1932

Abstract

Plant leaves display considerable variation in shape. Here, we introduce key aspects of leaf development, focusing on the morphogenetic basis of leaf shape diversity. We discuss the importance of the genetic control of the amount, duration, and direction of cellular growth for the emergence of leaf form. We highlight how the combined use of live imaging and computational frameworks can help conceptualize how regulated cellular growth is translated into different leaf shapes. In particular, we focus on the morphogenetic differences between simple and complex leaves and how carnivorous plants form three-dimensional insect traps. We discuss how evolution has shaped leaf diversity in the case of complex leaves, by tinkering with organ-wide growth and local growth repression, and in carnivorous plants, by modifying the relative growth of the lower and upper sides of the leaf primordium to create insect-digesting traps.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-080720-101613
2021-06-17
2024-05-06
Loading full text...

Full text loading...

/deliver/fulltext/arplant/72/1/annurev-arplant-080720-101613.html?itemId=/content/journals/10.1146/annurev-arplant-080720-101613&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Abley K, De Reuille PB, Strutt D, Bangham A, Prusinkiewicz P et al. 2013. An intracellular partitioning-based framework for tissue cell polarity in plants and animals. Development 140:2061–74
    [Google Scholar]
  2. 2. 
    Aida M, Ishida T, Tasaka M. 1999. Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes. Development 126:1563–70
    [Google Scholar]
  3. 3. 
    Ali O, Mirabet V, Godin C, Traas J. 2014. Physical models of plant development. Annu. Rev. Cell Dev. Biol. 30:59–78
    [Google Scholar]
  4. 4. 
    Alvarez JP, Furumizu C, Efroni I, Eshed Y, Bowman JL. 2016. Active suppression of a leaf meristem orchestrates determinate leaf growth. eLife 5:e15023
    [Google Scholar]
  5. 5. 
    Andres RJ, Coneva V, Frank MH, Tuttle JR, Samayoa LF et al. 2017. Modifications to a LATE MERISTEM IDENTITY1 gene are responsible for the major leaf shapes of Upland cotton (Gossypium hirsutum L.). PNAS 114:E57–66
    [Google Scholar]
  6. 6. 
    Andriankaja M, Dhondt S, De Bodt S, Vanhaeren H, Coppens F et al. 2012. Exit from proliferation during leaf development in Arabidopsis thaliana: a not-so-gradual process. Dev. Cell 22:64–78
    [Google Scholar]
  7. 7. 
    Bar M, Israeli A, Levy M, Ben Gera H, Jiménez-Gómez JM et al. 2016. CLAUSA is a MYB transcription factor that promotes leaf differentiation by attenuating cytokinin signaling. Plant Cell 28:1602–15
    [Google Scholar]
  8. 8. 
    Bar M, Ori N. 2014. Leaf development and morphogenesis. Development 141:4219–30
    [Google Scholar]
  9. 9. 
    Bar M, Ori N. 2015. Compound leaf development in model plant species. Curr. Opin. Plant Biol. 23:61–69
    [Google Scholar]
  10. 10. 
    Barbier de Reuille P, Routier-Kierzkowska A-L, Kierzkowski D, Bassel GW, Schüpbach T et al. 2015. MorphoGraphX: a platform for quantifying morphogenesis in 4D. eLife 4:e05864
    [Google Scholar]
  11. 11. 
    Barkoulas M, Hay A, Kougioumoutzi E, Tsiantis M. 2008. A developmental framework for dissected leaf formation in the Arabidopsis relative Cardamine hirsuta. Nat. Genet. 40:1136–41
    [Google Scholar]
  12. 12. 
    Bassel GW, Smith RS. 2016. Quantifying morphogenesis in plants in 4D. Curr. Opin. Plant Biol. 29:87–94
    [Google Scholar]
  13. 13. 
    Bassel GW, Stamm P, Mosca G, Barbier de Reuille P, Gibbs DJ et al. 2014. Mechanical constraints imposed by 3D cellular geometry and arrangement modulate growth patterns in the Arabidopsis embryo. PNAS 111:8685–90
    [Google Scholar]
  14. 14. 
    Berna G, Robles P, Micol JL. 1999. A mutational analysis of leaf morphogenesis in Arabidopsis thaliana. Genetics 152:729–42
    [Google Scholar]
  15. 15. 
    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 296:1858–60
    [Google Scholar]
  16. 16. 
    Bhatia N, Bozorg B, Larsson A, Ohno C, Jonsson H, Heisler MG. 2016. Auxin acts through MONOPTEROS to regulate plant cell polarity and pattern phyllotaxis. Curr. Biol. 26:3202–8
    [Google Scholar]
  17. 17. 
    Bhatia N, Heisler MG. 2018. Self-organizing periodicity in development: organ positioning in plants. Development 145:dev149336
    [Google Scholar]
  18. 18. 
    Bilsborough GD, Runions A, Barkoulas M, Jenkins HW, Hasson A et al. 2011. Model for the regulation of Arabidopsis thaliana leaf margin development. PNAS 108:3424–29
    [Google Scholar]
  19. 19. 
    Blein T, Pulido A, Vialette-Guiraud A, Nikovics K, Morin H et al. 2008. A conserved molecular framework for compound leaf development. Science 322:1835–39
    [Google Scholar]
  20. 20. 
    Bolduc N, Yilmaz A, Mejia-Guerra MK, Morohashi K, O'Connor D et al. 2012. Unraveling the KNOTTED1 regulatory network in maize meristems. Genes Dev 26:1685–90
    [Google Scholar]
  21. 21. 
    Bozorg B, Krupinski P, Jönsson H. 2014. Stress and strain provide positional and directional cues in development. PLOS Comput. Biol. 10:e1003410
    [Google Scholar]
  22. 22. 
    Bresso EG, Chorostecki U, Rodriguez RE, Palatnik JF, Schommer C. 2018. Spatial control of gene expression by miR319-regulated TCP transcription factors in leaf development. Plant Physiol 176:1694–708
    [Google Scholar]
  23. 23. 
    Breuil-Broyer S, Morel P, De Almeida-Engler J, Coustham V, Negrutiu I, Trehin C. 2004. High-resolution boundary analysis during Arabidopsis thaliana flower development. Plant J 38:182–92
    [Google Scholar]
  24. 24. 
    Briggs WH, McMullen MD, Gaut BS, Doebley J. 2007. Linkage mapping of domestication loci in a large maize-teosinte backcross resource. Genetics 177:1915–28
    [Google Scholar]
  25. 25. 
    Byrne ME, Barley R, Curtis M, Arroyo JM, Dunham M et al. 2000. Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 408:967–71
    [Google Scholar]
  26. 26. 
    Caggiano MP, Yu X, Bhatia N, Larsson A, Ram H et al. 2017. Cell type boundaries organize plant development. eLife 6:e27421Demonstrated that a prepattern of adaxial–abaxial gene expression in the shoot apical meristem establishes leaf positioning and adaxial–abaxial polarity and influences laminar growth.
    [Google Scholar]
  27. 27. 
    Carroll SB. 2008. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134:25–36
    [Google Scholar]
  28. 28. 
    Chan J, Coen E. 2020. Interaction between autonomous and microtubule guidance systems controls cellulose synthase trajectories. Curr. Biol. 30:941–47.e2
    [Google Scholar]
  29. 29. 
    Chickarmane V, Roeder AH, Tarr PT, Cunha A, Tobin C, Meyerowitz EM. 2010. Computational morphodynamics: a modeling framework to understand plant growth. Annu. Rev. Plant Biol. 61:65–87
    [Google Scholar]
  30. 30. 
    Chitwood DH, Nogueira FT, Howell MD, Montgomery TA, Carrington JC, Timmermans MC. 2009. Pattern formation via small RNA mobility. Genes Dev 23:549–54
    [Google Scholar]
  31. 31. 
    Coen E, Kennaway R, Whitewoods C. 2017. On genes and form. Development 144:4203–13
    [Google Scholar]
  32. 32. 
    Coen E, Rebocho AB. 2016. Resolving conflicts: modeling genetic control of plant morphogenesis. Dev. Cell 38:579–83
    [Google Scholar]
  33. 33. 
    Conklin PA, Johnston R, Conlon BR, Shimizu R, Scanlon MJ. 2020. Plant homeodomain proteins provide a mechanism for how leaves grow wide. Development 147:dev193623
    [Google Scholar]
  34. 34. 
    Conklin PA, Strable J, Li S, Scanlon MJ. 2019. On the mechanisms of development in monocot and eudicot leaves. New Phytol 221:706–24
    [Google Scholar]
  35. 35. 
    Cope JS, Corney D, Clark JY, Remagnino P, Wilkin P. 2012. Plant species identification using digital morphometrics: a review. Expert Syst. Appl. 39:7562–73
    [Google Scholar]
  36. 36. 
    Cosgrove DJ. 2018. Diffuse growth of plant cell walls. Plant Physiol 176:16–27
    [Google Scholar]
  37. 37. 
    Cosgrove DJ. 2018. Nanoscale structure, mechanics and growth of epidermal cell walls. Curr. Opin. Plant Biol. 46:77–86
    [Google Scholar]
  38. 38. 
    Costa MMR, Yang S, Critchley J, Feng X, Wilson Y et al. 2012. The genetic basis for natural variation in heteroblasty in Antirrhinum. New Phytol 196:1251–9
    [Google Scholar]
  39. 39. 
    Craft J, Samalova M, Baroux C, Townley H, Martinez A et al. 2005. New pOp/LhG4 vectors for stringent glucocorticoid-dependent transgene expression in Arabidopsis. Plant J 41:899–918
    [Google Scholar]
  40. 40. 
    Dengler N, Kang J. 2001. Vascular patterning and leaf shape. Curr. Opin. Plant Biol. 4:50–56
    [Google Scholar]
  41. 41. 
    Doebley J. 2004. The genetics of maize evolution. Annu. Rev. Genet. 38:37–59
    [Google Scholar]
  42. 42. 
    Donnelly PM, Bonetta D, Tsukaya H, Dengler RE, Dengler NG. 1999. Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev. Biol. 215:407–19
    [Google Scholar]
  43. 43. 
    Efroni I, Blum E, Goldshmidt A, Eshed Y. 2008. A protracted and dynamic maturation schedule underlies Arabidopsis leaf development. Plant Cell 20:2293–306
    [Google Scholar]
  44. 44. 
