Skip to main content

Chapter 4 C4 Photosynthesis: Kranz Forms and Single-Cell C4 in Terrestrial Plants

  • Chapter
  • First Online:

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

Summary

Plants identified as having C4 photosynthesis have a C4 metabolic cycle with phosphoenolpyruvate carboxylase as the initial catalyst for fixation of atmospheric CO2, and a C4 acid decarboxylase (NADP-malic enzyme, NAD-malic enzyme, or phosphoenolpyruvate carboxykinase), which releases CO2 for fixation by the C3 cycle. Effective donation of CO2 to Rubisco minimizes competition by O2 and photorespiration, and thus increases photosynthesis under conditions where CO2 is limiting. To achieve this, fixation of atmospheric CO2 in the cytosol by phosphoenolpyruvate carboxylase must be separated from the donation of CO2 to Rubisco by the decarboxylation of C4 acids. In most documented C4 plants, this is accomplished through evolution of various forms of Kranz anatomy, with fixation of atmospheric CO2 in mesophyll cells and donation of CO2 from C4 acids to Rubisco in bundle sheath cells. In the family Chenopodiaceae, two alternative means of accomplishing this spatial separation evolved within individual photosynthetic cells, whereby one cytoplasmic compartment specializes in fixation of atmospheric CO2 in the carboxylation phase of the C4 cycle, and the other cytoplasmic compartment specializes in donating CO2 from C4 acids to Rubisco. In this chapter, biochemical and structural variations of Kranz anatomy in three major C4-containing families, Poaceae, Cyperaceae, and Chenopodiaceae, as well as other known forms for dicots, are summarized. Then, the phylogeny, biogeography, development, and structure-function relationships of the single-cell C4 systems are discussed in comparison to Kranz type C4 plants.

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

Buying options

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

BS:

Bundle sheath(s);

Kranz cells:

An inner layer of chlorenchyma cells specialized for C4 photosynthesis, irrespective of whether there is contact with vascular bundles (sometimes referred to as BS cells in C4 plants);

M:

Mesophyll;

MS:

Mestome sheath(s);

NAD-ME:

NAD-malic enzyme;

NADP-ME:

NADP-malic enzyme;

PEPC:

Phosphoenolpyruvate carboxylase;

PEP-CK:

Phosphoenolpyruvate carboxykinase;

PGA:

3-Phosphoglyceric acid;

PPDK:

Pyruvate,Pi dikinase;

PSI:

Photosystem I;

PSII:

Photosystem II;

RuBP:

Ribulose 1,5-bisphosphate;

SL:

Suberin lamella

References

  • Akhani H and Ghasemkhani M (2007) Diversity of photosynthetic organs in Chenopodiaceae from Golestan National Park (NE Iran) based on carbon isotope composition and anatomy of leaves and cotyledons. Nova Hedwigia Suppl 131: 265–277

    Google Scholar 

  • Akhani H, Trimborn P and Ziegler H (1997) Photosynthetic pathways in Chenopodiaceae from Africa, Asia and Europe with their ecological, phytogeographical and taxonomical importance. Plant Syst Evol 206: 187–221

    Google Scholar 

  • Akhani H, Ghobadnejhad M and Hashemi SMH (2003) Ecology, biogeography and pollen morphology of Bienertia cycloptera Bunge ex Boiss. (Chenopodiaceae), an enigmatic C4 plant without Kranz anatomy. Plant Biol 5: 167–178

    Google Scholar 

  • Akhani H, Barroca J, Koteeva N, Voznesenskaya E, Franceschi V, Edwards G, Ghaffari SM and Ziegler H (2005) Bienertia sinuspersici (Chenopodiaceae): a new species from Southwest Asia and discovery of a third terrestrial C4 plant without Kranz anatomy. Syst Bot 30: 290–301

    Google Scholar 

  • Akhani H, Ghasemkhani M, Chuong SDX and Edwards GE (2008) Occurrence and forms of Kranz anatomy and characterization of NAD-ME subtype C4 photosynthesis in Blepharis ciliaris (L) B.L. Burtt (Acanthaceae). J Exp Bot 59: 1755–1765

    PubMed  CAS  Google Scholar 

  • Akhani H, Lara MV, Ghasemkhani M, Ziegler H and Edwards GE (2009) Does Bienertia cycloptera with the single-cell system of C4 photosynthesis exhibit a seasonal pattern of δ13C values in nature similar to co-existing C4 Chenopodiaceae having the dual-cell (Kranz) system? Photosyn Res 99: 23–36

    PubMed  CAS  Google Scholar 

  • Aliscioni SS, Giussani LM, Zuloaga FO and Kellogg EA (2003) A molecular phylogeny of Panicum (Poaceae: Paniceae): Tests of monophyly and phylogenetic placement within the Panicoideae. Am J Bot 90: 796–821

    PubMed  CAS  Google Scholar 

  • Anderson JM (1999) Insights into the consequences of grana stacking of thylakoid membranes in vascular plants: a personal perspective. Aust J Plant Physiol 26: 625–639

