Journal of Plant Research

, Volume 108, Issue 4, pp 407–416 | Cite as

Developmental genetics of leaf morphogenesis in dicotyledonous plants

  • Hirokazu Tsukaya


A full understanding of the leaf is essential for a full understanding of plant morphology. However, leaf morphogenesis is still poorly understood, in particular in dicotyledonous plants, because of the complex nature of the development of leaves. Mutational analysis seems to be the most suitable strategy for investigations of such processes, and should allow us to dissect the developmental pathways into genetically programmed unit processes. The techniques of developmental genetics have been applied to the study of leaf morphogenesis in model plants, such asArabidopsis thaliana, and several key processes in leaf morphogenesis have been identified. The fundamental processes in leaf morphogenesis include the identification of leaf organs, determination of leaf primordia (occurrence of marginal meristem), and the polar or non-polar elongation of leaf cells. This review will focus on the genes that are essential for these processes and have been identified in mutational analyses. Mutational analyses of the photomorphogenesis is also briefly summarized from the perspective of the plasticity of leaf morphogenesis.

Key words

Arabidopsis Developmental genetics Dicots Leaf Morphogenesis Mutants 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Aeschbacher, R.A., Hauser, M.-T., Feldmann, K.A. andBenfey, P.N. 1995. TheSABRE gene is required for normal cell expansion inArabidopsis. Genes Dev.9: 330–340.PubMedGoogle Scholar
  2. Avery, G.S.Jr. 1933. Structure and development of the tobacco leaf. Amer. J. Bot.20: 565–592.Google Scholar
  3. Barabas, Z. andRédei, G.P. 1971. Facilitation of crossing by the use of appropriate parental stocks. Arabidopsis Inf. Ser.8: 7–8.Google Scholar
  4. Barton, M.K. andPoethig, R.S. 1993. Formation of the shoot apical meristem inArabidopsis thaliana: an analysis of development in the wild type and in theshoot meristemsless mutant. Development119: 823–831.Google Scholar
  5. Caruso, J.L. 1968. Morphogenetic aspects of a leafless mutant in tomato I. General pattern in development. Amer. J. Bot.55: 1169–176.Google Scholar
  6. Child, R., Morgan, D.C. andSmith, H. 1981. Control of development inChenopodium album L. by shadelight. The effect of light quality (red: far-red ratio) on morphogenesis. New Phytol.89: 545–555.Google Scholar
  7. Chory, J. 1992. A genetic model for light-regulated seedling development inArabidopsis. Development115: 337–354.Google Scholar
  8. Coen, E.S. andMeyerowitz, E.M. 1991. The war of the whorls: genetic interactions controlling flower development. Nature353: 31–37.CrossRefPubMedGoogle Scholar
  9. Cusset, G. 1986. La morphogenèse du limbe des Dicotylédones. Can. J. Bot.64: 2807–2839.Google Scholar
  10. Dale, J.E. 1988. The control of leaf expansion. Annu. Rev. Plant Physiol. Plant Mol. Biol.39: 267–295.CrossRefGoogle Scholar
  11. Deng, X.-W. andQuail, P.H. 1992. Genetic and phenotypic characterization ofcop1 mutants ofArabidopsis thaliana. Plant J.2: 83–95.CrossRefGoogle Scholar
  12. Duke, S.O. andLane, A.D. 1984. Phytochrome control of its own accumulation and leaf expansion in tentoxinand norflurazon-treated mung bean seedlings. Physiol. Plant.60: 341–346.Google Scholar
  13. Engelke, A.L., Hamzi, Q.H. andSkoog, F. 1973. Cytokinin-gibberellin regulation of shoot development and leaf form in tobacco plantlets. Amer. J. Bot.60: 491–495.Google Scholar
  14. Eschrich, W., Burchardt, R. andEssiamah, S. 1989. The induction of sun and shade leaves of the European beech (Fagus sylvatica L.): anatomical studies. Trees3: 1–10.CrossRefGoogle Scholar
  15. Evans, M.W. andGrover, F.O. 1940. Developmental morphology of the growing point of the shoot and the inflorescence in grasses. J. Agricul. Res.61: 481–520.Google Scholar
  16. Foster, A.S. 1936. Leaf differentiation in angiosperms. Bot. Rev.2: 349–372.Google Scholar
  17. Goto, N., Kumagai, T. andKoornneef, M. 1991. Flowering responses to light-breaks in photomorphogenic mutants ofArabidopsis thaliana, a long-day plant. Physiol. Plant.83: 209–215.CrossRefGoogle Scholar
  18. Gottlieb, L.D. 1984. Genetics and morphological evolution in plants. Amer. Natl.123: 681–709.Google Scholar
  19. Hara, N. 1957. On the types of the marginal growth in dicotyledonous foliage leaves. Bot. Mag. Tokyo70: 108–114.Google Scholar
  20. Hara, N. 1959. Marginal growth of leaves. Nature183: 1409–1410.Google Scholar
  21. Harte, C. 1979. Phänogenetik der Blattform beiAntirrhinum majus L. I. Variabilität des Formindex in Abhängigkeit von Genotyp und Umwelt. Biol. Zbl.98: 21–35.Google Scholar
  22. Hill, A.W. 1938. The monocotyledonous seedlings of certain dicotyledons. With special reference to the Gesneriaceae. Ann. Bot.2: 127–143.Google Scholar
  23. Hilu, K.W. 1983. The role of single-gene mutations in the flowering plants. Evol. Biol.16: 97–128.Google Scholar
  24. Hou, Y., von Arnim, A.G. andDeng, X.-W. 1993. A new class ofArabidopsis constitutive photomorphogenic genes involved in regulating cotyledon development. Plant Cell5: 329–339.CrossRefPubMedGoogle Scholar
  25. Imai, Y. 1938. The genes of the Japanese morning glory. Japan. J. Genet.14: 24–33.Google Scholar
  26. Imaichi, R. andKato, M. 1992. Comparative leaf development ofOsmunda lancea andO. japonica (Osmundaceae): heterochronic origin of rheophytic stenophylly. Bot. Mag. Tokyo105: 199–213Google Scholar
  27. Jackson, D., Veit, B. andHake, S. 1994. Expression of maizeKNOTTED1-related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development120: 405–413.Google Scholar
  28. Jones, C.S. 1993. Heterochrony and heteroblastic leaf development in two subspecies ofCucurbita argyrosperma (Cucurbitaceae). Amer. J. Bot.80: 778–795.Google Scholar
  29. Jong, K. andBurtt, B.L. 1975. The evolution of morphological novelty exemplified in the growth patterns of some Gesneriaceae. New Phytol.75: 297–311.Google Scholar
  30. Kaplan, D.R. andHagemann, W. 1991. The relationship of cell and organism in vascular plants. — Are cells the building block of plant form? BioScience41: 693–703.Google Scholar
  31. Kato, M. andImaichi, R. 1991. Leaf anatomy of tropical fern rheophytes, with its evolutionary and ecological implications. Can. J. Bot.70: 165–174.Google Scholar
  32. Koornneef, M., van Eden, J., Hanhart, C.J., Stam, P., Braaksma, F.J. andFeenstra, W.J. 1983. Linkage map ofArabidopsis thaliana. J. Hered.74: 265–272.Google Scholar
  33. Lichtenthaler, H.K., Buschmann, C., Döll, M., Fietz, H.-J., Bach, T., Kozel, U., Meler, D. andRahmsdorf, U. 1981. Photosynthetic activity, chloroplast ultrastructure, and leaf characteristics of high-light and low-light plants and of sun and shade leaves. Photosynthesis Res.2: 115–141.Google Scholar
  34. Lightner, J., James Jr., D.W., Dooner, H.K. andBrowse, J. 1994. Altered body morphology is caused by increased stearate levels in a mutant ofArabidopsis. Plant J.6: 401–412.CrossRefGoogle Scholar
  35. Lincoln, C., Britton, J.H. andEstelle, M. 1990. Growth and development of theaxr1 mutants ofArabidopsis. Plant Cell2: 1071–1080.CrossRefPubMedGoogle Scholar
  36. Lincoln, C., Long, J., Yamaguchi, J., Serikawa, K. andHake, S. 1994. AKnotted1-like homeobox gene inArabidopsis is expressed in the vegetative meristem and dramatically alters leaf morphology when overex-pressed in transgenic plants. Plant Cell6: 1859–1876.CrossRefPubMedGoogle Scholar
  37. Maksymowych, R. 1963. Cell division and cell elongation in leaf development ofXanthium pennsylvanicum. Amer. J. Bot.50: 891–901.Google Scholar
