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C4 Photosynthesis and Related CO2 Concentrating Mechanisms pp 147–159Cite as

Chapter 9 Development of Leaves in C4 Plants: Anatomical Features That Support C4 Metabolism

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

Summary

C4 metabolism is a metabolic cooperation between distinct sites for primary carbon assimilation and primary carbon reduction. In most C4 species, the cooperating sites are in specialized cell types – ­mesophyll and bundle sheath – organized around a dense pattern of leaf venation and joined by abundant plasmodesmata. There is much recent information on the formation of venation, plasmodesmata, and barriers to gas diffusion in leaves. Recent evidence suggests that the specialized patterns of these features in C4 leaves come from quantitative and spatial regulation of gene networks and protein interactions present in all higher plants. These networks and their regulatory points should emerge from the computational modeling of biological systems data from developing C4 and C3 leaves.

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Abbreviations

BS:

Bundle sheath

DC:

Distinctive cell

M:

Mesophyll

PAT:

Polar auxin transport

PCA:

Primary carbon assimilation

PCR:

Primary carbon reduction

PD:

Plasmodesmata

PIN:

PIN-LIKE (auxin efflux protein)

References

  • Adams WW, 3rd, Watson AM, Mueh KE, Amiard V, Turgeon R, Ebbert V, Logan BA, Combs AF and Demmig-Adams B (2007) Photosynthetic acclimation in the context of structural constraints to carbon export from leaves. Photosynth Res 94: 455–466

    PubMed  CAS  Google Scholar 

  • Agarie S, Kai M, Takatsuji H and Ueno O (1997) Expression of C-3 and C-4 photosynthetic characteristics in the amphibious plant Eleocharis vivipara: Structure and analysis of the expression of isogenes for pyruvate, orthophosphate dikinase. Plant Mol Biol 34: 363–369

    PubMed  CAS  Google Scholar 

  • Aloni R (2001) Foliar and axial aspects of vascular differentiation: Hypotheses and evidence. J Plant Growth Regul 20: 22–34

    CAS  Google Scholar 

  • Aloni R, Schwalm K, Langhans M and Ullrich CI (2003) Gradual shifts in sites of free-auxin production during leaf-primordium development and their role in vascular differentiation and leaf morphogenesis in Arabidopsis. Planta 216: 841–853

    PubMed  CAS  Google Scholar 

  • Akyildiz M, Gowik U, Engelmann S, Koczor M, Streubel M and Westhoff P (2007) Evolution and Function of a cis-Regulatory module for mesophyll-specific gene expression in the C4 dicot Flaveria trinervia. Plant Cell 107: 3391–3402

    Google Scholar 

  • Amiard V, Mueh KE, Demmig-Adams B, Ebbert V, Turgeon R and Adams WW, 3rd (2005) Anatomical and photosynthetic acclimation to the light environment in species with differing mechanisms of phloem loading. Proc Natl Acad Sci U S A 102: 12968–73

    PubMed  CAS  Google Scholar 

  • Baima S, Nobili F, Sessa G, Lucchetti S, Ruberti I and Morelli G (1995) The expression of the Athb-8 homeobox gene is restricted to provascular cells in Arabidopsis thaliana. Development 121: 4171–4182

    PubMed  CAS  Google Scholar 

  • Barabasi AL and Oltvai ZN (2004) Network biology: understanding the cell’s functional organization. Nat Rev Genet 5: 101–113

    PubMed  CAS  Google Scholar 

  • Benkova E, Michniewicz M, Sauer M, Teichmann T, Seifertova D, Jurgens G and Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115: 591–602

    PubMed  CAS  Google Scholar 

  • Berleth T and Mattsson J (2000) Vascular development: tracing signals along veins. Curr Opin Plant Biol 3: 406–411

    PubMed  CAS  Google Scholar 

  • Berleth T, Mattsson J and Hardtke CS (2000a) Vascular ­continuity and auxin signals. Trends Plant Sci 5: 387–393

    PubMed  CAS  Google Scholar 

  • Berleth T, Mattsson J and Hardtke CS (2000b) Vascular ­continuity, cell axialisation and auxin. Plant Growth Regul 32: 173–185

    CAS  Google Scholar 

  • Berleth T, Scarpella E and Prusinkiewicz P (2007) Towards the systems biology of auxin-transport-mediated patterning. Trends Plant Sci 12: 151–159

