Skip to main content
SpringerLink
Log in

Developmental Aspects of C4 Photosynthesis

  • Chapter
Photosynthesis

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 9))

Summary

Development of a fully functional C4 leaf requires modification of the C3 ground state at several hierarchical levels, including vein spacingin whole leaves, cell division and cell enlarge ment patterns within the photosynthetic tissue precursors, ultrastructural changes in bundle sheath (BS) and mesophyll (M) cells, and regulation of gene expression through differential transcription, translation, and protein turnover. Both spatial and temporal patterns of BS and M cell differentiation indicate that cell position is the primary determinate of photosynthetic cell fate and that cell-to-cell communicationi sessential for interpretation of position. The nature of signaling pathways in C4 development is unknown, but recent demonstrations of macromolecular trafficking through plasmodesmata and of the role of receptor-like kinases in tissue pattern formation provide clues to the mechanisms co-opted by C4 plants. The regulation of photosynthetic gene expression occurs at two levels (which may coincide temporally) in C4 plants: gene expression occurs first in an organ- and cell-specific way only in those cells where chloroplasts develop and replicate tohigh numbers; the positional signals involved are likely common to both C3 and C4 plants. Second, gene expression patterns that are restricted to either BS or M cells occur; these patterns are limited to C4 plants, but may use some of the same positional signals to achieve differentiation of BS and M cells. Experimental approaches that are providing insights into the developmental regulation of these genes include reporter gene fusions to identify cis-acting sequences and screens to identify mutations that disrupt C4 developmental patterns. The evidence to date indicates that each C4 gene uses its own regulatory mechanism to achieve cell specificity; even ifall cell-specific genes respond to the same signal, these signals appear to activate different mechanisms which in turn activate or repress the expression of C4 genes.

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

Access this chapter

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 509.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 649.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 649.99
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

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Abbreviations

BS:

bundle sheath

CA:

carbonic anhydrase

Cab:

chlorophyll a/b binding protein of Photosystem II light harvesting complex

chp:

chloroplastic

cyt:

cytoplasmic

E:

epidermis

GDCST:

T subunit of glycine carboxylase complex

LSu:

RuBPCase large subunit

M:

mesophyll

NAD-ME:

NAD-malic enzyme

NADP-MDH:

NADP-dependentmalic dehydrogenase

NADP-ME:

NADP-malic enzyme

P:

parenchyma

PCK.:

PEP carboxykinase

PEP:

phosphoenolpyruvate

PEPCase:

phosphoenolpyruvate carboxylase

PPDK:

pyruvate, orthophosphate dikinase

PS II:

Photosystem II

RuBPCase:

ribulose-1,5-bisphosphate carboxylase/oxygenase

V:

vein

References

  • Bauwe H and Chollet R (1986) Kinetic properties of phosphoenolpyruvate carboxylase from C3, C4, and C3-C4 intermediate species of Flaveria (Asteraceae). Plant Physiol 82: 695–699

    CAS  Google Scholar 

  • Bauwe H, Keerberg O, BassÃœner R, Pärnik T and BassÃœner B (1987) Reassimilation of carbon dioxide by Flaveria (Asteraceae) species representing different types of photosynthesis. Planta 172: 214–218

    Article  CAS  Google Scholar 

  • Becraft PW, Stinard PS and McCarty DR (1996) CRINKLY4: a TNFR-like receptor kinase involved in maize epidermal differentiation. Science 273: 1406–1409

    CAS  PubMed  Google Scholar 

  • Boffey SA (1992) Chloroplast replication. In Baker N and Thomas H (eds) Crop Photosynthesis: Spatial and Temporal Determinants, pp 361–379. Elsevier, Amsterdam

    Google Scholar 

  • Botha CEJ and Evert RF (1988) Plasmodesmatal distribution and frequency in vascular bundles and contiguous tissues of the leaf of Themeda triandra. Planta 173: 433–441

    Article  Google Scholar 

  • Bower and Birch R (1992) Transgenic sugarcane plants via microprojectile bombardment. Plant J 2: 409–416

    Article  CAS  Google Scholar 

  • Brangeon J (1973) Compared ontogeny of the two types of chloroplasts of Zea mays. J Micros 16: 233–242

    Google Scholar 

  • Broglie R, Coruzzi G, Keith B and Chua N-H (1984) Molecular biology of C4 photosynthesis in Zea mays: Differential localization of proteins and mRNAs in the two leaf cell types. Plant Molec Biol 3: 431–444

    CAS  Google Scholar 

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

    Google Scholar 

  • Bruhl JJ (1995) Sedge genera of the world: Relationships and a new classification of the Cyperaceae. Aust J Syst Bot 8: 125–305

