Control of Leaf Morphogenesis by Long- and Short-Distance Signaling: Differentiation of Leaves Into Sun or Shade Types and Compensated Cell Enlargement

  • Ali Ferjani
  • Satoshi Yano
  • Gorou Horiguchi
  • Hirokazu Tsukaya
Part of the Plant Cell Monographs book series (CELLMONO, volume 10)


The flattened, thin lamina of leaves captures sunlight for photosynthesis and facilitates gas exchange. Therefore, the size and shape of a leaf are fundamentally important features of its integrity and function. Progress in developmental studies has suggested that long- and short-distance signaling pathways are involved in leaf formation. In this chapter, we introduce these signaling pathways, both of which can control final leaf shape and structure: a long-distance signaling pathway that governs the differentiation of leaves into sun and shade types, and a short-distance signaling pathway that appears to be involved in an organ-wide system that integrates cell proliferation and cell enlargement. Although none of the molecules involved in these two pathways have been identified, plausible mechanisms of these pathways are discussed based on present data.


Mature Leaf Leaf Development Leaf Primordia Leaf Thickness Shade Leave 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Ashton PMS, Berlyn GP (1994) A comparison of leaf physiology and anatomy of Quercus (section Erythrobalanus-Fagaceae) species in different light environments. Am J Bot 81:589–597 CrossRefGoogle Scholar
  2. Autran D, Jonak C, Belcram K, Beemster GT, Kronenberger J, Grandjean O, Inzé D, Traas J (2002) Cell numbers and leaf development in Arabidopsis: a functional analysis of the STRUWWELPETER gene. EMBO J 21:6036–6049 PubMedCrossRefGoogle Scholar
  3. Avery GS (1933) Structure and development of tobacco leaf. Am J Bot 20:565–592 CrossRefGoogle Scholar
  4. Barrôco RM, Peres A, Droual AM, De Veylder L, le Nguyen SL, De Wolf J, Mironov V, Peerbolte R, Beemster GT, Inzé D, Broekaert WF, Frankard V (2006) The cyclin-dependent kinase inhibitor Orysa; KRP1 plays an important role in seed development of rice. Plant Physiol 142:1053–1064 PubMedCrossRefGoogle Scholar
  5. Beemster GT, Vercruysse S, De Veylder L, Kuiper M, Inze D (2006) The Arabidopsis leaf as a model system for investigating the role of cell cycle regulation in organ growth. J Plant Res 119:43–50 PubMedCrossRefGoogle Scholar
  6. Björkman O (1981) In: Encyclopedia of Plant Physiology, Physiological Plant Ecology I. New Series vol 12A. Springer, Berlin Heidelberg, New York, pp 57–107 Google Scholar
  7. Boardman NK (1977) Comparative photosynthesis of sun and shade plants. Annu Rev Plant Physiol 28:355–377 CrossRefGoogle Scholar
  8. Boudolf V, Barrôco R, Engler Jde A, Verkest A, Beeckman T, Naudts M, Inzé D, De Veylder L (2004) B1-type cyclin-dependent kinases are essential for the formation of stomatal complexes in Arabidopsis thaliana. Plant Cell 16:945–955 PubMedCrossRefGoogle Scholar
  9. Brand L, Horler M, Nuesch E, Vassalli S, Barrell P, Yang W, Jefferson RA, Grossniklaus U, Curtis MD (2006) A versatile and reliable two-component system for tissue-specific gene induction in Arabidopsis. Plant Physiol 141:1194–1204 PubMedCrossRefGoogle Scholar
  10. Chabot BF, Chabot JF (1977) Effects of light and temperature on leaf anatomy and photosynthesis in Fragaria vesca. Oecologia 26:363–377 CrossRefGoogle Scholar
  11. Chabot BF, Jurik TW, Chabot JF (1979) Influence of instantaneous and integrated light-flux density on leaf anatomy and photosynthesis. Am J Bot 66:940–945 CrossRefGoogle Scholar
  12. Cho Y-H, Yoo S-D, Sheen J (2006) Regulatory functions of nuclear hexokinase1 complex in glucose signaling. Cell 127:579–589 PubMedCrossRefGoogle Scholar
  13. Clay NK, Nelson T (2005) The recessive epigenetic swellmap mutation affects the expression of two step II splicing factors required for the transcription of the cell proliferation gene STRUWWELPETER and for the timing of cell cycle arrest in the Arabidopsis leaf. Plant Cell 17:1994–2008 PubMedCrossRefGoogle Scholar
  14. Coupe SA, Palmer BG, Lake JA, Overy SA, Oxborough K, Woodward FI, Gray JE, Quick WP (2006) Systemic signalling of environmental cues in Arabidopsis leaves. J Exp Bot 57:329–341 PubMedCrossRefGoogle Scholar
