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Plant Biol (Stuttg) 2003; 5(4): 341-349
DOI: 10.1055/s-2003-42718
Review Article

Georg Thieme Verlag Stuttgart · New York

The Molecular Regulation of Leaf Form

A. J. Fleming 1
  • 1Institute of Plant Sciences, Swiss Federal Institute of Technology, Zurich, Switzerland
Further Information

Publication History

Publication Date:
02 October 2003 (online)

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Abstract

Recent research has provided significant advances in the identification of gene products which influence leaf form. In this review, a summary of this progress is made and an outline sketched of the future directions and challenges facing workers in this area. An overall view is taken in which the present characterisation of the molecular architects of leaf morphogenesis is envisaged to link up eventually with the final downstream elements of differential tissue growth which, integrated over developmental time, lead to the range of leaf forms observed in nature.

Key words

Leaf - morphogenesis - growth - molecular genetics.

References

  • 1 Aida M., Ishida T., Fukaki H., Fujisawa H., Tasaka M.. Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant.  Plant Cell. (1997);  9 841-857
    CrossrefPubMedGoogle Scholar
  • 2 Autran D., Jonak C., Belcram K., Beemster G. T. S., Kronenberger J., Grandjean O., Inzé D., Traas J.. Cell numbers and leaf development in Arabidopsis: a functional analysis.  EMBO J.. (2002);  21 6036-6049
    CrossrefPubMedGoogle Scholar
  • 3 Bell A. D.. Plant form: an ilustrated guide to flowering plant morphology. Oxford, UK; OUP (1991)
    Google Scholar
  • 4 Bharathan G., Goliber T., Moore C., Kessler S., Pham T., Sinha N. R.. Homologies in leaf form inferred from KNOXL gene expression during development.  Science. (2002);  296 1858-1860
    CrossrefPubMedGoogle Scholar
  • 5 Burk D. H., Ye Z-H.. Alteration of oriented deposition of cellulose microfibrils by mutation of a katenin-like microtubule-severing protein.  Plant Cell. (2002);  14 2145-2160
    CrossrefPubMedGoogle Scholar
  • 6 Byrne M. E., Barley R., Curtis M., Arroyo J. A., Dunham M., Hudson A., Martienssen R. A.. Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. .  Nature. (2000);  408 967-971
    CrossrefPubMedGoogle Scholar
  • 7 Byrne M. E., Timmermans M., Kidner C., Martienssen R.. Development of leaf shape.  Curr. Opin. Plant Biol.. (2001);  4 38-43
    CrossrefPubMedGoogle Scholar
  • 8 Byrne M. E., Simorowski J., Martienssen R. A.. ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis.  Development. (2002);  129 1957-1965
    PubMedGoogle Scholar
  • 9 Chen J.-J., Janssen B.-J., Williams A., Sinha N.. A gene fusion at a homeobox locus: alternations in leaf shape and implications for morphological evolution.  Plant Cell. (1997);  9 1289-1304
    CrossrefPubMedGoogle Scholar
  • 10 Cho H.-T., Cosgrove D. J.. Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana. .  Proc. Natl. Acad. Sci. (USA). (2000);  97 9783-9788
    CrossrefPubMedGoogle Scholar
  • 11 Cho H.-T., Kende H.. Tissue localization of expansins in deepwater rice.  Plant J.. (1998);  15 805-812
    CrossrefPubMedGoogle Scholar
  • 12 Chuck G., Lincoln C., Hake S.. Knat1 induces lobed leaves with ectopic meristems when overexpressed in Arabidopsis. .  Plant Cell. (1996);  8 1277-1289
    CrossrefPubMedGoogle Scholar
