Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Comparative plant development: the time of the leaf?

Nature Reviews Genetics volume 4, pages 169–180 (2003)Cite this article

This article has been updated

Key Points

  • The leaves of higher plants are derived from the shoot apical meristem.

  • In the Arabidopsis meristem, signalling between CLV and WUS genes creates a feedback loop that maintains the stem-cell population and controls meristem size.

  • Mutually repressive interactions between KNOX proteins and AS1 and AS2 proteins contribute to the delimitation of leaf founder cells in the shoot apex of Arabidopsis.

  • ARP MYB-like proteins are required to repress KNOX expression in both monocot and eudicot plants.

  • Leaf-polarity determinants either promote (adaxial polarity genes PHB/PHV/REV) or antagonize (abaxial polarity genes YAB and KAN) meristem function.

  • Comparative studies of KNOX expression patterns and leaf morphology show a correlation between KNOX expression in leaf primordia and dissected leaf form.

  • KNOX and UFO/LFY define developmental pathways that act in meristems. These might have been co-opted in evolution to function in the generation of the dissected leaf form.

  • Quantitative trait loci analyses indicate that alterations in the regulatory regions of regulatory genes might be responsible for species-specific morphological variation.

Abstract

A key problem in developmental biology is understanding the origin of morphological innovations. Comparative studies in plants with different leaf morphologies indicate that the developmental pathway defined by KNOTTED1-type homeodomain proteins could be involved in generating different leaf forms. The differential expression of regulatory proteins has emerged as an important factor in driving morphological innovations in the plant kingdom — an idea that is well supported by quantitative trait locus analyses.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: A typical vascular plant.
Figure 2: Consistent correlation between leaf form and KNOX expression in Brassicaceae.
Figure 3: Variation in leaf form in F2 progeny from an interspecific cross between Antirrhinum majus and Antirrhinum molle.

Similar content being viewed by others

Change history

  • 23 February 2003

    genus <i>Fabales</i> corrected to order Fabales

Notes

  1. *A correction was made to this article on the 25 February 2003. The order Fabales was incorrectly referred to as the genus Fabales.

References

  1. Nusslein-Volhard, C. Of flies and fishes. Science 266, 572–574 (1994).

    CAS  PubMed  Google Scholar 

  2. Coen, E. S. & Meyerowitz, E. M. The war of the whorls: genetic interactions controlling flower development. Nature 353, 31–37 (1991).

    CAS  PubMed  Google Scholar 

  3. Theissen, G. & Saedler, H. The golden decade of molecular floral development (1990–1999): a cheerful obituary. Dev. Genet. 25, 181–193 (1999).

    CAS  PubMed  Google Scholar 

  4. Kramer, E. M. & Irish, V. F. Evolution of genetic mechanisms controlling petal development. Nature 399, 144–148 (1999).

    CAS  PubMed  Google Scholar 

  5. Soltis, D. E. et al. Missing links: the genetic architecture of flower and floral diversification. Trends Plant Sci. 7, 22–31 (2002).

    CAS  PubMed  Google Scholar 

  6. Kenrick, P. & Crane, P. R. The Origin and Early Diversification of Land Plants: A Cladistic Study (Smithsonian Institution, Washington, District of Columbia, 1997).

    Google Scholar 

  7. Theophrastus. Enquiry into Plants (Harvard University Press, Cambridge, Massachusetts and London, UK, 1999).

  8. Bharathan, G. et al. Homologies in leaf form inferred from KNOX1 gene expression during development. Science 296, 1858–1860 (2002). The first comprehensive comparative study of KNOX expression and leaf form, set in a phylogenetic context.

    CAS  PubMed  Google Scholar 

  9. Evans, M. M. S. & Barton, M. K. Genetics of angiosperm shoot apical meristem development. Ann. Rev. Plant Physiol. Plant Mol. Biol. 48, 673–701 (1997).

    CAS  Google Scholar 

  10. Clark, S. E. Cell signalling at the shoot meristem. Nature Rev. Mol. Cell Biol. 2, 276–284 (2001).

    CAS  Google Scholar 

  11. Fletcher, J. C. Shoot and floral meristem maintenance in Arabidopsis. Annu. Rev. Plant Biol. 53, 45–66 (2002).

    CAS  PubMed  Google Scholar 

  12. Clark, S. E., Running, M. P. & Meyerowitz, E. M. CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development 119, 397–418 (1993).

