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The Botanical Review

, Volume 78, Issue 4, pp 463–489 | Cite as

Leaf Development, Metamorphic Heteroblasty and Heterophylly in Berberis s. l. (Berberidaceae)

  • Natalia Pabón-MoraEmail author
  • Favio González
Article

Abstract

Shoot development of temperate and tropical members of Berberis s. l. was examined in order to assess: (1) the homology of the spines along the long shoots and the foliage leaves that form on the short shoots; (2) the occurrence of heterophylly and/or heteroblasty in the genus; and (3) the structural correspondence between cataphylls, spines, and foliage leaves. The 1-5-armed spines have been interpreted as modified compound leaves lacking stipules, as a modified lamina (central spine) with stipules (lateral spines), or less often, as transformed branches, or as epidermal outgrowths. On the other hand, the foliage leaves of the short shoots have been interpreted as leaflets of palmately compound leaves. Our results indicate that there are three distinct leaf types per node: (1) Leaves modified in spines spirally arranged in long shoots; (2) foliage, expanded leaves densely arranged in short shoots; and (3) cataphylls protecting axillary buds. The spines are leaf homologs with a clear distinction between the leaf base with stipules, and a laminar portion modified into the 1-5-armed spine; the lateral spines are not stipules as they arise from the marginal meristem of the laminar portion, and not from the leaf base. The foliage leaves also have stipules flanking the leaf base. Both spiny leaves and foliage leaves develop an articulation between the base and the laminar portion. Cataphylls of the short shoots of Berberis s. str. and those of the reproductive short shoots of Mahonia correspond to the entire leaf base, but those of the renewal (vegetative) shoots of Mahonia are spiny and have an odd vestigial pinnately compound lamina. Heterochrony due to ontogenetic truncation caused by the formation of the terminal inflorescence at the apex of the short shoots could be responsible for the lack of petiole/lamina differentiation in the foliage leaves. The spiny long-shoot/foliose short-shoot system of branching in Berberis s. str. appears to be genetically and phylogenetically fixed and not environment-dependent. This represents a clear example of metamorphic heteroblasty sensu Zotz et al. (Botanical Review 77:109–151, 2011) with further occurrence of heterophylly along the short shoots.

Keywords

Berberidaceae Berberis Heterochrony Heterophylly Leaf Development Long Shoots Mahonia Metamorphic Heteroblasty Short Shoots 

Notes

Acknowledgments

We thank D. W. Stevenson (The New York Botanical Garden) for inviting us to participate in the present issue of Botanical Review. We thank Barbara Ambrose for comments on the manuscript. We thank the Facultad de Ciencias, Universidad Nacional de Colombia, Bogotá, and the staff of the Structural Laboratory, The New York Botanical Garden, for logistic support. We also thank J. Hennig, D. Basile, and M. Baxter (Lehmann College, City University of New York), for access to living collections and microscopy facilities.