  • 13 Clouse S. D., Sasse J. M.. Brassinosteroids: essential regulators of plant growth and development.  Annu. Rev. Physiol. Plant Mol. Biol.. (1998);  49 427-451
    PubMedGoogle Scholar
  • 14 Cockcroft C. E., den Boer B. G. W., Healy J. M. S., Murray J. A. H.. Cyclin D control of growth rate in plants.  Nature. (2000);  405 575-578
    CrossrefPubMedGoogle Scholar
  • 15 Curaba J., Herzog M., Vachon G.. GeBP, the first member of a new gene family in Arabidopsis, encodes a nuclear protein with DNA binding activity and is regulated by KNAT1.  Plant J.. (2003);  33 305-317
    CrossrefPubMedGoogle Scholar
  • 16 De Veylder L., Beeckman T., Beemster G. T. S., Engler J. D., Ormenese S., Maes S., Naudts M., Van der Schueren E., Jacqmard A., Engler G., Inzé D.. Control of proliferation, endoreduplication and differentiation by the Arabidopsis E2Fa-DPa transcription factor.  EMBO J.. (2002);  21 1360-1368
    CrossrefPubMedGoogle Scholar
  • 17 De Veylder L., Beeckman T., Beemster G. T. S., Krols L., Terras F., Landrieu I., Van Der Schueren E., Maes S., Naudts M., Inzé D.. Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. .  Plant Cell. (2001);  13 1653-1667
    CrossrefPubMedGoogle Scholar
  • 18 Donnelly P. M., Bonetta D., Tsukaya H., Dengler R. E., Dengler N. G.. Cell cycling and cell enlargement in developing leaves of Arabidopsis. .  Dev. Biol.. (1999);  215 407-419
    CrossrefPubMedGoogle Scholar
  • 19 Eshed Y., Baum S. F., Perea J. V., Bowman J. L.. Establishment of polarity in lateral organs of plants.  Curr. Biol.. (2001);  11 1251-1260
    CrossrefPubMedGoogle Scholar
  • 20 Fleming A. J.. The mechanism of leaf morphogenesis.  Planta. (2001);  216 17-22
    PubMedGoogle Scholar
  • 21 Fleming A. J., Mandel T., McQueen-Mason S., Kuhlemeier C.. Induction of leaf primordia by the cell wall protein expansin.  Science. (1997);  276 1415-1418
    CrossrefPubMedGoogle Scholar
  • 22 Folkers U., Kirik V., Scöbinger U., Falk S., Krishnakumar S., Pollock M. A., Oppenheimer D. G., Day I., Reddy A. R., Jürgens G., Hülskamp M.. The cell morphogenesis gene ANGUSTOFOLIA encodes a CtBP/BARS-like protein and is involved in the control of the microtubule cytoskeleton.  EMBO J.. (2002);  21 1280-1288
    CrossrefPubMedGoogle Scholar
  • 23 Frugis G., Gianno D., Mele G., Nicolodi C., Innocenti A. M., Chiappetta A., Bitonti M. B., Dewitte W., van Onckolen H., Mariotti D.. Are homeobox Knotted-like genes and cytokinins the leaf architects?.  Plant Phys.. (1999);  119 371-373
    PubMedGoogle Scholar
  • 24 Golz J. F., Hudson A.. Signalling in plant lateral organ development.  Plant Cell. (2002);  S277-S288
    PubMedGoogle Scholar
  • 25 Gourlay C. W., Hofer J. M., Ellis T. H.. Pea compound leaf architecture is regulated by interactions among the genes UNIFOLIATA, COCHLEATA, AFILA and TENDRIL-LESS.  Plant Cell. (2000);  12 1279-1294
    CrossrefPubMedGoogle Scholar
  • 26 Green P. B.. Mechanism for plant cellular morphogenesis.  Science. (1962);  138 1404-1405
    PubMedGoogle Scholar
  • 27 Green P. B.. Expression of pattern in plants: combining molecular and calculus-based biophysical paradigms.  Amer. J. Bot.. (1999);  86 1059-1064
    PubMedGoogle Scholar
  • 28 Ha C. M., Kim G.-T., Kim B. C., Jun J. H., Soh M. S., Ueno Y., Machida Y., Tsukaya H., Nam H. G.. The BLADE-ON-PETIOLE 1 gene controls leaf pattern formation through the modulation of meristemmatic activity in Arabidopsis. .  Development. (2003);  130 161-172
    CrossrefPubMedGoogle Scholar