    CAS  PubMed  Google Scholar 

  13. Clark, S. E., Running, M. P. & Meyerowitz, E. M. CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1. Development 121, 2057–2067 (1995).

    CAS  Google Scholar 

  14. Steeves, T. A. & Sussex, I. M. Patterns in Plant Development (Cambridge University Press, Cambridge, UK, 1989).

    Google Scholar 

  15. Vollbrecht, E., Veit, B., Sinha, N. & Hake, S. The developmental gene Knotted-1 is a member of a maize homeobox gene family. Nature 350, 241–243 (1991).

    CAS  PubMed  Google Scholar 

  16. Vollbrecht, E., Reiser, L. & Hake, S. Shoot meristem size is dependent on inbred background and presence of the maize homeobox gene, knotted1. Development 127, 3161–3172 (2000).

    CAS  PubMed  Google Scholar 

  17. Long, J. A., Moan, E. I., Medford, J. I. & Barton, M. K. A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379, 66–69 (1996).

    CAS  PubMed  Google Scholar 

  18. Kerstetter, R. et al. Sequence analysis and expression patterns divide the maize knotted1-like homeobox genes into two classes. Plant Cell 6, 1877–1887 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Smith, L. G., Greene, B., Veit, B. & Hake, S. A dominant mutation in the maize homeobox gene, Knotted-1, causes its ectopic expression in leaf cells with altered fates. Development 116, 21–30 (1992).

    CAS  PubMed  Google Scholar 

  20. 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 120, 405–413 (1994).

    CAS  Google Scholar 

  21. Lincoln, C., Long, J., Yamaguchi, J., Serikawa, K. & Hake, S. A Knotted1-like homeobox gene in Arabidopsis is expressed in the vegetative meristem and dramatically alters leaf morphology when overexpressed in transgenic plants. Plant Cell 6, 1859–1876 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Kerstetter, R. A., Laudencia-Chingcuanco, D., Smith, L. G. & Hake, S. Loss of function mutations in the maize homeobox gene, knotted1, are defective in shoot meristem maintenance. Development 124, 3045–3054 (1997).

    CAS  PubMed  Google Scholar 

  23. Sinha, N. R., Williams, R. E. & Hake, S. Overexpression of the maize homeobox gene, KNOTTED-1, causes a switch from determinate to indeterminate cell fates. Genes Dev. 7, 787–795 (1993).

    CAS  PubMed  Google Scholar 

  24. Chuck, G., Lincoln, C. & Hake, S. Knat1 induces lobed leaves with ectopic meristems when overexpressed in Arabidopsis. Plant Cell 8, 1277–1289 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Waites, R., Selvadurai, H. R., Oliver, I. R. & Hudson, A. The PHANTASTICA gene encodes a MYB transcription factor involved in growth and dorsoventrality of lateral organs in Antirrhinum. Cell 93, 779–789 (1998).

    CAS  PubMed  Google Scholar 

  26. Timmermans, 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 284, 151–153 (1999).

    CAS  PubMed  Google Scholar 

  27. 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 284, 154–156 (1999).

    CAS  PubMed  Google Scholar 

  28. Byrne, M. E. et al. Asymmetric leaves 1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 408, 967–971. (2000).

    CAS  PubMed  Google Scholar 

  29. Byrne, M. E., Simorowski, J. & Martienssen, R. A. ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis. Development 129, 1957–1965 (2002).

    CAS  PubMed  Google Scholar 

  30. Moore, I., Galweiler, L., Grosskopf, D., Schell, J. & Palme, K. A transcription activation system for regulated gene expression in transgenic plants. Proc. Natl Acad. Sci. USA 95, 376–381 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Schwabe, W. W. in Positional Controls in Plant Development (eds Barlow, P. W. & Carr, D. J.) 403–440 (Cambridge University Press, Cambridge, UK, 1984).

    Google Scholar 

  32. Reinhardt, D., Mandel, T. & Kuhlemeier, C. Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 12, 507–518 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Snow, M. & Snow, R. Auxin and leaf formation. New Phytol. 36, 1–18 (1937).