Literature Cited

  1. Ahrendt, L. W. A. 1961. Berberis and Mahonia, a taxonomic revision. Botanical Journal of the Linnean Society 57: 1–410.CrossRefGoogle Scholar
  2. Allsopp, A. 1965. Heteroblastic development in cormophytes. Pp 1172–1221. In: W. Ruhland (ed). Handbuch der Pflanzenphysiologie XV/1. Springer, Heidelberg.Google Scholar
  3. Ashby, E. 1948. Studies in the morphogenesis of leaves. I. An essay on leaf shape. New Phytologist 47: 153–176.CrossRefGoogle Scholar
  4. Bharathan, G., T. E. Goliber, C. Moore, S. Kessler, T. Pham & N. R. Sinha. 2002. Homologies in leaf form inferred from KNOXI gene expression during development. Science 296: 1858–1860.PubMedCrossRefGoogle Scholar
  5. Beck, P. V. 1927. Comparative anatomy of certain hybrid shrubs and their parents. The University of Kansas Science Bulletin 16: 367–396.Google Scholar
  6. Bell, A. D. 1991. Plant Form. An illustrated guide to flowering plant morphology. Oxford University Press.Google Scholar
  7. ———. 2008. Plant Form. An illustrated guide to flowering plant morphology. Second edition. Timber Press.Google Scholar
  8. Berger, Y., S. Harpaz-Saad, A. Brand, H. Melnik, N. Sirding, J. P. Alvarez, M. Zinder, A. Samach, Y. Eshed & N. Ori. 2009. The NAC-domain transcription factor GOBLET specifies leaflet boundaries in compound tomato leaves. Development 136: 823–832.PubMedCrossRefGoogle Scholar
  9. Blein, T., A. Pulido, A. Vialette-Guiraud, K. Nikovics, H. Morin, A. Hay, I. E. Johansen, M. Tsiantis & P. Laufs. 2008. A conserved molecular framework for compound leaf development. Science 322: 1835–1839.PubMedCrossRefGoogle Scholar
  10. Brodribb, T. & R. S. Hill. 1993. A physiological comparison of leaves and phyllodes in Acacia melanoxylon. Australian Journal of Botany 41: 293–305.CrossRefGoogle Scholar
  11. Burns, K. C. & J. W. Dawson. 2006. A morphological comparison of leaf heteroblasty between New Caledonia and New Zealand. New Zealand Journal of Botany 44: 387–396.CrossRefGoogle Scholar
  12. ——— & ———. 2009. Heteroblasty on Chatham Island: A comparison with New Zealand and New Caledonia. New Zealand Journal of Ecology 33: 156–163.Google Scholar
  13. Byrne, M. E., R. Barley, M. Curtis, J. M. Arroyo, M. Dunham, A. Hudson & R. A. Martienssen. 2000. ASYMMETRIC LEAVES1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 104: 967–971.Google Scholar
  14. ———, J. Simorowski & R. A. Martienssen. 2002. ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis. Development 129: 1957–1965.PubMedGoogle Scholar
  15. Camargo, L. A. 1960. A critical taxonomic study of 15 colombian species of Berberis. M. Sc. Thesis, Catholic University of America, Washington, D. C.Google Scholar
  16. ———. 1966. Especies nuevas del género Berberis. Caldasia 9:313–351.Google Scholar
  17. ———. 1981. Especies nuevas del género Berberis. II. Caldasia 13:203–222.Google Scholar
  18. ———. 1983. Especies nuevas del género Berberis. III. Caldasia 13:675–691.Google Scholar
  19. ———. 1991. Especies nuevas del género Berberis. IV. Caldasia 16:419–424.Google Scholar
  20. Cameron, R. J. 1970. Light intensity and growth of Eucalyptus seedlings. I. Ontogenetic variation in E. fastigiata. Australian Journal of Botany 18: 29–43.CrossRefGoogle Scholar
  21. Champagne, C. & N. Sinha. 2004. Compound leaves: equal to the sum of their parts? Development 131: 4401–4412.PubMedCrossRefGoogle Scholar