  15. De Veylder L, Beeckman T, Beemster GT, Krols L, Terras F, Landrieu I, van der Schueren E, Maes S, Naudts M, Inzé D (2001) Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell 13:1653–1668 PubMedCrossRefGoogle Scholar
  16. Dengler NG (1980) Comparative histological basis of sun and shade leaf dimorphism in Helianthus annuus. Can J Bot 58:717–730 CrossRefGoogle Scholar
  17. Donnelly PM, Bonetta D, Tsukaya H, Dengler RE, Dengler NG (1999) Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev Biol 215:407–419 PubMedCrossRefGoogle Scholar
  18. Elliott RC, Betzner AS, Huttner E, Oakes MP, Tucker WQJ, Gerentes D, Perez P, Smyth DR (1996) AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 8:155–168 PubMedCrossRefGoogle Scholar
  19. Esau K (1977) Anatomy of Seed Plants. Wiley, New York Google Scholar
  20. Escoubas J-M, Lmas M, LaRoshe J, Falkowski PG (1995) Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool. Proc Natl Acad Sci USA 92:10237–10241 PubMedCrossRefGoogle Scholar
  21. Exner V, Taranto P, Schonrock N, Gruissem W, Henning L (2006) Chromatin assembly factor CAF-1 is required for cellular differentiation during plant development. Development 133:4163–4172 PubMedCrossRefGoogle Scholar
  22. Ferjani A, Horiguchi G, Yano S, Tsukaya H (2007) Analysis of leaf development in fugu mutants of Arabidopsis thaliana reveals three compensation modes that modulate cell expansion in determinate organs. Plant Physiol 144:988–999 PubMedCrossRefGoogle Scholar
  23. Fujikura U, Horiguchi G, Tsukaya H (2007) Dissection of enhanced cell expansion processes in leaves triggered by a defect in cell proliferation, with reference to roles of endoreduplication. Plant Cell Physiol 48:278–286 PubMedCrossRefGoogle Scholar
  24. Givnish TJ (1988) Adaptation to sun and shade: a whole-plant perspective. In: Evans JR, Von Caemmerer S, Adams WW III (eds) Ecology of Photosynthesis in Sun and Shade. CSIRO, Melbourne, pp 63–92 Google Scholar
  25. Haberlandt G (1914) Physiological Plant Anatomy. Macmillan, London Google Scholar
  26. Hagemann W (1992) The relationship of anatomy to morphology in plants: a new theoretical perspective. Int J Plant Sci 153:S38–48 CrossRefGoogle Scholar
  27. Hanson J, Johannesson H, Engström P (2001) Sugar-dependent alterations in cotyledon and leaf development in transgenic plants expressing the HDZhdip gene ATHB13. Plant Mol Biol 45:247–262 PubMedCrossRefGoogle Scholar
  28. Hemerly A, Engler Jde A, Bergounioux C, Van Montagu M, Engler G, Inzé D, Ferreira P (1995) Dominant negative mutants of the Cdc2 kinase uncouple cell division from iterative plant development. EMBO J 14:3925–3936 PubMedGoogle Scholar
  29. Heraut-Bron V, Robin C, Varlet-Grancher C, Afif D, Guckert A (1999) Light quality (red:far-red ratio): does it affect photosynthetic activity, net CO2 assimilation, and morphology of young white clover leaves? Can J Bot 77:1425–1431 CrossRefGoogle Scholar
  30. Héraut-Bron V, Robin C, Varlet-Grancher C, Guckert A (2001) Phytochrome-mediated effects on leaves of white clover: consequences for light interception by the plant under competition for light. Ann Bot 88:737–743 CrossRefGoogle Scholar
  31. Horiguchi G, Kim G-T, Tsukaya H (2005) The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf primordia of Arabidopsis thaliana. Plant J 43:68–78 PubMedCrossRefGoogle Scholar
  32. Horiguchi G, Ferjani A, Fujikura U, Tsukaya H (2006a) Coordination of cell proliferation and cell expansion in the control of leaf size in Arabidopsis thaliana. J Plant Res 119:37–42 PubMedCrossRefGoogle Scholar
  33. Horiguchi G, Fujikura U, Ferjani A, Ishikawa N, Tsukaya H (2006b) Large-scale histological analysis of leaf mutants using two simple leaf observation methods: identification of novel genetic pathways governing the size and shape of leaves. Plant J 48:638–644 PubMedCrossRefGoogle Scholar
  34. Johnston GC, Pringle JR, Hartwell LH (1977) Coordination of growth with cell division in the yeast Saccharomyces cerevisiae. Exp Cell Res 105:79–98 PubMedCrossRefGoogle Scholar