    CAS  Google Scholar 

  34. Schwabe, W. W. Chemical modification of phyllotaxis and its implications. Symp. Soc. Exp. Biol. 25, 301–322 (1971).

    CAS  PubMed  Google Scholar 

  35. Galweiler, L. et al. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282, 2226–2230 (1998).

    CAS  PubMed  Google Scholar 

  36. Aida, M., Vernoux, T., Furutani, M., Traas, J. & Tasaka, M. Roles of PIN-FORMED1 and MONOPTEROS in pattern formation of the apical region of the Arabidopsis embryo. Development 129, 3965–3974 (2002).

    CAS  PubMed  Google Scholar 

  37. Siegfried, K. R. et al. Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 126, 4117–4128 (1999).

    CAS  PubMed  Google Scholar 

  38. Kerstetter, R. A., Bollman, K., Taylor, R. A., Bomblies, K. & Poethig, R. S. KANADI regulates organ polarity in Arabidopsis. Nature 411, 706–709 (2001).

    CAS  PubMed  Google Scholar 

  39. Eshed, Y., Baum, S. F., Perea, J. V. & Bowman, J. L. Establishment of polarity in lateral organs of plants. Curr. Biol. 11, 1251–1260 (2001).

    CAS  PubMed  Google Scholar 

  40. McConnell, J. R. & Barton, M. K. Leaf polarity and meristem formation in Arabidopsis. Development 125, 2935–2942 (1998).

    CAS  PubMed  Google Scholar 

  41. McConnell, J. R. et al. Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411, 709–713 (2001).

    CAS  PubMed  Google Scholar 

  42. Talbert, P. B., Adler, H. T., Parks, D. W. & Comai, L. The revoluta gene is necessary for apical meristem development and for limiting cell divisions in the leaves and stems of Arabidopsis thaliana. Development 121, 2723–2735 (1995).

    CAS  PubMed  Google Scholar 

  43. Otsuga, D., DeGuzman, B., Prigge, M. J., Drews, G. N. & Clark, S. E. REVOLUTA regulates meristem initiation at lateral positions. Plant J. 25, 223–236 (2001).

    CAS  PubMed  Google Scholar 

  44. Kumaran, M. K., Bowman, J. L. & Sundaresan, V. YABBY polarity genes mediate the repression of KNOX homeobox genes in Arabidopsis. Plant Cell 14, 2761–2770 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Waites, R. & Hudson, A. phantastica: a gene required for dorsoventrality of leaves in Antirrhinum majus. Development 121, 2143–2154 (1995).

    CAS  Google Scholar 

  46. Aida, M., Ishida, T. & Tasaka, M. Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes. Development 126, 1563–1570 (1999).

    CAS  PubMed  Google Scholar 

  47. Shuai, B., Reynaga-Pena, C. G. & Springer, P. S. The LATERAL ORGAN BOUNDARIES gene defines a novel, plant-specific gene family. Plant Physiol. 129, 747–761 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Elliott, R. C. et al. AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 8, 155–168 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Long, J. A. & Barton, M. K. The development of apical embryonic pattern in Arabidopsis. Development 125, 3027–3035 (1998). A detailed analysis of early gene-expression patterns during embryogenesis in wild-type Arabidopsis and in stm mutants.

    CAS  PubMed  Google Scholar 

  50. Sentoku, N., Sato, Y. & Matsuoka, M. Overexpression of rice OSH genes induces ectopic shoots on leaf sheaths of transgenic rice plants. Dev. Biol. 220, 358–364 (2000).

    CAS  PubMed  Google Scholar 

  51. Coyne, J. A. & Lande, R. The genetic basis of species differences in plants. Am. Nat. 126, 141–145 (1985).

    Google Scholar 

  52. Stark, J., Bonacum, J., Remsen, J. & DeSalle, R. The evolution and development of dipteran wing veins: a systematic approach. Annu. Rev. Entomol. 44, 97–129 (1999).

    CAS  PubMed  Google Scholar 

  53. Hareven, D., Gutfinger, T., Parnis, A., Eshed, Y. & Lifschitz, E. The making of a compound leaf: genetic manipulation of leaf architecture in tomato. Cell 84, 735–744 (1996). The first demonstration of the relationship between KNOX gene-expression patterns and dissected leaf morphology by expression analysis and KNOX overexpression phenotypes.

    CAS  PubMed  Google Scholar 

  54. Janssen, B. J., Lund, L. & Sinha, N. Overexpression of a homeobox gene, LeT6, reveals indeterminate features in the tomato compound leaf. Plant Physiol. 117, 771–786 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Pavlopoulos, A. & Averof, M. Developmental evolution: Hox proteins ring the changes. Curr. Biol. 12, R291–R293 (2002).