    PubMed  CAS  Google Scholar 

  • Bosabalidis AM, Evert RF and Russin WA (1994) Ontogeny of the vascular bundles and contiguous tissues in the maize leaf blade. Am J Bot 81: 745–752

    Google Scholar 

  • Botha CEJ (1992) Plasmodesmatal distribution structure and frequency in relation to assimilation in C-3 and C-4 grasses in southern africa. Planta 187: 348–358

    CAS  Google Scholar 

  • Botha CEJ, Hartley BJ and Cross RHM (1993) The ultrastructure and computer-enhanced digital image analysis of plasmodesmata at the Kranz mesophyll-bundle sheath interface of Themeda triandra var. imberbis (Retz) A. camus in conventionally-fixed leaf blades. Ann Bot 72: 255–261

    Google Scholar 

  • Brutnell TP and Langdale JA (1998) Signals in leaf development. In: J. A. Callow (Ed). Advances in Botanical Research 28 (ed.). pp. 161–195. Academic, London

    Google Scholar 

  • Brutnell TP, Sawers RJ, Mant A and Langdale JA (1999) BUNDLE SHEATH DEFECTIVE2, a novel protein required for post-translational regulation of the rbcL gene of maize. Plant Cell 11: 849–864

    PubMed  CAS  Google Scholar 

  • Burton RF (2004) The mathematical treatment of leaf venation: the variation in secondary vein length along the midrib. Ann Bot 93: 149–156

    PubMed  Google Scholar 

  • Carland FM, Berg BL, FitzGerald JN, Jinamornphongs S, Nelson T and Keith B (1999) Genetic regulation of vascular tissue patterning in Arabidopsis. Plant Cell 11: 2123–2137

    PubMed  CAS  Google Scholar 

  • Cilia ML and Jackson D (2004) Plasmodesmata form and function. Curr Opin Cell Biol 16: 500–506

    PubMed  CAS  Google Scholar 

  • Cribb L, Hall LN and Langdale JA (2001) Four mutant ­alleles elucidate the role of the G2 protein in the development of C4 and C3 photosynthesizing maize tissues. Genetics 159: 787–797

    PubMed  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 

  • Dengler N and Kang J (2001) Vascular patterning and leaf shape. Curr Opin Plant Biol 4: 50–56

    PubMed  CAS  Google Scholar 

  • Dengler N and Nelson T (1999) Leaf structure and development in C4 plants. In: R. F. Sage and R. K. Monson (Eds). C4 Plant Biology. pp. 133–172. Academic, San Diego, CA

    Google Scholar 

  • Dengler N and Taylor WC (2000) Developmental aspects of C4 photosynthesis. In: R. C. Leegood, T. D. Sharkey and S. von Caemmerer (Eds). Photosynthesis: Physiology and Metabolism. pp. 471–495. Kluwer, Dordrecht, ­Netherlands

    Google Scholar 

  • Dengler NG (2001) Regulation of vascular development. J Plant Growth Regul 20: 1–13

    CAS  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

    Google Scholar 

  • Dengler NG, Dengler RE and Grenville DJ (1990) Comparison of photosynthetic carbon reduction kranz cells having different ontogenetic origins in the 4-carbon NADP malic enzyme grass Arundinella hirta. Can J Bot 68: 1222–1232

    Google Scholar 

  • Dengler NG, Donnelly PM and Dengler RE (1995) Differentiation of photosynthetic tissue in the atypical C4 grass Arundinella hirta. Am J Bot 82: 16–17

    Google Scholar 

  • Dengler NG, Donnelly PM and Dengler RE (1996a) Differentiation of bundle sheath, mesophyll, and distinctive cells the C-4 grass Arundinella hirta (Poaceae). Am J Bot 83: 1391–1405

    Google Scholar 

  • Dengler NG, Woodvine AMA and Donnelly PM (1996b). Formation of vascular pattern in developing leaves of the unusual C4 grass, Arundinella hirta. Am J Bot 83: 37

    Google Scholar 

  • Dengler NG, Woodvine MA, Donnelly PM and Dengler RE (1997) Formation of vascular pattern in developing leaves of the C-4 grass Arundinella hirta. Int J Plant Sci 158: 1–12

    Google Scholar 

  • Dimitrov P and Zucker SW (2006) A constant production hypothesis guides leaf venation patterning. Proc Natl Acad Sci U S A 103: 9363–8

    PubMed  CAS  Google Scholar 

  • Donnelly PM, Bonetta D, Tsukaya H, Dengler and RE Dengler NG (1999) Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev Biol 215: 407–419

    PubMed  CAS  Google Scholar 

  • Edwards GE, Franceschi VR, Ku MS, Voznesenskaya EV, Pyankov VI and Andreo CS (2001a) Compartmentation of photosynthesis in cells and tissues of C4 plants. J Exp Bot 52: 577–590

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker NP, Izhaki A, Baum SF and Bowman JL (2003) Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr Biol 13: 1768–1774

    PubMed  CAS  Google Scholar 

  • Evert RF, Eschrich W and Heyser W (1977) Distribution and structure of the plasmodesmata in mesophyll and bundle sheath cells of Zea mays L. Planta 136: 77–89

    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

    Google Scholar 

  • Ferjani A, Horiguchi G, Yano S and Tsukaya H (2007) Analysis of leaf development in fugu mutants of Arabidopsis reveals three compensation modes that modulate cell expansion in determinate organs. Plant Physiol 144: 988–999

    PubMed  CAS  Google Scholar 

  • Feugier FG and Iwasa Y (2006) How canalization can make loops: a new model of reticulated leaf vascular pattern formation. J Theor Biol 243: 235–244

    PubMed  Google Scholar 

  • Fladung M (1994) Genetic variants of Panicum maximum (Jacq) in C-4 photosynthetic traits. J Plant Physiol 143: 165–172

    CAS  Google Scholar 

  • Franke R and Schreiber L (2007). Suberin – a biopolyester forming apoplastic plant interfaces. Curr Opin Plant Biol 10: 252–259

    PubMed  CAS  Google Scholar 

  • Fujita H and Mochizuki A (2006) The origin of the diversity of leaf venation pattern. Dev Dyn 235: 2710–2721

    PubMed  Google Scholar 

  • Fujita H and Mochizuki A (2006) Pattern formation of leaf veins by the positive feedback regulation between auxin flow and auxin efflux carrier. J Theor Biol 241: 541–551

    PubMed  CAS  Google Scholar 

  • Fukuda H (2004) Signals that control plant vascular cell differentiation. Nat Rev Mol Cell Biol 5: 379–391

    PubMed  CAS  Google Scholar 

  • Furbank RT, Agostino A and Hatch MD (1990) C4 acid decarboxylation and photosynthesis in bundle sheath cells of NAD-malic enzyme-type C4 plants: mechanism and the role of malate and orthophosphate. Arch Biochem Biophys 276: 374–381

    PubMed  CAS  Google Scholar 

  • Furbank RT, Jenkins CL and Hatch MD (1989) CO2 concentrating mechanism of C4 photosynthesis: Permeability of isolated bundle sheath cells to inorganic carbon. Plant Physiol 91: 1364–1371

    PubMed  CAS  Google Scholar 

  • Gowik U, Burscheidt J, Akyildiz M, Schlue U, Koczor M, Streubel M and Westhoff P (2004) cis-Regulatory elements for mesophyll-specific gene expression in the C4 plant Flaveria trivervia, the promoter of the C4 phosphoenolpyruvate carboxylase gene. Plant Cell 16: 1077–1090

    PubMed  CAS  Google Scholar 

  • Graca J and Santos S (2007) Suberin: a biopolyester of plants’ skin. Macromol Biosci 7: 128–135

    PubMed  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 (1914) Physiological Plant Anatomy. Macmillan, London

    Google Scholar 

  • Hall LN, Roth R, Brutnell TP and Langdale JA (1998) ­Cellular differentiation in the maize leaf is disrupted by bundle sheath defective mutations. Symp Soc Exp Biol 51: 27–31

    PubMed  CAS  Google Scholar 

  • Hartwell LH, Hopfield JJ, Leibler S and Murray AW (1999). From molecular to modular cell biology. Nature 402: C47–C52

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Hattersley PW and Watson L (1976) C4 grasses: an anatomical criterion for distinguishing between NADP -malic enzyme species and PCK or NAD-malic enzyme species. Aust J Bot 24: 297–308

    Google Scholar 

  • Haywood V, Kragler F and Lucas WJ (2002) Plasmodesmata: pathways for protein and ribonucleoprotein signaling. Plant Cell 14 Suppl: S303–S325

    Google Scholar 

  • Helliker BR and Ehleringer JR (2000) Establishing a grassland signature in veins: 18O in the leaf water of C3 and C4 grasses. Proc Natl Acad Sci U S A 97: 7894–7898

    PubMed  CAS  Google Scholar 

  • Hofmann C, Sambade A and Heinlein M (2007) Plasmodesmata and intercellular transport of viral RNA. Biochem Soc Trans 35: 142–145

    PubMed  CAS  Google Scholar 

  • Izhaki A and Bowman JL (2007) KANADI and class III HD-Zip gene families regulate embryo patterning and modulate auxin flow during embryogenesis in Arabidopsis. Plant Cell 19: 495–508

    PubMed  CAS  Google Scholar 

  • Jankovsky JP, Smith LG and Nelson T (2001) Specification of bundle sheath cell fates during maize leaf development: Roles of lineage and positional information evaluated through analysis of the tangled1 mutant. Development 128: 2747–2753

    PubMed  CAS  Google Scholar 

  • Jenkins CL, Furbank RT and Hatch MD (1989) Inorganic carbon diffusion between C4 mesophyll and bundle sheath cells: Direct bundle sheath CO2 assimilation in intact leaves in the presence of an inhibitor of the C4 pathway. Plant Physiol 91: 1356–1363

    PubMed  CAS  Google Scholar 

  • Jiao Y, S. Tausta SL, Gandotra N, Sun N, Liu T, Clay NK, Ceserani T, Chen M, Ma L, Holford M, Zhang H-Y, Zhao H, Deng X-W and Nelson T (2009) A transcriptome atlas of rice cell types reveals cellular, functional and developmental hierarchies. Nat Genet 41: 258–263

    PubMed  CAS  Google Scholar 

  • Kanai R and Edwards G (1999) The biochemistry of C4 ­photosynthesis. In: R. F. Sage and R. K. Monson (Eds). C4 Plant Biology. pp. 49–87. Academic, San Diego, CA

    Google Scholar 

  • Kang J and Dengler N (2002) Cell cycling frequency and expression of the homeobox gene ATHB-8 during leaf vein development in Arabidopsis. Planta 216: 212–9

    PubMed  CAS  Google Scholar 

  • Kang J, Tang J, Donnelly P and Dengler NG (2003) Primary vascular pattern and expression of ATHB-8 in shoots of Arabidopsis. New Phytol 158: 443–454

    CAS  Google Scholar 

  • Kang J and Dengler NG (2004) Vein pattern development in adult leaves of Arabidopsis thaliana. Int J Plant Sci 165: 231–242

    Google Scholar 

  • Kang J, Mizukami Y, Wang H, Fowke L and Dengler NG (2007) Modification of cell proliferation patterns alters leaf vein architecture in Arabidopsis thaliana. Planta 226: 1207–1218

    PubMed  CAS  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 

  • Kellogg EA (1999) Phylogenetic aspects of the evolution of C4 photosynthesis. In: R. F. Sage and R. K. Monson (Eds). C4 Plant Biology. pp. 411–444. Academic, San Diego, CA

    Google Scholar 

  • Kim I, Kobayashi K, Cho E and Zambryski PC (2007) Regulation of plant intercellular communication via plasmodesmata. Genet Eng (NY) 28: 1–15

    Google Scholar 

  • Kim JY (2005) Regulation of short-distance transport of RNA and protein. Curr Opin Plant Biol 8: 45–52

    PubMed  CAS  Google Scholar 

  • Ko JH, Beers EP and Han KH (2006) Global comparative transcriptome analysis identifies gene network regulating secondary xylem development in Arabidopsis thaliana. Mol Genet Genomics 276: 517–531

    PubMed  CAS  Google Scholar 

  • Koizumi K, Naramoto S, Sawa S, Yahara N, Ueda T, Nakano A, Sugiyama M and Fukuda H (2005) VAN3 ARF-GAP-mediated vesicle transport is involved in leaf vascular ­network formation. Development 132: 1699–1711

    PubMed  CAS  Google Scholar 

  • Koizumi K, Sugiyama M and Fukuda H (2000) A series of novel mutants of Arabidopsis thaliana that are defective in the formation of continuous vascular network: calling the auxin signal flow canalization hypothesis into question. Development 127: 3197–3204

    PubMed  CAS  Google Scholar 

  • Kolattukudy PE (2001) Polyesters in higher plants. Adv Biochem Eng Biotechnol 71: 1–49

    PubMed  CAS  Google Scholar 

  • Kubo M, Udagawa M, Nishikubo N, Horiguchi G, Yamaguchi M, Ito J, Mimura T, Fukuda H and Demura T (2005) Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev 19: 1855–1860

    PubMed  CAS  Google Scholar 

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

    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

    PubMed  CAS  Google Scholar 

  • Langdale JA, Zelitch I, Miller E and Nelson T (1988) Cell position and light influence C4 versus C3 patterns of photosynthetic gene expression in maize. EMBO J 7: 3643–3651

    PubMed  CAS  Google Scholar 

  • Leegood RC (2002) C4 photosynthesis: principles of CO2 concentration and prospects for its introduction into C3 plants. J Exp Bot 53: 581–590

    PubMed  CAS  Google Scholar 

  • Matsuoka M, Furbank RT, Fukayama H and Miyao M (2001) Molecular engineering of C4 photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 52: 297–314

    PubMed  CAS  Google Scholar 

  • Mattsson J, Ckurshumova W and Berleth T (2003) Auxin signaling in Arabidopsis leaf vascular development. Plant Physiol 131: 1327–1339

    PubMed  CAS  Google Scholar 

  • Mattsson J, Sung ZR and Berleth T (1999) Responses of plant vascular systems to auxin transport inhibition. Development 126: 2979–2991

    PubMed  CAS  Google Scholar 

  • McKown AD and Dengler NG (2007) Key innovations in the evolution of Kranz anatomy and C-4 vein pattern in Flaveria (Asteraceae). Am J Bot 94: 382–399

    PubMed  Google Scholar 

  • Meinhardt H (1996) Models of biological pattern formation: Common mechanism in plant and animal development. Intl J Dev Biol 40: 123–134

    PubMed  CAS  Google Scholar 

  • Motose H, Sugiyama M and Fukuda H (2004) A proteoglycan mediates inductive interaction during plant vascular development. Nature 429: 873–878

    PubMed  CAS  Google Scholar 

  • Muhaidat R, Sage RF and Dengler NG (2007) Diversity of Kranz anatomy and biochemistry in C-4 eudicots. Am J Bot 94: 362–381

    PubMed  CAS  Google Scholar 

  • Nelson T and Dengler N (1997) Leaf vascular pattern formation. Plant Cell 9: 1121–1135

    PubMed  CAS  Google Scholar 

  • Nelson T and Dengler NG (1992) Photosynthetic tissue ­differentiation in C-4 plants. Int J Plant Sci 153: S93–S105

    Google Scholar 

  • Nishitani C, Demura T and Fukuda H (2001). Primary phloem-specific expression of a Zinnia elegans homeobox gene. Plant Cell Physiol 42: 1210–8

    PubMed  CAS  Google Scholar 

  • Ogle K (2003) Implications of interveinal distance for quantum yield in C-4 grasses: a modeling and meta-analysis. Oecologia 136: 532–542

    PubMed  Google Scholar 

  • Ohashi-Ito K and Fukuda H (2003) HD-zip III homeobox genes that include a novel member, ZeHB-13 (Zinnia)/ATHB-15 (Arabidopsis), are involved in procambium and xylem cell differentiation. Plant Cell Physiol 44: 1350–1358

    PubMed  CAS  Google Scholar 

  • Ohashi-Ito K, Kubo M, Demura T and Fukuda H (2005) Class III homeodomain leucine-zipper proteins regulate xylem cell differentiation. Plant Cell Physiol 46: 1646–1656

    PubMed  CAS  Google Scholar 

  • Ormenese S, Havelange A, Deltour R and Bernier G (2000) The frequency of plasmodesmata increases early in the whole shoot apical meristem of Sinapis alba L. during ­floral transition. Planta 211: 370–375

    PubMed  CAS  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 

  • Roberts IM, Boevink P, Roberts AG, Sauer N, Reichel C and Oparka KJ (2001) Dynamic changes in the frequency and architecture of plasmodesmata during the sink-source transition in tobacco leaves. Protoplasma 218: 31–44

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Rolland-Lagan AG and Prusinkiewicz P (2005) Reviewing models of auxin canalization in the context of leaf vein pattern formation in Arabidopsis. Plant J 44: 854–865