  35. Jorgensen P, Tyers M (2004) How cells coordinate growth and division. Curr Biol 14:R1014–R1027 PubMedCrossRefGoogle Scholar
  36. Kaplan DR, Hagemann W (1991) The relationship of cell and organism in vascular plants. Bioscience 41:693–703 CrossRefGoogle Scholar
  37. Kaplan DR (1992) The relationship of organisms to cells in plants: problems and implications of an organismal perspective. Int J Plant Sci 153:S28–S37 CrossRefGoogle Scholar
  38. Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P (1999) Systematic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284:654–657 PubMedCrossRefGoogle Scholar
  39. Kaya H, Shibahara K, Taoka K, Iwabuchi M, Stillman B, Araki T (2001) FASCIATA genes for chromatin assembly factor-1 in Arabidopsis maintain the cellular organization of apical meristems. Cell 104:131–142 PubMedCrossRefGoogle Scholar
  40. Kim G-T, Shoda K, Tsuge T, Cho KH, Uchimiya H, Yokoyama R, Nishitani K, Tsukaya H (2002) The ANGUSTIFOLIA gene of Arabidopsis, a plant CtBP gene, regulates leaf-cell expansion, the arrangement of cortical microtubules in leaf cells and expression of a gene involved in cell-wall formation. EMBO J 21:1267–1279 PubMedCrossRefGoogle Scholar
  41. Kim G-T, Yano S, Kozuka T, Tsukaya H (2005) Photomorphogenesis of leaves: shade-avoidance and differentiation of sun and shade leaves. Photochem Photobiol Sci 4:770–774 PubMedCrossRefGoogle Scholar
  42. Kim JH, Kende H (2004) A transcriptional coactivator, AtGIF1, is involved in regulating leaf growth and morphology in Arabidopsis. Proc Natl Acad Sci USA 101:13374–13379 PubMedCrossRefGoogle Scholar
  43. Koch KE, Ying Z, Wu Y, Avigne WT (2000) Multiple paths of sugar-sensing and a sugar/oxygen overlap for genes of sucrose and ethanol metabolism. J Exp Bot 51:417–427 PubMedCrossRefGoogle Scholar
  44. Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7:235–246 PubMedCrossRefGoogle Scholar
  45. Lake JA, Quick QP, Beerling DJ, Woodward FI (2001) Signals from mature to new leaves. Nature 411:154 PubMedCrossRefGoogle Scholar
  46. Lopéz-Juez E, Bowyer JR, Sakai T (2001) Distinct leaf developmental and gene expression responses to light quantity depend on blue-photoreceptor or plastid-derived signals, and can occur in the absence of phototropins. Planta 227:113–123 CrossRefGoogle Scholar
  47. Maksymowych R (1963) Cell division and cell elongation in leaf development in Xanthium pennsylvanicum. Am J Bot 50:891–901 CrossRefGoogle Scholar
  48. Melaragno JE, Mehrotra B, Coleman AW (1993) Relationship between endopolyploidy and cell size in epidermal tissue of Arabidopsis. Plant Cell 5:1661–1668 PubMedCrossRefGoogle Scholar
  49. Menges M, Samland AK, Planchais S, Murray JA (2006) The D-type cyclin CYCD3;1 is limiting for the G1-to-S-phase transition in Arabidopsis. Plant Cell 18:893–906 PubMedCrossRefGoogle Scholar
  50. Miyazawa S-I, Livingston NJ, Turpin DH (2006) Stomatal development in new leaves is related to the stomatal conductance of mature leaves in poplar (Populus trichocarpa × P deltoides). J Exp Bot 57:373–380 PubMedCrossRefGoogle Scholar
  51. Mizukami Y, Fischer RL (2000) Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proc Natl Acad Sci USA 97:942–947 PubMedCrossRefGoogle Scholar
  52. Nelissen H, Clarke JH, De Block M, De Block S, Vanderhaeghen R, Zielinski RE, Dyer T, Lust S, Inzé D, Van Lijsebettens M (2003) DRL1, a homolog of the yeast TOT4/KTI12 protein, has a function in meristem activity and organ growth in plants. Plant Cell 15:639–654 PubMedCrossRefGoogle Scholar
  53. Nishimura C, Ohashi Y, Sato S, Kato T, Tabata S, Ueguchi C (2004) Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell 16:1365–1377 PubMedCrossRefGoogle Scholar
  54. Nobel PS (2005) Physicochemical and Environmental Pant Physiology 3rd edn. Elsevier, USA Google Scholar
  55. Osborn JM, Taylor TN (1990) Morphological and ultrastructural studies on plant cuticular membranes. I. Sun and shade leaves of Quercus velutina (Fagaceae). Bot Gaz 151:465–476 CrossRefGoogle Scholar
  56. Pfannschmidt T, Nilesson A, Allen JF (1999) Photosynthetic control of chloroplast gene expression. Nature 397:625–628 CrossRefGoogle Scholar