  22. Champagne, C. E., T. E. Goliber, M. F. Wojciechowski, R. W. Mei, B. T. Townsley, K. Wang, M. M. Paz, R. Geeta & N. R. Sinha. 2007. Compound leaf development and evolution in the legumes. The Plant Cell 19: 3369–3378.Google Scholar
  23. Croizat, L. 1960. Principia Botanica, or beginnings of botany. N. V. Drukkerij Salland Deventer, Netherlands.Google Scholar
  24. Cronk, Q. C. B. 2009. The molecular organography of plants. Oxford University Press, Oxford.CrossRefGoogle Scholar
  25. Cronquist, A. 1981. An integrated system of classification of flowering plants. Columbia University Press, New York.Google Scholar
  26. Curtis, J. D. & N. L. Lersten. 1978. Heterophylly in Populus grandidentata (Salicaceae) with emphasis on resin glands and extrafloral nectarines. American Journal of Botany 65: 1003–1010.CrossRefGoogle Scholar
  27. Darrow, H. E., P. Bannister, D. J. Burritt & P. E. Jameson. 2002. Are juvenile forms of New Zealand heteroblastic trees more resistant to water loss than their mature counterparts? New Zealand Journal of Botany 40: 313–325.CrossRefGoogle Scholar
  28. Day, J. D. 1998. Light conditions and the evolution of heteroblasty (and the divaricate form) in New Zealand. New Zealand Journal of Ecology 22: 43–54.Google Scholar
  29. De Witt, T. J., A. Sih, & D. S. Wilson. 1998. Costs and limits of phenotypic plasticity. Trends in Ecology and Evolution 13: 77–81.Google Scholar
  30. Diggle, P. K. 1999. Heteroblasty and the evolution of flowering phenologies. International Journal of Plant Sciences 160(S6): S123–S134.PubMedCrossRefGoogle Scholar
  31. Eckenwalder, J. E. 1980. Foliar heteromorphism in Populus (Salicaceae), a source of confusion in the taxonomy of Tertiary leaf remains. Systematic Botany 5: 366–383.CrossRefGoogle Scholar
  32. Efroni, I., Y. Eshed & E. Lifschitz. 2010. Morphogenesis of simple and compound leaves: a critical review. The Plant Cell 22: 1019–1032.PubMedCrossRefGoogle Scholar
  33. Ehrenfeld, J. G. 1997. Invasion of deciduous forest preserves in the New York metropolitan region by Japanese berberry (Berberis thunbergii DC.). Journal of the Torrey Botanical Society 124: 210–215.CrossRefGoogle Scholar
  34. Emery, J. F., S. K. Floyd, J. Alvarez, Y. Eshed, N. P. Hawker, A. Izhaki, S. F. Baum & J. L. Bowman. 2003. Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Current Biology 13: 1768–1774.PubMedCrossRefGoogle Scholar
  35. Ernst, W. R. 1964. The genera of Berberidaceae, Lardizabalaceae and Menispermaceae in the southeastern United States. Journal of the Arnold Arboretum 45: 1–35.Google Scholar
  36. Eshed, Y., S. F. Baum, J. V. Perea & J. L. Bowman. 2001. Establishment of polarity in lateral organs of plants. Current Biology 11: 1251–1260.PubMedCrossRefGoogle Scholar
  37. ———, A. Izhaki, S. F. Baum, S. K. Floyd & J. L. Bowman. 2004. Asymmetric leaf development and blade expansion in Arabidopsis are mediated by KANADI and YABBY activities. Development 131: 2997–3006.PubMedCrossRefGoogle Scholar
  38. Fedde, F. 1902. Versuch einer Monographie der Gattung Mahonia. Botanische Jahrbücher 31: 30–133.Google Scholar
  39. Foster, A. 1928. Salient features of the problem of bud scale morphology. Biological Reviews 3: 123–164.CrossRefGoogle Scholar
  40. Gamage, H. K. & L. Jesson. 2007. Leaf heteroblasty is not an adaptation to shade: seedling anatomical and physiological responses to light. New Zealand Journal of Ecology 31: 245–254.Google Scholar
  41. Gardner, S., A. Drinnan, E. Newbigin & P. Ladiges. 2008. Leaf ontogeny and morphology in Acacia Mill. (Mimosaceae). Muelleria 26: 43–50.Google Scholar
  42. Gerrath, J. M. & C. R. Lacroix. 1997. Heteroblastic sequence and leaf development in Leea guineensis. International Journal of Plant Sciences 158: 747–756.CrossRefGoogle Scholar
  43. Givnish, T. J., K. J. Systma, J. F. Smith & W. J. Hahn. 1994. Thorn-like prickles and heterophylly in Cyanea—Adaptations to extinct avian browsers on Hawaii. Proceedings of the National Academy of Sciences, USA 91: 2810–2814.CrossRefGoogle Scholar
  44. Glück, H. 1919. Pp 696. Blatt- und blütenmorphologische Studien. Eine morphologische Untersuchung über die Stipulargebilde, über die Intravaginalpapillen, über die Blattscheide und über die Bewertung der Blütenblattgebilde. Verlag von Gustav Fischer, Jena.Google Scholar
  45. Goebel, K. 1891. Pp 1–50. Die Vegetation der venezuelanischen Paramos. Pflanzenbiologische Schilderungen, Vol. 2. N. G. Elwert’sche Verlagsbuchhandlung, Marburg.Google Scholar
  46. ———. 1900–1905. Organography of plants. Two volumes. Oxford University Press, Oxford.Google Scholar
  47. von Goethe, J. W. 1790. Versuch, die Metamorphose der Pflanzen zu erklären. Carl Wilhelm Ettinger, Gotha.Google Scholar
  48. Green, S., T. L. Green & Y. Heslop-Harrison. 1979. Seasonal heterophylly and leaf gland features in Triphyophyllum (Dioncophyllaceae), a new carnivorous plant genus. Botanical Journal of the Linnean Society 78: 99–116.CrossRefGoogle Scholar
  49. Groom, P. K., B. B. Lamont & L. Kupsky. 1994. Contrasting morphology and ecophysiology of co-ocurring broad and terete leaves in Hakea trifurcata (Proteaceae). Australian Journal of Botany 42: 307–320.Google Scholar
  50. Hallé, F., R. A. A. Oldeman & P. B. Tomlinson. 1978. Tropical trees and forests. An architectural analysis. Springer, New York.Google Scholar
  51. Hansen, D. H. 1996. Establishment and persistence characteristics in juvenile leaves and phyllodes of Acacia koa (Leguminosae) in Hawaii. International Journal of Plant Sciences 157: 123–128.CrossRefGoogle Scholar
  52. Hareven, D., T. Gutfinger, A. Parnis, Y. Eshed & E. Lifschitz. 1996. The making of a compound leaf: Genetic manipulation of leaf architecture in tomato. Cell 84: 735–744.PubMedCrossRefGoogle Scholar
  53. Harvey-Gibson, R. J. & E. Horsman. 1919. The anatomy of stem of the Berberidaceae. Transactions of the Royal Society of Edinburgh 52: 501–515.Google Scholar
  54. Hay, A. & M. Tsiantis. 2010. KNOX genes: Versatile regulators of plant development and diversity. Development 137: 3153–3165.PubMedCrossRefGoogle Scholar
  55. Hofer, J., L. Turner, R. Hellens, M. Ambrose, P. Mathews, A. Michael & N. Ellis. 1997. UNIFOLIATA regulates leaf and flower morphogenesis in pea. Current Biology 7: 581–587.PubMedCrossRefGoogle Scholar
  56. Holm, T. 1899. Podophyllum peltatum: A morphological study. Botanical Gazette 27: 419–433.CrossRefGoogle Scholar
  57. Jaya, E., D. S. Kubien, P. E. Jameson & J. Clemens. 2010. Vegetative phase change and photosynthesis in Eucalyptus occidentalis: architectural simplification prolongs juvenile traits. Tree Physiology 30: 393–403.PubMedCrossRefGoogle Scholar
  58. Jones, C. S. 1993. Heterochrony and heteroblastic leaf development in two subspecies of Cucurbita argyrosperma (Cucurbitaceae). American Journal of Botany 80: 778–795.CrossRefGoogle Scholar
  59. ———. 1995. Does shade prolong juvenile development? A morphological analysis of leaf shape changes in Cucurbita argyrosperma subsp. sororia (Cucurbitaceae). American Journal of Botany 82:346–359.CrossRefGoogle Scholar
  60. ———. 1999. An essay on juvenility, phase change, and heteroblasty in seed plants. International Journal of Plant Sciences 160: S105–S111.PubMedCrossRefGoogle Scholar
  61. ———. 2001. The functional correlates of heteroblastic variation in leaves: changes in form and ecophysiology with whole plant ontogeny. Boletín de la Sociedad Argentina de Botánica 36:171–184.Google Scholar
  62. ———, & M. A. Watson. 2001. Heteroblasty and preformation in mayapple, Podophyllum peltatum (Berberidaceae): Developmental flexibility and morphological constraint. American Journal of Botany 88: 1340–1358.PubMedCrossRefGoogle Scholar
  63. Katayama, N., S. Koi & M. Kato. 2010. Expression of SHOOT MERISTEMLESS, WUSHEL, and ASYMMETRIC LEAVES1 homologs in the shoots of Podostemaceae: implications for the evolution of novel shoot organogenesis. The Plant Cell 22: 2131–2140.PubMedCrossRefGoogle Scholar
  64. Kato, M. & H. Setoguchi. 1998. An rbcL-based phylogeny and heteroblastic leaf morphology of Matoniaceae. Systematic Botany 23: 391–400.CrossRefGoogle Scholar
  65. Kerstetter, R. A., K. Bollman, R. A. Tayler, K. Bomblies & R. S. Poethig. 2001. KANADI regulates organ polarity in Arabidopsis. Nature 411: 706–709.PubMedCrossRefGoogle Scholar
  66. Kidner, C. A. & M. C. P. Timmermans. 2010. Signaling sides: adaxial-abaxial patterning in leaves. In: M. C. P. Timmermans (ed). Plant Development. Elsevier, San Diego.Google Scholar
  67. Kim, M., S. McCormick, M. C. P. Timmermans & N. Sinha. 2003. The expression domain of PHANTASTICA determines leaflet placement in compound leaves. Nature 424: 438–443.PubMedCrossRefGoogle Scholar
  68. Kunze, H. 1986. Studien zur Blattmetamorphose. Beiträge zur Biologie der Pflanzen 61: 49–77.Google Scholar
  69. Landrum, L. R. 1999. Revision of Berberis (Berberidaceae) in Chile and adjacent Southern Argentina. Annals of the Missouri Botanical Garden 86: 793–834.CrossRefGoogle Scholar
  70. Lee, D. W. & J. H. Richards. 1991. Heteroblastic development in vines. Pp 205–243. In: F. E. Putz & H. A. Mooney (eds). The Biology of Vines. Cambridge University Press, Cambridge.Google Scholar
  71. Lindley, J. 1831. An introduction to the natural system of botany; or, a systematic view of the organization, natural affinities, and geographical distribution of the whole vegetable kingdom. G. & C. & H. Carvill, New York.CrossRefGoogle Scholar
  72. Long, J. A., E. I. Moan, J. I. Medford & M. K. Barton. 1996. A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379: 66–69.PubMedCrossRefGoogle Scholar
  73. Mabberley, D. J. 2008. The plant book. Cambridge University Press, Cambridge.Google Scholar
  74. Mallory, A. C., B. J. Reinhart, M. W. Jones-Rhoades, G. Tang, P. D. Zamore, M. K. Barton & D. P. Bartel. 2004. MicroRNA conrol of PHABULOSA in leaf development: importance of pairing to the microRNA 5’ region. EMBO J 23: 3356–3364.PubMedCrossRefGoogle Scholar
  75. Masters, M. T. 1869. Vegetable teratology. Ray Society, R. Hadwicke, London.CrossRefGoogle Scholar
  76. McAlpine, K. G. & L. K. Jesson. 2008. Linking seed dispersal, germination and seedling recruitment in the invasive species Berberis darwinii (Darwin’s barberry). Plant Ecology 197: 119–129.CrossRefGoogle Scholar
  77. McConnell, J. R. & M. K. Barton. 1998. Leaf polarity and meristem formation in Arabidopsis. Development 125: 2935–2942.PubMedGoogle Scholar
  78. ———, J. Emery, Y. Eshed, N. Bao, J. L. Bowman & M. K. Barton. 2001. Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411: 709–713.PubMedCrossRefGoogle Scholar
  79. McGlone, M. S. & C. J. Webb. 1981. Selective forces influencing the evolution of divaricating plants. New Zealand Journal of Ecology 4: 20–28.Google Scholar
  80. McHale, N. A. & R. E. Koning. 2004. MicroRNA- Directed cleavage of Nicotiana sylvestris PHAVOLUTA mRNA regulates the vascular cambium and structure of apical meristems. The Plant Cell 16: 1730–1740.PubMedCrossRefGoogle Scholar
  81. McLellan, T. 1993. The roles of heterochrony and heteroblasty in the diversification of leaf shapes in Begonia dregei (Begoniaceae). American Journal of Botany 80: 796–804.CrossRefGoogle Scholar
  82. Meacham, C. A. 1980. Phylogeny of the Berberidaceae with an evaluation of classifications. Systematic Botany 5: 149–172.CrossRefGoogle Scholar
  83. Merrill, E. K. 1986. Heteroblastic seedlings of green ash. I. Predictability of leaf form and primordial length. Canadian Journal of Botany 64: 2645–2649.CrossRefGoogle Scholar
  84. Minorsky, P. V. 2003. The hot and the classic. Plant Physiology 133: 1671–1672.CrossRefGoogle Scholar
  85. Nakata, M., N. Matsumoto, R. Tsugeki, E. Rikirsch, T. Laux & K. Okada. 2012. Roles of the middle domain-specific WUSCHEL-RELATED HOMEOBOX genes in early development of leaves in Arabidopsis. The Plant Cell 24: 519–535.PubMedCrossRefGoogle Scholar
  86. Nishimura, A., M. Tamaoki & M. Matsuoka. 1998. Expression pattern of KN-1 type tobacco homeobox genes. Plant Cell and Physiology 39: S60.CrossRefGoogle Scholar
  87. Ori, N., Y. Eshed, G. Chuck, J. L. Bowman & S. Hake. 2000. Mechanisms that control Knox gene expression in Arabidopsis shoot. Development 125: 2935–2942.Google Scholar
  88. Pabón-Mora, N. 2012. Functional evolution of the APETALA1/FRUITFULL gene lineage. PhD. Dissertation, The City University of New York, NY.Google Scholar
  89. Poethig, R. S. 2003. Phase change and the regulation of developmental timing in plants. Science 301: 334–336.PubMedCrossRefGoogle Scholar
  90. Prigge, M. J., D. Otsuga, J. M. Alonso, J. R. Ecker, G. N. Drew & S. E. Clark. 2005. Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. The Plant Cell 17: 61–76.PubMedCrossRefGoogle Scholar
  91. Pulido, A. & P. Laufs. 2010. Co-ordination of developmental processes by small RNAs during leaf development. Journal of Experimental Botany 61: 1277–1291.PubMedCrossRefGoogle Scholar
  92. Ramírez, J. L. & S. R. S. Cevallos-Ferriz. 2000. Leaves of Berberidaceae (Berberis and Mahonia) from Oligocene sediments, near Tepexi de Rodríguez, Puebla. Review of Palaeobotany and Palynology 110: 247–257.PubMedCrossRefGoogle Scholar
  93. Rauh, W. 1950. Morphologie der Nutzpflanzen. Quelle & Meyer, Heidelberg.Google Scholar
  94. Ray, T. S. 1987. Cyclic heterophylly in Syngonium (Araceae). American Journal of Botany 74: 16–26.CrossRefGoogle Scholar
  95. ———. 1990. Metamorphosis in the Araceae. American Journal of Botany 77:1599–1609.CrossRefGoogle Scholar
  96. Reinhart, B. J., E. G. Weinstein, M. W. Rhoades, B. Bartel & D. P. Bartel. 2002. MicroRNAs in plants. Genes and Development 16: 1616–1626.PubMedCrossRefGoogle Scholar
  97. Rhoades, M. W., B. J. Reinhart, L. P. Lim, C. B. Burge, B. Bartel & D. P. Bartel. 2002. Prediction of plant microRNA targets. Cell 110: 513–520.PubMedCrossRefGoogle Scholar
  98. Sawa, S., K. Watanabe, K. Goto, E. Kanaya, E. H. Morita & K. Okada. 1999. FILAMENTOUS FLOWER, a meristem and organ identity gene of Arabidopsis, encodes a protein with zinc finger and HMG-related domains. Genes and Development 13: 1079–1088.PubMedCrossRefGoogle Scholar
  99. Schmidt, E. 1928. Untersuchungen über Berberidaceen. Beihefte zum Botanischen Centralblatt 45: 329–396.Google Scholar
  100. Schneeberger, R., M. Tsiantis, M. Freeling & J. A. Langdale. 1998. The rough sheath2 gene negatively regulates homeobox gene expression during maize leaf development. Development 125: 2857–2865.PubMedGoogle Scholar
  101. Schneider, C. K. 1905. Die Gattung Berberis (Euberberis). Vorarbeiten für eine Monographie. Bulletin del Herbier Boissier, ser. 2, 5: 33–48, 133–148, 391–403, 449–464, 655–670, 800–831.Google Scholar
  102. ———. 1908. Weitere Beitrage zur Kenntnis der Gattung Berberis (Euberberis). Bulletin del Herbier Boissier, ser. 2, 8: 192–204, 258–266.Google Scholar
  103. Siegfried, K. R., Y. Eshed, S. F. Baum, D. Otsuga, G. N. Drews & J. L. Bowman. 1999. Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 126: 4117–4128.PubMedGoogle Scholar
  104. Sliander, J. A. & D. M. Klepeis. 1999. The invasion ecology of Japanese barberry (Berberis thunbergii) in the New England landscape. Biological Invasions 1: 189–201.CrossRefGoogle Scholar
  105. Smith, L. G., Greene, B., Veit, B. and Hake, S. 1992. A dominant mutation in the maize homeobox gene, Knotted-1, causes its ectopic expression in leaf cells with altered fates. Development 116: 21–30.Google Scholar
  106. Sugiyama, M. & N. Hara. 1988. Comparative study on early ontogeny of coumpound leaves in Lardizabalaceae. American Journal of Botany 75: 1598–1605.Google Scholar
  107. Takhtajan, A. L. 1997. Diversity and classification of flowering plants. Columbia University Press, New York.Google Scholar
  108. Taylor, T. N., E. L. Taylor & M. Krings. 2009. Paleobotany, the biology and evolution of fossil plants. Academic Press, New York.Google Scholar
  109. Timmermans, M. C. P., A. Hudson, P. W. Becraft & T. Nelson. 1999. ROUGH SHEATH2: a Myb protein that represses Knox homeobox genes in maize lateral organ primordia. Science 284: 151–153.PubMedCrossRefGoogle Scholar
  110. Tischler, G. 1902. Die Berberidaceen und Podophyllaceen. Versuch einer morphologisch-biologischen Monographie. Botanische Jahrbücher 31: 596–727.Google Scholar
  111. Troll, W. 19371943. Vergleichende Morphologie der höheren Pflanzen. Band 1 (1–3). Gebrüder Borntraeger, Berlin.Google Scholar
  112. ———. 1954. Praktische Einführung in die Pflanzenmorphologie. Gustav Fischer, Jena.Google Scholar
  113. ———. 1959. Allgemeine Botanik. Ferdinand Enke, Stuttgart.Google Scholar
  114. ———. 1969. Die Infloreszenzen. Typologie und Stellung im Aufbau des Vegetationskörpers. Vol. 2, part 1. Gustav Fischer, Stuttgart.Google Scholar
  115. Tsiantis, M., R. Schneeberger, J. F. Golz, M. Freeling & J. A. Langdale. 1999. The maize rough sheath2 gene and leaf development in monocot and dicot plants. Science 284: 154–156.PubMedCrossRefGoogle Scholar
  116. Tsukaya, H. 2006. Mechanism of leaf-shape determination. Annual Review in Plant Biology 57: 477–496.CrossRefGoogle Scholar
  117. Venglat, S. P., T. Dumonceaux, K. Rozwadowki, L. Parnell, V. Babic, W. Keller, R. Martienssen, G. Selvaraj & R. Datla. 2002. The homeobox gene BREVIPEDICELLUS is a key regulator of inflorescence architecture in Arabidopsis. Proceedings of the National Academy of Sciences USA 99: 4730–4735.CrossRefGoogle Scholar
  118. Vollbrecht, E., L. Reiser & S. Hake. 2000. Shoot meristem size is dependent on inbred background and presence of the of the maize homeobox gene, knotted1. Development 127: 3161–3172.PubMedGoogle Scholar
  119. Waites, R., H. R. N. Selvadurai, I. R. Oliver & A. Hudson. 1998. The phantastica gene encodes a MYB transcription factor involved in growth and dorsoventrality of lateral organs in Antirrhinum. Cell 93: 779–789.PubMedCrossRefGoogle Scholar
  120. Wang, W., A.-M. Lu, Y. Ren, M. E. Endress & Z.-D. Chen. 2009. Phylogeny and classification of Ranunculales: Evidence from four molecular loci and morphological data. Perspectives in Plant Ecology, Evolution and Systematics 11: 81–110.CrossRefGoogle Scholar
  121. Wiltshire, R. J. E., J. B. Reid & B. M. Potts. 1998. Genetic control of reproductive and vegetative phase change in the Eucalyptus risdonii-E. tenuiramis complex. Australian Journal of Botany 46: 45–63.CrossRefGoogle Scholar
  122. Winn, A. A. 1996. The contribution of programmed developmental change and phenotypic plasticity to within-individual variation in leaf traits in Dicerandra linearifolia. Journal of Evolutionary Biology 9: 737–752.CrossRefGoogle Scholar
  123. ———.1999. The functional significance and fitness consequences of the heterophylly. International Journal of Plant Sciences 160(6 Suppl.): S113–S121.PubMedCrossRefGoogle Scholar
  124. Xu, C.-Y., K. L. Griffin & W. S. F. Schuster. 2007. Leaf phenology and seasonal variation of photosynthesis of invasive Berberis thunbergii (Japanese barberry) and two co-occurring native understory shrubs in a northeastern United States deciduous forest. Oecologia 154: 11–21.PubMedCrossRefGoogle Scholar
  125. Zgurski, J. M., R. Sharma, D. A. Bolokosi & E. A. Schultz. 2005. Asymmetric auxin response precedes asymmetric growth and differentiation of asymmetric leaf 1 and asymmetric leaf 2 Arabidopsis leaves. The Plant Cell 17: 77–91.PubMedCrossRefGoogle Scholar
  126. Zotz, G., K. Wilhelm & A. Becker. 2011. Heteroblasty—A review. Botanical Review 77: 109–151.CrossRefGoogle Scholar

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© The New York Botanical Garden 2012

Authors and Affiliations

  1. 1.The New York Botanical GardenBronxUSA
  2. 2.Instituto de Ciencias NaturalesUniversidad Nacional de ColombiaBogotáColombia
  3. 3.Instituto de BiologíaUniversidad de AntioquiaMedellínColombia

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