    PubMed  CAS  Google Scholar 

  • Roth R, Hall LN, Brutnell TP and Langdale JA (1996) ­bundle sheath defective2, a mutation that disrupts the coordinated development of bundle sheath and mesophyll cells in the maize leaf. Plant Cell 8: 915–927

    PubMed  CAS  Google Scholar 

  • Sachs T (1991). Pattern Formation in Plant Tissues. Cambridge University Press, Cambridge, UK/New York

    Google Scholar 

  • Sage RF (2001) Environmental and evolutionary preconditions for the origin and diversification of the C-4 photosynthetic syndrome. Plant Biology 3: 202–213

    CAS  Google Scholar 

  • Sage RF (2004) The evolution of C-4 photosynthesis. New Phytol 161: 341–370

    CAS  Google Scholar 

  • Sage RF, Li M Monson RK (1999) The taxonomic distribution of C4 photosynthesis. In: R. F. Sage and R. K. Monson (Eds). C4 Plant Biology. pp. 551–584. Academic, San Diego, CA

    Google Scholar 

  • Sage RF and McKown AD (2006) Is C4 photosynthesis less phenotypically plastic than C3 photosynthesis? J Exp Bot 57: 303–317

    PubMed  CAS  Google Scholar 

  • Sawa S, Kinoshita A, Nakanomyo I and Fukuda H (2006) CLV3/ESR-related (CLE) peptides as intercellular signaling molecules in plants. Chem Rec 6: 303–310

    PubMed  CAS  Google Scholar 

  • Sawa S, Koizumi K, Naramoto S, Demura T, Ueda T, Nakano A and Fukuda H (2005) DRP1A is responsible for vascular continuity synergistically working with VAN3 in Arabidopsis. Plant Physiol 138: 819–826

    PubMed  CAS  Google Scholar 

  • Scarpella E, Boot KJ, Rueb S and Meijer AH (2002) The procambium specification gene Oshox1 promotes polar auxin transport capacity and reduces its sensitivity toward inhibition. Plant Physiol 130: 1349–1360

    PubMed  CAS  Google Scholar 

  • Scarpella E, Francis P and Berleth T (2004) Stage-specific markers define early steps of procambium development in Arabidopsis leaves and correlate termination of vein ­formation with mesophyll differentiation. Development 131: 3445–3455

    PubMed  CAS  Google Scholar 

  • Scarpella E, Marcos D, Friml J and Berleth T (2006) Control of leaf vascular patterning by polar auxin transport. Genes Dev 20: 1015–1027

    PubMed  CAS  Google Scholar 

  • Sieburth LE (1999) Auxin is required for leaf vein pattern in Arabidopsis. Plant Physiol 121: 1179–1190

    PubMed  CAS  Google Scholar 

  • Sieburth LE and Deyholos MK (2006) Vascular development: the long and winding road. Curr Opin Plant Biol 9: 48–54

    PubMed  CAS  Google Scholar 

  • Sinha NR and Kellogg EA (1996) Parallelism and diversity in multiple origins of C-4 photosynthesis in the grass family. Am J Bot 83: 1458–1470

    Google Scholar 

  • Soros CL and Dengler NG (1998) Quantitative leaf anatomy of C3 and C4 Cyperaceae and comparisons with the Poaceae. Intl 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 

  • Sud RM and Dengler NG (2000) Cell lineage of vein formation in variegated leaves of the C4 grass Stenotaphrum secundatum. Ann Bot 86: 99–112

    Google Scholar 

  • Tanaka H, Dhonukshe P, Brewer PB and Friml J (2006) Spatiotemporal asymmetric auxin distribution: a means to coordinate plant development. Cell Mol Life Sci 63: 2738–2754

    PubMed  CAS  Google Scholar 

  • Tsiantis M, Brown MI, Skibinski G and Langdale JA (1999) Disruption of auxin transport is associated with aberrant leaf development in maize. Plant Physiol 121: 1163–1168

    PubMed  CAS  Google Scholar 

  • Tsukaya H (2002) Interpretation of mutants in leaf ­morphology: genetic evidence for a compensatory system in leaf morphogenesis that provides a new link between cell and organismal theories. Int Rev Cytol 217: 1–39

    PubMed  CAS  Google Scholar 

  • Tsukaya H (2003) Organ shape and size: a lesson from studies of leaf morphogenesis. Curr Opin Plant Biol 6: 57–62