    CAS  PubMed  Google Scholar 

  56. Sinha, N. R. Simple and compound leaves: reduction or multiplication? Trends Plant Sci. 2, 396–402 (1997).

    Google Scholar 

  57. Hofer, J., Gourlay, C., Michael, A. & Ellis, T. H. Expression of a class 1 knotted1-like homeobox gene is downregulated in pea compound leaf primordia. Plant Mol. Biol. 45, 387–398 (2001).

    CAS  PubMed  Google Scholar 

  58. Hofer, J. et al. UNIFOLIATA regulates leaf and flower morphogenesis in pea. Curr. Biol. 7, 581–587 (1997). Shows for the first time that UNI — the orthologue of the Arabidopsis LFY protein — regulates leaf form in pea.

    CAS  PubMed  Google Scholar 

  59. Weigel, D., Alvarez, J., Smyth, D. R., Yanofsky, M. F. & Meyerowitz, E. M. LEAFY controls floral meristem identity in Arabidopsis. Cell 69, 843–859 (1992).

    CAS  PubMed  Google Scholar 

  60. Coen, E. S. et al. FLORICAULA: a homeotic gene required for flower development in Antirrhinum majus. Cell 63, 1311–1322 (1990).

    CAS  PubMed  Google Scholar 

  61. Taylor, S., Hofer, J. & Murfet, I. I. Stamina pistilloida, the pea ortholog of Fim and UFO, is required for normal development of flowers, inflorescences, and leaves. Plant Cell 13, 31–46 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Ingram, G. C. et al. Parallels between UNUSUAL FLORAL ORGANS and FIMBRIATA, genes controlling flower development in Arabidopsis and Antirrhinum. Plant Cell 7, 1501–1510 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Lee, I., Wolfe, D. S., Nilsson, O. & Weigel, D. A LEAFY co-regulator encoded by UNUSUAL FLORAL ORGANS. Curr. Biol. 7, 95–104 (1997).

    PubMed  Google Scholar 

  64. Molinero-Rosales, N. et al. FALSIFLORA, the tomato orthologue of FLORICAULA and LEAFY, controls flowering time and floral meristem identity. Plant J. 20, 685–693 (1999).

    CAS  PubMed  Google Scholar 

  65. Estruch, J. J., Prinsen, E., Van Onckelen, H., Schell, J. & Spena, A. Viviparous leaves produced by somatic activation of an inactive cytokinin-synthesizing gene. Science 254, 1364–1367 (1991).

    CAS  PubMed  Google Scholar 

  66. Li, Y., Hagen, G. & Guilfoyle, T. J. Altered morphology in transgenic tobacco plants that overproduce cytokinins in specific tissues and organs. Dev. Biol. 153, 386–395 (1992).

    CAS  PubMed  Google Scholar 

  67. Kusaba, S. et al. Alteration of hormone levels in transgenic tobacco plants overexpressing the rice homeobox gene OSH1. Plant Physiol. 116, 471–476 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Tanaka-Ueguchi, M., Itoh, H., Oyama, N., Koshioka, M. & Matsuoka, M. Overexpression of a tobacco homeobox gene, NTH15, decreases the expression of a gibberellin biosynthetic gene encoding GA 20-oxidase. Plant J. 15, 391–400 (1998).

    CAS  PubMed  Google Scholar 

  69. Ori, N. et al. Leaf senescence is delayed in tobacco plants expressing the maize homeobox gene knotted1 under the control of a senescence-activated promoter. Plant Cell 11, 1073–1080 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Sakamoto, T., Kamiya, N., Ueguchi-Tanaka, M., Iwahori, S. & Matsuoka, M. KNOX homeodomain protein directly suppresses the expression of a gibberellin biosynthetic gene in the tobacco shoot apical meristem. Genes Dev. 15, 581–590 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Hay, A. et al. The gibberellin pathway mediates KNOTTED1-type homeobox function in plants with different body plans. Curr. Biol. 12, 1557–1565 (2002). The authors propose that a regulatory module — defined by KNOX transcription factors and GA — functions in the shoot meristem to control indeterminacy and has been co-opted to function in leaves to control dissected form.

    CAS  PubMed  Google Scholar 

  72. Dover, G. How genomic and developmental dynamics affect evolutionary processes. Bioessays 22, 1153–1159 (2000).

    CAS  PubMed  Google Scholar 

  73. Müller, K. et al. The barley Hooded mutation caused by a duplication in a homeobox gene intron. Nature 374, 727–730 (1995).

