAS  Google Scholar 

  • Bruhl JJ, Stone NE and Hattersley PW (1987) C4 acid decarboxylation enzymes and anatomy in sedges (Cyperaceae): first record of NAD-malic enzyme species. Aust J Plant Physiol 14: 719–728

    Article  CAS  Google Scholar 

  • Casati P, Lara MV and Andreo CS (2000) Induction of a C4-like mechanism of CO2 fixation in Egeria densa, a submersed aquatic species. Plant Physiol 123:1611–1621

    Article  PubMed  CAS  Google Scholar 

  • Chi W, Zhou J-S, Zhang F and Wu N-H (2004) Photosynthetic features of transgenic rice expressing sorghum C4 type NADP-ME. Acta Bot Sin 46:873–882

    CAS  Google Scholar 

  • Cooper TG, Filmer D, Wishnick M and Lane MD (1969) The active species of “CO2” utilized by ribulose diphosphate carboxylase. J Biol Chem 244: 1081–1083

    PubMed  CAS  Google Scholar 

  • Cooper TG and Wood HG (1971) The carboxylation of phosphoenolpyruvate and pyruvate. II. The active species of “CO2” utilized by phosphoenolpyruvate carboxylase and pyruvate carboxylase. J Biol Chem 246: 5488–5490

    PubMed  CAS  Google Scholar 

  • DeGroote D and Kennedy RA (1977) Photosynthesis in Elodea canadensis Michx. Four-carbon acid synthesis. Plant Physiol 59: 1133–1135

    CAS  Google Scholar 

  • Downton WJS and Tregunna EB (1968) Carbon dioxide compensation – its relation to photosynthetic carboxylation reactions, systematics of the Gramineae, and leaf anatomy. Can J Bot 46:207–215

    Article  CAS  Google Scholar 

  • Eighmy TT, Jahnke LS and Fagerberg WR (1991) Studies of Elodea nuttallii grown under photorespiratory conditions. 2. Evidence for bicarbonate active-transport. Plant Cell Environ 14: 157–165

    Article  CAS  Google Scholar 

  • Elzenga JTM and Prins HBA (1989) Light-induced polar pH changes in leaves of Elodea canadensis. I. Effects of carbon concentration and light intensity. Plant Physiol 91: 62–67

    Article  PubMed  CAS  Google Scholar 

  • Estavillo GM, Rao SK, Reiskind JB and Bowes G (2007) Characterization of the NADP malic enzyme gene family in the facultative, single-cell C4 monocot Hydrilla verticillata. Photosynth Res 94: 43–57

    Article  PubMed  CAS  Google Scholar 

  • Evans JR, von Caemmerer S, Setchell BA and Hudson GS (1994) The relationship between CO2 transfer conductance and leaf anatomy in transgenic tobacco with a reduced content of rubisco. Aust J Plant Physiol 21: 475–495

    Article  CAS  Google Scholar 

  • Flexas J, Ribas-Carbó M, Hanson DT, Bota J, Otto B, Cifre J, McDowell, Medrano H and Kaldenhoff R (2006) Tobacco aquaporin NtAQP1 is involved in mesophyll conductance to CO2 in vivo. Plant J 48: 427–439

    Article  PubMed  CAS  Google Scholar 

  • Hatch MD and Slack CR (1970) Photosynthetic CO2-fixation pathways. Annu Rev Plant Physiol 21: 141–162

    Article  CAS  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-dicarboxylic acid. Biochem J 125: 425–432

    PubMed  CAS  Google Scholar 

  • Hatch MD, Droscher L, Flügge, UI and Heldt HW (1984) A specific translocator for oxaloacetate transport in chloroplasts. FEBS Lett 178: 15–19

    Article  CAS  Google Scholar 

  • Holaday AS and Bowes G (1980) C4 acid metabolism and dark CO2 fixation in a submersed aquatic macrophyte (Hydrilla verticillata). Plant Physiol 65: 331–335

    Article  PubMed  CAS  Google Scholar 

  • Holaday AS, Salvucci ME and Bowes G (1983) Variable photosynthesis/photorespiratory ratios in Hydrilla and other submersed aquatic macrophyte species. Can J Bot 61:229–236