    PubMed  Google Scholar 

  • Tsukaya H (2005) Leaf shape: genetic controls and environmental factors. Int J Dev Biol 49: 547–55

    PubMed  Google Scholar 

  • Tsukaya H (2006) Mechanism of leaf-shape determination. Annu Rev Plant Biol 57: 477–496

    PubMed  CAS  Google Scholar 

  • Ueno O (1995) Occurrence of distinctive cells in leaves of C-4 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 (1996) Structural characterization of photosynthetic cells in an amphibious sedge Eleocharis vivipara, in relation to C-3 and C-4 metabolism. Planta 199: 382–393

    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: 571–584

    PubMed  CAS  Google Scholar 

  • Ueno O (2001). Environmental regulation of C3 and C4 differentiation in the amphibious sedge Eleocharis vivipara. Plant Physiol 127: 1524–1532

    PubMed  CAS  Google Scholar 

  • Ueno O, Kawano Y, Wakayama M and Takeda T (2006) Leaf vascular systems in C3 and C4 grasses: a two-­dimensional analysis. Ann Bot 97: 611–621

    PubMed  CAS  Google Scholar 

  • Ueno O, Samejima M and Koyama T (1989) Distribution and evolution of C-4 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 (1988) Photosynthetic characteristics of an amphibious plant, Eleocharis vivipara: Expression of C4 and C3 modes in contrasting environments. Proc Natl Acad Sci U S A 85: 6733–6737.

    PubMed  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: 433–41

    PubMed  CAS  Google Scholar 

  • Vieten A, Sauer M, Brewer PB and Friml J (2007) Molecular and cellular aspects of auxin-transport-mediated development. Trends Plant Sci 12: 160–168

    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 

  • 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 veins. Plant Cell Physiol 44: 1330–1340

    PubMed  CAS  Google Scholar 

  • Weiner H, Burnell JN, Woodrow IE, Heldt HW and Hatch MD (1988) Metabolite diffusion into bundle sheath cells from C4 plants: Relation to C4 photosynthesis and plasmodesmatal function. Plant Physiol 88: 815–822

    PubMed  CAS  Google Scholar 

  • Wenzel CL, Schuetz M, Yu Q and Mattsson J (2007) Dynamics of MONOPTEROS and PIN-FORMED1 expression during leaf vein pattern formation in Arabidopsis thaliana. Plant J 49: 387–398

    PubMed  CAS  Google Scholar 

  • Yamamoto R, Fujioka S, Iwamoto K, Demura T, Takatsuto S, Yoshida S and Fukuda H (2007) Co-regulation of brassinosteroid biosynthesis-related genes during xylem cell differentiation. Plant Cell Physiol 48: 74–83

    PubMed  Google Scholar 

  • Yu H, Xia Y, Trifonov V and Gerstein M (2006) Design ­principles of molecular networks revealed by global ­comparisons and composite motifs. Genome Biol 7: R55

    PubMed  Google Scholar 

  • Yu J, Holland JB, McMullen MD and Buckler ES (2008) Genetic design and statistical power of nested association mapping in maize. Genetics 178: 539–551

    PubMed  Google Scholar 

  • Zhao C, Craig JC, Petzold HE, Dickerman AW and Beers EP (2005) The xylem and phloem transcriptomes from secondary tissues of the Arabidopsis root-hypocotyl. Plant Physiol 138: 803–818

    PubMed  CAS  Google Scholar 

  • Zhu X, Gerstein M and Snyder M (2007) Getting connected: analysis and principles of biological networks. Genes Dev 21: 1010–1024

    PubMed  CAS  Google Scholar 

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Acknowledgments

The author is grateful to S. Lori Tausta and Neeru Gandotra for helpful comments. The author’s work on C4 biology, vein patterning, and cell-specific transcriptomes is supported by US National ­Science Foundation awards DBI-0701736, IOS-0718881 andDBI-0325821, respectively.

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  1. Department of Molecular, Cellular and Developmental Biology, Yale University, 208104, New Haven, CT, 06520-8104, USA

    Timothy Nelson

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Correspondence to Timothy Nelson .

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  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

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Nelson, T. (2010). Chapter 9 Development of Leaves in C4 Plants: Anatomical Features That Support C4 Metabolism. 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_9

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