    PubMed  Google Scholar 

  74. Williams-Carrier, R. E., Lie, Y. S., Hake, S. & Lemaux, P. G. Ectopic expression of the maize kn1 gene phenocopies the Hooded mutant of barley. Development 124, 3737–3745 (1997).

    CAS  PubMed  Google Scholar 

  75. Golz, J. F., Keck, E. J. & Hudson, A. Spontaneous mutations in KNOX genes give rise to a novel floral structure in Antirrhinum. Curr. Biol. 12, 515–522 (2002). The authors characterize two dominant floral mutants caused by regulatory mutations in KNOX genes and propose that similar regulatory changes could be responsible for the evolution of petal spurs in Antirrhinum species.

    CAS  PubMed  Google Scholar 

  76. Muehlbauer, G. J., Fowler, J. E. & Freeling, M. Sectors expressing the homeobox gene liguleless3 implicate a time-dependent mechanism for cell fate acquisition along the proximal–distal axis of the maize leaf. Development 124, 5097–5106 (1997).

    CAS  PubMed  Google Scholar 

  77. Parnis, A. et al. The dominant developmental mutants of tomato, Mouse-Ear and Curl, are associated with distinct modes of abnormal transcriptional regulation of a Knotted gene. Plant Cell 9, 2143–2158 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Chen, J. -J., Janssen, B. -J., Williams, A. & Sinha, N. A gene fusion at a homeobox locus: alterations in leaf shape and implications for morphological evolution. Plant Cell 9, 1289–1304 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Muller, J. et al. In vitro interactions between barley TALE homeodomain proteins suggest a role for protein–protein associations in the regulation of Knox gene function. Plant J. 27, 13–23 (2001).

    CAS  PubMed  Google Scholar 

  80. Bellaoui, M. et al. The Arabidopsis BELL1 and KNOX TALE homeodomain proteins interact through a domain conserved between plants and animals. Plant Cell 13, 2455–2470 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Smith, H. M., Boschke, I. & Hake, S. Selective interaction of plant homeodomain proteins mediates high DNA-binding affinity. Proc. Natl Acad. Sci. USA 99, 9579–9584 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Burglin, T. R. Analysis of TALE superclass homeobox genes (MEIS, PBC, KNOX, Iroquois, TGIF) reveals a novel domain conserved between plants and animals. Nucleic Acids Res. 25, 4173–4180 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Rieckhof, G. E., Casares, F., Ryoo, H. D., Abu-Shaar, M. & Mann, R. S. Nuclear translocation of extradenticle requires homothorax, which encodes an extradenticle-related homeodomain protein. Cell 91, 171–183 (1997).

    CAS  PubMed  Google Scholar 

  84. Spit, A., Hyland, R. H., Mellor, E. J. C. & Casselton, L. A. A role for heterodimerization in nuclear localization of a homeodomain protein. Proc. Natl Acad. Sci. USA 95, 6228–6233 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Lucas, W. J. et al. Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 270, 1980–1983 (1995).

    CAS  PubMed  Google Scholar 

  86. 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 99, 4103–4108 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  87. Perbal, M. -C., Haughn, G., Saedler, H. & Schwarz-Sommer, Z. Non-cell-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking. Development 122, 3433–3441 (1996).

    CAS  PubMed  Google Scholar 

  88. Sessions, A., Weigel, D. & Yanofsky, M. F. The Arabidopsis thaliana MERISTEM LAYER 1 promoter specifies epidermal expression in meristems and young primordia. Plant J. 20, 259–263 (1999).

    CAS  PubMed  Google Scholar 

  89. Helariutta, Y. et al. The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101, 555–567 (2000).

    CAS  PubMed  Google Scholar 

  90. Ori, N., Eshed, Y., Chuck, G., Bowman, J. L. & Hake, S. Mechanisms that control knox gene expression in the Arabidopsis shoot. Development 127, 5523–5532 (2000). Characterization of two mutants that confer ectopic KNOX expression in Arabidopsis leaves and genetic interactions that enhance these mutant phenotypes in a KNOX-independent manner. The results indicate that KNOX expression might be controlled at the chromatin level.

