Kranz Anatomy and the C4 Pathway

C4 photosynthesis incorporates novel leaf anatomy, metabolic specializations and modified gene expression. Plants that utilize this pathway typically possess a distinctive Kranz (or wreath) leaf anatomy, consisting of two photosynthetic cell types. These are the bundle sheath (bs) cells, which surround the vascular centres, and the mesophyll (mp) cells, which surround the bs cells. This structural framework allows for the compartmentalization and functional separation of two sets of carboxylation and decarboxylation reactions. Within C4 leaves, selective expression of bs and mp cell-specific genes leads to the selective accumulation of key photosynthetic enzymes which catalyse the different sets of cell-type-specific reactions, thereby enabling these plants to assimilate atmospheric carbon dioxide with very high efficiency. For some plants, C4 photosynthesis has facilitated their adaptation to arid conditions, high temperatures and marginal environments. Understanding the basis of this pathway has applications for improvements in agricultural productivity and alternative fuel development.

Keywords: C4; photosynthesis; bundle sheath and mesophyll cells; evolution and adaptability; C4 enzymes; gene regulation; biotechnology

Figure 1. Diagrammatic representation of Kranz anatomy and the C4 pathway. (a) Typical Kranz leaf anatomy as observed within a leaf cross-section. (b) Simplified representation of the C4 pathway superimposed on an enlarged diagram of the two cell types, indicating the cellular localization of carboxylation, decarboxylation and reassimilation reactions. v, vascular centre; bs, bundle sheath cells; mp, mesophyll cells; e, upper or lower leaf epidermal cells.
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 References
    Berry JO, McCormac DJ, Long JJ, Boinski JJ and Corey A (1997) Photosynthetic gene expression in amaranth, an NAD-ME type C4 dicot. Australian Journal of Plant Physiology 24: 423–428.
    Bevan MW and Franssen MCR (2006) Investing in green and white biotech. Nature Biotechnology 24: 765–767.
    von Caemmerer S (1992) Carbon isotope discrimination in C3-C4 intermediates. Plant, Cell & Environment 15: 1063–1072.
    von Caemmerer S and Furbank RT (2003) The C4 pathway: An efficient C4 pump. Photosynthesis Research 77: 191–207.
    Chivasa S, Berry JO, ap Rees T and Carr JP (1999) Changes in gene expression during development and thermogenesis in Arum. Australian Journal of Plant Physiology 26: 391–399.
    Chuong SDX, Vincent R, 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.
    book Dengler NG and Nelson T (1999) "Leaf structure and development in C4 plants". In: Sage RF and Monson RK (eds) C4 Plant Biology, pp 133–172. San Diego: Academic Press.
    Edwards GE, Franceschi VR, Ku MSB et al. (2001) Compartmentation of photosynthesis in cells and tissues of C4 plants. Journal of Experimental Botany 52: 577–590.
    Ehleringer JR, Cerling TE and Helliker BR (1997) C4 photosynthesis, atmospheric CO2, and climate. Oecologia 112: 285–299.
    Engelmann S, Wiludda C, Burscheidt J et al. (2008) The gene for the P-subunit of glycine decarboxylase from the C4 species Flaveria trinervia: analysis of transcriptional control in transgenic Flaveria bidentis (C4) and Arabidopsis (C3). Plant Physiology 146: 1773–1785.
    Farquhar GD, Ehleringer JR and Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40: 503–537.
    Furbank RT and Taylor WC (1995) Regulation of photosynthesis in C3 and C4 plants: a molecular approach. Plant Cell 7: 797–807.
    Harrison PA and Black CC (1982) Two-dimensional electrophoretic mapping of proteins of bundle sheath and mesophyll cells of the C4 grass Digitaria sanguinalis (L.) Scop. (Crabgrass). Plant Physiology 70: 1359–1366.