    Google Scholar 

  • Burgess DG and Taylor WC (1987) Chloroplast photooxidation affects the accumulation of cytosolic mRNAs encoding chloroplast proteins in maize. Planta 170: 520–527

    Article  CAS  Google Scholar 

  • Carland FM and McHale MA (1996) LOP1: A gene involved in auxin transport and vascular patterning in Arabidopsis. Development 122: 1811–1819

    CAS  PubMed  Google Scholar 

  • Casas AM, Kononowicz AK, Zehr UB, Tomes DT, Axtell JD, Butler LG, Bressan RA and Hasegawa PM (1993) Transgenic sorghum plants via microprojectile bombardment. Proc Natl Acad Sci USA 90: 11212–11216

    CAS  PubMed  Google Scholar 

  • Chapman EA, Bain JM and Gove DW (1975) Mitochondria and chloroplast peripheral reticulum in the C4 plants. Aust J Plant Physiol 2: 207–223

    Google Scholar 

  • Chatterjee M, Sparvoli S, Edmunds C, Garosi P, Findlay K and Martin C (1996) DAG, a gene required for chloroplast differentiation and palisade development in Antirrhinum majus. EMBO J 15: 4194–4207

    CAS  PubMed  Google Scholar 

  • Chitty JA, Furbank RT, Marshall JS, Chen Z and Taylor WC (1994) Genetic transformation of the C4 plant Flaveria bidentis. Plant J 6: 949–956

    Article  CAS  Google Scholar 

  • Chory J (1993) Out of darkness: Mutants reveal pathways controlling light-regulated development in plants. Trends Genet 9: 167–172

    Article  CAS  PubMed  Google Scholar 

  • Chu C-C, Qu N, Bassüner B and Bauwe H (1997) Genetic transformation of the C3-C4 intermediate species, Flaveria pubescens (Asteraceae). Plant Cell Rep 16: 715–718

    Article  CAS  Google Scholar 

  • Crookston RK and Moss DN (1974) Interveinal distance for carbohydrate transport in leaves of C3 and C4 grasses. Crop Sci 14: 123–125

    Google Scholar 

  • Cyr RJ (1994) Microtubules in plant morphogenesis: Role of the cortical array. Annu Rev Cell Biol 10: 153–180

    Article  CAS  PubMed  Google Scholar 

  • Dengler NG and Nelson T (1999) Leafstructure and development in C4 plants. In: Sage RF and Monson RK (eds) C4 Plant Biology, 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). Amer J Bot 72: 284–302

    Google Scholar 

  • Dengler NG, Dengler RE and Hattersley PW (1986) Comparative bundle sheath and mesophyll differentiation in the leaves of the C4 grasses Panicum effusum and P. bulbosum. Amer J Bot 73: 1431–1442

    Google Scholar 

  • Dengler NG, Dengler RE, Donnelly PM and Hattersley PW (1994) Quantitative leaf anatomy of C3 and C4 grasses (Poaceae): Bundle sheath and mesophyll surface area relationships. Ann Bot 73: 241–255

    Article  Google Scholar 

  • Dengler NG, Dengler RE, Donnelly PM and Filosa M (1995) Expression of the C4 pattern of photosynthetic enzyme accumulation during leaf development in Atripex rosea (Chenopodiaceae) Amer J Bot 82: 318–327

    CAS  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) Amer J Bot 83: 1391–1405

    Google Scholar 

  • Dengler NG, Woodvine MA, Donnelly PM and Dengler RE (1997) Formation of vascular pattern in developing leaves of the C4 grass Arundinella hirta. Int J Plant Sci. 158: 1–12

    Article  Google Scholar 

  • Downton WJS (1975) The occurrence of C4 photosynthesis among plants. Photosynthetica 9: 96–105

    Google Scholar 

  • Eastman PAK, Dengler MG and Peterson CA (1988) Suberized bundle sheaths in grasses (Poaceae) of different photosynthetic types. I. Anatomy, ultrastructure and histochemistry. Protoplasma 142: 92–111

    CAS  Google Scholar 

  • Edwards G and Walker D (1983) C3, C4: Mechanism, and Cellular and Environmental Regulation of Photosynthesis. Blackwell Scientific Publications, Oxford.