    CAS  PubMed  Google Scholar 

  91. Eshed, Y., Baum, S. F. & Bowman, J. L. Distinct mechanisms promote polarity establishment in carpels of Arabidopsis. Cell 99, 199–209 (1999).

    CAS  PubMed  Google Scholar 

  92. Ogas, J., Kaufmann, S., Henderson, J. & Somerville, C. PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis. Proc. Natl Acad. Sci. USA 96, 13839–13844 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Prigge, M. J. & Wagner, D. R. The Arabidopsis serrate gene encodes a zinc-finger protein required for normal shoot development. Plant Cell 13, 1263–1279 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Cong, B., Liu, J. & Tanksley, S. D. Natural alleles at a tomato fruit size quantitative trait locus differ by heterochronic regulatory mutations. Proc. Natl Acad. Sci. USA 99, 13606–13611 (2002). Powerful use of QTL analysis to identify regulatory changes in the fw2.2 locus that are responsible for natural variation in fruit size.

    CAS  PubMed  PubMed Central  Google Scholar 

  95. Wang, R. L., Stec, A., Hey, J., Lukens, L. & Doebley, J. The limits of selection during maize domestication. Nature 398, 236–239 (1999). The authors present compelling evidence that selection in regulatory regions of tb1 has driven changes in gene expression and consequent changes in branching patterns during the domestication of maize.

    CAS  PubMed  Google Scholar 

  96. Briggs, D. & Walters, S. M. Plant Variation and Evolution (Cambridge University Press, Cambridge, UK, 1997).

    Google Scholar 

  97. Comai, L. et al. Phenotypic instability and rapid gene silencing in newly formed Arabidopsis allotetraploids. Plant Cell 12, 1551–1568 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Nasrallah, M. E., Yogeeswaran, K., Snyder, S. & Nasrallah, J. B. Arabidopsis species hybrids in the study of species differences and evolution of amphiploidy in plants. Plant Physiol. 124, 1605–1614 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  99. Lee, H. S. & Chen, Z. J. Protein-coding genes are epigenetically regulated in Arabidopsis polyploids. Proc. Natl Acad. Sci. USA 98, 6753–6758 (2001). The analysis of gene-expression profiles during polyploidization reported by this paper and reference 97 indicate that epigenetic regulation might be important in generating diversity during abrupt speciation.

    CAS  PubMed  PubMed Central  Google Scholar 

  100. Finnegan, E. J. Epialleles — a source of random variation in times of stress. Curr. Opin. Plant Biol. 5, 101–106 (2002).

    CAS  PubMed  Google Scholar 

  101. Furlong, R. F. & Holland, P. W. Were vertebrates octoploid? Phil. Trans. R. Soc. Lond. B 357, 531–544 (2002).

    CAS  Google Scholar 

  102. Cubas, P., Vincent, C. & Coen, E. An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401, 157–161 (1999). By showing that an epigenetic mutation in CYC is responsible for differences in floral symmetry in a variant of Linaria , this paper shows the importance of epigenetic regulation in driving changes in form.

    CAS  PubMed  Google Scholar 

  103. Yu, L. P., Simon, E. J., Trotochaud, A. E. & Clark, S. E. POLTERGEIST functions to regulate meristem development downstream of the CLAVATA loci. Development 127, 1661–1670 (2000).

    CAS  PubMed  Google Scholar 

  104. Bowman, J. L. et al. The story of CRABS CLAW (or how we learned to love the mutagen). Flowering Newsletter (2001). Excellent exposition of the logic and merits of using second-site mutagenesis to understand shoot development in the post-sequencing era.

    Google Scholar 

  105. Davidson, E. H. et al. A genomic regulatory network for development. Science 295, 1669–1678 (2002).

    CAS  PubMed  Google Scholar 

  106. Brown, C. T. et al. New computational approaches for analysis of cis-regulatory networks. Dev. Biol. 246, 86–102 (2002).

    CAS  PubMed  Google Scholar 

  107. Brand, U., Fletcher, J. C., Hobe, M., Meyerowitz, E. M. & Simon, R. Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289, 617–619 (2000).

    CAS  PubMed  Google Scholar 

  108. Schoof, H. et al. The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100, 635–644 (2000).

    CAS  PubMed  Google Scholar 

  109. Riechmann, J. L. et al. Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290, 2105–2110 (2000).

    CAS  PubMed  Google Scholar 

  110. Groot, E. P. & Meicenheimer, R. D. Comparison of leaf plastochron index and allometric analyses of tooth development in Arabidopsis thaliana. J. Plant Growth Regul. 19, 77–89 (2000).