    Hatch MD (1987) C4 photosynthesis: a unique blend of modified biochemistry, anatomy, and ultrastructure. Biochemica et Biophysica Acta 895: 81–106.
    Hibberd JM and Quick WP (2002) Characteristics of C4 photosynthesis in stems and petioles of C3 flowering plants. Nature 415: 451–454.
    book Kani R and Edwards GE (1999) "The biochemistry of C4 photosynthesis". In: Sage RF and Monson RK (eds) C4 Plant Biology, pp 49–87. San Diego: Academic Press.
    Koprivova A, Melzer M, von Ballmoos P et al. (2001) Assimilatory sulfate reduction in C3, C3-C4, and C4 species of Flaveria. Plant Physiology 127: 543–550.
    Lai LB, Wang L and Nelson TM (2002) Distinct but conserved functions for two chloroplastic NADP-malic enzyme isoforms in C3 and C4 Flaveria Species. Plant Physiology 128: 125–139.
    Majeran W, Cai Y, Sun Q and van Wijka KJ (2005) Functional differentiation of bundle sheath and mesophyll maize chloroplasts determined by comparative proteomics. Plant Cell 17: 3111–3140.
    Matsuoka M, Furbank RT, Fukayama H and Miyao M (2001) Molecular engineering of C4 photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 52: 297–314.
    Nelson T and Langdale JA (1992) Developmental genetics of C4 photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 43: 25–47.
    Patel M and Berry JO (2008) Rubisco gene expression in C4 plants. Journal of Experimental Botany 59: 1625–1634.
    Patel M, Siegle A and Berry JO (2006) Untranslated regions of FbRbcS1 mRNA mediate bundle sheath cell-specific gene expression in leaves of C4 Flaveria bidentis. Journal of Biological Chemistry 281: 25485–25491.
    Reinfelder JR, Milligan AJ and Morel FMM (2004) The role of the C4 pathway in carbon accumulation and fixation in a marine diatom. Plant Physiology 135: 1–6.
    Sage RF (2004) The evolution of C4 photosynthesis. New Phytologist 161: 341–370.
    Sawers RJH, Liu P, Anufrikova K et al. (2007) A multi-treatment experimental system to examine photosynthetic differentiation in the maize leaf. BMC Genomics 8: 12 (doi: 10.1186/1471-2164-8-12).
    Sheen J (1999) C4 gene expression. Annual Review of Plant Physiology and Plant Molecular Biology 50: 187–217.
    Ueno O (2001) Environmental regulation of C3 and C4 differentiation in the amphibious sedge Eleocharis vivipara. Plant Physiology 127: 1524–1532.
    Westhoff P and Gowik U (2004) Evolution of C4 phosphoenolpyruvate carboxylase genes and proteins: a case study with the genus Flaveria. Annals of Botany 93: 1–11.
 Further Reading
    other von Caemmerer S and Furbank RT (eds) (1997) C4 photosynthesis: 30 (or 40) years on. Australian Journal of Plant Physiology 24 (4): 409–554.
    Edwards GE, Franceschi VR and Voznesenskaya EV (2004) Single cell C4 photosynthesis versus the dual-cell (Kranz) paradigm. Annual Review of Plant Physiology and Plant Molecular Biology 55: 173–196.
    Edwards GE, Furbank RT, Hatch MD and Osmond BC (2001) What does it take to be C4? Lessons from the evolution of C4 photosynthesis. Plant Physiology 125: 46–49.
    Gutierrez M, Gracen VE and Edwards GE (1974) Biochemical and cytological relationships in C4 plants. Planta 119: 279–300.
    Hatch MD (1992) C4 photosynthesis: an unlikely process full of surprises. Plant and Cell Physiology 33: 333–342.
    book Hattersley PW and Watson L (1992) "Diversification of photosynthesis". In: Chapman GP (ed.) Grass Evolution and Domestication. Cambridge: Cambridge University Press.
    Leegood RC (2002) C4 photosynthesis: principles of CO2 concentration and prospects for its introduction into C3 plants. Journal of Experimental Botany 53: 581–590.
    book Sage RF and Monson RK (eds) (1999) C4 Plant Biology. San Diego: Academic Press.
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Berry, James O, and Patel, Minesh(Dec 2008) Kranz Anatomy and the C4 Pathway. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001295.pub2]