  38. Maksymowych, R. andMaksymowych, A.B. 1973. Induction of morphogenetic changes and acceleration of leaf initiation by gibberellic acid inXanthium pennsylvanicum. Amer. J. Bot.60: 901–906.Google Scholar
  39. Marx, G.A. 1983. Developmental mutants in some annual seed plants. Annu. Rev. Plant Physiol.34: 389–417.CrossRefGoogle Scholar
  40. Matsuoka, M., Ichlkawa, H., Saito, A., Tada, Y., Fujimura, T. andKano-Murakami, K. 1993. Expression of a rice homeobox gene causes altered morphology of transgenic plants. Plant Cell5: 1039–1048.CrossRefPubMedGoogle Scholar
  41. McHale, N.A. 1993.LAM-1 andFAT genes control development of the leaf blade inNicotiana sylvestris. Plant Cell5: 1029–1038.CrossRefPubMedGoogle Scholar
  42. McLaren, J.S. andSmith, H. 1978. Phytochrome control of the growth and development ofRumex obtusifolius under simulated canopy light environments. Plant Cell Environ.1: 61–67.Google Scholar
  43. McLellan, T. 1993. The roles of heterochrony and heteroblasty in the diversification of leaf shapes inBegonia dregei (Begoniaceae). Amer. J. Bot.80: 796–804.Google Scholar
  44. Meinke, D.W. 1992. A homoeotic mutant ofArabidopsis thaliana with leafy cotyledons. Science258: 1647–1650.Google Scholar
  45. Meinke, D.W., Franzmann, L.H., Nickle, T.C. andYeung, E. 1994.Leafy cotyledon mutants ofArabidopsis. Plant Cell6: 1049–1064.CrossRefPubMedGoogle Scholar
  46. Meyerowitz, E.M. andPruitt, R.E. 1985.Arabidopsis thaliana and plant molecular genetics. Science229: 1214–1218.Google Scholar
  47. Morgan, D.C. andSmith, H. 1979. A systematic relationship between phytochrome-controlled development and species habitat, for plants grown in simulated natural radiation. Planta145: 253–258.CrossRefGoogle Scholar
  48. Morgan, D.C. andSmith, H. 1981. Control of development inChenopodium album L. by shadelight: the effect of light quantity (total fluence rate) and light quality (red: far-red ratio). New Phytol.88: 239–248.Google Scholar
  49. Nagatani, A., Chory, J. andFuruya, M. 1991. Phytochrome B is not detectable in thehy3 mutant ofArabidopsis, which is deficient in responding to end-of-day far-red light treatments. Plant Cell Physiol.32: 1119–1122.Google Scholar
  50. Nagatani, A., Reed, J.W. andChory, J. 1993. Isolation and initial characterization ofArabidopsis mutants that are deficient in phytochrome A. Plant Physiol.102: 269–277.PubMedGoogle Scholar
  51. Poethig, R.S. andSussex, I.M. 1985. The developmental morphology and growth dynamics of the tobacco leaf. Planta165: 158–169.Google Scholar
  52. Pyke, K.A., Marrison, J.L. andLeech, R.M. 1991. Temporal and spatial development of the cells of the expanding first leaf ofArabidopsis thaliana (L.) Heynh. J. Exp. Bot.42: 1407–1416.Google Scholar
  53. Rédei, G.P. 1962. Single locus heterosis. Z. Vererbungs.93: 164–170.Google Scholar
  54. Reed, J.W., Nagpal, P., Poole, D.S., Furuya, M. andChory, J. 1993. Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughoutArabidopsis development. Plant Cell5: 147–157.CrossRefPubMedGoogle Scholar
  55. Röbbelen, G. 1957. Über heterophyllie beiArabidopsis thaliana (L.) Heynh. Ber. Dt. Bot. Ges.70: 39–44.Google Scholar
  56. Robson, P.R., Whitelam, G.C. andSmith, H. 1993. Selected components of the shade-avoidance syndrome are displayed in a normal manner in mutants ofArabidopsis thaliana andBrassica rapa deficient in phytochrome B. Plant Physiol.102: 1179–1184.PubMedGoogle Scholar
  57. Roe, J.L., Rivin, C.J., Sessions, R.A., Feldmann, K.A. andZambryski, P.C. 1993. TheTousled gene inA. thaliana encodes a protein kinase homolog that is required for leaf and flower development. Cell75: 939–950.CrossRefPubMedGoogle Scholar
  58. Sinnott, E.W. 1958. The genetic basis of organic form. Ann. N.Y. Acad. Sci.71: 1223–1233.PubMedGoogle Scholar
  59. Smith, H. 1995. Physiological and ecological function within the phytochrome family. Annu. Rev. Plant Physiol. Plant Mol. Biol.46: 289–315.CrossRefGoogle Scholar