    Article  Google Scholar 

  • Holm LG, Weldon LW and Blackburn RD (1969) Aquatic weeds. Science 166: 699–709

    Article  PubMed  CAS  Google Scholar 

  • Hough RA (1974) Photorespiration and productivity in ­submersed aquatic vascular plants. Limnol Oceanogr 19: 912–927

    Article  CAS  Google Scholar 

  • Hough RA and Wetzel RG (1972) 14C-assay for photorespiration in aquatic plants. Plant Physiol 49: 987–990

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Kaplan A and Reinhold L (1999) CO2 concentrating mechanisms in photosynthetic microorganisms. Annu Rev Plant Physiol Plant Mol Biol 50: 539–570

    Article  PubMed  CAS  Google Scholar 

  • Keeley JE (1998a) CAM photosynthesis in submerged aquatic plants. Bot Rev 64: 121–175

    Article  Google Scholar 

  • Keeley JE (1998b) C4 photosynthetic modifications in the evolutionary transition from land to water in aquatic grasses. Oecologia 116: 85–97

    Article  Google Scholar 

  • Keeley JE (1999) Photosynthetic pathway diversity in a seasonal pool community. Funct Ecol 13: 106–118

    Article  Google Scholar 

  • Keeley JE and Bowes G (1982) Gas exchange characteristics of the submerged aquatic crassulacean acid metabolism plant Isoetes howellii. Plant Physiol 70: 1455–1458

    Article  PubMed  CAS  Google Scholar 

  • Kortschak HP, Hartt CE and Burr GO (1965) Carbon dioxide fixation in sugar cane leaves. Plant Physiol 40: 209–213

    Article  PubMed  CAS  Google Scholar 

  • Kvaček Z (1995) The Hydrocharitaceae foliage from the North Bohemian Early Miocene. Vestn Cesk Geol Ústavu 70: 21–28

    Google Scholar 

  • Langeland KA (1996) Hydrilla verticillata (L.f) Royle (Hydrocharitaceae), “the perfect aquatic weed”. Castanea 61: 293–304

    Google Scholar 

  • Lara MV, Casati P and Andreo CS (2001) In vivo phosphorylation of phosphoenolpyruvate carboxylase in Egeria densa, a submersed aquatic species. Plant Cell Physiol 42: 441–445

    Article  PubMed  CAS  Google Scholar 

  • Lara MV, Casati P and Andreo CS (2002) CO2-concentrating mechanisms in Egeria densa, a submersed aquatic plant. Physiol Plant 115: 487–495

    Article  PubMed  CAS  Google Scholar 

  • Lara MV, Chuong SDX, Akhani H, Andreo CS and Edwards GE (2006) Species having C4 single-cell-type photosynthesis in the Chenopodiaceae family evolved a photosynthetic phosphoenolpyruvate carboxylase like that of Kranz-type C4 species. Plant Physiol 142: 673–684

    Article  PubMed  CAS  Google Scholar 

  • Maberly SC and Madsen TV (2002) Freshwater angiosperm carbon concentrating mechanisms: processes and patterns. Funct Plant Biol 29: 393–405

    Article  CAS  Google Scholar 

  • Madsen TV and Sand-Jensen K (1991) Photosynthetic carbon assimilation in aquatic macrophytes. Aquat Bot 41: 5–40

    Article  CAS  Google Scholar 

  • Madsen TV, Maberly SC and Bowes G (1996) Photosynthetic acclimation of submersed angiosperms to CO2 and HCO -3 . Aquat Bot 53: 15–30

    Article  Google Scholar 

  • Magnin NC, Cooley BC, 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

    PubMed  CAS  Google Scholar 

  • Mai DH and Walther H (1985) Die obereozänen floren des Weisselster-Beckens und seiner Randgebiete. Abh Staatlichen Mus Minerol Geol Dresden 33: 1–260

    Google Scholar 

  • Morton BA and Keeley JE (1990) C4 acid fixation in photosynthesis of the submerged aquatic Eleocharis acicularis (L.) R. & S. Aquat Bot 36: 379–388