    Google Scholar 

  • Ellis JR and Leech RM (1985) Cell size and chloroplast size in relation to chloroplast replication in light-grown wheat leaves. Planta 165: 120–125

    Article  Google Scholar 

  • Ernst K and Westhoff P (1997) The phosphoenolpyruvate carboxylase (ppc) gene family of Flaveria trinervia (C4) and F. pringlei (C3): Molecular characterisation and expression analysis of the ppcB and ppcC genes. Plant Molec Biol 34: 427–443

    CAS  Google Scholar 

  • Esau K (1965) Plant Anatomy. John Wiley and Sons, New York

    Google Scholar 

  • Evert RF, Russin WA and Bosabalidis AM (1996) Anatomical and ultrastructural changes associated with sink-to-source transition in developing maize leaves. Int J Plant Sci 157: 247–261

    Article  Google Scholar 

  • Ewing RM, Jenkins GI and Langdale JA (1998) Transcripts of maize RbcS genes accumulate differentially in C3-and C4-tissues. Plant Molec Biol 36: 593–599

    CAS  Google Scholar 

  • Fladung M (1994) Genetic variants of Panicum maximum (Jacq.) in C4 photosynthetic traits. J Plant Physiol 143: 165–172

    CAS  Google Scholar 

  • Fowler JE and Freeling M (1996) Genetic analysis of mutations that alter cell fates in maize leaves: Dominant liguleless mutations. Devel Genet 18: 198–222

    CAS  Google Scholar 

  • Fromm ME, Morrish F, Armstrong C, Williams R, Thomas J and Klein TM (1990) Inheritance and expression of chimeric genes in the progeny of transgenic maize plants. Bio/Technology 8: 833–839

    Article  CAS  PubMed  Google Scholar 

  • Furbank RT and Taylor WC (1995) Regulation of photosynthesis in C3 and C4 plants: A molecular approach. Plant Cell 7: 797–807

    Article  CAS  PubMed  Google Scholar 

  • Furbank RT, Chitty JA, Jenkins CLD, Taylor WC, Trevanion SJ, von Caemmerer S and Ashton AR (1997) Genetic manipulation of key photosynthetic enzymes in the C4 plant Flaveria bidentis. Aust J Plant Physiol 24: 477–485

    CAS  Google Scholar 

  • Glackin CA and Grula JW (1990) Organ-specific transcripts of different size and abundance derive from the same pyruvate, orthophosphate dikinase gene in maize. Proc Natl Acad Sci USA 87: 3004–3008

    CAS  PubMed  Google Scholar 

  • Gordon-Kamm WJ, Spencer TM, Mangano ML, Adams TR, Daines RJ, Start WG, O’ Brien JV, Chambers SA, Adams WR, Willetts NG, Rice TB, Mackey CJ, Krueger RW, Kausch AP and Lemaux PG (1990) Transformation of maize cells and regeneration of fertile transgenic plants. Plant Cell 2: 603–618

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hake S and Freeling M (1986) Analysis of genetic mosaics shows that the extra epidermal cell division in Knotted mutant maize plants are induced by adjacent mesophyll cells. Nature 320: 621–623

    Article  Google Scholar 

  • Hall LN, Rossini L, Cribb L and Langdale JA (1998) GOLDEN 2, a novel transcriptional regulator of cellular differentiation in the maize leaf. Plant Cell 10: 925–936

    Article  CAS  PubMed  Google Scholar 

  • Harpster M and Taylor WC (1986) Maize phosphoenolpyryvate carboxylase: Cloning and characterization of mRNAs encoding isozymic forms. J Biol Chem 261: 6132–6136

    CAS  PubMed  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 and Burnell JN (1990) Carbonic anhydrase activity in leaves and its role in the first step in C4 photosynthesis. Plant Physiol 93: 380–383

    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 (1984) Characterization of C4 leaf anatomy in grasses (Poaceae). Mesophyll:bundle sheath ratios. Ann Bot 53: 163–179

    Google Scholar 

  • Hattersley, PW (1987) Variation in photosynthetic pathway. In: Soderstrom TR, Campbell CS and Barkworth ME (eds) Grass Systematics and Evolution, pp 49–64. Smithsonian Institution Press, Washington DC

    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

    Article  Google Scholar 

  • Hattersley PW and Watson L (1975) Anatomical parameters for predicting photosynthetic pathways of grassleaves: The ‘maximum lateral cell count’ and the ‘maximum cells distant count’. Phytomorphology 25: 325–333

    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 

  • Haupt W (1982) Light-mediated movement of chloroplasts. Annu Rev Plant Physiol 33: 205–233

    Article  CAS  Google Scholar 

  • Hermans J and Westhoff P (1990) Analysis of expression and evolutionary relationships of phosphoenolpyruvate carboxylase genes in Flaveria trinervia (C4) and F. pringlei (C3). Molec Gen Genet 224: 459–468