  57. Popescu SC, Tumer NE (2004) Silencing of ribosomal protein L3 genes in N. tabacum reveals coordinate expression and significant alterations in plant growth, development and ribosome biogenesis. Plant J 39:29–44 PubMedCrossRefGoogle Scholar
  58. Rhichter T, Fukshansky L (1998) Optics of a bifacial leaf: 3. Implications for photosynthetic performance. Photochem Photobiol 68:337–352 CrossRefGoogle Scholar
  59. Riou-Khamlichi C, Huntley R, Jacqmard A, Murray JA (1999) Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283:1541–1544 PubMedCrossRefGoogle Scholar
  60. Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18:1121–1133 PubMedCrossRefGoogle Scholar
  61. Sitte P (1992) A modern concept of the cell theory: a perspective on competing hypotheses of structure. Int J Plant Sci 153:S1-S6 Google Scholar
  62. Smith H (1994) Sensing the light environment: the functions of the phytochrome family. In: Kendrick RE, Kronenberg GHM (eds) Photomorphogenesis in Plants, 2nd edn. Kluwer Academic, Dordrecht, pp 337–416 Google Scholar
  63. Smith LG, Hake S (1992) The initiation and determination of leaves. Plant Cell 4:1017–1027 PubMedCrossRefGoogle Scholar
  64. Terashima I, Miyazawa S-I, Hanba YT (2001) Why are sun leaves thicker than shade leaves? Consideration based on analyses of CO2 diffusion in the leaf. J Plant Res 114:93–105 CrossRefGoogle Scholar
  65. Thomas PW, Woodward FI, Quick WP (2004) Systemic irradiance signalling in tobacco. New Phytol 161:193–198 CrossRefGoogle Scholar
  66. Tichá I (1982) Photosynthetic characteristics during ontogenesis of leaves. 7. Stomata density and sizes. Photosynthetica 11:357–471 Google Scholar
  67. Tsuge T, Tsukaya H, Uchimiya H (1996) Two independent and polarized processes of cell elongation regulate leaf blade expansion in Arabidopsis thaliana (L.) Heynh. Development 122:1589–1600 PubMedGoogle Scholar
  68. 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 PubMedCrossRefGoogle Scholar
  69. Tsukaya H (2003) Organ shape and size: a lesson from studies of leaf morphogenesis. Curr Opin Plant Biol 6:57–62 PubMedCrossRefGoogle Scholar
  70. Tsukaya H (2006) Mechanism of leaf-shape determination. Annu Rev Plant Biol 57:477–496 PubMedCrossRefGoogle Scholar
  71. Tsukaya H, Beemster GT (2006) Genetics, cell cycle and cell expansion in organogenesis in plants. J Plant Res 119:1–4 PubMedCrossRefGoogle Scholar
  72. Ullah H, Chen JG, Young JC, Im KH, Sussman MR, Jones AM (2001) Modulation of cell proliferation by heterotrimeric G protein in Arabidopsis. Science 292:2066–2069 PubMedCrossRefGoogle Scholar
  73. Wang H, Zhou Y, Gilmer S, Whitwill S, Fowke LC (2000) Expression of the plant cyclin-dependent kinase inhibitor ICK1 affects cell division, plant growth and morphology. Plant J 24:613–623 PubMedCrossRefGoogle Scholar
  74. Weston E, Thorogood K, Vinti G, Lopéz-Juez E (2000) Light quantity controls leaf-cell and chloroplast development in Arabidopsis thaliana wild-type and blue-light-perception mutants. Planta 211:807–815 PubMedCrossRefGoogle Scholar
  75. White DWR (2006) PEAPOD regulates lamina size and curvature in Arabidopsis. Proc Natl Acad Sci USA 103:13238–13243 PubMedCrossRefGoogle Scholar
  76. Woodward FI (1987) Stomatal numbers are sensitive to increase in CO2 from pre-industrial levels. Nature 327:617–618 CrossRefGoogle Scholar
  77. Woodward FI, Lake JA, Quick WP (2002) Stomatal development and CO2: ecological consequences. New Phytol 153:477–484 CrossRefGoogle Scholar
  78. Yano S, Terashima I (2001) Separate localization of light signal perception for sun or shade type chloroplast and palisade tissue differentiation in Chenopodium album. Plant Cell Physiol 42:1303–1310 PubMedCrossRefGoogle Scholar
  79. Yano S, Terashima I (2004) Developmental process of sun and shade leaves in Chenopodium album L. Plant Cell Env 27:781–793 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2008

Authors and Affiliations

  • Ali Ferjani
    • 1
  • Satoshi Yano
    • 2
  • Gorou Horiguchi
    • 1
  • Hirokazu Tsukaya
    • 1
    • 2
  1. 1.Graduate School of ScienceUniversity of TokyoTokyoJapan
  2. 2.National Institute for Basic Biology/Okazaki Institute for Integrated BioscienceAichiJapan

Personalised recommendations