    Article  CAS  Google Scholar 

  • Ogren WL and Bowes G (1971) Ribulose diphosphate ­carboxylase regulates soybean photorespiration. Nature 230: 159–160

    CAS  Google Scholar 

  • Pearcy RW and Björkman O (1970) Biochemical characteristics. Carnegie Inst Wash YB 69: 632–640

    Google Scholar 

  • Rao SK, Magnin NC, Reiskind JB and Bowes G (2002) Photosynthetic and other phosphoenolpyruvate carboxylase isoforms in the single-cell, facultative C4 system of Hydrilla verticillata. Plant Physiol 130: 876–886

    Article  PubMed  CAS  Google Scholar 

  • Rao SK, Fukayama H, Reiskind JB, Miyao M and Bowes G (2006a) Identification of C4 responsive genes in the facultative C4 plant Hydrilla verticillata. Photosynth Res 88: 173–183

    Article  PubMed  CAS  Google Scholar 

  • Rao S, Reiskind J and Bowes G (2006b) Light regulation of the photosynthetic phosphoenolpyruvate carboxylase (PEPC) in Hydrilla verticillata. Plant Cell Physiol 47: 1206–1216

    Article  PubMed  CAS  Google Scholar 

  • Rao SK, Reiskind JB and Bowes G (2008) Kinetic analyses of recombinant isoforms of phosphoenolpyruvate carboxylase from Hydrilla verticillata leaves and the impact of substituting a C4-signature serine. Plant Sci 174: 475–483

    Article  CAS  Google Scholar 

  • Rao VS, Rao SK, Reiskind JB and Bowes G (2005) ­Carbonic anhydrase isoforms in the C4 CCM of Hydrilla. In: A. van der Est and D. Bruce (eds). Photosynthesis: Fundamental Aspects to Global Perspectives, pp 954–955. Allen Press, Kansas.

    Google Scholar 

  • Raven JA, Johnson AM. Kübler JE, Korb R, McInory SG, Handley LL, Scrimgouer CM, Walker DJ, Beardall J, Vanderklift M, Fredriksen S and Dunton KH (2002) Mechanistic determination of carbon isotope discrimination by marine macroalgae and seagrasses. Funct Plant Biol 29: 355–378

    Article  CAS  Google Scholar 

  • Reinfelder JR, Kraepiel AMI and Morel FMM (2001) ­Unicellular C4 photosynthesis in a marine diatom. Nature 407: 996–999

    Article  CAS  Google Scholar 

  • Reinfelder JR, Milligan AJ and Morel FMM (2004) The role of the C4 pathway in carbon accumulation and fixation in a marine diatom. Plant Physiol 135: 2106–2111

    Article  PubMed  CAS  Google Scholar 

  • Reiskind JB, Seamon PT and Bowes G (1988) Alternative methods of photosynthetic carbon assimilation in marine macroalgae. Plant Physiol 87: 686–692

    Article  PubMed  CAS  Google Scholar 

  • 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 43–52

    Google Scholar 

  • Reiskind JB and Bowes G (1991) The role of phosphoenolpyruvate carboxykinase in a marine macroalga with C4-like photosynthetic characteristics. Proc Natl Acad Sci USA 88: 2883–2887

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Renne P, Dressen U, Hebbeker U, Hille D, Flügge UI, ­Westhoff P and Weber AP (2003) The Arabidopsis mutant dct is deficient in the plastidic glutamate/malate translocator DiT2. Plant J 35: 316–331

    Article  PubMed  CAS  Google Scholar 

  • Roberts K, Granum E, Leegood RC and Raven JA (2007) C3 and C4 pathways of photosynthetic carbon assimilation in marine diatoms are under genetic, not environmental, control. Plant Physiol 145: 230–235

    Article  PubMed  CAS  Google Scholar 

  • Sage RF (2001) Environmental and evolutionary preconditions for the origin and diversification of the C4 photosynthetic syndrome. Plant Biol 3: 202–213