    Article  CAS  PubMed  Google Scholar 

  • Hermans J and Westhoff P (1992) Homologous genes for the C4 isoform of phosphoenolpyruvate carboxylase in a C3 and a C4Flaveria species. Molec Gen Genet 234: 275–284

    Article  CAS  PubMed  Google Scholar 

  • Hudspeth RL, Glackin CA, Bonner J and Grula JW (1986) Genomic and cDNA clones for maize phosphoenolpyruvate carboxylase and pyruvate, orthophosphate dikinase: Expression of different genefamily members in leaves and roots. Proc Natl Acad Sci USA 83: 2884–2888

    CAS  Google Scholar 

  • Hylton CM, Rawsthorne S, Smith AM and Jones DA (1988) Glycine decarboxylase is confined to the bundle-sheath cells of leaves of C3-C4 intermediate species. Planta 175: 452–459

    Article  CAS  Google Scholar 

  • Ishida Y, Saito H, Ohta S, Hiei Y, Komari T and Kumashiro T (1996) High efficiency transformation of maize mediated by Agrobacterium tumefaciens. Natur Biotech 14: 745–750

    CAS  Google Scholar 

  • Jackson E, Veit B and Hake S (1994) Expression of maize KNOTTED-related homeobox genes in the shoot apical meristem predicts pattern of morphogenesis in the vegetative shoot. Development 120: 405–413

    CAS  Google Scholar 

  • Jang J-C and Sheen J (1997) Sugar sensing in higher plants. Trends Plant Sci 2: 208–214

    Article  Google Scholar 

  • Kawamitsu Y, Hakoyama S, Agata W and Takeda T (1985) Leaf interveinal distances corresponding to anatomical types in grasses. Plant Cell Physiol 26: 589–593

    Google Scholar 

  • Keddie J, Carroll B, Jones JDG and Gruissem W (1996) The DCL gene of tomato is required for chloroplast development and palisade cell morphogenesis in leaves. EMBO J 15: 4208–4217

    CAS  PubMed  Google Scholar 

  • Kellogg EA (1996) Integrating genetics, phylogenetics, and developmental biology. In: Sobral BWS (ed) The Impact of Plant Molecular Genetics, pp 159–172. Birhauser, Boston

    Google Scholar 

  • Kirchanski SJ (1975) The ultrastructural development of the dimorphic plastids of Zea mays. Amer J Bot 62: 695–705

    Google Scholar 

  • Koch KE (1996) Carbohydrate-modulated gene expression in plants. Annu Rev Plant Physiol Plant Molec Biol 47: 509–540

    CAS  Google Scholar 

  • Kopriva S, Cossu R and Bauwe H (1995) Alternative splicing results in two different transcripts for the H-protein of the glycine cleavage system in the C4 species Flaveria trinervia. Plant J 8: 435–441

    Article  CAS  PubMed  Google Scholar 

  • Kragler F. Lucas WJ and Monzer J (1998) Plasmodesmata: Dynamics, domains and patterning. Ann Bot 81: 1–10

    Article  Google Scholar 

  • Ku MSB, Kano-Murakami Y and Matsuoka M (1996) Evolution and expression of C4 photosynthesis genes. Plant Physiol 111: 949–957

    Article  CAS  PubMed  Google Scholar 

  • Kubicki A, Steinmuller K and Westhoff P (1994) Differential transcription of plastome-encoded genes in the mesophyll and bundle-sheath chloroplasts of the monocotyledonous NADP-malic enzyme-type C4 plants maize and Sorghum. Plant Mol Biol 25: 669–679

    Article  CAS  PubMed  Google Scholar 

  • Laetsch WM (1974) The C4 syndrome: A structural analysis Ann Rev Plant Physiol 25: 27–52

    CAS  Google Scholar 

  • Laetsch WM and Price I (1969) Development of the dimorphic chloroplasts of sugar cane. Amer J Bot 56: 77–87

    Google Scholar 

  • Lal A and Edwards GE (1996) Analysis of inhibition of photosynthesis under water stress in the C4 species Amaranthus cruentus and Zea mays: Electron transport, CO2 fixation and carboxylation capacity. Aust J Plant Physiol 23: 403–412

    CAS  Google Scholar 

  • Langdale JA and Kidner CA (1994) bundle sheath defective, a mutation that disrupts cellular differentiation in maize leaves. Development 120: 673–681

    Google Scholar 

  • Langdale JA and Nelson T (1991) Spatial regulation of photosynthetic development in C4 plants. Trends Genet 7: 191–196

    CAS  PubMed  Google Scholar 

  • Langdale JA, Rothermel BA and Nelson T. (1988a) Cellular patterns of photosynthetic gene expression in developing maize leaves. Genes Devel 2: 106–115