  • 29 Hagemann W., Gleissberg S.. Organogenetic capacity of leaves: the significance of marginal blastozones in angiosperms.  Plant Syst. Evol.. (1996);  199 121-152
    CrossrefPubMedGoogle Scholar
  • 30 Hareven D., Gutfinger T., Parnis A., Eshed Y., Lifschitz E.. The making of a compound leaf: genetic manipulation of leaf architecture in tomato.  Cell. (1996);  84 735-744
    CrossrefPubMedGoogle Scholar
  • 31 Hay A., Kaur H., Phillips A., Hedden P., Hake S., Tsiantis M.. The gibberelin pathway mediates KNOTTED1-type homeobox function in plants with different body plans.  Current Biol.. (2002);  12 1557-1565
    PubMedGoogle Scholar
  • 32 Hemerley A., Engler J. A., Bergounioux C., Van Montagu M., Engler G., Inzé D., Ferreira P.. Dominant negative mutants of the Cdc2 kinase uncouple cell division from iterative plant development.  EMBO J.. (1995);  14 3936
    PubMedGoogle Scholar
  • 33 Jackson D., Veit B., Hake S.. Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot.  Development. (1994);  120 405-413
    PubMedGoogle Scholar
  • 34 Jackson D., Hake S.. Control of phyllotaxy in maize by the ABPHYL1 gene.  Development. (1999);  126 315-323
    PubMedGoogle Scholar
  • 35 Kaplan D. R.. Fundamental concepts of leaf morphology and morphogenesis: a contribution to the interpretation of molecular genetic mutants.  Int. J. Plant Sci.. (2001);  162 465-474
    PubMedGoogle Scholar
  • 36 Kerstetter R. A., Bollman K., Taylor R. A., Bomblies K., Poethig R. S.. KANADI regulates organ polarity in Arabidopsis. .  Nature. (2001);  411 706-708
    CrossrefPubMedGoogle Scholar
  • 37 Kessler S., Kim M., Pham T., Weber N., Sinha N.. Mutations altering leaf morphology in tomato.  Int. J. Plant Sci.. (2001);  162 475-492
    PubMedGoogle Scholar
  • 38 Kim M., Canio W., Kessler S., Sinha N.. Developmental changes due to long-distance movement of a homeobox fusion transcript in tomato.  Science. (2001);  293 287-289
    CrossrefPubMedGoogle Scholar
  • 39 Kim G. T., Shoda K., Tsuge T., Cho K.-H., Uchimiya H., Yokoyama R., Nishitani K., Tsukaya H.. The ANGUSTIFOLIA gene of Arabidopsis, a plant CtBP gene, regulates leaf-cell expansion, the arrangement ofcortical microtubules in leaf cells and expression of a gene involved in cell-wall formation.  EMBO J.. (2002);  21 1267-1279
    CrossrefPubMedGoogle Scholar
  • 40 Kim G. T., Tsukaya H., Uchimaya H.. The ROTUNDIFOLIA3 gene of Arabidopsis thaliana encodes a new member of the cytochrome P-450 family that is required for the regulated polar elongation of leaf cells. Genes &.  Dev.. (1998);  12 2381-2391
    PubMedGoogle Scholar
  • 41 Kim J. Y., Yuan Z., Cilia M., Khalfan-Jagani Z., Jackson D.. Intercellular trafficking of a KNOTTED1 green fluorescent protein fusion in the leaf and shoot meristem of Arabidopsis. .  Proc. Natl. Acad. Sci. (USA). (2002 b);  99 4103-4108
    CrossrefPubMedGoogle Scholar
  • 42 Long J. A., Moan E. I., Medford J. I., Barton M. K.. A member of the KNOTTED class of homeodomain proteins encoded by the SHOOTMERISTEMLESS gene of Arabidopsis.  Nature. (1996);  379 66-69
    CrossrefPubMedGoogle Scholar
  • 43 Marcotrigiano M.. Genetic mosaics and the analysis of leaf development.  Int. J. Plant Sci.. (2001);  162 513-525
    PubMedGoogle Scholar
  • 44 Matsumato N., Okada K.. A homeobox gene, PRESSED FLOWER, regulates lateral axis-dependent development of Arabidopsis flowers. Genes &.  Dev.. (2001);  15 3355-3364
    PubMedGoogle Scholar