    Article  CAS  Google Scholar 

  • Sage RF (2004) The evolution of C4 photosynthesis. New Phytol 161: 341–370

    Article  CAS  Google Scholar 

  • Salvucci ME and Bowes G (1981) Induction of reduced ­photorespiratory activity in submersed and amphibious macrophytes. Plant Physiol 67: 335–340

    Article  PubMed  CAS  Google Scholar 

  • Salvucci ME and Bowes G (1983a) Two photosynthetic mechanisms mediating the low photorespiratory state in submersed aquatic angiosperms. Plant Physiol 73: 488–496

    Article  PubMed  CAS  Google Scholar 

  • Salvucci ME and Bowes G (1983b) Ethoxyzolamide repression of the low photorespiration state in two submersed angiosperms. Planta 158: 27–34

    Article  CAS  Google Scholar 

  • Sculthorpe CD (1967) The Biology of Aquatic Vascular Plants. Edward Arnold, London

    Google Scholar 

  • Sheehy JE, Ferrer AB, Mitchell PL, Elmido-Mabilangan A, Pablico P and Dionora MJA (2007) How the rice crop works and why it needs a new engine. In: Sheehy JE, Mitchell PL and Hardy B (eds). Charting New Pathways to C4 rice, pp 3–26. International Rice Research Institute, Los Baños, Philippines

    Google Scholar 

  • Spencer W and Bowes G (1990) Ecophysiology of the world’s most troublesome aquatic weeds. In: Pieterse AH and Murphy KY (eds) Aquatic Weeds. The Ecology and Management of Nuisance Aquatic Vegetation, pp 39–73. Oxford University Press, Oxford, UK

    Google Scholar 

  • Spencer WE, Teeri J and Wetzel RG (1994) Acclimation of photosynthetic phenotype to environmental heterogeneity. Ecology 75: 301–314

    Article  Google Scholar 

  • Steward KK, Van TK, Carter V and Pieterse AH (1984) Hydrilla invades Washington DC and the Potomac. Am J Bot 71: 162–163

    Article  Google Scholar 

  • Takeuchi K, Akagi H, Kamasawa N, Osumi M and Honda H (2000) Aberrant chloroplasts in transgenic rice plants expressing a high level of maize NADP-dependent malic enzyme. Planta 211: 265–274

    Article  PubMed  CAS  Google Scholar 

  • Taniguchi Y, Nagasaki J, Kawasaki M, Miyake H, Sugiyama T and Taniguchi M (2004) Differentiation of dicarboxylate transporters in mesophyll and bundle sheath chloroplasts of maize. Plant Cell Physiol 45: 187–200

    Article  PubMed  CAS  Google Scholar 

  • Tetlow IJ, Rawsthorne S, Raines C and Emes MJ (2005) Plastid metabolic pathways. In: Moller S (ed) Plastids (Annu Plant Rev 13), pp 60–125. CRC Press, Blackwell Publishing Ltd, Oxford, UK

    Google Scholar 

  • Uehlein N, Lovisolo C, Siefritz E and Kaldenhoff R (2003) The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature 425: 734–737

    Article  PubMed  CAS  Google Scholar 

  • Uchino A, Samejima M, Ishii R and Ueno O (1995) Photosynthetic carbon metabolism in an amphibious sedge, ­Eleocharis baldwinii (Torr.) Chapman: modified expression of C4 characteristics under submerged aquatic conditions. Plant Cell Physiol 36: 229–238

    CAS  Google Scholar 

  • Ueno O (1996) Immunocytochemical localization of enzymes involved in the C3 and C4 pathways in the photosynthetic cells of an amphibious sedge, Eleocharis vivipara. Planta 199: 394–403

    CAS  Google Scholar 

  • Ueno O (1998) Induction of Kranz anatomy and C4-like biochemical characteristics in a submerged amphibious plant by abscisic acid. Plant Cell 10: 571–583

    PubMed  CAS  Google Scholar 

  • Ueno O, Samejima M, Muto S and Miyachi S (1988) Photosynthetic characteristics of an amphibious plant, Eleocharis vivipara: expression of C4 and C3 modes in contrasting environments. Proc Natl Acad Sci USA 85: 6733–6737

    Article  PubMed  CAS  Google Scholar 

  • Van TK, Haller WT and Bowes G (1976) Comparison of the photosynthetic characteristics of three submersed aquatic macrophytes. Plant Physiol 58: 761–768

    Article  PubMed  CAS  Google Scholar 

  • Van TK, Haller WT and Bowes G (1978) Some aspects of the competitive biology of Hydrilla. Proceedings of European Weed Research Society, Fifth Symposium on Aquatic Weeds, pp 117–126. Amsterdam, The Netherlands

    Google Scholar 

  • Van TK, Haller WT, Bowes G and Garrard LA (1977) Effects of light quality on growth and chlorophyll composition in Hydrilla. J Aquat Plant Manage 15: 29–31

    CAS  Google Scholar 

  • Van TK (1989) Differential responses to photoperiods in monoecious and dioecious Hydrilla verticillata. Weed Sci 37: 552–556

    Google Scholar 

  • van Ginkel LC, Bowes G, Reiskind JB and Prins HBA (2001) A CO2-flux mechanism operating via pH-polarity in Hydrilla verticillata leaves with C3 and C4 photosynthesis. Photosynth Res 68: 81–88

    Article  PubMed  Google Scholar 

  • von Caemmerer S (2003) C4 photosynthesis in a single C3 cell is theoretically inefficient but may ameliorate internal CO2 diffusion limitations of C3 leaves. Plant Cell Environ 26: 1191–1197

    Article  Google Scholar 

  • von Caemmerer S, Evans JR, Cousins AB, Badger MR and Furbank RT (2007) C4 photosynthesis and CO2 diffusion. In: Sheehy JE, Mitchell PL and Hardy B. (eds) Charting New Pathways to C4 rice, pp 95–115. International Rice Research Institute, Los Baños, Philippines

    Google Scholar 

  • Weber A and Flügge UI (2002) Interaction of cytosolic and plastidic nitrogen metabolism in plants. J Exp Bot 53: 865–874

    Article  PubMed  CAS  Google Scholar 

  • Weig A, Deswarte C and Chrispeels MJ (1997) The major intrinsic protein family of Arabidopsis has 23 members that form three distinct groups with functional aquaporins in each group. Plant Physiol 114: 1347–57

    Article  PubMed  CAS  Google Scholar 

  • White A, Reiskind JB and Bowes G (1996) Dissolved inorganic carbon influences the photosynthetic responses of Hydrilla to photoinhibitory conditions. Aquat Bot 53: 3–13

    Article  CAS  Google Scholar 

  • Yeoh H-H and Hattersley P (1985) K m(CO2) values of ribulose-1,5-bisphosphate carboxylase in grasses of different C4 type. Phytochemistry 24: 2277—2279

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The credit for the research that emanated from my laboratory goes to the many colleagues and students with whom it has been my privilege and pleasure to work over the past 35 years. Financial support has been provided by the United States Department of Agriculture, National Research Initiatives Competitive Grants Program; the National Science Foundation, Integrative Plant Biology; Florida Department of Environmental Protection, Center for Aquatic and Invasive Plants, University of Florida; Florida Institute of Oceanography; and NATO, Scientific and Environmental Affairs Division, Collaborative Research Grants.

Author information

Authors and Affiliations

  1. Department of Biology, University of Florida, 220 Bartram Hall, Gainesville, FL, 32611, USA

    George Bowes

Authors
  1. George Bowes
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to George Bowes .

Editor information

Editors and Affiliations

  1. School of Life Sciences, University of Hyderabad, Hyderabad, 500046, India

    Agepati S. Raghavendra

  2. Dept. Botany, University of Toronto, Willcocks Street 25, Toronto, M5S 3B2, Ontario, Canada

    Rowan F. Sage

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Netherlands

About this chapter

Cite this chapter

Bowes, G. (2010). Chapter 5 Single-Cell C4 Photosynthesis in Aquatic Plants. In: Raghavendra, A., Sage, R. (eds) C4 Photosynthesis and Related CO2 Concentrating Mechanisms. Advances in Photosynthesis and Respiration, vol 32. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-9407-0_5

Download citation

Publish with us

Policies and ethics

Search

Navigation