  60. Smith, L.G., Greene, B., Veit, B. andHake, S. 1992. A dominant mutation in the maize homeobox gene,Knotted-1, causes its ectopic expression in leaf cells with altered fates. Development116: 21–30.PubMedGoogle Scholar
  61. Smith, L.G. andHake, S. 1992. The initiation and determination of leaves. Plant Cell4: 1017–1027.CrossRefPubMedGoogle Scholar
  62. Smith, L.G. andHake, S. 1993. Molecular genetic approaches to leaf development:Knotted and beyond. Can. J. Bot.72: 617–625.Google Scholar
  63. Steeves, T.A. 1961. A study of the developmental potentialities of excised leaf primordia in sterile culture. Phytomorphology11: 346–349.Google Scholar
  64. Steeves, T., Hicks, G., Steeves, M. andRetallack, B. 1993. Leaf determination in the fernOsmunda cinnamomea — A reinvestigation. Ann. Bot.71: 511–517.CrossRefGoogle Scholar
  65. Steeves, T.A. andSussex, I.M. 1989. Patterns in Plant Development. 2nd ed., Cambridge University Press, Cambridge.Google Scholar
  66. Takahashi, T., Gasche, A., Nishizawa, N. andChua, N.-H. 1995. TheDIMINUTO gene ofArabidopsis is involved in regulating cell elongation. Genes Dev.9: 97–107.PubMedGoogle Scholar
  67. Tsuge, T., Tsukaya, H. and Uchimiya, H. 1990. Two independent and polarized processes of cell elongation regulate leaf blade expansion inArabidopsis thaliana (L.) Heynh. Development (in press).Google Scholar
  68. Tsukaya, H. 1995. The genetic control of morphogenesis inArabidopsis and its relevance to the development of biodiversity.In R. Arai, M. Kato and Y. Doi, eds., Biodiversity and Evolution, The National Science Museum Foundation, Tokyo, (in press).Google Scholar
  69. Tsukaya, H., Inaba-Higano, K. andKomeda, Y. 1995. Phenotypic and molecular mapping of anacaulis2 mutant ofArabidopsis thaliana with flower stalks of much reduced length. Plant Cell Physiol.36: 239–246.Google Scholar
  70. Tsukaya, H., Naito, S., Rédei, G.P. andKomeda, Y. 1993. A new class of mutations inArabidopsis thaliana, acaulis1, affecting the development of both inflorescences and leaves. Development118: 751–764.Google Scholar
  71. Tsukaya, H., Tsuge, T. andUchimiya, H. 1994. The cotyledon: a superior system for studies of leaf development. Planta195: 309–312.CrossRefGoogle Scholar
  72. Usukura, M., Imaichi, R. andKato, M. 1994. Leaf morphology of a facultative rheophyte,Farfugium japonicum var.luchuense (Compositae). J. Plant Res.107: 263–267.Google Scholar
  73. Van Lijsebettens, M., Vanderhaeghen, R. andVan Montague, M. 1991. Insertional mutagenesis inArabidopsis thaliana: isolation of a T-DNA-linked mutation that alters leaf morphology. Theor. Appl. Genet.81: 277–284.CrossRefGoogle Scholar
  74. Van Lijsebettens, M., Vanderhaeghen, R., De Block, M., Bauw, G., Villarroel, R. andVan Montague, M. 1994. An S18 ribosomal protein gene copy at theArabidopsis PFL locus affects plant development by its specific expression in meristems. EMBO J.13: 3378–3388.PubMedGoogle Scholar
  75. Vollbrecht, E., Veit, B., Sinha, N. andHake, S. 1991. The developmental geneKnotted-1 is a member of a maize homeobox gene family. Nature350: 241–243.CrossRefPubMedGoogle Scholar
  76. Waites, R. andHudson, A. 1995.phantastica: a gene required for dorsoventrality of leaves inAntirrhinum majus. Development121: 2143–2154.Google Scholar
  77. West, M.A.L., Yee, K.M., Danao, J., Zimmerman, J.L., Fischer, R.L., Goldberg, R.B. andHarada, J.J. 1994.LEAFY COTYLEDON1 is an essential regulator of late embryogenesis and cotyledon identity inArabidopsis. Plant Cell6: 1731–1745.CrossRefPubMedGoogle Scholar
  78. Zimmermann, W. 1953. Main results of the “telome theory”. Paleobot.1: 456–470.Google Scholar

Copyright information

© The Botanical Society of Japan 1995

Authors and Affiliations

  • Hirokazu Tsukaya
    • 1
  1. 1.Institute of Molecular and Cellular BiosciencesThe University of TokyoTokyoJapan

Personalised recommendations