  • 45 Mayer K. F. X., Schoof H., Haeker A., Lenhard M., Jürgens G., Laux T.. Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem.  Cell. (1998);  95 805-815
    CrossrefPubMedGoogle Scholar
  • 46 McConnell J. R., Emery J., Eshed Y., Bao N., Bowman J., Barton M. K.. Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots.  Nature. (2001);  411 709-713
    CrossrefPubMedGoogle Scholar
  • 47 Nath U., Crawford B. C. W., Carpenter R., Coen E.. Genetic control of surface curvature.  Science. (2003);  299 1404-1407
    CrossrefPubMedGoogle Scholar
  • 48 Ogas J., Cheng J.-C., Renee Sung Z., Somerville Chris. Cellular differentiation regulated by gibberellin in the Arabidopsis thaliana pickle mutant.  Science. (1997);  277 91-94
    CrossrefPubMedGoogle Scholar
  • 49 Okada K., Ueda J., Komaki M. K., Bell C. J., Shimura Y.. Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation.  Plant Cell,. (1991);  3 677-684
    CrossrefPubMedGoogle Scholar
  • 50 Ori N., Eshed Y., Chuck G., Bowman J. L., Hake S.. Mechanisms that control knox gene expression in the Arabidopsis shoot.  Development. (2000);  127 5523-5532
    PubMedGoogle Scholar
  • 51 Pien S., Wyrzykowska J., McQueen-Mason S., Smart C., Fleming A.. Local expression of expansin induces the entire proces of leaf development and modifies leaf shape.  Proc. Natl. Acad. Sci. (USA). (2001);  98 11812-11817
    CrossrefPubMedGoogle Scholar
  • 52 Poethig R. S., Sussex I. M.. The developmental morphology and growth dynamics of the tobacco leaf.  Planta. (1985 a);  165 158-169
    CrossrefPubMedGoogle Scholar
  • 53 Poethig R. S., Sussex I. M.. The cellular parameters of leaf development in tobacco: a clonal analysis.  Planta. (1985 b);  165 170-184
    CrossrefPubMedGoogle Scholar
  • 54 Reinhardt D., Mandel T., Kuhlemeier C.. Auxin regulates the initiation and radial position of plant lateral organs.  Plant Cell. (2000);  12 507-518
    CrossrefPubMedGoogle Scholar
  • 55 Reinhardt D., Wittwer F., Mandel T., Kuhlemeier C.. Localized upregulation of a new expansin gene predicts the site of leaf formation in the tomato meristem.  Plant Cell. (1998);  10 1427-1437
    CrossrefPubMedGoogle Scholar
  • 56 Reinhart B. J., Weinstein E. G., Rhoades M. W., Bartel B., Bartel D. P.. MicroRNAs in plants. Genes &.  Dev.. (2002);  16 2313
    PubMedGoogle Scholar
  • 57 Roberts K.. The plant extracellular matrix in a new expansive mood.  Curr. Opin. Cell Biol.. (1994);  6 688-694
    CrossrefPubMedGoogle Scholar
  • 58 Rupp H.-M., Frank M., Werner T., Strnad M., Scmülling T.. Increased steady state mRNA levels of the STM and KNAT1 homeobox genes in cytokinin overproducing Arabidopsis thaliana indicate a role for cytokinins in the shoot apical meristem.  The Plant J.. (1999);  18 557-563
    PubMedGoogle Scholar
  • 59 Sakamoto T., Kamiya N., Ueguchi-Tanaka M., Iwahori S., Matsouka M.. KNOX homeodomain protein directly suppresses the expression of a gibberellin biosynthetic gene in the tobacco shoot apical meristem. Genes &.  Dev.. (2001);  15 581-590
    PubMedGoogle Scholar
  • 60 Sato Y., Tamaoki M., Murakami T., Yamamoto N., Kano-Murakami Y., Matsouka M.. Abnormal cell divisions in leaf primordia caused by the expression of the rice homeobox gene OSH1 lead to altered morphology of leaves in transgenic tobacco.  Mol. Gen. Genet.. (1996);  251 13-22
    PubMedGoogle Scholar
  • 61 Scanlon M. J., Schneeberger R. G., Freeling M.. The maize mutant narrow sheath fails to establish leaf margin identity in a meristematic domain.  Development. (1996);  122 1683-1691