    CAS  Google Scholar 

  • Bisalputra T, Downton WJS and Tregunna EB (1969) The distribution and ultrastructure of chloroplasts in leaves differing in photosynthetic carbon metabolism. I. Wheat, Sorghum and Aristida (Gramineae). Can J Bot 47: 15–21

    CAS  Google Scholar 

  • Boyd CN, Franceschi VR, Chuong SDX, Akhani H, Kiirats O, Smith M and Edwards GE (2007) Flowers of Bienertia cycloptera and Suaeda aralocaspica (Chenopodiaceae) complete the life cycle performing single-cell C4 photosynthesis. Funct Plant Biol 34: 268–281

    CAS  Google Scholar 

  • Brown WV (1958) Leaf anatomy in grass systematics. Bot Gaz 119: 170–178

    Google Scholar 

  • Brown WV (1975) Variations in anatomy, associations, and origin of Kranz tissue. Am J Bot 62: 395–402

    Google Scholar 

  • Brown WV (1977) The Kranz syndrome and its subtypes in grass systematics. Mem Torrey Bot Club 23: 1–97

    CAS  Google Scholar 

  • Bruhl JJ and Perry S (1995) Photosynthetic pathway-related ultrastructure of C3, C4 and C3-like C3-C4 intermediate sedges (Cyperaceae), with special reference to Eleocharis. Aust J Plant Physiol 22: 521–530

    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

    CAS  Google Scholar 

  • Burnell JN and Hatch MD (1988) Photosynthesis in phosphoenolpyruvate carboxykinase-type C4 plants: pathways of C4 acid decarboxylation in bundle sheath cells of Urochloa panicoides. Arch Biochem Biophys 260: 187–199

    PubMed  CAS  Google Scholar 

  • Butnik AA (1979) Types of seedling development of Chenopodiaceae Vent. Bot Zh 64: 834–842 (In Russian)

    Google Scholar 

  • Butnik AA (1984) The adaptation of anatomical structure of the family Chenopodiaceae Vent. species to arid conditions. Summary of biological science doctor degree thesis. Academy of Sciences of Uzbek SSR, Tashkent (In Russian)

    Google Scholar 

  • Butnik AA (1991) Family Chenopodiaceae. In: AL Tachtadjan (ed) Comparative seed anatomy. Dicotyledonous. Caryophyllidae-Dilleniidae, pp 77–82 (In Russian). Nauka, Leningrad

    Google Scholar 

  • Butnik AA, Ashurmetov OA, Nigmatova RN and Paizieva SA (2001) Ecological anatomy of desert plants of Middle Asia. V. 2. Subshrubs, Subshrublets FAN, Tashkent (In Russian)

    Google Scholar 

  • Carolin RC, Jacobs SWL and Vesk M (1973) The structure of the cells of the mesophyll and parenchymatous bundle sheath of the Gramineae. Bot J Linn Soc 66: 259–275

    Google Scholar 

  • Carolin RC, Jacobs SWL and Vesk M (1975) Leaf structure in Chenopodiaceae. Bot Jahrbuch Syst Pflanzengesch Pflanzengeogr 95: 226–255

    Google Scholar 

  • Carolin RC, Jacobs SWL and Vesk M (1977) The ultrastructure of Kranz cells in the family Cyperaceae. Bot Gaz 138: 413–419

    Google Scholar 

  • Carolin RC, Jacobs SWL and Vesk M (1978) Kranz cells and mesophyll in the Chenopodiales. Aust J Bot 26: 683–698

    Google Scholar 

  • Carolin RC, Jacobs SWL and Vesk M (1982) The chlorenchyma of some members of the Salicornieae (Chenopodiaceae). Aust J Bot 30: 387–392

    Google Scholar 

  • Christin P-A, Besnard G, Samaritani E, Duvall MR, Hodkinson TR, Savolainen V and Salamin N (2008) Oligocene CO2 decline promoted C4 photosynthesis in grasses. Current Biol 18: 37–43

    CAS  Google Scholar 

  • Christin P-A, Salamin N, Kellogg EA, Vicentini A and Besnard G (2009) Integrating phylogeny into studies of C4 variation in the grasses. Plant Physiol 149: 82–87

    PubMed  CAS  Google Scholar 

  • Chuong SDX, Franceschi VR and Edwards GE (2006) The cytoskeleton maintains organelle partitioning required for single-cell C4 photosynthesis in Chenopodiaceae species. Plant Cell 18: 2207–2223

    PubMed  CAS  Google Scholar 

  • Craig S and Goodchild DJ (1977) Leaf ultrastructure of Triodia irritans: a C4 grass possessing an unusual arrangement of photosynthetic tissues. Aust J Bot 25: 277–290

    CAS  Google Scholar 

  • Crookston RK and Moss DN (1972) C-4 and C-3 carboxylation characteristics in the genus Zygophyllum (Zygophyllaceae). Ann MO Bot Gard 59: 465–470

    Google Scholar 

  • Crookston RK and Moss DN (1973) A variation of C4 leaf anatomy in Arundinella hirta (Gramineae). Plant Physiol 52: 397–402