    CAS  PubMed  Google Scholar 

  111. Hagemann, W. & Gleissberg, S. Organogenetic capacity of leaves: the significance of marginal blastozones in angiosperms. Plant Syst. Evol. 199, 121–152 (1996). A complete and clearly discussed exposition of the morphological analysis of dissected leaf development in a variety of angiosperms.

    Google Scholar 

  112. Gleissberg, S. in Developmental Genetics and Plant Evolution Vol. 65 (eds Cronk, Q. C., Bateman, R. M. & Hawkins, J. A.) 404–417 (Taylor & Francis, London, UK and New York, 2002).

    Google Scholar 

  113. Kaplan, D. R. Fundamental concepts of leaf morphology and morphogenesis: a contribution to the interpretation of molecular genetic mutants. Int. J. Plant Sci. 162, 465–474 (2001).

    CAS  Google Scholar 

  114. Carroll, S., Grenier, J. K. & Weatherbee, S. D. From DNA to Diversity (Blackwell Science, London, UK (2001).

    Google Scholar 

  115. Ronshaugen, M., McGinnis, N. & McGinnis, W. Hox protein mutation and macroevolution of the insect body plan. Nature 415, 914–917 (2002).

    PubMed  Google Scholar 

  116. Galant, R. & Carroll, S. B. Evolution of a transcriptional repression domain in an insect Hox protein. Nature 415, 910–913 (2002).

    CAS  PubMed  Google Scholar 

  117. Frary, A. et al. fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289, 85–88 (2000).

    CAS  PubMed  Google Scholar 

  118. Doebley, J., Stec, A. & Hubard, L. The evolution of apical dominance in maize. Nature 386, 485–488 (1997).

    CAS  PubMed  Google Scholar 

  119. Simpson, P. Evolution of development in closely related species of flies and worms. Nature Rev. Genet. 3, 907–917 (2002).

    CAS  PubMed  Google Scholar 

  120. Markstein, M., Markstein, P., Markstein, V. & Levine, M. S. Genome-wide analysis of clustered Dorsal binding sites identifies putative target genes in the Drosophila embryo. Proc. Natl Acad. Sci. USA 99, 763–768 (2002).

    CAS  PubMed  Google Scholar 

  121. Fosket, D. E. Plant Growth and Development: a Molecular Approach (Academic Press, San Diego, 1994).

    Google Scholar 

Download references

Acknowledgements

We thank N. Sinha for providing figure 1, A Hudson for helpful discussions and S. McCormick for comments on the manuscript. M.T. is a recipient of a Royal Society Fellowship and his laboratory is funded by the Biotechnology and Biological Sciences Research Council.

Author information

Authors and Affiliations

  1. Department of Plant Sciences, University of Oxford, South Parks Road, Oxford, OX1 3RB, UK

    Miltos Tsiantis & Angela Hay

Authors
  1. Miltos Tsiantis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Angela Hay
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Miltos Tsiantis.

Related links

Related links

DATABASES

TAIR

ANT

AS1

AS2

LFY

PIN1

SE

STM

UFO

WUS

FURTHER INFORMATION

Andrew Hudson's laboratory

Enrico Coen's laboratory

John Doebley's laboratory

Neelima Sinha's laboratory

New York Plant Genomics Consortium

NSF Consortium Plant Genome Project

Steven Tanksley's laboratory

Glossary

MEGAPHYLLOUS LEAVES

The basic leaf type in ferns and seed plants. They are typically large, with a distinct adaxial and abaxial plane and have a complex branched vascular structure.

MERISTEM

A structure that is found at the growing tip of the roots or shoots of a plant and in which stem cells (undifferentiated cells that can undergo unlimited division) are maintained and organogenesis occurs.

PLASTOCHRON

The time interval between successive primordia.

HIGHER PLANTS

Seed plants, including gymnosperms (in which the seed is 'naked') and angiosperms, or flowering plants (in which the seed is contained in an ovary).

INDETERMINATE

Refers to a pattern of growth and development that is open-ended. In meristems, this is associated with the continuous ability to produce determinate lateral organs (such as leaves). By contrast, determinate refers to growth and development that is restricted in time or space.