    CAS  PubMed  Google Scholar 

  • Langdale JA, Zelitch I, Miller E and Nelson T (1988b) Cell position and light influence C4 versus C3 patterns of photosynthetic gene expression in maize. EMBO J 7: 3643–351

    CAS  PubMed  Google Scholar 

  • Larkin JC, Young N, Prigge M and Marks MD (1996) The control of trichome spacing and number in Arabidopsis. Development 122: 997–1005

    CAS  PubMed  Google Scholar 

  • Lepiniec L, Keryer E, Philippe H, Gadal P and Cretin C (1993) Sorghum phosphoenolpyruvate carboxylase gene family: Structure, function and molecular evolution. Plant Molec Biol 21: 487–502

    CAS  Google Scholar 

  • Liu YQ and Dengler NG (1994) Bundle sheath and meosphyll cell differentiation in the C4 dicotyledon Atriplex rosea: Quantitative ultrastructure. Can J Bot 72: 644–657

    Google Scholar 

  • Lloyd CW, Venverloo CJ, Goodbody KC and Shaw PJ (1992) Confocal lasermicroscopy and three-dimensional reconstruction of nucleus-associated microtubules in the division plane of vacuolated plant cells. J Micros 166: 99–109

    Google Scholar 

  • Long JJ and Berry JO (1996) Tissue-specific and light-mediated expression of the C4 photosynthetic NAD-dependent malic enzyme of amaranth mitochondria. Plant Physiol 112: 473–482

    CAS  PubMed  Google Scholar 

  • Lucas WJ (1995) Plasmodesmata: Intercellular channels for macromolecular transport in plants. Curr Opinion Cell Biol 7: 673–680

    Article  CAS  PubMed  Google Scholar 

  • Lucas WJ, Bouche-Pillon S, Jackson DO, Nguyen L Baker L, Ding B and Hake S (1995) Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 270: 1980–1983

    CAS  PubMed  Google Scholar 

  • Lukowitz W, Mayer U and Jurgens G (1996) Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product. Cell 84: 61–71

    Article  CAS  PubMed  Google Scholar 

  • Marshall JS, Stubbs JD and Taylor WC (1996) Two genes encode highly similar chloroplastic NADP-malic enzymes in Flaveria: Implications for the evolution of C1 photosynthesis. Plant Physiol 111: 1251–1261

    Article  CAS  PubMed  Google Scholar 

  • Marshall JS, Stubbs JD, Chitty JA, Surin B and Taylor WC (1997) Expression of the C4Mel gene from Flaveria bidentis requires an interaction between 5′ and 3′ and sequences. Plant Cell 9: 1515–1525

    Article  CAS  PubMed  Google Scholar 

  • Matsuoka M (1995) The gene for pyruvate, or thophosphate dikinase in C4 plants: Structure, regulation and evolution. Plant Cell Physiol 36: 1–7

    Google Scholar 

  • Matsuoka M and Numazawa T (1991) Cis-acting elements in the pyruvate, orthophosphate dikinase gene in maize. Molec Gen Genet 228: 143–152

    Article  CAS  PubMed  Google Scholar 

  • Matsuoka M, Tada Y, Fujimura T and Kano-Murakami Y (1993) Tissue-specific light-regulated expression directed by the promoter of a C4 gene, maize pyruvate, or thophosphate dikinase, in a C3 plant, rice. Proc Natl Acad Sci USA 90: 9586–9590

    CAS  PubMed  Google Scholar 

  • Matsuoka M, Kyozuka J, Shimamoto K, Kano-Murakami Y (1994) The promoters of two carboxylases in a C4 plant (maize) direct cell-specific, light-regulated expression in a C3 plant (rice). Plant J 6: 311–319

    Article  CAS  PubMed  Google Scholar 

  • McCormac D, Boinski JJ, Ramsperger VC and Berry JO (1997) C4 gene expression in photosynthetic and non-photosynthetic leaf regions of Amaranthus tricolor. Plant Physiol 114: 801–815

    CAS  PubMed  Google Scholar 

  • Meierhoff K and Westhoff P (1993) Differential biogenesis of Photosystem II in mesophyll and bundle-sheath cells of monocotyledonous NADP-malic enzyme-type C4 plants: The non-stoichiometric abundance of the subunits of Photosystem II in the bundle sheath chloroplasts and the translational activity of the plastome-encoded genes. Planta 191: 23–33

    Article  CAS  Google Scholar 

  • Miyake H and Nakamura M (1993) Some factors concerning the centripetal disposition of bundle sheath chloroplasts during the leaf development of Eleusine coracana. Ann Bot 72: 205–211

    Article  Google Scholar 

  • Miyake H and Yamamoto Y (1987) Centripetal disposition of bundle sheath chloroplasts during the leaf development of Eleusine coracana. Ann Bot 60: 641–647

    Google Scholar 

  • Monson RK (1996) The use of phylogenetic perspective in comparative plant physiology and developmental biology. Ann Missouri Bot Gard 83: 3–16

    Google Scholar 

  • Moore PD (1982) Evolution of photosynthetic pathways in flowering plants. Nature 295: 647–648

    Google Scholar 

  • Moose SP and Sisco PH (1996) Glossy 15, an APETALA2-like gene from maize that regulates leaf epidermal cell identity. Genes Devel 10: 3018–3027

    CAS  PubMed  Google Scholar 

  • Nelson T and Dengler NG (1992) Photosynthetic tissue differentiation in C4 plants. Intl J Plant Sci 153: 93–105

    Google Scholar 

  • Nelson T and Langdale JA (1992) Developmental genetics of C4 plants. Ann Rev Plant Physiol Mol Biol 43: 25–47

    Article  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: 629–637

    Article  CAS  Google Scholar 

  • O’Brien TP and Carr DJ (1970) A suberized layer in the cell walls of the bundle sheath of grasses. Aust J Biol Sci 23: 275–287

    Google Scholar 

  • Oelmuller R (1989) Photooxidative destruction of chloroplasts and its effects on nuclear gene expression and extraplastidic enzyme levels. Photochem Photobiol 49: 229–239

    Google Scholar 

  • Ohnishi J and Kanai R (1983) Differentiation of photorespiratory activity between mesophyll and bundle sheath cells of C4 plants. I. Glycine oxidation by mitochondria. Plant Cell Physiol 24: 1411–1420

    CAS  Google Scholar 

  • Oswald A, Streubel M, Ljungberg U, Hermans J, Eskins K and Westhoff P (1990) Differential biogenesis of photosystem-II in mesophyll and bundle-sheath cells of ‘malic’ enzyme NADP=-type C4 plants. Eur J Biochem 190: 185–194

    Article  CAS  PubMed  Google Scholar 

  • Przemack GKH, Mattsson J, Hardtke CS, Sung ZR and Berleth T (1996) Studies on the role of the Arabidopsis gene MONOPTEROS in vascular development and plant cell axialization. Planta 200: 229–237

    Google Scholar 

  • Pyke KA and Leech RM (1992) Chloroplast division and expansion is radically altered by nuclear mutations in Arabidopsis thaliana. Plant Physiol 99: 1005–1008

    CAS  Google Scholar 

  • Pyke KA and Leech RM (1994) A genetic analysis of chloroplast division and expansion in Arabidopsis thaliana. Plant Physiol 104: 201–207

    CAS  PubMed  Google Scholar 

  • Pyke KA, Rutherford SM, Robertson EJ and Leech RM (1994) arc6, a fertile Arabidopsis mutant with only two mesophyll cell chloroplasts. Plant Physiol 106: 1169–1177

    CAS  PubMed  Google Scholar 

  • Raghavendra AS and Das VSR (1978) The occurrence of C4-photosynthesis: A supplementary list of C4 plants reported during late 1974-mid 1977. Photosynthetica 12: 200–208

    CAS  Google Scholar 

  • Ramsperger VC, Summers RG and Berry JO (1996) Photosynthetic gene expression in meristems and during initial leaf development in a C4 dicotyledonous plant. Plant Physiol 111: 999–1010

    CAS  PubMed  Google Scholar 

  • Reiter RS, Coomber SA, Bourett TM, Bartley GE and Scolnik PA (1994) Control of leaf and chloroplast development by the Arabidopsis gene pale cress. Plant Cell 6: 1253–1264

    Article  CAS  PubMed  Google Scholar 

  • Robinson-Beers K and Evert RF (1991a) Ultrastructure of and plasmodesmatal frequency in mature leaves of sugarcane. Planta 184: 291–306

    Google Scholar 

  • Robinson-Beers and Evert RF (1991b) Fine structure of plasmodesmata in mature leaves of sugarcane. Planta 184: 307–318

    Google Scholar 

  • Rosche E and Westhoff P (1995) Genomic structure and expression of the pyruvate, orthophosphate dikinase gene of the dicotyledonous C4 plant Flaveria trinervia (Asteraceae). Plant Molec Biol 29: 663–678

    CAS  Google Scholar 

  • Rosche E, Chitty J, Westhoff P and Taylor WC (1998) Analysis of promoter activity for the gene encoding pyruvate, or thophosphate dikinase in stably transformed C4Flaveria. Plant Physiol 117: 821–829

    Article  CAS  PubMed  Google Scholar 

  • Roth R, Hall LN, Brutnell TP and Langdale JA (1996) bundle sheath defective 2, a mutation that disrupts the coordinated development of bundle sheath and mesophyll cells in the maize leaf. Plant Cell 8: 915–927

    Article  CAS  PubMed  Google Scholar 

  • Rydzik E, Boinski JJ, Long JJ and Berry JO (1996) Copy number of C4 photosynthetic genes in Amaranthus hypochondriacus. Legacy, Newsletter of the American Amaranth Institute 9: 12–16

    Google Scholar 

  • Sachs T (1981) The control of patterned differentiation of vascular tissues. Adv Bot Res 9: 151–262

    Google Scholar 

  • Sachs T (1989) The development of vascular networks during leaf development. Curr Top Plant Biochem Physiol 8: 168–183

    Google Scholar 

  • Sachs T (1991) Cell polarity and tissue patterning in plants. Development (Supplement) 1: 83–93

    Google Scholar 

  • Schäffner AR and Sheen J (1991) Maize rbcS promoter activity depends on sequence elements not found in dicot rbcS promoters. Plant Cell 3: 997–1012

    PubMed  Google Scholar 

  • Schäffner A and Sheen J (1992) Maize C4 photosyn thesis involves differential regulation of phosphoenolpyruvate carboxylase genes. Plant J 2: 221–232

    PubMed  Google Scholar 

  • Schuster G, Ohad I, Martineau B and Taylor WC (1985) Differentiation and development of bundle sheath and mesophyll thylakoids in maize. J Biol Chem 260: 11866–11873

    CAS  PubMed  Google Scholar 

  • Sheen J (1990) Metabolic repression of transcription in higher plants. Plant Cell 2: 1027–1038

    Article  CAS  PubMed  Google Scholar 

  • Sheen J (1991) Molecular mechanisms underlying the differential expression of maize pyruvate, orthophosphate dikinase genes. Plant Cell 3: 225–245

    Article  CAS  PubMed  Google Scholar 

  • Sheen J-Y and Bogorad L (1986) Differential expression of six light-harvesting chlorophyll a/b binding protein genes in maize leaf cell types. Proc Natl Acad Sci USA 83: 7811–7815

    CAS  PubMed  Google Scholar 

  • Sheen J-Y and Bogorad L (1987) Expression of the ribulose-1,5-bisphosphate carboxylase large subunit gene and three small subunit genes in two cell types of maize leaves. EMBO J 5: 3417–3422

    Google Scholar 

  • Sinha NR and Kellogg EA (1996) Parallelism and diversity in multiple origins of C4 photosynthesis in the grass family. Amer J Bot 83: 1458–1470

    Google Scholar 

  • Smith LG, Greene B, Veit B and Hake S (1992) A dominant mutation in the maize homeobox gene, Knotted-1, causes its ectopic expression in leafcells with altered fates. Development 116: 21–30

    CAS  PubMed  Google Scholar 

  • Sprey B and Laetsch WM (1978) Structural studies of peripheral reticulum in C4 plant chloroplasts of Portulaca oleracea. Z Pflanzenphysiol 87: 37–53

    Google Scholar 

  • Stockhaus J, Poetsch W, Steinmüller K and Westhoff P (1994) Evolution of the C4 phosphoenolpyruvate carboxylase promoter of the C4 dicot Flaveria trinervia: An expression analysis in the C3 plant tobacco. Molec Gen Genet 245: 286–293

    Article  CAS  PubMed  Google Scholar 

  • Stockhaus J, Schlue U, Koczor M, Chitty JA, Taylor WC and Westhoff P (1997) The promoter of the gene encoding the C4 form of phosphoenolpyruvate carboxylase directs mesophyll specific expression in transgenic C4 Flaveria. Plant Cell 9: 479–489

    Article  PubMed  Google Scholar 

  • Taylor WC (1989) Regulatory interactions between nuclear and plastid genomes. Ann Rev Plant Physiol Plant Molec Biol 40: 211–233

    CAS  Google Scholar 

  • Telfer A, Bollman KM and Poethig RS (1997) Phase change and the regulation of trichome distribution in Arabidopsis thaliana. Development 124: 645–654

    CAS  PubMed  Google Scholar 

  • Thompson WF and White MJ (1991) Physiological and molecular studies oflight-regulated nuclear genes in higher plants. Annu Rev Plant Physiol Plant Molec Biol 42: 423–466

    CAS  Google Scholar 

  • Tobin EM and Silverthorne J (1985) Light regulation of gene expression in higher plants. Annu Rev Plant Physiol 36: 569–593

    Article  CAS  Google Scholar 

  • Torii KU, Mitsukawa N, Oosumi T, Matsuura Y, Yokoyama R, Whittier RF and Komeda Y (1996) The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell 8: 735–746

    Article  CAS  PubMed  Google Scholar 

  • Torres-Ruiz R and Jurgens G (1994) Mutations in the FASS gene uncouple pattern formation and morphogenesis in Arabidopsis development. Development 120: 2967–2978

    CAS  PubMed  Google Scholar 

  • Traas JA, Bellini C, Macry P, Kronenberger P, Bouchez D and Caboche M (1995) Normal differentiation patterns in plants lacking microtubular preprophase bands. Nature 375: 676–677

    Article  CAS  Google Scholar 

  • Ueno O (1996) 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, Takeda T and Maeda E (1988) Leaf ultrastructure of C4 species possessingdifferent Kranz anatomical types in the Cyperaceae. Bot Mag 101: 141–152

    Google Scholar 

  • Viret J-F, Mabrouk Y and Bogorad L (1994) Transcriptional photo-regulation of cell-type-preferred expression of maize rbcS-m3: 3′ and 5′ sequences are involved. Proc Natl Acad Sci USA 91: 8577–8581

    CAS  PubMed  Google Scholar 

  • von Arnim A and Deng X-W (1996) Light control of seedling development. Annu Rev Plant Physiol Plant Molec Biol 47: 215–243

    Google Scholar 

  • Walker JC (1994) Structure and function of the receptor-like protein kinases of higher plants. Plant Mol Biol 26: 1599–1609

    Article  CAS  PubMed  Google Scholar 

  • Wang J-L, Long JJ, Hotchkiss T and Berry JO (1993a) Regulation of C4 gene expression in light-and dark-grown amaranth cotyledons. Plant Physiol 102: 1085–1093

    Article  CAS  PubMed  Google Scholar 

  • Wang J-L, Turgeon R, Carr JP and Berry JO (1993b) Carbon sink-to-source transition is coordinated with establishment of cell-specific gene expression in a C4 plant. Plant Cell 5: 289–296

    CAS  PubMed  Google Scholar 

  • Williamson RE (1986) Organelle movements along actin filaments and microtubules. Plant Physiol 82: 631–634

    CAS  Google Scholar 

  • Woo KC, Anderson JM, Boardman NK, Downton WJS, Osmond CR and Thorne SW (1970) Deficient Photosystem II in agranal bundle sheath chloroplasts of C4 plants. Proc Natl Acad Sci USA 67: 18–25

    CAS  Google Scholar 

  • Wrischer M (1989) Ultrasrructural localization of photosynthetic activity in thylakoids during chloroplast development in maize. Planta 177: 18–23

    Article  CAS  Google Scholar 

  • Yanagisawa S and Sheen J (1998) Involvement of maize Dof zinc finger proteins in tissue-specific and light-regulated gene expression. Plant Cell 10: 75–89

    Article  CAS  PubMed  Google Scholar 

  • Yang M and Sack FD (1995) The too many mouths and four lips mutations affect stomatal production in Arabidopsis. Plant Cell 7: 2227–2239

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Botany, University of Toronto, Toronto, Ontario, M5S 1A1, Canada

    Nancy G. Dengler

  2. CSIRO Plant Industry, GPO Box 1600, Canberra, 2601, Australia

    William C. Taylor

Authors
  1. Nancy G. Dengler
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. William C. Taylor
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Robert Hill Institute, University of Sheffield, UK

    Richard C. Leegood

  2. Department of Botany, University of Wisconsin, USA

    Thomas D. Sharkey

  3. Research School of Biological Sciences, Australian National University, Australia

    Susanne von Caemmerer

Rights and permissions

Reprints and permissions

Copyright information

© 2000 Kluwer Academic Publishers

About this chapter

Cite this chapter

Dengler, N.G., Taylor, W.C. (2000). Developmental Aspects of C4 Photosynthesis. In: Leegood, R.C., Sharkey, T.D., von Caemmerer, S. (eds) Photosynthesis. Advances in Photosynthesis and Respiration, vol 9. Springer, Dordrecht. https://doi.org/10.1007/0-306-48137-5_20

Download citation

  • DOI: https://doi.org/10.1007/0-306-48137-5_20

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-0-7923-6143-5

  • Online ISBN: 978-0-306-48137-6

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation