A Consideration of Leaf Shape Evolution in the Context of the Primary Function of the Leaf as a Photosynthetic Organ

  • Hirokazu TsukayaEmail author
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 44)


Leaf shape evolution in angiosperms is reviewed from an evolutionary developmental (evo/devo) viewpoint. Leaves have evolved as photosynthetic organs in land plants, while leaves in some angiosperms have lost their photosynthetic role, e.g., in some cacti, saprophytes/mycoheterotrophs, and parasitic plants. Although the roles are the same among leaves, their morphologies and developmental systems vary significantly, in part because of the need to maximize their photosynthetic efficiency for survival under particular environmental constraints. An example is the narrow leaves of the rheophyte plants located along river banks where frequent flooding occurs. Narrow leaves are less efficient at absorbing sunlight than are leaves with wider blades; however, they can withstand the destructive force of the water flow in full flood. In contrast, in some xerophytic epiphytes, the narrow leaves are effective at catching water from fog. Narrow leaf blade formation is also present in submerged amphibious plants, likely an adaptation to the underwater conditions. The leaf index, i.e., the ratio of leaf length to width, is regulated by several genetic factors, mutations of which may be driving the evolution of leaf shape. However, not all leaf shapes can be explained by environmental adaptation. For example, data on the relationship between leaf shape diversification and environmental habitats in terms of thermo regulation remain controversial.

In contrast, understanding of the genetic/cellular mechanisms underlying leaf blade shape is increasing. Leaf blade organogenesis is governed by adaxial/abaxial identities, in which the plate meristem, responsible for flat leaf blade development, is activated along the interface between the adaxial and abaxial domains. Thus, some morphological diversity in leaves can be partly attributed to changes in the adaxial/abaxial patterning. For example, unifacial leaves, which have only an abaxial identity in the leaf blade, develop into stick-like or terete forms. They can stand vertically and thus live in densely populated areas, unlike plants with bifacial leaves which extend, in most cases, horizontally. Interestingly, some unifacial leaves are flat or ensiform, as seen in the genera Iris and Juncus. In such cases, since the plate meristem is not available, they rely on thickening growth to create flat lamina from the terete primordia. Lotus-like or peltate leaves are also derived from partial alterations in the adaxial/abaxial patterning; however, the pitcher leaves of carnivorous plants, once considered an extreme deformation of the peltate leaves, result from local alterations in cell division. In compound leaves, the major genetic regulatory components are shared with those of serrated leaf margins. The proportion of serrated-leaf species in any particular habitat precisely correlates with the average air temperature, and thus serration mechanisms are likely linked to physiological adaptations to the external environment. The evolution of determinate and indeterminate leaves in angiosperms is also discussed. While leaves are usually determinate and discarded periodically, some species develop indeterminate leaves, with some looking like twigs or lateral branches and functioning as twigs. Some are simple leaves and have an intermediate nature between a leaf and a shoot. We also see the evolution of leaf-like, photosynthetic organs. Some plants develop cladodes, which are modified lateral shoots that resemble leaves. Molecular analysis revealed that recruitment of dorsiventral control mechanisms in leaves has resulted in lateral shoots changing into leaf-like cladodes in the genus Asparagus. All of the above can be interpreted from an evo/devo viewpoint, but the question of why such great diversification occurred in angiosperm leaves remains.








AS1, AS2



Arabidopsis thaliana GIF1


Arabidopsis thaliana GRF








C-terminal Binding Protein/ /BFA–ADP-Ribosylation Substrate










evolutionary developmental biology


gibberellic acid














Class I KNOX


Layer 1






micro RNA


















shoot apical meristem




trans-acting siRNA






extra-small sisters





This work was supported by the Bio-Next project in NINS, the Japan Society for the Promotion of Science (Grants-in-Aid for Creative Scientific Research and Scientific Research A), The Ministry of Education, Culture, Sports, Science and Technology, Japan (Scientific Research on Priority Areas and Scientific Research on Innovative Areas No. 25113002). In addition, the author thanks reviewers of the manuscript who helped him to polish it. Dr. Hiroyuki Koga of the University of Tokyo also kindly checked the final version of the manuscript.


  1. Adams WW III, Stewart J, Cohu CM, Muller O, Demmig-Adams B (2016) Habitat temperature and precipitation of Arabidopsis thaliana ecotypes determine the response of foliar vasculature, photosynthesis, and transpiration to growth temperature. Front Plant Sci 25:1026Google Scholar
  2. Alvarez JP, Furumizu C, Efroni I, Eshed Y, Bowman JL (2016) Active suppression of a leaf meristem orchestrates determinate leaf growth. eLIFE 5:e15023PubMedPubMedCentralCrossRefGoogle Scholar
  3. Andriankaja M, Dhondt S, De Bodt S, Vanhaeren H, Coppens F, De Milde L, Mühlenbock P, Skirycz A, Gonzalez N, Beemster GT, Inzé D (2012) Exit from proliferation during leaf development in Arabidopsis thaliana: a not-so-gradual process. Dev Cell 22:64–78PubMedCrossRefPubMedCentralGoogle Scholar
  4. Bailey LW, Sinnott EW (1916) The climate distribution of certain types of angiosperm leaves. Am J Bot 3:24–39CrossRefGoogle Scholar
  5. Barkoulas M, Hay A, Kougioumoutzi E, Tsiantis M (2007) A developmental framework for dissected leaf formation in the Arabidopsis relative Cardamine hirsuta. Nat Genet 40:1136–1141CrossRefGoogle Scholar
  6. Bharathan G, Goliber TE, Moore C, Kessler S, Pham T, Sinha NR (2002) Homologies in leaf form inferred from KNOXI gene expression during development. Science 296:1858–1860PubMedCrossRefPubMedCentralGoogle Scholar
  7. Bilsborough GD, Runions A, Barkoulas M, Jenkins HW, Hasson A, Glinha C, Laufs P, Hay A, Prusinkiewicz P, Tsiantis M (2011) Model for the regulation of Arabidopsis thaliana leaf margin development. Proc Natl Acad Sci U S A 108:3424–3429PubMedPubMedCentralCrossRefGoogle Scholar
  8. Blein T, Pulido A, Vialette-Guiraud A, Nikovics K, Morin H, Hay A, Johansen IE, Tsiantis M, Laufs P (2008) A conserved molecular framework for compound leaf development. Science 322:1835–181839PubMedCrossRefPubMedCentralGoogle Scholar
  9. Boyce CK (2007) Mechanisms of laminar growth in morphologically convergent leaves and flower petals. Int J Plant Sci 168:1151–1156CrossRefGoogle Scholar
  10. Brennan EB, Weinbaum SA, Rosenheim JA, Karban R (2001) Heteroblasty in Eucalyptus globulus (Myricales, Myricaceae) affects ovipositional and settling preferences of Ctenarytaina eucalypti and C. spatulata (Homoptera: Psyllidae). Environ Entomol 30:1144–1149CrossRefGoogle Scholar
  11. Chitwood DH, Headland LR, Ranjan A, Martinez CC, Braybrook SA, Koenig DP, Kuhlemeier C, Smith RS, Sinha N (2012) Leaf asymmetry as a developmental constraint imposed by auxin-dependent phyllotactic patterning. Plant Cell 24:2318–2327PubMedPubMedCentralCrossRefGoogle Scholar
  12. Cronk QCB, Bateman RM, Hawkins JA (eds) (2002) Developmental genetics and plant evolution. Taylor & Francis, London/New YorkGoogle Scholar
  13. de Reuille PB, Bohn-Courseau I, Ljung K, Morin H, Carrano N, Godin C, Traas J (2006) Computer simulations reveal properties of the cell-cell signaling network at the shoot apex in Arabidopsis. Proc Natl Acad Sci U S A 103:1627–1632PubMedPubMedCentralCrossRefGoogle Scholar
  14. Dengler NG (1999) Anisophylly and dorsiventral shoot symmetry. Int J Plant Sci 160:S67–S80PubMedCrossRefPubMedCentralGoogle Scholar
  15. Dengler NG, Dengler RE (1984) The mechanism of plication inception in palm leaves: Histogenic observations on the pinnate leaf of Chrysalidocarpus lutescens. Can J Bot 60:2976–2998CrossRefGoogle Scholar
  16. Deschamp PA, Cooke TJ (1984) Causal mechanisms of leaf dimorphism in the aquatic angiosperm Callitriche heterophylla. Am J Bot 71:319–329CrossRefGoogle Scholar
  17. Donnelly PM, Bonetta D, Tsukaya H, Dengler R, Dengler NG (1999) Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev Biol 215:407–419PubMedCrossRefPubMedCentralGoogle Scholar
  18. Efroni I, Eshed Y, Lifschitz E (2010) Morphogenesis of simple and compound leaves: a critical review. Plant Cell 22:1019–1032PubMedPubMedCentralCrossRefGoogle Scholar
  19. Feild T, Sage T, Czerniak C (2005) Hydathodal leaf teeth of Chloranthus japonicas (Chlorantheceae) prevent guttation-induced flooding of mesophyll. Plant Cell Environ 28:1179–1190CrossRefGoogle Scholar
  20. Fisher JB, Rutishauser R (1990) Leaves and epiphyllous shoots in Chisocheton (Meliaceae), a continuum of woody leaf and stem axes. Can J Bot 68:2316–2328CrossRefGoogle Scholar
  21. Fonseca CA, Overton JM, Collins B, Westoby M (2000) Shifts in trait-combinations along rainfall and phosphorus gradients. J Ecol 158:509–525Google Scholar
  22. Fujikura U, Horiguchi G, Tsukaya H (2007) Dissection of enhanced cell expansion processes in leaves triggered by defect in cell proliferation, with reference to roles of endoreduplication. Plant Cell Physiol 48:278–286PubMedCrossRefPubMedCentralGoogle Scholar
  23. Fujikura U, Horiguchi G, Ponce MR, Micol JL, Tsukaya H (2009) Coordination of cell proliferation and cell expansion mediated by ribosome-related processes in the leaves of Arabidopsis thaliana. Plant J 59:499–508PubMedCrossRefPubMedCentralGoogle Scholar
  24. Fukuda T, Yokoyama J, Tsukaya H (2003) The evolutionary origin of indeterminate leaves in Meliaceae: phylogenetic relationships among species in the genera Chisocheton and Guarea, as inferred from sequences of chloroplast DNA. Int J Plant Sci 164:13–24CrossRefGoogle Scholar
  25. Fukushima K, Fujita H, Yamaguchi T, Masayoshi K, Tsukaya H, Hasebe M (2015) Oriented cell division shapes carnivorous pitcher leaves of Sarracenia purpurea. Nat Commun 6:6450. CrossRefPubMedPubMedCentralGoogle Scholar
  26. Givnish TJ (1987) Comparative studies of leaf form: assessing the relative roles of selective pressures and phylogenetic constrains. New Phytol 106:131–160CrossRefGoogle Scholar
  27. Givnish TJ, Kriebel R (2017) Causes of ecological gradients in leaf margin entirety: evaluating the roles of biomechanics, hydraulics, vein geometry, and bud packing. Am J Bot 104:354–366PubMedCrossRefPubMedCentralGoogle Scholar
  28. Gleissberg S, Groot EP, Schmalz M, Eichert M, Kölsch A, Hutter S (2015) Developmental events leading to peltate leaf structure in Tropaeolum majus (Tropaeolaceae) are associated with expression domain changes of a YABBY gene. Dev Genes Evol 215:313–319CrossRefGoogle Scholar
  29. Guo P, Yoshimura A, Ishikawa N, Yamaguchi T, Guo Y, Tsukaya H (2015) Comparative analysis of the RTFL peptide family on the control of plant organogenesis. J Plant Res 128:497–510PubMedPubMedCentralCrossRefGoogle Scholar
  30. Gupta MD, Nath U (2015) Divergence in patterns of leaf growth polarity is associated with the expression divergence of miR396. Plant Cell 27:2785–2799PubMedPubMedCentralCrossRefGoogle Scholar
  31. Ha CM, Kim GT, Kim BC, Jun JH, Soh MS, Ueno Y, Machida Y, Tsukaya H, Nam H-G (2003) The BLADE-ON PETIOLE gene controls leaf pattern formation through regulation of meristematic activity. Development 130:161–172PubMedCrossRefPubMedCentralGoogle Scholar
  32. Harrison J, Möller M, Langdale J, Cronk Q, Hudson A (2005) The role of KNOX genes in the evolution of morphological novelty in Streptocarpus. Plant Cell 17:430–443PubMedPubMedCentralCrossRefGoogle Scholar
  33. Hay A, Tsiantis M (2010) KNOX genes: versatile regulators of plant development and diversity. Development 137:3153–3165PubMedCrossRefPubMedCentralGoogle Scholar
  34. Hay A, Kaur H, Phillips A, Hedden S, Hake S, Tsiantis M (2002) The gibberellin pathway mediates KNOTTED1-type homeobox function in plants with different body plans. Curr Biol 12:1557–1565PubMedCrossRefPubMedCentralGoogle Scholar
  35. Hirayama Y, Yamada T, Oya Y, Ito M, Kato M, Imaichi R (2007) Expression patterns of class I KNOX and YABBY genes in Ruscus aculeatus (Asparagaceae) with implications for phylloclade homology. Dev Genes Evol 217:363–372PubMedCrossRefPubMedCentralGoogle Scholar
  36. Hofer J, Turner L, Hellens R, Ambrose M, Matthews P, Michael A, Ellis N (1997) UNIFOLIATA regulates leaf and flower morphogenesis in pea. Curr Biol 7:581–587PubMedCrossRefPubMedCentralGoogle Scholar
  37. Horiguchi G, Kim GT, Tsukaya H (2005) The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf primordia of Arabidopsis thaliana. Plant J 43:68–78CrossRefGoogle Scholar
  38. Horiguchi G, Nakayama H, Ishikawa N, Kubo M, Demura T, Fukuda H, Tsukaya H (2011) ANGUSTIFOLIA3 plays roles in adaxial/abaxial patterning and growth in leaf morphogenesis. Plant Cell Physiol 52:112–124PubMedCrossRefGoogle Scholar
  39. Ichihashi Y, Kawade K, Usami T, Horiguchi G, Takahashi T, Tsukaya H (2011) Key proliferative activity in the junction between the leaf blade and the leaf petiole of Arabidopsis thaliana. Plant Physiol 157:1151–1162PubMedPubMedCentralCrossRefGoogle Scholar
  40. Ichihashi Y, Aquilar-Martinez JA, Farhi M, Chitwood DH, Kumar R, Milon LV, Peng J, Maloof JN, Sinha N (2014) Evolutionary developmental transcriptomics reveals a gene network module regulating interspecific diversity in plant leaf shape. Proc Natl Acad Sci U S A 111:E2616–E2621PubMedPubMedCentralCrossRefGoogle Scholar
  41. Ikeuchi M, Igarashi H, Okada K, Tsukaya H (2014) Acropetal leaflet initiation of Eschscholzia californica is achieved by constant spacing of leaflets and differential growth of leaf. Planta 240:125–135PubMedCrossRefPubMedCentralGoogle Scholar
  42. Imaichi R, Kato M (1992) Comparative leaf development of Osmunda lancea and Osmunda japonica (Osmundaceae) – heterochronic origin of rheophytic stenophylly. Bot Mag Tokyo 105:199–213CrossRefGoogle Scholar
  43. Ishikawa N, Takahashi H, Nakazono M, Tsukaya H (2017) Molecular bases for phyllomorph development in a one-leaf plant, Monophyllaea glabra. Am J Bot 104:233–240PubMedCrossRefGoogle Scholar
  44. Jasinski S, Piazza P, Craft J, Hay A, Woolley L, Rieu I, Phillips A, Hedden P, Tsiantis M (2005) KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr Biol 15:1560–1565PubMedCrossRefPubMedCentralGoogle Scholar
  45. Jönsson H, Heisler MG, Shapiro BE, Meyerowitz EM, Mijolsness E (2006) An auxin-driven polarized transport model for phyllotaxis. Proc Natl Acad Sci U S A 103:1633–1638PubMedPubMedCentralCrossRefGoogle Scholar
  46. Kane M, Albert LS (1987) Abscisic-acid induces aerial leaf morphology and vasculature in submerged Hippuris vulgaris L. Aquat Bot 28:81–88CrossRefGoogle Scholar
  47. Kato M, Imaichi R (1992a) Leaf anatomy of tropical fern rheophytes, with its evolutionary and ecological implications. Can J Bot 70:165–174CrossRefGoogle Scholar
  48. Kato M, Imaichi R (1992b) A broad-leaved variant of the fern rheophyte, Tectaria lobbii. Int J Plant Sci 153:212–216CrossRefGoogle Scholar
  49. Kawamura E, Horiguchi G, Tsukaya H (2010) Mechanisms of leaf tooth formation in Arabidopsis. Plant J 62:429–441PubMedCrossRefPubMedCentralGoogle Scholar
  50. Kazama T, Ichihashi Y, Murata S, Tsukaya H (2010) The mechanism of cell cycle arrest front progression explained by a KLUH/CYP78A5-dependent mobile growth factor in developing leaves of Arabidopsis thaliana. Plant Cell Physiol 51:1046–1054PubMedCrossRefPubMedCentralGoogle Scholar
  51. Kim JH, Kende H (2004) A transcriptional coactivator, AtGIF1, is involved in regulating leaf growth and morphology in Arabidopsis. Proc Natl Acad Sci U S A 101:13374–13379PubMedPubMedCentralCrossRefGoogle Scholar
  52. Kim JH, Tsukaya H (2015) Regulation of plant growth and development by the GROWTH-REGULATING FACTOR and GRF-INTERACTING FACTOR duo. J Exp Bot 66:6093–6107. CrossRefPubMedPubMedCentralGoogle Scholar
  53. Kim G-T, Tsukaya H, Uchimiya H (1998) The ROTUNDIFOLIA3 gene of Arabidopsis thaliana encodes a new member of the cytochrome P450 family that is required for the regulated polar elongation of leaf cells. Genes Dev 12:2381–2391PubMedPubMedCentralCrossRefGoogle Scholar
  54. Kim M, McCormick S, Timmermans M, Sinha N (2003) The expression domain of PHANTASTICA determines leaflet placement in compound leaves. Nature 424:438–443PubMedCrossRefPubMedCentralGoogle Scholar
  55. Kim G-T, Yano S, Kozuka T, Tsukaya H (2005) Photomorphogenesis of leaves: shade-avoidance syndrome and differentiation of sun/shade leaves. Photochem Photobiol Sci 4:770–774PubMedCrossRefPubMedCentralGoogle Scholar
  56. Kobayashi K, Baba S, Obayashi T, Sato M, Toyooka K, Karänen M, Aro EM, Fukaki H, Ohta H, Sugimoto K, Masuda T (2012) Regulation of root greening by light and auxin/cytokinin signaling in Arabidopsis. Plant Cell 24:1081–1095PubMedPubMedCentralCrossRefGoogle Scholar
  57. Koenig D, Bayer E, Kang J, Kuhlemeier C, Sinha N (2009) Auxin patterns Solanum lycopersicum leaf morphogenesis. Development 136:2997–3006PubMedCrossRefPubMedCentralGoogle Scholar
  58. Kozuka T, Kong SG, Nagatani A (2011) Tissue-autonomous promotion of palisade cell development by phototropin2 in Arabidopsis. Plant Cell 23:3684–3695PubMedPubMedCentralCrossRefGoogle Scholar
  59. Kuwabara A, Ikegami K, Koshiba T, Nagata T (2003) Effects of ethylene and abscisic acid upon heterophylly in Ludwigia arcuata (Onagraceae). Planta 217:880–887PubMedCrossRefPubMedCentralGoogle Scholar
  60. Lee YK, Kim G-T, Kim I-J, Park J, Kwak S-S, Choi G, Chung W-I (2006) LONGIFOLIA1 and LONGIFOLIA2, two homologous genes, regulate longitudinal cell elongation in Arabidopsis. Development 133:4305–4314PubMedCrossRefGoogle Scholar
  61. Leigh A, Close JD, Ball MC, Siebke K, Nicotra AB (2006) Leaf cooling curves: measuring leaf temperature in sunlight. Funct Plant Biol 33:515–519CrossRefGoogle Scholar
  62. Li Y, Zheng L, Corke F, Smith C, Bevan MW (2008) Control of final seed and organ size by the DA1 gene family in Arabidopsis thaliana. Genes Dev 2:1331–1336CrossRefGoogle Scholar
  63. Mano E, Horiguchi G, Tsukaya H (2006) Gravitropism in leaves of Arabidopsis thaliana (L.) Heynh. Plant Cell Physiol 47:217–223PubMedCrossRefPubMedCentralGoogle Scholar
  64. Martorell C, Ezcurra E (2007) The narrow-leaf syndrome: a functional and evolutionary approach to the form of fog-harvesting rosette plants. Oecologia 151:561–573PubMedCrossRefPubMedCentralGoogle Scholar
  65. Minamisawa N, Sato M, Cho K-H, Ueno H, Takeuchi K, Kajiwara M, Yamato KT, Ohyama K, Toyooka K, Kim G-T, Horiguchi G, Takano H, Ueda T, Tsukaya H (2011) AUNGUSTIFOLIA, a plant homolog of CtBP/BARS, functions outside the nucleus. Plant J 68:788–799PubMedCrossRefPubMedCentralGoogle Scholar
  66. Nakata M, Matsumoto N, Tsugeki R, Rikirsch E, Laux T, Okada K (2012) Roles of the middle domain-specific WUSCHEL-RELATED HOMEOBOX genes in early development of leaves in Arabidopsis. Plant Cell 24:519–535PubMedPubMedCentralCrossRefGoogle Scholar
  67. Nakayama H, Yamaguchi T, Tsukaya H (2010) Expression patterns of AaDL, a CRABS CLAW ortholog in Asparagus asparagoides (Asparagaceae), demonstrate a stepwise evolution of CRC/DL subfamily of YABBY genes. Am J Bot 97:591–600PubMedCrossRefPubMedCentralGoogle Scholar
  68. Nakayama H, Yamaguchi T, Tsukaya H (2013) Modification and co-option of leaf developmental programs for the acquisition of flat structures in monocots: unifacial leaves in Juncus and cladodes in Asparagus. Front Plant Sci 4:248. CrossRefPubMedPubMedCentralGoogle Scholar
  69. Nakayama H, Nakayama N, Seiki S, Kojima M, Sakakibara H, Sinha N, Kimura S (2014) Regulation of the KNOX-GA gene module induces heterophyllic alteration in North American lake cress. Plant Cell 26:4733–4748PubMedPubMedCentralCrossRefGoogle Scholar
  70. Nardmann J, Werr W (2013) Symplesiomorphies in the WUSCHEL clade suggest that the last common ancestor of seed plants contained at least four independent stem cell niches. New Phytol 199:1081–1092PubMedCrossRefPubMedCentralGoogle Scholar
  71. Narita NN, Moore S, Horiguchi G, Kubo M, Demura T, Fukuda H, Goodrish J, Tsukaya H (2004) Overexpression of a novel small peptide ROTUNDIFOLIA4 decreases cell proliferation and alters leaf shape in Arabidopsis thaliana. Plant J 38:699–713PubMedCrossRefPubMedCentralGoogle Scholar
  72. Nelissen H, Rymen B, Jilumaru Y, Demuynck K, Van Lijsebettens M, Kamiya Y, Inzé D, Beemster GTS (2012) A local maximum in gibberellin levels regulates maize leaf growth by spatial control of cell division. Curr Biol 22:1183–1187PubMedCrossRefPubMedCentralGoogle Scholar
  73. Nelissen H, Eeckhout D, Demuynck K, Persiau G, Walton A, van bel M, Vervoot M, Candaele J, De Block J, Aesaert S, Van Lijsebettens M, Goormachtig S, Vandepoele K, Van Leene J, Muszynski M, Gevaert K, Inzé D, De Jaeger G (2015) Dynamic changes in ANGUSTIFOLIA3 complex composition reveal a growth regulatory mechanism in the maize leaf. Plant Cell 27:1605–1619PubMedPubMedCentralCrossRefGoogle Scholar
  74. Nicotra AB, Cosgrove MJ, Cowling A, Schilichting CD, Jones CS (2008) Leaf shape linked to photosynthetic rates and temperature optima in south African Pelargonium species. Oecologia 154:625–635PubMedCrossRefPubMedCentralGoogle Scholar
  75. Nicotra AB, Leigh A, Boyce CK, Jones CS, Niklas KJ, Royer DL, Tsukaya H (2011) The evolution and functional significance of leaf shape in the angiosperms. Funct Plant Biol 38:535–552CrossRefGoogle Scholar
  76. Nowak JS, Bolduc N, Dengler NG, Posluszny U (2011) Compound leaf development in the palm Chamaedorea elegans is KNOX-independent. Am J Bot 98:1575–1582PubMedCrossRefPubMedCentralGoogle Scholar
  77. Ohnishi T, Szatmari A-M, Watanabe B, Fujita S, Bancos S, Koncz C, Lafos M, Shibata K, Yokota T, Sakata K, Yokota T, Sakata K, Szakeres M, Mizutani M (2006) C-23 hydroxylation by Arabidopsis CYP90C1 and CYP90D1 reveals a novel shortcut in Brassinosteroid biosynthesis. Plant Cell 18:3275–3288PubMedPubMedCentralCrossRefGoogle Scholar
  78. Okajima Y, Taneda H, Noguchi K, Terashima I (2012) Optimum leaf size predicted by a novel leaf energy balance model incorporating dependencies of photosynthesis on light and temperature. Ecol Res 27:333–346CrossRefGoogle Scholar
  79. Omidbakhshfard MA, Proost S, Fujikura U, Mueller-Roeder B (2015) Growth-Regulating Factors (GRFs): a small transcription factor family with important functions in plant biology. Mol Plant 8:998–1010PubMedCrossRefPubMedCentralGoogle Scholar
  80. Poethig RS (2013) Vegetative phase change and shoot maturation in plants. Curr Top Dev Biol 105:125–152PubMedPubMedCentralCrossRefGoogle Scholar
  81. Royer DL, Wilf P, Janesko DA, Kowalski EA, Dilcher DL (2005) Correlations of climate and plant ecology to leaf size and shape: potential proxies for the fossil record. Am J Bot 92:1141–1151PubMedCrossRefPubMedCentralGoogle Scholar
  82. Royer DL, Meyerson LA, Robertson KM, Adams JM (2009) Phenotypic plasticity of leaf shape along a temperature gradient in Acer rubrum. PLoS One 4:e7653PubMedPubMedCentralCrossRefGoogle Scholar
  83. Sakamoto T, Kamiya N, Ueguchi-Tanaka M, Iwahori S, Matsuoka M (2001) KNOX homeodomain protein directly suppresses the expression of a gibberellin biosynthetic gene in the tobacco shoot apical meristem. Genes Dev 15:581–590PubMedPubMedCentralCrossRefGoogle Scholar
  84. Schmerler SB, Clement WL, Beauliue JM, Chatelet DS, Sack L, Donoghue MJ, Edwards EJ (2012) Evolution of leaf form correlates with tropical-temperate transitions in Viburnum (Adoxaceae). Proc Roy Soc B 279:3905–3913CrossRefGoogle Scholar
  85. Smith RS, Guyomarc’h S, Mandel T, Reinhardt D, Kuhlemeier C, Prusinkiewicz P (2006) A plausible model of phyllotaxis. Proc Natl Acad Sci U S A 103:1301–1306PubMedPubMedCentralCrossRefGoogle Scholar
  86. Steingraeber DA, Fisher JB (1986) Indeterminate growth of leaves in Guarea (Meliaceae): a twig analogue. Am J Bot 73:852–862CrossRefGoogle Scholar
  87. Sussex IM (1951) Experiments on the cause of dorsiventrality in leaves. Nature 167:651–652PubMedCrossRefPubMedCentralGoogle Scholar
  88. Takahashi H, Iwakawa H, Ishibashi N, Kojima S, Matsumura Y, Prananingrum P, Iwasaki M, Takahashi A, Ikezaki M, Luo LL, Kobayashi T, Machida Y, Machida C (2013) Meta-analyses of microarrays of Arabidopsis asymmetric leaves1 (as1), as2 and their modifying mutants reveal a critical role for the ETT pathway in stabilization of adaxial-abaxial patterning and cell division during leaf development. Plant Cell Physiol 54:418–431PubMedPubMedCentralCrossRefGoogle Scholar
  89. Tozer WC, Rice B, Westoby M (2015) Evolutionary convergence of leaf width and its correlates. Am J Bot 102:367–378PubMedCrossRefPubMedCentralGoogle Scholar
  90. Tsuge T, Tsukaya H, Uchimiya H (1996) Two independent and polarized processes of cell elongation regulate leaf blade expansion in Arabidopsis thaliana (L.). Heynh. Develop 122:1589–1600Google Scholar
  91. Tsukaya H (1997) Determination of the unequal fate of cotyledons of a one-leaf plant, Monophyllaea. Development 124:1275–1280PubMedPubMedCentralGoogle Scholar
  92. Tsukaya H (2000) The role of meristematic activities in the formation of leaf blades. J Plant Res 113:119–126CrossRefGoogle Scholar
  93. Tsukaya H (2002a) The leaf index: heteroblasty, natural variation, and the genetic control of polar processes of leaf expansion. Plant Cell Physiol 43:372–378PubMedCrossRefGoogle Scholar
  94. Tsukaya H (2002b) Leaf anatomy of a rheophyte, Dendranthema yoshinaganthum (Asteraceae), and of hybrids between D. yoshinaganthum and a closely related non-rheophyte species, D. indicum. J Plant Res 115:329–333PubMedCrossRefPubMedCentralGoogle Scholar
  95. Tsukaya H (2006) Mechanism of leaf shape determination. Annu Rev Plant Biol 57:477–496PubMedCrossRefPubMedCentralGoogle Scholar
  96. Tsukaya H (2013) Leaf development, 2nd edn. The Arabidopsis Book 11:e0163, American Society of Plant Biologists, Rockville. doi: PubMedPubMedCentralCrossRefGoogle Scholar
  97. Tsukaya H (2014) Comparative leaf development in angiosperms. Curr Opin Plant Biol 17:103–109PubMedCrossRefPubMedCentralGoogle Scholar
  98. Tsukaya H (2018) How have leaves of mycoheterotrophic plants evolved—from the view point of a developmental biologist. New Phytol 217:1401–1406 PubMedCrossRefPubMedCentralGoogle Scholar
  99. Tsukaya H, Uchimiya H (1997) Genetic analyses of developmental control of serrated margin of leaf blades in Arabidopsis: combination of a mutational analysis of leaf morphogenesis with characterization of a specific marker gene expressed in hydathodes and stipules. Mol Gen Genet 256:231–238PubMedCrossRefPubMedCentralGoogle Scholar
  100. Tsukaya H, Tsuge T, Uchimiya H (1994) The cotyledon: a superior system for studies of leaf development. Planta 195:309–312CrossRefGoogle Scholar
  101. Tsukaya H, Tsujino R, Ikeuchi M, Isshiki Y, Kono M, Takeuchi T, Araki T (2007) Morphological variation in leaf shape in Ainsliaea apiculata with special reference to the endemic characters of populations on Yakushima Island, Japan. J Plant Res 120:351–358PubMedCrossRefPubMedCentralGoogle Scholar
  102. Usami T, Horiguchi G, Yano S, Tsukaya H (2009) The more and smaller cells mutants of Arabidopsis thaliana identify novel roles for SQUAMOSA PROMOTER BINDING PROTEIN-LIKE genes in the control of heteroblasty. Development 136:955–964PubMedCrossRefPubMedCentralGoogle Scholar
  103. Usukura M, Imaichi R, Kato M (1994) Leaf morphology of a facultative rheophyte, Farfugium japonicum var. luchuense (Compositae). J Plant Res 107:263–267CrossRefGoogle Scholar
  104. van Steenis CGGJ (1981) Rheophytes of the world. Sijthoff & Noordhoff, Alphen aan den Rijn, The NetherlandsGoogle Scholar
  105. Vlad D, Kierzkowski D, Rast M, Vuolo F, Ioio RD, Galinha C, Gan X, Haijeidari M, Hay A, Smith RS, Huijser P, Bailey CD, Tsiantis M (2014) Leaf shape evolution through duplication, regulatory diversification, and loss of a homeobox gene. Science 343:780–783PubMedCrossRefPubMedCentralGoogle Scholar
  106. Waites R, Hudson A (1995) Phantastica: a gene required for dorsoventrality of leaves in Antirrhinum majus. Development 121:2143–2154Google Scholar
  107. Wang H, Jones B, Li Z, Frasse P, Delalande C, Regad F, Chaabouni S, Latché A, Pech J-C, Bouzayen M (2005) The tomato Aux/IAA transcription factor IAA9 is involved in fruit development and leaf morphogenesis. Plant Cell 17:2676–2692PubMedPubMedCentralCrossRefGoogle Scholar
  108. Wang J-W, Park MY, Wang L-J, Koo YJ, Chen X-Y, Weigel D, Poethig RS (2011) MiRNA control of vegetative phase changes in trees. PLoS Genet 7:e1002012PubMedPubMedCentralCrossRefGoogle Scholar
  109. Wen J, Lease KA, Walker JC (2004) DVL, a novel class of small polypeptides: overexpression alters Arabidopsis development. Plant J 37:668–677PubMedCrossRefPubMedCentralGoogle Scholar
  110. Xu L, Xu Y, Dong A, Sun Y, Pi L, Xu Y, Huang H (2003) Novel as1 and as2 defects in leaf adaxial-abaxial polarity reveal the requirement for ASYMMETRIC LEAVES1 and 2 and ERECTA functions in specifying leaf adaxial identity. Development 130:4097–4107PubMedCrossRefPubMedCentralGoogle Scholar
  111. Yamada T, Okuda T, Abdullah M, Awang M, Furukawa A (2000) The leaf development process and its significance for reducing self-shading of a traopical pioneer tree species. Oecologia 125:476–482PubMedCrossRefPubMedCentralGoogle Scholar
  112. Yamaguchi T, Ikeuchi M, Tsukaya H (2013) Chapter 11: ROTUNDIFOLIA4. In: Matsuzaki Y (ed) Handbook of biologically active peptides, 2nd edn. Elsevier, San Diego, pp 53–57CrossRefGoogle Scholar
  113. Yamaguchi T, Nagasawa N, Kawasaki S, Matsuoka M, Nagato Y, Hirano H-Y (2004) The YABBY gene DROOPING LEAF regulates carpel specification and midrib development in Oryza sativa. Plant Cell 16:500–509PubMedPubMedCentralCrossRefGoogle Scholar
  114. Yamaguchi T, Yano S, Tsukaya H (2010) Genetic framework for flattened leaf blade formation in unifacial leaves of Juncus prismatocarpus. Plant Cell 22:2141–2155PubMedPubMedCentralCrossRefGoogle Scholar
  115. Yano S, Terashima I (2004) Developmental process of sun and shade leaves in Chenopodium album L. Plant Cell Physiol 27:781–793Google Scholar
  116. Yorifuji E, Ishikawa N, Okada H, Tsukaya H (2015) Arundina graminifolia var. revoluta (Arethuseae, Orchidaceae) has fern-type rheophyte characteristics in the leaves. J Plant Res 128:239–247PubMedCrossRefPubMedCentralGoogle Scholar
  117. Young JP, Dengler NG, Horton RF (1987) Heterophylly in Ranunculus flabellis: the effect of abscisic acid on leaf anatomy. Ann Bot 60:117–125CrossRefGoogle Scholar
  118. Zurakowski K, Gifford EM (1988) Quantitative studies of pinnule development in the ferns Adiantum raddianum and Cheilanthes viridis. Am J Bot 75:1559–1570CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biological Sciences, Graduate School of ScienceThe University of TokyoTokyoJapan
  2. 2.Bio-Next Project, Okazaki Institute for Integrative BioscienceNational Institutes of Natural SciencesOkazakiJapan

Personalised recommendations