LEAF FOUNDER CELLS

A group of cells that encompasses several layers of the shoot apical meristem and from which a leaf primordium is derived. Founder cells do not function as stem cells but rather have a determinate fate and can be defined by histological, clonal and molecular criteria.

LATERAL ORGAN

Organs that are produced from the shoot apical meristem such as leaves and putatively homologous organs such as cotyledons (embryonic leaves), bracts (modified leaves that subtend reproductive structures) and floral organs.

HOMEOBOX

A 180-base-pair sequence that encodes a DNA-binding helix–turn–helix motif termed a homeodomain.

CYCADS

(Phylum Cycadophyta). One of four divisions of gymnosperms. They resemble palms but have naked seeds on the scales of cones.

CLASS I KNOX GENES

Knotted1-like homeobox (KNOX) genes in all plants can be divided into two classes based on sequence similarity and expression pattern. The sequenced genome of Arabidopsis contains four class I KNOX genes (STM, KNAT1 (KN1-like in Arabidopsis thaliana 1), KNAT2 and KNAT6).

MONOCOT

(Monocotyledonous plants). Angiosperms with one cotyledon (seed leaf).

DICOT

(Eudicotyledonous plants). The largest group of angiosperms, characterized by two cotyledons (seed leaves) and three symmetrically placed pollen apertures.

MYB TRANSCRIPTION FACTOR

A family of transcription factors defined by the presence of a structurally conserved DNA binding domain first identified in a viral oncogene. The Arabidopsis genome contains over one hundred MYB-like genes that function in diverse regulatory systems, including secondary metabolism, cell morphogenesis, the cell cycle and circadian rhythms.

HOMEODOMAIN

A highly conserved sequence motif. It comprises 60 amino acids and contains a DNA-binding helix–turn–helix motif, indicating that homeodomain-containing proteins function as transcription factors.

HIGH MOBILITY GROUP (HMG) DOMAIN

A conserved domain that is present in HMG proteins, which are non-histone proteins involved in chromatin structure and gene regulation.

GARP DOMAIN

A conserved DNA-binding domain that is distantly related to the MYB DNA-binding domain. It is defined by the acronym of the founding members of the GARP family: maize Golden 2, ARR (Arabidopsis response regulators) and Psr1 (phosphorus stress response1 from Chlamydomonas).

AUXINS

A class of plant hormones, typified by indole-3-acetic acid, that is required for many aspects of plant development and for plant cell growth in culture. The term auxin is derived from the Greek afksano, meaning 'to increase'.

CAMV 35S PROMOTER

35S RNA promoter from cauliflower mosaic virus that is commonly used to drive constitutive gene expression in plants.

ABAXIAL

The side of a lateral organ that initiates away from (ab, away from) the meristem.

ADAXIAL

The side of a lateral organ that initiates next to (ad, close to) the meristem.

LAMINA

The (usually flattened) parts of a leaf on either side of the midvein.

PINNATE

A dissected leaf with a central axis and a single order of leaflets (or pinnae) on either side of it.

BIPINNATE

A dissected leaf that has two orders of leaflets (or pinnae) so the first-order leaflets are themselves dissected into a second order of leaflets.

PALMATE

A dissected leaf with leaflets arising from a central point at the end of the leaf stem

INTERCALARY LEAFLETS

Leaflets that develop between the primary leaflets of a dissected leaf. They are usually smaller than primary leaflets.

QA REPRESSION DOMAIN

A repressive domain that is conserved in insect Ultrabithorax proteins. It contains a Gln-Ala-Gln-Ala-Lys motif and a stretch of Ala residues.

HETEROCHRONIC REGULATORY MUTATIONS

Mutations that alter the relative timing of developmental events as an organism grows (from the Greek heteros, meaning 'other' or 'different', and chronos, meaning 'time').

AWN

A slender bristle-like structure found on the spikelets (structure that contains the flowers) of many grasses.

PETAL SPUR

An outgrowth of a petal in which nectar can collect.

PLASMODESMATA

Cell-wall channels that allow symplastic connections between plant cells.

NON-AUTONOMOUS

Function of a gene product that is not restricted to the cell in which it is expressed.

PHENOCOPY

A mimic of another phenotype.

CARPEL

The female reproductive organ of a flower that encloses the ovules.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tsiantis, M., Hay, A. Comparative plant development: the time of the leaf?. Nat Rev Genet 4, 169–180 (2003). https://doi.org/10.1038/nrg1002

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrg1002

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing