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

Botanical Review

Volumn 78, Issue 4, 2012, Pages 463-489

  Pabón Mora, Natalia ^a,c   González, Favio ^b  

^a NEW YORK BOTANICAL GARDEN   (United States)

^b UNIVERSIDAD NACIONAL DE COLOMBIA   (Colombia)

^c UNIVERSIDAD DE ANTIOQUIA   (Colombia)

Author keywords

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

Indexed keywords

BERBERIDACEAE; BERBERIS; MAHONIA;

EID: 84871276341     PISSN: 00068101     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12229-012-9107-2     Document Type: Article

References (126)

1. Ahrendt, L. W. A. 1961. Berberis and Mahonia, a taxonomic revision. Botanical Journal of the Linnean Society 57: 1-410.
2. Allsopp, A. 1965. Heteroblastic development in cormophytes. Pp 1172-1221. In: W. Ruhland (ed). Handbuch der Pflanzenphysiologie XV/1. Springer, Heidelberg.
3. Ashby, E. 1948. Studies in the morphogenesis of leaves. I. An essay on leaf shape. New Phytologist 47: 153-176.
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.
5. Beck, P. V. 1927. Comparative anatomy of certain hybrid shrubs and their parents. The University of Kansas Science Bulletin 16: 367-396.
6. Bell, A. D. 1991. Plant Form. An illustrated guide to flowering plant morphology. Oxford University Press.
7. ---. 2008. Plant Form. An illustrated guide to flowering plant morphology. Second edition. Timber Press.
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.
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.
10. Brodribb, T. & R. S. Hill. 1993. A physiological comparison of leaves and phyllodes in Acacia melanoxylon. Australian Journal of Botany 41: 293-305.
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.
12. --- & ---. 2009. Heteroblasty on Chatham Island: A comparison with New Zealand and New Caledonia. New Zealand Journal of Ecology 33: 156-163.
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.
14. ---, J. Simorowski & R. A. Martienssen. 2002. ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis. Development 129: 1957-1965.
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.
16. ---. 1966. Especies nuevas del género Berberis. Caldasia 9: 313-351.
17. ---. 1981. Especies nuevas del género Berberis. II. Caldasia 13: 203-222.
18. ---. 1983. Especies nuevas del género Berberis. III. Caldasia 13: 675-691.
19. ---. 1991. Especies nuevas del género Berberis. IV. Caldasia 16: 419-424.
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.
21. Champagne, C. & N. Sinha. 2004. Compound leaves: equal to the sum of their parts? Development 131: 4401-4412.
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.
23. Croizat, L. 1960. Principia Botanica, or beginnings of botany. N. V. Drukkerij Salland Deventer, Netherlands.
24. Cronk, Q. C. B. 2009. The molecular organography of plants. Oxford University Press, Oxford.
25. Cronquist, A. 1981. An integrated system of classification of flowering plants. Columbia University Press, New York.
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.
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.
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.
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.
30. Diggle, P. K. 1999. Heteroblasty and the evolution of flowering phenologies. International Journal of Plant Sciences 160(S6): S123-S134.
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.
32. Efroni, I., Y. Eshed & E. Lifschitz. 2010. Morphogenesis of simple and compound leaves: a critical review. The Plant Cell 22: 1019-1032.
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.
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.
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.
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.
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.
38. Fedde, F. 1902. Versuch einer Monographie der Gattung Mahonia. Botanische Jahrbücher 31: 30-133.
39. Foster, A. 1928. Salient features of the problem of bud scale morphology. Biological Reviews 3: 123-164.
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.
41. Gardner, S., A. Drinnan, E. Newbigin & P. Ladiges. 2008. Leaf ontogeny and morphology in Acacia Mill. (Mimosaceae). Muelleria 26: 43-50.
42. Gerrath, J. M. & C. R. Lacroix. 1997. Heteroblastic sequence and leaf development in Leea guineensis. International Journal of Plant Sciences 158: 747-756.
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.
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.
45. Goebel, K. 1891. Pp 1-50. Die Vegetation der venezuelanischen Paramos. Pflanzenbiologische Schilderungen, Vol. 2. N. G. Elwert'sche Verlagsbuchhandlung, Marburg.
46. ---. 1900-1905. Organography of plants. Two volumes. Oxford University Press, Oxford.
47. von Goethe, J. W. 1790. Versuch, die Metamorphose der Pflanzen zu erklären. Carl Wilhelm Ettinger, Gotha.
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.
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.
50. Hallé, F., R. A. A. Oldeman & P. B. Tomlinson. 1978. Tropical trees and forests. An architectural analysis. Springer, New York.
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.
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.
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.
54. Hay, A. & M. Tsiantis. 2010. KNOX genes: Versatile regulators of plant development and diversity. Development 137: 3153-3165.
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.
56. Holm, T. 1899. Podophyllum peltatum: A morphological study. Botanical Gazette 27: 419-433.
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.
58. Jones, C. S. 1993. Heterochrony and heteroblastic leaf development in two subspecies of Cucurbita argyrosperma (Cucurbitaceae). American Journal of Botany 80: 778-795.
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.
60. ---. 1999. An essay on juvenility, phase change, and heteroblasty in seed plants. International Journal of Plant Sciences 160: S105-S111.
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.
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.
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.
64. Kato, M. & H. Setoguchi. 1998. An rbcL-based phylogeny and heteroblastic leaf morphology of Matoniaceae. Systematic Botany 23: 391-400.
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.
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.
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.
68. Kunze, H. 1986. Studien zur Blattmetamorphose. Beiträge zur Biologie der Pflanzen 61: 49-77.
69. Landrum, L. R. 1999. Revision of Berberis (Berberidaceae) in Chile and adjacent Southern Argentina. Annals of the Missouri Botanical Garden 86: 793-834.
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.
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.
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.
73. Mabberley, D. J. 2008. The plant book. Cambridge University Press, Cambridge.
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.
75. Masters, M. T. 1869. Vegetable teratology. Ray Society, R. Hadwicke, London.
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.
77. McConnell, J. R. & M. K. Barton. 1998. Leaf polarity and meristem formation in Arabidopsis. Development 125: 2935-2942.
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.
79. McGlone, M. S. & C. J. Webb. 1981. Selective forces influencing the evolution of divaricating plants. New Zealand Journal of Ecology 4: 20-28.
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.
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.
82. Meacham, C. A. 1980. Phylogeny of the Berberidaceae with an evaluation of classifications. Systematic Botany 5: 149-172.
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.
84. Minorsky, P. V. 2003. The hot and the classic. Plant Physiology 133: 1671-1672.
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.
86. Nishimura, A., M. Tamaoki & M. Matsuoka. 1998. Expression pattern of KN-1 type tobacco homeobox genes. Plant Cell and Physiology 39: S60.
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.
88. Pabón-Mora, N. 2012. Functional evolution of the APETALA1/FRUITFULL gene lineage. PhD. Dissertation, The City University of New York, NY.
89. Poethig, R. S. 2003. Phase change and the regulation of developmental timing in plants. Science 301: 334-336.
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.
91. Pulido, A. & P. Laufs. 2010. Co-ordination of developmental processes by small RNAs during leaf development. Journal of Experimental Botany 61: 1277-1291.
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.
93. Rauh, W. 1950. Morphologie der Nutzpflanzen. Quelle & Meyer, Heidelberg.
94. Ray, T. S. 1987. Cyclic heterophylly in Syngonium (Araceae). American Journal of Botany 74: 16-26.
95. ---. 1990. Metamorphosis in the Araceae. American Journal of Botany 77: 1599-1609.
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.
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.
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.
99. Schmidt, E. 1928. Untersuchungen über Berberidaceen. Beihefte zum Botanischen Centralblatt 45: 329-396.
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.
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.
102. ---. 1908. Weitere Beitrage zur Kenntnis der Gattung Berberis (Euberberis). Bulletin del Herbier Boissier, ser. 2, 8: 192-204, 258-266.
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.
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.
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.
106. Sugiyama, M. & N. Hara. 1988. Comparative study on early ontogeny of coumpound leaves in Lardizabalaceae. American Journal of Botany 75: 1598-1605.
107. Takhtajan, A. L. 1997. Diversity and classification of flowering plants. Columbia University Press, New York.
108. Taylor, T. N., E. L. Taylor & M. Krings. 2009. Paleobotany, the biology and evolution of fossil plants. Academic Press, New York.
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.
110. Tischler, G. 1902. Die Berberidaceen und Podophyllaceen. Versuch einer morphologisch-biologischen Monographie. Botanische Jahrbücher 31: 596-727.
111. Troll, W. 1937-1943. Vergleichende Morphologie der höheren Pflanzen. Band 1 (1-3). Gebrüder Borntraeger, Berlin.
112. ---. 1954. Praktische Einführung in die Pflanzenmorphologie. Gustav Fischer, Jena.
113. ---. 1959. Allgemeine Botanik. Ferdinand Enke, Stuttgart.
114. ---. 1969. Die Infloreszenzen. Typologie und Stellung im Aufbau des Vegetationskörpers. Vol. 2, part 1. Gustav Fischer, Stuttgart.
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.
116. Tsukaya, H. 2006. Mechanism of leaf-shape determination. Annual Review in Plant Biology 57: 477-496.
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.
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.
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.
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.
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.
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.
123. ---. 1999. The functional significance and fitness consequences of the heterophylly. International Journal of Plant Sciences 160(6 Suppl.): S113-S121.
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.
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.
126. Zotz, G., K. Wilhelm & A. Becker. 2011. Heteroblasty-A review. Botanical Review 77: 109-151.