    PubMed  CAS  Google Scholar 

  • Das VSR and Raghavendra AS (1976) C4 photosynthesis and a unique type of Kranz anatomy in Glossocordia boswallaea (Asteraceae). Proc Indian Acad Sci 84B: 12–19

    Google Scholar 

  • Dengler RE and Dengler NG (1990) Leaf vascular architecture in the atypical C4 NADP-malic enzyme grass Arundinella hirta. Can J Bot 68: 1208–1221

    Google Scholar 

  • Dengler NG and Nelson T (1999) Leaf structure and development in C4 plants. In: Sage RF and Monson RK (eds) C4 Plant Biology. Physiological Ecology series, pp 133–172. Academic Press, New York

    Google Scholar 

  • Dengler NG, Dengler RE and Hattersley PW (1985) Differing ontogenetic origins of PCR (“Kranz”) sheaths in leaf blades of C4 grasses (Poaceae). Am J Bot 72: 284–302

    Google Scholar 

  • Dengler NG, Dengler RE and Drenville DJ (1990) Comparison of photosynthetic carbon reduction (Kranz) cells having different ontogenetic origins in the C4 NADP-malic enzyme grass Arundinella hirta. Can J Bot 68: 1222–1232

    Google Scholar 

  • Dengler NG, Donnelly PM and Dengler RE (1996) Differentiation of bundle sheath, mesophyll, and distinctive cells in the C4 grass Arundinella hirta (Poaceae). Am J Bot 83: 1391–1405

    Google Scholar 

  • Edwards GE and Ku MSB (1987) The biochemistry of C3-C4 intermediates. In: Hatch MD and Boardman NK (eds) The Biochemistry of Plants, pp 275–325. Academic Press, New York

    Google Scholar 

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

    Google Scholar 

  • Edwards GE, Furbank RT, Hatch MD and Osmond CB (2001) What does it take to be C4? Lessons from the evolution of C4 photosynthesis. Plant Physiol 125: 46–49

    PubMed  CAS  Google Scholar 

  • Edwards GE, Franceschi VR and Voznesenskaya EV (2004) Single-cell C4 photosynthesis versus the dual-cell (Kranz) paradigm. Ann Rev Plant Biol 55: 173–196

    CAS  Google Scholar 

  • Edwards GE, Voznesenskaya EV, Smith M, Koteyeva N, Park Y-I, Park JH, Kiirats O, Okita TW and Chuong SDX (2007) Breaking the Kranz paradigm in terrestrial C4 plants: Does it hold promise for C4 rice? In: Sheehy JE, Mitchell PL and Hardy B (eds) Charting New Pathways to C4 rice, pp 249–273. International Rice Research Institute, World Scientific, Los Banos, Philippines

    Google Scholar 

  • Ellis RP (1977) Distribution of the Kranz syndrome in the Southern African Eragrostoideae and Panicoideae according to bundle sheath anatomy and cytology. Agroplantae 9: 73–110

    Google Scholar 

  • Fisher DD, Schenk HJ, Thorsch JA and Ferren WR, Jr. (1997) Leaf anatomy and subgeneric affiliation of C3 and C4 species of Suaeda (Chenopodiaceae) in North America. Am J Bot 84: 1198–1210

    PubMed  CAS  Google Scholar 

  • Frean ML, Ariovich D and Cresswell CF (1983) C3 and C4 photosynthetic and anatomical forms of Alloteropsis semialata (R. Br.) Hitchcock. II. A comparative investigation of leaf ultrastructure and distribution of chlorenchyma in the two forms. Ann Bot 51: 811–821

    Google Scholar 

  • Freitag H and Stichler W (2000) A remarkable new leaf type with unusual photosynthetic tissue in a central Asiatic genus of Chenopodiaceae. Plant Biol 2: 154–160

    Google Scholar 

  • Freitag H and Stichler W (2002) Bienertia cycloptera Bunge ex Boiss., Chenopodiaceae, another C4 plant without Kranz tissues. Plant Biol 4: 121–132

    Google Scholar 

  • Gamaley YV (1985) The variations of the Kranz-anatomy in Gobi and Karakum plants. Bot Zh 70: 1302–1314 (In Russian)

    Google Scholar 

  • Gamaley YV and Voznesenskaya EV (1986) Structural-biochemical types of C4 plants. Sov Plant Physiol 33: 616–630

    Google Scholar 

  • Gilliland MG and Gordon-Gray KD (1978) Kranz and non-kranz cells in Cyperaceae. Proc Electron Microsc Soc Southern Africa 8: 85–86

    Google Scholar 

  • Glagoleva TA, Voznesenskaya EV, Kol’chevskii KG, Kocharyan NI, Pakhomova MV, Chulanovskaya MV and Gamalei YV (1991) Structural-functional characteristics of halophytes of the Ararat valley. Sov Plant Physiol 37: 822

    Google Scholar 

  • GPWG (2001) Phylogeny and subfamilial classification of the grasses (Poaceae). Ann MO Bot Gard 88: 373–457

    Google Scholar 

  • Guissani LM, Cota-Sanches JH, Zuloaga FO and Kellogg EA (2001) A molecular phylogeny of the grass subfamily Panicoideae (Poaceae) shows multiple origins of C4 photosynthesis. Am J Bot 88: 1993–2012

    Google Scholar 

  • Guralnick LJ, Edwards GE, Ku MSB, Hockema B and Franceschi VR (2002) Photosynthetic and anatomical characteristics in the C4-Crassulacean acid metabolism-cycling plant, Portulaca grandiflora. Funct Plant Biol 29: 763–773

    CAS  Google Scholar 

  • Gutierrez M, Gracen VE and Edwards GE (1974) Biochemical and cytological relationships in C4 plants. Planta 119: 279–300

    CAS  Google Scholar 

  • Haberlandt G (1884) Physiologische Pflanzenanatomie. Engelmann, Leipzig

    Google Scholar 

  • Hatch MD (1971) Mechanism and function of C4 photosynthesis. In: Hatch MD, Osmond CB and Slatyer RO (eds) Photosynthesis and Photorespiration, pp 139–152. Wiley-Interscience, New York

    Google Scholar 

  • Hatch MD (1987) C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochim Biophys Acta 895: 81–106

    CAS  Google Scholar 

  • Hatch MD (1999) C4 photosynthesis: a historical overview. In: Sage RF and Monson RK (eds) C4 plant biology. Physiological Ecology series, pp 17–46. Academic Press, San Diego

    Google Scholar 

  • Hatch MD, Kagawa T and Craig S (1975) Subdivision of C4-pathway species based on differing C4 acid decarboxylating systems and ultrastructural features. Aust J Plant Physiol 2: 111–128

    CAS  Google Scholar 

  • Hattersley PW (1987) Variations in photosynthetic pathway. In: Soderstrom, TR Hilu KW, Campbell CS and Barkworth ME (eds) Grass systematics and evolution, pp 49–64. Smithsonian Institution Press, Washington, DC

    Google Scholar 

  • Hattersley PW (1992) C4 photosynthetic pathway variation in grasses (Poaceae): its significance for arid and semi-arid lands. In: Chapman GP (ed) Desertified Grasslands: Their Biology and Management, pp 181–212. Academic Press, London

    Google Scholar 

  • Hattersley PW and Browning AJ (1981) Occurrence of the suberized lamella in leaves of grasses of different photosynthetic types. I. In parenchymatous bundle sheaths and PCR (“Kranz”) sheaths. Protoplasma 109: 371–401

    Google Scholar 

  • Hattersley PW and Watson L (1992) Diversification of photosynthesis. In: Chapman GP (ed) Grass evolution and domestication, pp 38–116. Cambridge University Press, Cambridge

    Google Scholar 

  • Hattersley PW, Wong S-C, Perry S and Roksandic Z (1986) Comparative ultrastructure and gas exchange characteristics of the C3-C4 intermediate Neurachne minor S.T. Blake (Poaceae). Plant Cell Environ 9: 217–233

    CAS  Google Scholar 

  • Ibrahim DG, Burke T, Ripley BS and Osborne CP (2009) A molecular phylogeny of the genus Alloteropsis (Panicoideae, Poaceae) suggests an evolutionary reversion from C4 to C3 photosynthesis. Ann Bot 103: 127–136

    PubMed  CAS  Google Scholar 

  • Jacobs SWL (2001) Review of leaf anatomy and ultrastructure in the Chenopodiaceae (Caryophyllales). J Torrey Bot Soc 128: 236–253

    Google Scholar 

  • Johnson MSC (1964) An electron microscope study of the photosynthetic apparatus in plants, with special reference to the Gramineae. Ph.D. thesis, The University of Texas.

    Google Scholar 

  • Kadereit G, Borsch T, Weising K and Freitag H (2003) Phylogeny of Amaranthaceae and Chenopodiaceae and the evolution of C4 photosynthesis. Int J Plant Sci 164: 959–986

    CAS  Google Scholar 

  • Kanai R and Edwards G (1999) The biochemistry of C4 photosynthesis. In: Sage RF and Monson RK (eds) C4 Plant Biology. Physiological Ecology series, pp 49–87. Academic Press, San Diego

    Google Scholar 

  • Kapralov MV, Akhani H, Voznesenskaya E, Edwards G, Franceschi VR and Roalson EH (2006) Phylogenetic relationships in the Salicornioideae /Suaedoideae /Salsoloideae s.l. (Chenopodiaceae) clade and a clarification of the phylogenetic position of Bienertia and Alexandra using multiple DNA sequence datasets. Syst Bot 31: 571–585

    Google Scholar 

  • Kennedy RA and Laetsch WM (1974) Plant species intermediate for C3, C4 photosynthesis. Science 184: 1087–1089

    PubMed  CAS  Google Scholar 

  • Kim I and Fisher DG (1990). Structural aspects of the leaves of seven species of Portulaca growing in Hawaii. Can J Bot 68: 1803–1811

    Google Scholar 

  • Laetsch WM (1968) Chloroplast specialization in dicotyledons possessing the C4-dicarboxylic acid pathway of photosynthetic CO2 fixation. Am J Bot 55: 875–883

    CAS  Google Scholar 

  • Laetsch WM (1974) The C4 syndrome: a structural analysis. Annu Rev Plant Physiol 25: 27–52

    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

    PubMed  CAS  Google Scholar 

  • Marshall DM, Muhaidat R, Brown NJ, Liu Z, Stanley S, Griffiths H, Sage RF and Hibberd JM (2007) Cleome, a genus closely related to Arabidopsis, contains species spanning a developmental progression from C3 to C4 photosynthesis. Plant J 207: 886–896

    Google Scholar 

  • McKown AD, Moncalvo J-M and Dengler NG (2005) Phylogeny of Flaveria (Asteraceae) and inference of C4 photosynthesis evolution. Am J Bot 92: 1911–1928

    PubMed  CAS  Google Scholar 

  • Meister M, Agostino A and Hatch MD (1996) The roles of malate and aspartate in C4 photosynthetic metabolism of Flaveria bidentis (L.). Planta 199: 262–269

    CAS  Google Scholar 

  • Monson RK and Moore Bd (1989) On the significance of C3-C4 intermediate photosynthesis to the evolution of C4 photosynthesis. Plant Cell Env 12: 689–699

    CAS  Google Scholar 

  • Monson RK, Edwards GE and Ku MSB (1984) C3-C4 intermediate photosynthesis in plants. BioScience 34: 563–574

    CAS  Google Scholar 

  • Moore Bd, Ku MSB and Edwards GE (1984) Isolation of leaf bundle sheath protoplasts from C4 dicot species and intracellular localization of selected enzymes. Plant Sci Lett 35: 127–138

    CAS  Google Scholar 

  • Muhaidat RM, Sage RF and Dengler NG (2007) Diversity of Kranz anatomy and biochemistry in C4 eudicots. Am J Bot 94: 362–381

    PubMed  CAS  Google Scholar 

  • Murphy LR, Barroca J, Franceschi VR, Lee R, Roalson EH, Edwards GE and Ku MSB (2007) Diversity and plasticity of C4 photosynthesis in Eleocharis (Cyperaceae). Funct Plant Biol 34: 571–580

    CAS  Google Scholar 

  • Nishioka D, Miyake H and Taniguchi T (1996) Suppression of granal development and accumulation of Rubisco in different bundle sheath chloroplasts of the C4 succulent plant Portulaca grandiflora. Ann Bot 77: 629

    CAS  Google Scholar 

  • Ocallaghan M (1992) The ecology and identification of the southern African Salicornieae (Chenopodiaceae). South Afr J Bot 58: 430–439

    Google Scholar 

  • Ohsugi R and Murata T (1980) Leaf anatomy, post-illumination CO2 burst and NAD-malic enzyme activity of Panicum dichotomiflorum. Plant Cell Physiol 21: 1329–1333

    CAS  Google Scholar 

  • Ohsugi R, Murata T and Chonan N (1982) C4 syndrome of the species in the Dichotomiflora group of the genus Panicum (Gramineae). Bot Mag 95: 339–347

    CAS  Google Scholar 

  • Park J, Okita TW and Edwards GE (2010) Expression profiling and proteomic analysis of isolated photosynthetic cells of the non-Kranz C4 species Bienertia sinuspersici. Funct Plant Biol 37: 1–13

    Google Scholar 

  • Peter G and Katinas L (2003) A new type of Kranz anatomy in Asteraceae. Aust J Bot 51: 217–226

    Google Scholar 

  • Prendergast HDV and Hattersley PW (1987) Australian C4 grasses (Poaceae): leaf blade anatomical features in relation to C4 acid decarboxylation types. Aust J Bot 35: 355–382

    Google Scholar 

  • Prendergast HDV, Hattersley PW, Stone NE and Lazarides M (1986) C4 acid decarboxylation type in Eragrostis (Poaceae): patterns of variation in chloroplast position, ultrastructure, and geographical distribution. Plant Cell Env 9: 333–344

    Google Scholar 

  • Prendergast HDV, Hattersley PW and Stone NE (1987) New structural/biochemical associations in leaf blades of C4 grasses (Poaceae). Aust J Plant Physiol 14: 403–420

    CAS  Google Scholar 

  • Pyankov VI and Vakhrusheva DV (1989) Pathways of primary CO2 fixation in C4 plants of the family Chenopodiaceae from the arid zone of Central Asia. Sov Plant Physiol 36: 178–187

    Google Scholar 

  • Pyankov VI, Kuzmin AN, Demidov ED and Maslov AI (1992) Diversity of biochemical pathways of CO2 fixation in plants of the families Poaceae and Chenopodiaceae from the arid zone of Central Asia. Sov Plant Physiol 39: 411–420

    Google Scholar 

  • Pyankov VI, Artyusheva EG and Edwards G (1999) Formation of C4 syndrome in leaves and cotyledons of Kochia scoparia and Salsola collina (Chenopodiaceae). Russian J Plant Phys 46: 452–466