    PubMedGoogle Scholar
  • 62 Siegfried K. R., Eshed Y., Baum S., Otsuga D., Drews G. N., Bowman J. L.. Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. .  Development. (1999);  126 4117-4128
    PubMedGoogle Scholar
  • 63 Sinha N.. Leaf development in angiosperms.  Annu. Rev. Plant Physiol. Plant Mol. Biol.. (1999);  50 419-446
    CrossrefPubMedGoogle Scholar
  • 64 Sinha N. R., Williams R. E., Hake S.. Overexpression of the maize homeo box gene, KNOTTED-1, causes a switch from determinate to indeterminate cell fates. Genes &.  Dev.. (1993);  7 787-795
    PubMedGoogle Scholar
  • 65 Steeves T. A., Sussex I. M.. Patterns in plant development. Cambridge; Cambridge University Press (1989)
    Google Scholar
  • 66 Tamaoki M., Kusaba S., Kano-Murakami Y., Matsouka M.. Ectopic expression of a tobacco homeobox gene, NTH15, dramatically alters leaf morphology and hormone levels in transgenic tobacco.  Plant Cell Physiol.. (1997);  38 917-927
    PubMedGoogle Scholar
  • 67 Timmermams M. C., Hudson A., Becraft P. W., Nelson T.. ROUGH SHEATH2: a Myb protein that represses knox homeobox genes in maize lateral organ primordia.  Science. (1999);  284 151-153
    CrossrefPubMedGoogle Scholar
  • 68 Timmermans M. C. P., Schultes N. P., Jankovsky J. P., Nelson T.. Leafbladeless1 is required for dorsoventrality of lateral organs in maize.  Development. (1998);  125 2813-2823
    PubMedGoogle Scholar
  • 69 Tsiantis M., Schneeberger R., Golz J. F., Freeling M., Langdale J. A.. The maize rough sheath2 gene and leaf development programs in monocot and dicot plants.  Science. (1999);  284 154-156
    CrossrefPubMedGoogle Scholar
  • 70 Van der Graaf E., Dulk-ras A. D., Hooykas P. J. J., Keller B.. Activation tagging of the LEAFY PETIOLE gene affects leaf petiole development in Arabidopsis.  Development. (2000);  127 4971-4980
    PubMedGoogle Scholar
  • 71 Van Lijsebettens M., Vanderhaeghen R., De Block M., Bauw G., Villarroel R., Van Montagu M.. An S18 ribosomal protein gene copy at the Arabidopsis PFL locus affects plant development by its specific expression in meristems.  EMBO J.. (1994);  13 3378-3388
    PubMedGoogle Scholar
  • 72 Vollbrecht E., Reiser L., Hake S.. Shoot meristem size is dependent on inbred background and presence of the maize homeobox gene, knotted1. .  Development. (2000);  127 3161-3172
    PubMedGoogle Scholar
  • 73 Waites R., Hudson A.. phantastica: a gene required for dorsoventrality of leaves in Antirrhinum majus. .  Development. (1995);  121 2143-2154
    PubMedGoogle Scholar
  • 74 Waites R., Selvadurai H., Oliver I. R., Hudson A.. The PHANTASTICA gene encodes a MYB transcription factor involved in growth and dorsoventrality of lateral organs in Antirrhinum. .  Cell. (1998);  93 779-789
    CrossrefPubMedGoogle Scholar
  • 75 Wang H., Zhou Y., Gilmer S., Whitwill S., Fowke L. C.. Expression of the plant cyclin-dependent kinase inhibitor ICK1 affects cell division, plant growth and morphology.  The Plant J.. (2000);  24 613-623
    PubMedGoogle Scholar
  • 76 Wyrzykowska J., Pien S., Shen W.-H., Fleming A. J.. Manipulation of leaf shape by modulation of cell division.  Development. (2002);  129 957-964
    PubMedGoogle Scholar

A. J. Fleming

Institute of Plant Sciences
Swiss Federal Institute of Technology

Universitätsstrasse 2

8092 Zurich

Switzerland

Email: andrew.fleming@ipw.biol.ethz.ch

Section Editor: L. A. C. J. Voesenek

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