    CAS  Google Scholar 

  • Pyankov VI, Gunin PD, Tsoog S and Black CC (2000a)C4 plants in the vegetation of Mongolia: their natural occurrence and geographical distribution in relation to climate. Oecologia 123: 15–31

    Google Scholar 

  • Pyankov VI, Voznesenskaya EV, Kuzmin A, Ku MSB, Black CC and Edwards GE (2000b) Diversity of CO2 fixation pathways in leaves and cotyledons of Salsola (Chenopodiaceae) plants. Dokl Bot Sci 370: 1–5

    Google Scholar 

  • Pyankov VI, Voznesenskaya EV, Kuzmin AN, Ku MSB, Ganko E, Franceschi VR, Black CC, Jr. and Edwards GE (2000c) Occurrence of C3 and C4 photosynthesis in cotyledons and leaves of Salsola species (Chenopodiaceae). Photosyn Res 63: 69–84

    PubMed  CAS  Google Scholar 

  • Rathnam CKM, Raghavendra AS and Das VSR (1976) Diversity in the arrangements of mesophyll cells among leaves of certain C4 dicotyledons in relation to C4 physiology. Z Pflanzenphysiol 77: 283–291

    Google Scholar 

  • Rawsthorne S and Bauwe H (1998) C3-C4 intermediate photosynthesis. In: Raghavendra AS (ed) Photosynthesis. A comprehensive treatise, pp 150–162. Cambridge University Press, Cambridge

    Google Scholar 

  • Sage RF (2002) C4 photosynthesis in terrestrial plants does not require Kranz anatomy. Trends Plant Sci 7: 283–285

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Sage RF and Monson RK (1999) C4 Plant Biology. Academic Press, San Diego

    Google Scholar 

  • Sage RF, Li M and Monson RK (1999) The taxonomic distribution of C4 photosynthesis. In: RF Sage and RK Monson (eds) C4 Plant Biology, pp 551–584. Academic Press, New York

    Google Scholar 

  • Sanchez-Ken JG, Clark LG, Kellogg EA and Kay EE (2007) Reinstatement and emendation of subfamily Micrairoideae (Poaceae). Syst Bot 32: 71–80

    Google Scholar 

  • Schütze P, Freitag H and Weising K (2003) An integrated molecular and morphological study of the subfamily Suaedoideae Ulbr. (Chenopodiaceae). Plant Syst Evol 239: 257–286

    Google Scholar 

  • Sede SM, Morrone O, Aliscioni SS, Giussani LM and Zuloaga FO (2009) Oncorachis and Sclerochlamys, two new segregated genera from Streptostachys (Poaceae, Panicoideae, Paniceae): a revision based on molecular, morphological and anatomical characters. Taxon 58: 365–374

    Google Scholar 

  • Shepherd KA and Wilson PG (2007) Incorporation of the Australian genera Halosarcia, Pachycornia, Sclerostegia and Tegicornia into Tecticornia (Salicornioideae, Chenopodiaceae). Aust Syst Bot 20: 319–331

    Google Scholar 

  • Shomer-Ilan A, Beer S and Waisel Y (1975) Suaeda monoica, a C4 plant without typical bundle sheaths. Plant Physiol 56: 676–679

    PubMed  CAS  Google Scholar 

  • Shomer-Ilan A, Neumann-Ganmore R and Waisel Y (1979) Biochemical specialization of photosynthetic cell layers and carbon flow paths in Suaeda monoica. Plant Physiol 64: 963–965

    PubMed  CAS  Google Scholar 

  • Shomer-Ilan AS, Nissenbaum A and Waisel Y (1981) Photosynthetic pathways and the ecological distribution of the Chenopodiaceae in Israel. Oecologia 48: 244–248

    Google Scholar 

  • Soros CL and Dengler NG (1998) Quantitative leaf anatomy of C3 and C4 Cyperaceae and comparisons with the Poaceae. Int J Plant Sci 159: 480–491

    Google Scholar 

  • Soros CL and Dengler NG (2001) Ontogenetic derivation and cell differentiation in photosynthetic tissues of C3 and C4 Cyperaceae. Am J Bot 88: 992–1005

    PubMed  CAS  Google Scholar 

  • Takeda T, Ueno O and Agata W (1980) The occurrence of C4 species in the genus Rhynchospora and its significance in Kranz anatomy of the Cyperaceae. Bot Mag 93: 55–65

    CAS  Google Scholar 

  • Taniguchi Y, Taniguchi M, Kawasaki M and Miyake H (2003) Strictness of the centrifugal location of bundle sheath chloroplasts in different NADP-ME type C4 grasses. Plant Prod Sci 6: 274–280

    Google Scholar 

  • Tateoka T (1958) Notes on some grasses. VIII. On leaf structure of Arundinella and Garnotia. Bot Gaz 120: 101–109

    Google Scholar 

  • Ueno O (1995) Occurrence of distinctive cells in leaves of C4 species in Arthraxon and Microstegium (Andropogoneae-Poaceae) and the structural and immunocytochemical characterization of these cells. Int J Plant Sci 156: 270–289

    Google Scholar 

  • Ueno O (1996a) Structural characterization of photosynthetic cells in an amphibious sedge, Eleocharis vivipara, in relation to C3 and C4 metabolism. Planta 199: 382–393

    CAS  Google Scholar 

  • Ueno O (1996b) 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 (1998a) Immunogold localization of photosynthetic enzymes in leaves of various C4 plants, with particular reference to pyruvate orthophosphate dikinase. J Exp Bot 49: 1637–1646

    CAS  Google Scholar 

  • Ueno O (1998b) 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 (2004) Environmental regulation of photosynthetic metabolism in the amphibious sedge Eleocharis baldwinii and comparisons with related species. Plant Cell Env 27: 627–639

    CAS  Google Scholar 

  • Ueno O and Samejima M (1989) Structural features of NAD-malic enzyme type C4 Eleocharis: an additional report of C4 acid decarboxylation types of the Cyperaceae. Bot Mag 102: 393–402

    CAS  Google Scholar 

  • Ueno O and Sentoku N (2006) Comparison of leaf structure and photosynthetic characteristics of C3 and C4 Alloteropsis semialata subspecies. Plant Cell Env 29: 257–268

    CAS  Google Scholar 

  • Ueno O and Wakayama M (2004) Cellular expression of C3 and C4 photosynthetic enzymes in the amphibious sedge Eleocharis retroflexa ssp. chaetaria. J Plant Res 117: 433–441

    PubMed  CAS  Google Scholar 

  • Ueno O, Takeda T and Murata T (1986) C4 acid decarboxylating enzyme activities of the C4 species possessing Kranz anatomical types in the Cyperaceae. Photosynthetica 20: 111–116

    CAS  Google Scholar 

  • Ueno O, Takeda T and Maeda E (1988a) Leaf ultrastructure of C4 species possessing different Kranz anatomical types in the Cyperaceae. Bot Mag 101: 141–152

    Google Scholar 

  • Ueno O, Samejima M and Koyama T (1989). Distribution and evolution of C4 syndrome in Eleocharis, a sedge group inhabiting wet and aquatic environments, based on culm anatomy and carbon isotope ratios. Ann Bot 64: 425–438

    Google Scholar 

  • Ueno O, Samejima M, Muto S and Miyachi S (1988b) 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

    PubMed  CAS  Google Scholar 

  • Vasilevskaya VK and Butnik AA (1981) The types of the anatomical structure of the dicotyledon leaves (a contribution to the method of anatomical description). Bot Zh 66: 992–1001 (In Russian)

    Google Scholar 

  • Vicentini A, Barber JC, Aliscioni SS, Giussani LM and Kellogg EA (2008) The age of the grasses and clusters of origins of C4 photosynthesis. Global Change Biology 14: 2963–2977

    Google Scholar 

  • von Caemmerer S (1989) A model of photosynthetic CO2 assimilation and carbon-isotope discrimination in leaves of certain C3-C4 intermediates. Planta 178: 463–474

    Google Scholar 

  • Voznesenskaya EV and Gamaley YV (1986) The ultrastructural characteristics of leaf types with Kranz-anatomy. Bot Zh 71: 1291–1307 (In Russian)

    Google Scholar 

  • Voznesenskaya EV, Franceschi VR, Pyankov VI and Edwards GE (1999) Anatomy, chloroplast structure and compartmentation of enzymes relative to photosynthetic mechanisms in leaves and cotyledons of species in the tribe Salsoleae (Chenopodiaceae). J Exp Bot 50: 1779–1795

    CAS  Google Scholar 

  • Voznesenskaya EV, Franceschi VR, Kiirats O, Freitag H and Edwards GE (2001) Kranz anatomy is not essential for terrestrial C4 plant photosynthesis. Nature 414: 543–546

    PubMed  CAS  Google Scholar 

  • Voznesenskaya EV, Franceschi VR, Kiirats O, Artyusheva EG, Freitag H and Edwards GE (2002) Proof of C4 photosynthesis without Kranz anatomy in Bienertia cycloptera (Chenopodiaceae). Plant J 31: 649–662

    PubMed  CAS  Google Scholar 

  • Voznesenskaya EV, Edwards GE, Kiirats O, Artyusheva EG and Franceschi VR (2003) Development of biochemical specialization and organelle partitioning in the single celled C4 system in leaves of Borszczowia aralocaspica (Chenopodiaceae). Am J Bot 90: 1669–1680

    PubMed  CAS  Google Scholar 

  • Voznesenskaya EV, Franceschi VR and Edwards GE (2004) Light-dependent development of single cell C4 photosynthesis in cotyledons of Borszczowia aralocaspica (Chenopodiaceae) during transformation from a storage to a photosynthetic organ. Ann Bot 93: 1–11

    Google Scholar 

  • Voznesenskaya EV, Chuong SDX, Kirrats O, Franceschi VR and Edwards GE (2005a) Evidence that C4 species in genus Stipagrostis, family Poaceae, is NADP-malic enzyme subtype with nonclassical type of Kranz anatomy (Stipagrostoid). Plant Sci 168: 731–739

    CAS  Google Scholar 

  • Voznesenskaya EV, Chuong SDX, Koteeva NK, Edwards GE and Franceschi VR (2005b) Functional compartmentation of C4 photosynthesis in the triple-layered chlorenchyma of Aristida (Poaceae). Funct Plant Biol 32: 67–77

    CAS  Google Scholar 

  • Voznesenskaya EV, Koteyeva NK, Chuong SDX, Edwards GE, Akhani H and Franceschi VR (2005c) Differentiation of cellular and biochemical features of the single-cell C4 syndrome during leaf development in Bienertia cycloptera (Chenopodiaceae). Am J Bot 92: 1784–1795

    PubMed  CAS  Google Scholar 

  • Voznesenskaya EV, Franceschi VR, Chuong SDX and Edwards GE (2006) Functional characterization of phosphoenolpyruvate carboxykinase type C4 leaf anatomy: Immuno, cytochemical and ultrastructural analyses. Ann Bot 98: 77–91

    PubMed  CAS  Google Scholar 

  • Voznesenskaya EV, Chuong S, Koteyeva N, Franceschi VR, Freitag H and Edwards GE (2007) Structural, biochemical and physiological characterization of C4 photosynthesis in species having two vastly different types of Kranz anatomy in genus Suaeda (Chenopodiaceae). Plant Biol 9: 745–757

    PubMed  CAS  Google Scholar 

  • Voznesenskaya EV, Akhani H, Koteyeva NK, Chuong SDX, Roalson EH, Kiirats O, Franceschi VR and Edwards GE (2008) Structural, biochemical and physiological characterization of photosynthesis in two C4 subspecies of Tecticornia indica and the C3 species Tecticornia pergranulata (Chenopodiaceae). J Exp Bot 59: 1715–1734

    PubMed  CAS  Google Scholar 

  • Voznesenskaya EV, Koteyeva NK, Edwards GE and Ocampo G (2010) Anatomical and biochemical characterization of photosynthetic types in genus Portulaca L. (Portulacaceae). J Exp Bot 61:3647–3662

    Google Scholar 

  • Wakayama M, Ueno O and Ohnishi J (2002) Cellular accumulation of photosynthetic enzymes during leaf development of Arundinella hirta, a C4 grass with unusual Kranz cells without contact with vascular tissues. Plant Cell Physiol 43: S173–S173

    Google Scholar 

  • Wakayama M, Ueno O and Ohnishi J (2003) Photosynthetic enzyme accumulation during leaf development of Arundinella hirta, a C4 grass having Kranz cells not associated with vascular tissues. Plant Cell Physiol 44: 1330–1340

    PubMed  CAS  Google Scholar 

  • Wakayama M, Ohnishi J and Ueno O (2006) Structure and enzyme expression in photosynthetic organs of the atypical C4 grass Arundinella hirta. Planta 223: 1243–1255

    PubMed  CAS  Google Scholar 

  • Walker RP and Chen Z-H (2002) Phosphoenolpyruvate carboxykinase: Structure, function and regulation. In: Callow JA (ed) Advances in Botanical Research Incorporating Advances in Plant Pathology, pp 93–189. Academic Press, New York

    Google Scholar 

  • Wingler A, Walker RP, Chen Z-H and Leegood RC (1999) Phosphoenolpyruvate carboxykinase is involved in the decarboxylation of aspartate in the bundle sheath of maize. Plant Physiol 120: 539–545

    PubMed  CAS  Google Scholar 

  • Winter K (1981) C4 plants of high biomass in arid regions of Asia. Occurrence of C4 photosynthesis in Chenopodiaceae and Polygonaceae from the middle east and USSR. Oecologia 48: 100–106

    Google Scholar 

  • Winter K, Kramer D, Troughton JH and Card KA (1977) C4 pathway of photosynthesis in a member of the Polygonaceae: Calligonum persicum (Boiss. and Buhse) Boiss. Z Pflanzenphysiol 81: 341–346

    CAS  Google Scholar 

  • Yoshimura Y, Kubota F and Ueno O (2004) Structural and biochemical bases of photorespiration in C4 plants: quantification of organelles and glycine decarboxylase. Planta 220: 307–317

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This material is based upon work supported by the National Science Foundation under Grant Nos. IBN-0131098, IBN-0236959 and IBN-0641232, by Civilian Research and Development Foundation grants RB1-2502-ST-03 and RUB1-2829-ST-06, by Russian Foundation of Basic Research grant 05-04-49622 and 08-04-00936,and Bill and Melinda Gates Foundation to IRRI for C4 Rice Program. We also thank the Franceschi Microscopy and Imaging Center of Washington State University for use of their facilities and staff assistance, and C. Cody for plant growth management. The authors appreciate the helpful discussions with Dr. Nuria Koteyeva and the advice of two reviewers, especially in the sections devoted to grasses and sedges.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Gerald E. Edwards or Elena V. Voznesenskaya .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Netherlands

About this chapter

Cite this chapter

Edwards, G.E., Voznesenskaya, E.V. (2010). Chapter 4 C4 Photosynthesis: Kranz Forms and Single-Cell C4 in Terrestrial 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_4

Download citation

Publish with us

Policies and ethics