    Efroni I, Eshed Y, Lifschitz E. 2010. Morphogenesis of simple and compound leaves: a critical review. Plant Cell 22:1019–32
    [Google Scholar]
  45. 45. 
    Ellis B, Daly DC, Hickey LJ, Mitchell JD, Johnson KR. 2009. Manual of Leaf Architecture Ithaca, NY: Cornell Univ. Press
  46. 46. 
    Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker NP et al. 2003. Radial patterning of Arabidopsis shoots by Class III HD-ZIP and KANADI genes. Curr. Biol. 13:1768–74
    [Google Scholar]
  47. 47. 
    Eshed Y, Baum SF, Perea JV, Bowman JL. 2001. Establishment of polarity in lateral organs of plants. Curr. Biol. 11:1251–60
    [Google Scholar]
  48. 48. 
    Etournay R, Merkel M, Popovic M, Brandl H, Dye NA et al. 2016. TissueMiner: A multiscale analysis toolkit to quantify how cellular processes create tissue dynamics. eLife 5:e14334
    [Google Scholar]
  49. 49. 
    Eviatar-Ribak T, Shalit-Kaneh A, Chappell-Maor L, Amsellem Z, Eshed Y, Lifschitz E. 2013. A cytokinin-activating enzyme promotes tuber formation in tomato. Curr. Biol. 23:1057–64
    [Google Scholar]
  50. 50. 
    Floyd SK, Bowman JL. 2010. Gene expression patterns in seed plant shoot meristems and leaves: homoplasy or homology?. J. Plant Res. 123:43–55
    [Google Scholar]
  51. 51. 
    Fox S, Southam P, Pantin F, Kennaway R, Robinson S et al. 2018. Spatiotemporal coordination of cell division and growth during organ morphogenesis. PLOS Biol 16:e2005952
    [Google Scholar]
  52. 52. 
    Fruleux A, Verger S, Boudaoud A. 2019. Feeling stressed or strained? A biophysical model for cell wall mechanosensing in plants. Front. Plant Sci. 10:757
    [Google Scholar]
  53. 53. 
    Fukushima K, Fujita H, Yamaguchi T, Kawaguchi M, Tsukaya H, Hasebe M. 2015. Oriented cell division shapes carnivorous pitcher leaves of Sarracenia purpurea. Nat. Commun. 6:6450
    [Google Scholar]
  54. 54. 
    Fukushima K, Hasebe M. 2014. Adaxial–abaxial polarity: the developmental basis of leaf shape diversity. Genesis 52:1–18
    [Google Scholar]
  55. 55. 
    Furutani M, Vernoux T, Traas J, Kato T, Tasaka M, Aida M 2004. PIN-FORMED1 and PINOID regulate boundary formation and cotyledon development in Arabidopsis embryogenesis. Development 131:5021–30
    [Google Scholar]
  56. 56. 
    Gourlay CW, Hofer JM, Ellis TH 2000. Pea compound leaf architecture is regulated by interactions among the genes UNIFOLIATA, COCHLEATA, AFILA, and TENDRIL-LESS. Plant Cell 12:1279–94
    [Google Scholar]
  57. 57. 
    Green JB, Sharpe J. 2015. Positional information and reaction-diffusion: Two big ideas in developmental biology combine. Development 142:1203–11
    [Google Scholar]
  58. 58. 
    Guerrieri R, Belmecheri S, Ollinger SV, Asbjornsen H, Jennings K et al. 2019. Disentangling the role of photosynthesis and stomatal conductance on rising forest water-use efficiency. PNAS 116:16909–14
    [Google Scholar]
  59. 59. 
    Guirao B, Rigaud SU, Bosveld F, Bailles A, Lopez-Gay J et al. 2015. Unified quantitative characterization of epithelial tissue development. eLife 4:e08519
    [Google Scholar]
  60. 60. 
    Hagemann W, Gleissberg S. 1996. Organogenetic capacity of leaves: the significance of marginal blastozones in angiosperms. Plant Syst. Evol. 199:121–52
    [Google Scholar]
  61. 61. 
    Hajheidari M, Wang Y, Bhatia N, Vuolo F, Franco-Zorrilla JM et al. 2019. Autoregulation of RCO by low-affinity binding modulates cytokinin action and shapes leaf diversity. Curr. Biol. 29:4183–92.e6
    [Google Scholar]
  62. 62. 
    Hamant O. 2013. Widespread mechanosensing controls the structure behind the architecture in plants. Curr. Opin. Plant Biol. 16:654–60
    [Google Scholar]
  63. 63. 
    Hamant O, Haswell ES. 2017. Life behind the wall: sensing mechanical cues in plants. BMC Biol 15:59
    [Google Scholar]
  64. 64. 
    Hareven D, Gutfinger T, Parnis A, Eshed Y, Lifschitz E. 1996. The making of a compound leaf: genetic manipulation of leaf architecture in tomato. Cell 84:735–44Demonstrated that KNOX1 genes are expressed in complex leaves of tomato, where they are sufficient to increase leaf complexity.
    [Google Scholar]
  65. 65. 
    Hay A, Barkoulas M, Tsiantis M. 2006. ASYMMETRIC LEAVES1 and auxin activities converge to repress BREVIPEDICELLUS expression and promote leaf development in Arabidopsis. Development 133:3955–61
    [Google Scholar]
  66. 66. 
    Hay A, Kaur H, Phillips A, Hedden P, Hake S, Tsiantis M. 2002. The gibberellin pathway mediates KNOTTED1-type homeobox function in plants with different body plans. Curr. Biol. 12:1557–65
    [Google Scholar]
  67. 67. 
    Hay A, Tsiantis M. 2006. The genetic basis for differences in leaf form between Arabidopsis thaliana and its wild relative Cardamine hirsuta. Nat. Genet. 38:942–47Demonstrated that KNOX1 expression is required for complex leaf development and that cis-regulatory divergence contributed to KNOX1 expression in complex versus simple leaves.
    [Google Scholar]
  68. 68. 
    Hay A, Tsiantis M. 2010. KNOX genes: versatile regulators of plant development and diversity. Development 137:3153–65
    [Google Scholar]
  69. 69. 
    Heisler MG, Byrne ME. 2019. Progress in understanding the role of auxin in lateral organ development in plants. Curr. Opin. Plant Biol. 53:73–79
    [Google Scholar]
  70. 70. 
    Heisler MG, Ohno C, Das P, Sieber P, Reddy GV et al. 2005. Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr. Biol. 15:1899–911
    [Google Scholar]
  71. 71. 
    Hervieux N, Dumond M, Sapala A, Routier-Kierzkowska A-L, Kierzkowski D et al. 2016. A mechanical feedback restricts sepal growth and shape in Arabidopsis. Curr. Biol. 26:1019–28
    [Google Scholar]
  72. 72. 
    Hofer J, Turner L, Hellens R, Ambrose M, Matthews P et al. 1997. UNIFOLIATA regulates leaf and flower morphogenesis in pea. Curr. Biol. 7:581–87
    [Google Scholar]
  73. 73. 
    Honma T, Goto K. 2000. The Arabidopsis floral homeotic gene PISTILLATA is regulated by discrete cis-elements responsive to induction and maintenance signals. Development 127:2021–30
    [Google Scholar]
  74. 74. 
    Huang W, Pi L, Liang W, Xu B, Wang H et al. 2006. The proteolytic function of the Arabidopsis 26S proteasome is required for specifying leaf adaxial identity. Plant Cell 18:2479–92
    [Google Scholar]
  75. 75. 
    Husbands AY, Chitwood DH, Plavskin Y, Timmermans MC. 2009. Signals and prepatterns: new insights into organ polarity in plants. Genes Dev 23:1986–97
    [Google Scholar]
  76. 76. 
    Indjeian VB, Kingman GA, Jones FC, Guenther CA, Grimwood J et al. 2016. Evolving new skeletal traits by cis-regulatory changes in bone morphogenetic proteins. Cell 164:45–56
    [Google Scholar]
  77. 77. 
    Irvine KD, Rauskolb C. 2001. Boundaries in development: formation and function. Annu. Rev. Cell Dev. Biol. 17:189–214
    [Google Scholar]
  78. 78. 
    Iwakawa H, Ueno Y, Semiarti E, Onouchi H, Kojima S et al. 2002. The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana, required for formation of a symmetric flat leaf lamina, encodes a member of a novel family of proteins characterized by cysteine repeats and a leucine zipper. Plant Cell Physiol 43:467–78
    [Google Scholar]
  79. 79. 
    Janssen BJ, Lund L, Sinha N. 1998. Overexpression of a homeobox gene, LeT6, reveals indeterminate features in the tomato compound leaf. Plant Physiol 117:771–86
    [Google Scholar]
  80. 80. 
    Jasinski S, Kaur H, Fau-Tattersall A, Tattersall A, Fau-Tsiantis M, Tsiantis M. 2007. Negative regulation of KNOX expression in tomato leaves. Planta 226:51255–63
    [Google Scholar]
  81. 81. 
    Jasinski S, Piazza P, Craft J, Hay A, Woolley L et al. 2005. KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr. Biol. 15:1560–65
    [Google Scholar]
  82. 82. 
    Jonsson H, Heisler MG, Shapiro BE, Meyerowitz EM, Mjolsness E 2006. An auxin-driven polarized transport model for phyllotaxis. PNAS 103:1633–38Proposed a model for phyllotaxis based on intracellular auxin concentration gradients, which predicted a positive feedback loop between auxin and its polar transport (see also 148).
    [Google Scholar]
  83. 83. 
    Juarez MT, Kui JS, Thomas J, Heller BA, Timmermans MCP. 2004. microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 428:84–88
    [Google Scholar]
  84. 84. 
    Kasprzewska A, Carter R, Swarup R, Bennett M, Monk N et al. 2015. Auxin influx importers modulate serration along the leaf margin. Plant J 83:705–18
    [Google Scholar]
  85. 85. 
    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 51:1046–54
    [Google Scholar]
  86. 86. 
    Kennaway R, Coen E, Green A, Bangham A. 2011. Generation of diverse biological forms through combinatorial interactions between tissue polarity and growth. PLOS Comput. Biol. 7:e1002071
    [Google Scholar]
  87. 87. 
    Kerstetter R, Vollbrecht E, Lowe B, Veit B, Yamaguchi J, Hake S. 1994. Sequence analysis and expression patterns divide the maize knotted1-like homeobox genes into two classes. Plant Cell 6:1877–87
    [Google Scholar]
  88. 88. 
    Kerstetter RA, Bollman K, Taylor RA, Bomblies K, Poethig RS. 2001. KANADI regulates organ polarity in Arabidopsis. Nature 411:706–9
    [Google Scholar]
  89. 89. 
    Kiefer C, Willing EM, Jiao WB, Sun H, Piednoel M et al. 2019. Interspecies association mapping links reduced CG to TG substitution rates to the loss of gene-body methylation. Nat. Plants 5:846–55
    [Google Scholar]
  90. 90. 
    Kierzkowski D, Runions A, Vuolo F, Strauss S, Lymbouridou R et al. 2019. A growth-based framework for leaf shape development and diversity. Cell 177:1405–18.e17Produced cell-level growth and fate maps of simple and complex leaf surfaces and explained how these different leaf shapes emerge.
    [Google Scholar]
  91. 91. 
    Kim M, McCormick S, Timmermans M, Sinha N. 2003. The expression domain of PHANTASTICA determines leaflet placement in compound leaves. Nature 424:438–43
    [Google Scholar]
  92. 92. 
    Koch AJ, Meinhardt H. 1994. Biological pattern formation: from basic mechanisms to complex structures. Rev. Mod. Phys. 66:1481–507
    [Google Scholar]
  93. 93. 
    Kuchen EE, Fox S, Barbier de Reuille P, Kennaway R, Bensmihen S et al. 2012. Generation of leaf shape through early patterns of growth and tissue polarity. Science 335:1092–96Showed that organizing growth polarity patterns coupled with regional differences in the amount of growth shapes diverse simple leaf forms.
    [Google Scholar]
  94. 94. 
    Kuhlemeier C, Timmermans MC. 2016. The Sussex signal: insights into leaf dorsiventrality. Development 143:3230–37
    [Google Scholar]
  95. 95. 
    Landrein B, Ingram G. 2019. Connected through the force: mechanical signals in plant development. J. Exp. Bot. 70:3507–19
    [Google Scholar]
  96. 96. 
    Lee KJI, Bushell C, Koide Y, Fozard JA, Piao C et al. 2019. Shaping of a three-dimensional carnivorous trap through modulation of a planar growth mechanism. PLOS Biol 17:e3000427
    [Google Scholar]
  97. 97. 
    Lin W-c, Shuai B, Springer PS 2003. The Arabidopsis LATERAL ORGAN BOUNDARIES–domain gene ASYMMETRIC LEAVES2 functions in the repression of KNOX gene expression and in adaxial-abaxial patterning. Plant Cell 15:2241–52
    [Google Scholar]
  98. 98. 
    Lincoln C, Long J, Yamaguchi J, Serikawa K, Hake S. 1994. 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 6:1859–76
    [Google Scholar]
  99. 99. 
    Mao Y, Wu F, Yu X, Bai J, Zhong W, He Y. 2014. microRNA319a-targeted Brassica rapa ssp. pekinensis TCP genes modulate head shape in Chinese cabbage by differential cell division arrest in leaf regions. Plant Physiol 164:710–20
    [Google Scholar]
  100. 100. 
    Martin-Trillo M, Cubas P. 2010. TCP genes: a family snapshot ten years later. Trends Plant Sci 15:31–39
    [Google Scholar]
  101. 101. 
    Maugarny-Calès A, Cortizo M, Adroher B, Borrega N, Goncalves B et al. 2019. Dissecting the pathways coordinating patterning and growth by plant boundary domains. PLOS Genet 15:e1007913
    [Google Scholar]
  102. 102. 
    Maugarny-Calès A, Laufs P. 2018. Getting leaves into shape: a molecular, cellular, environmental and evolutionary view. Development 145:dev161646
    [Google Scholar]
  103. 103. 
    Mayer KF, Schoof H, Haecker A, Lenhard M, Jurgens G, Laux T. 1998. Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95:805–15
    [Google Scholar]
  104. 104. 
    McConnell JR, Barton MK. 1998. Leaf polarity and meristem formation in Arabidopsis. Development 125:2935–42
    [Google Scholar]
  105. 105. 
    McConnell JR, Emery J, Eshed Y, Bao N, Bowman J, Barton MK. 2001. Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411:709–13
    [Google Scholar]
  106. 106. 
    Meinhardt H. 1983. Cell determination boundaries as organizing regions for secondary embryonic fields. Dev. Biol. 96:375–85
    [Google Scholar]
  107. 107. 
    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 24:519–35
    [Google Scholar]
  108. 108. 
    Nakayama H, Nakayama N, Seiki S, Kojima M, Sakakibara H et al. 2014. Regulation of the KNOX-GA gene module induces heterophyllic alteration in North American lake cress. Plant Cell 26:4733–48
    [Google Scholar]
  109. 109. 
    Nakayama H, Rowland SD, Cheng Z, Zumstein K, Kang J et al. 2020. Leaf form diversification in an heirloom tomato results from alterations in two different HOMEOBOX genes. bioRxiv 2020.09.08.287011. https://doi.org/10.1101/2020.09.08.287011
    [Crossref]
  110. 110. 
    Nardmann J, Ji J, Werr W, Scanlon MJ 2004. The maize duplicate genes narrow sheath1 and narrow sheath2 encode a conserved homeobox gene function in a lateral domain of shoot apical meristems. Development 131:2827–39
    [Google Scholar]
  111. 111. 
    Nath U, Crawford BC, Carpenter R, Coen E. 2003. Genetic control of surface curvature. Science 299:1404–7
    [Google Scholar]
  112. 112. 
    Nelissen H, Rymen B, Jikumaru Y, Demuynck K, Van Lijsebettens M et al. 2012. A local maximum in gibberellin levels regulates maize leaf growth by spatial control of cell division. Curr. Biol. 22:1183–87
    [Google Scholar]
  113. 113. 
    Nikovics K, Blein T, Peaucelle A, Ishida T, Morin H et al. 2006. The balance between the MIR164A and CUC2 genes controls leaf margin serration in Arabidopsis. Plant Cell 18:2929–45
    [Google Scholar]
  114. 114. 
    Nogueira FT, Madi S, Chitwood DH, Juarez MT, Timmermans MC. 2007. Two small regulatory RNAs establish opposing fates of a developmental axis. Genes Dev 21:750–55
    [Google Scholar]
  115. 115. 
    Okada K, Ueda J, Komaki MK, Bell CJ, Shimura Y. 1991. Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3:677–84
    [Google Scholar]
  116. 116. 
    Ori N, Cohen AR, Etzioni A, Brand A, Yanai O et al. 2007. Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. Nat. Genet. 39:787–91Showed that CIN-TCP-dependent differences in the spatiotemporal regulation of growth arrest and differentiation at the leaf margin shape complex tomato leaves.
    [Google Scholar]
  117. 117. 
    Ori N, Eshed Y, Chuck G, Bowman JL, Hake S. 2000. Mechanisms that control knox gene expression in the Arabidopsis shoot. Development 127:5523–32
    [Google Scholar]
  118. 118. 
    Palatnik JF, Allen E, Wu X, Schommer C, Schwab R et al. 2003. Control of leaf morphogenesis by microRNAs. Nature 425:257–63
    [Google Scholar]
  119. 119. 
    Pekker I, Alvarez JP, Eshed Y. 2005. Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 17:2899–910
    [Google Scholar]
  120. 120. 
    Pelaz S, Ditta GS, Baumann E, Wisman E, Yanofsky MF. 2000. B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405:200–3
    [Google Scholar]
  121. 121. 
    Piazza P, Bailey CD, Cartolano M, Krieger J, Cao J et al. 2010. Arabidopsis thaliana leaf form evolved via loss of KNOX expression in leaves in association with a selective sweep. Curr. Biol. 20:2223–28
    [Google Scholar]
  122. 122. 
    Poethig RS. 1987. Clonal analysis of cell lineage patterns in plant development. Am. J. Bot. 74:581–94
    [Google Scholar]
  123. 123. 
    Prud'homme B, Gompel N, Carroll SB 2007. Emerging principles of regulatory evolution. PNAS 104:Suppl. 18605–12
    [Google Scholar]
  124. 124. 
    Prusinkiewicz P, Runions A. 2012. Computational models of plant development and form. New Phytol 193:549–69
    [Google Scholar]
  125. 125. 
    Qi Y, Sun Y, Xu L, Xu Y, Huang H. 2004. ERECTA is required for protection against heat-stress in the AS1/AS2 pathway to regulate adaxial–abaxial leaf polarity in Arabidopsis. Planta 219:270–76
    [Google Scholar]
  126. 126. 
    Rambaud-Lavigne L, Hay A. 2020. Floral organ development goes live. J. Exp. Bot. 71:2472–78
    [Google Scholar]
  127. 127. 
    Raspopovic J, Marcon L, Russo L, Sharpe J. 2014. Digit patterning is controlled by a Bmp-Sox9-Wnt Turing network modulated by morphogen gradients. Science 345:566–70
    [Google Scholar]
  128. 128. 
    Rast-Somssich MI, Broholm S, Jenkins H, Canales C, Vlad D et al. 2015. Alternate wiring of a KNOXI genetic network underlies differences in leaf development of A. thaliana and C. hirsuta. Genes Dev 29:2391–404
    [Google Scholar]
  129. 129. 
    Reinhardt D, Mandel T, Kuhlemeier C. 2000. Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 12:507–18
    [Google Scholar]
  130. 130. 
    Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K et al. 2003. Regulation of phyllotaxis by polar auxin transport. Nature 426:255–60
    [Google Scholar]
  131. 131. 
    Ren W, Wang H, Bai J, Wu F, He Y. 2018. Association of microRNAs with types of leaf curvature in Brassica rapa. Front. Plant Sci. 9:73
    [Google Scholar]
  132. 132. 
    Runions A, Tsiantis M, Prusinkiewicz P. 2017. A common developmental program can produce diverse leaf shapes. New Phytol 216:401–18
    [Google Scholar]
  133. 133. 
    Saddic LA, Huvermann B, Bezhani S, Su Y, Winter CM et al. 2006. The LEAFY target LMI1 is a meristem identity regulator and acts together with LEAFY to regulate expression of CAULIFLOWER. Development 133:1673–82
    [Google Scholar]
  134. 134. 
    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 15:581–90
    [Google Scholar]
  135. 135. 
    Salve P, Sardesai M, Manza R, Yannawar P 2016. Identification of the plants based on leaf shape descriptors. Proceedings of the Second International Conference on Computer and Communication Technologies S Satapathy, K Raju, J Mandal, V Bhateja 85–101 New Delhi: Springer India
    [Google Scholar]
  136. 136. 
    Scarpella E, Marcos D, Friml J, Berleth T 2006. Control of leaf vascular patterning by polar auxin transport. Genes Dev 20:1015–27
    [Google Scholar]
  137. 137. 
    Scholes NS, Schnoerr D, Isalan M, Stumpf MPH. 2019. A comprehensive network atlas reveals that Turing patterns are common but not robust. Cell Syst 9:515–17
    [Google Scholar]
  138. 138. 
    Seki K, Komatsu K, Tanaka K, Hiraga M, Kajiya-Kanegae H et al. 2020. A CIN-like TCP transcription factor (LsTCP4) having retrotransposon insertion associates with a shift from Salinas type to Empire type in crisphead lettuce (Lactuca sativa L.). Horticult. Res 7:15
    [Google Scholar]
  139. 139. 
    Semiarti E, Ueno Y, Tsukaya H, Iwakawa H, Machida C, Machida Y. 2001. The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana regulates formation of a symmetric lamina, establishment of venation and repression of meristem-related homeobox genes in leaves. Development 128:1771–83
    [Google Scholar]
  140. 140. 
    Serra L, Perrot-Rechenmann C. 2020. Spatiotemporal control of cell growth by CUC3 shapes leaf margins. Development 147:dev183277
    [Google Scholar]
  141. 141. 
    Shani E, Burko Y, Ben-Yaakov L, Berger Y, Amsellem Z et al. 2009. Stage-specific regulation of Solanum lycopersicum leaf maturation by class 1 KNOTTED1-LIKE HOMEOBOX proteins. Plant Cell 21:3078–92
    [Google Scholar]
  142. 142. 
    Sheth R, Marcon L, Bastida MF, Junco M, Quintana L et al. 2012. Hox genes regulate digit patterning by controlling the wavelength of a Turing-type mechanism. Science 338:1476–80
    [Google Scholar]
  143. 143. 
    Shleizer-Burko S, Burko Y, Ben-Herzel O, Ori N. 2011. Dynamic growth program regulated by LANCEOLATE enables flexible leaf patterning. Development 138:695–704
    [Google Scholar]
  144. 144. 
    Sicard A, Thamm A, Marona C, Lee YW, Wahl V et al. 2014. Repeated evolutionary changes of leaf morphology caused by mutations to a homeobox gene. Curr. Biol. 24:1880–86
    [Google Scholar]
  145. 145. 
    Siegfried KR, Eshed Y, Baum SF, Otsuga D, Drews GN, Bowman JL. 1999. Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 126:4117–28
    [Google Scholar]
  146. 146. 
    Skalák J, Vercruyssen L, Claeys H, Hradilová J, Černý M et al. 2019. Multifaceted activity of cytokinin in leaf development shapes its size and structure in Arabidopsis. Plant J 97:805–24
    [Google Scholar]
  147. 147. 
    Skopelitis DS, Benkovics AH, Husbands AY, Timmermans MCP. 2017. Boundary formation through a direct threshold-based readout of mobile small RNA gradients. Dev. Cell 43:265–73.e6
    [Google Scholar]
  148. 148. 
    Smith RS, Guyomarc'h S, Mandel T, Reinhardt D, Kuhlemeier C, Prusinkiewicz P 2006. A plausible model of phyllotaxis. PNAS 103:1301–6
    [Google Scholar]
  149. 149. 
    Steeves TA, Sussex IM. 1989. Patterns in Plant Development Cambridge, UK: Cambridge Univ. Press
  150. 150. 
    Stern DL. 2014. Identification of loci that cause phenotypic variation in diverse species with the reciprocal hemizygosity test. Trends Genet 30:547–54
    [Google Scholar]
  151. 151. 
    Stern DL, Orgogozo V. 2009. Is genetic evolution predictable?. Science 323:746–51
    [Google Scholar]
  152. 152. 
    Streubel S, Fritz MA, Teltow M, Kappel C, Sicard A. 2018. Successive duplication-divergence mechanisms at the RCO locus contributed to leaf shape diversity in the Brassicaceae. Development 145:dev164301
    [Google Scholar]
  153. 153. 
    Szakonyi D, Van Landeghem S, Baerenfaller K, Baeyens L, Blomme J et al. 2015. The KnownLeaf literature curation system captures knowledge about Arabidopsis leaf growth and development and facilitates integrated data mining. Curr. Plant Biol. 2:1–11
    [Google Scholar]
  154. 154. 
    Tadege M, Lin H, Bedair M, Berbel A, Wen J et al. 2011. STENOFOLIA regulates blade outgrowth and leaf vascular patterning in Medicago truncatula and Nicotiana sylvestris. Plant Cell 23:2125–42
    [Google Scholar]
  155. 155. 
    Takata N, Yokota K, Ohki S, Mori M, Taniguchi T, Kurita M. 2013. Evolutionary relationship and structural characterization of the EPF/EPFL gene family. PLOS ONE 8:e65183
    [Google Scholar]
  156. 156. 
    Tameshige T, Okamoto S, Lee JS, Aida M, Tasaka M et al. 2016. A secreted peptide and its receptors shape the auxin response pattern and leaf margin morphogenesis. Curr. Biol. 26:2478–85
    [Google Scholar]
  157. 157. 
    Tattersall AD, Turner L, Knox MR, Ambrose MJ, Ellis TH, Hofer JM. 2005. The mutant crispa reveals multiple roles for PHANTASTICA in pea compound leaf development. Plant Cell 17:1046–60
    [Google Scholar]
  158. 158. 
    Theophrastus 1916. (c. 350–285 BCE). Enquiry into Plants, transl. AF Hort Cambridge, MA: Harvard Univ. Press
    [Google Scholar]
  159. 159. 
    Tsiantis M. 2001. Control of shoot cell fate: beyond homeoboxes. Plant Cell 13:733–38
    [Google Scholar]
  160. 160. 
    Tsiantis M, Schneeberger R, Golz JF, Freeling M, Langdale JA. 1999. The maize rough sheath2 gene and leaf development programs in monocot and dicot plants. Science 284:154–56
    [Google Scholar]
  161. 161. 
    Vandenbussche M, Horstman A, Zethof J, Koes R, Rijpkema AS, Gerats T. 2009. Differential recruitment of WOX transcription factors for lateral development and organ fusion in Petunia and Arabidopsis. Plant Cell 21:2269–83
    [Google Scholar]
  162. 162. 
    Vernoux T, Kronenberger J, Grandjean O, Laufs P, Traas J. 2000. PIN-FORMED 1 regulates cell fate at the periphery of the shoot apical meristem. Development 127:5157–65
    [Google Scholar]
  163. 163. 
    Vlad D, Kierzkowski D, Rast MI, Vuolo F, Dello Ioio R et al. 2014. Leaf shape evolution through duplication, regulatory diversification, and loss of a homeobox gene. Science 343:780–83Discovered that RCO gene duplication coupled with cis-regulatory divergence and subsequent gene loss caused leaf shape diversity in crucifers.
    [Google Scholar]
  164. 164. 
    Vuolo F, Mentink RA, Hajheidari M, Bailey CD, Filatov DA, Tsiantis M. 2016. Coupled enhancer and coding sequence evolution of a homeobox gene shaped leaf diversity. Genes Dev 30:2370–75
    [Google Scholar]
  165. 165. 
    Waites R, Hudson A. 1995. phantastica: a gene required for dorsoventrality of leaves in Antirrhinum majus. Development 121:2143–54Through studies of the PHANTASTICA gene, showed that leaf laminar growth requires the juxtaposition of abaxial and adaxial cell types.
    [Google Scholar]
  166. 166. 
    Waites R, Selvadurai HR, Oliver IR, Hudson A. 1998. The PHANTASTICA gene encodes a MYB transcription factor involved in growth and dorsoventrality of lateral organs in Antirrhinum. Cell 93:779–89
    [Google Scholar]
  167. 167. 
    Whitewoods CD, Coen E. 2017. Growth and development of three-dimensional plant form. Curr. Biol. 27:R910–18
    [Google Scholar]
  168. 168. 
    Whitewoods CD, Gonçalves B, Cheng J, Cui M, Kennaway R et al. 2020. Evolution of carnivorous traps from planar leaves through simple shifts in gene expression. Science 367:91–96Proposed that a proximodistal polarity field directs abaxial surface growth to shape 3D-curved leaves (traps) of the carnivorous plant Utricularia.
    [Google Scholar]
  169. 169. 
    Wittkopp PJ, Haerum BK, Clark AG. 2004. Evolutionary changes in cis and trans gene regulation. Nature 430:85–88
    [Google Scholar]
  170. 170. 
    Wittkopp PJ, Vaccaro K, Carroll SB. 2002. Evolution of yellow gene regulation and pigmentation in Drosophila. Curr. Biol. 12:1547–56
    [Google Scholar]
  171. 171. 
    Wolpert L. 1969. Positional information and the spatial pattern of cellular differentiation. J. Theor. Biol. 25:1–47
    [Google Scholar]
  172. 172. 
    Xu L, Yang L, Pi L, Liu Q, Ling Q et al. 2006. Genetic interaction between the AS1–AS2 and RDR6–SGS3–AGO7 pathways for leaf morphogenesis. Plant Cell Physiol 47:853–63
    [Google Scholar]
  173. 173. 
    Yadav RK, Perales M, Gruel J, Ohno C, Heisler M et al. 2013. Plant stem cell maintenance involves direct transcriptional repression of differentiation program. Mol. Syst. Biol. 9:654
    [Google Scholar]
  174. 174. 
    Yifhar T, Pekker I, Peled D, Friedlander G, Pistunov A et al. 2012. Failure of the tomato trans-acting short interfering RNA program to regulate AUXIN RESPONSE FACTOR3 and ARF4 underlies the wiry leaf syndrome. Plant Cell 24:3575–89
    [Google Scholar]
  175. 175. 
    Yu T, Guan C, Wang J, Sajjad M, Ma L, Jiao Y. 2017. Dynamic patterns of gene expression during leaf initiation. J. Genet. Genom. 44:599–601
    [Google Scholar]
  176. 176. 
    Yu X, Wang H, Zhong W, Bai J, Liu P, He Y 2013. QTL mapping of leafy heads by genome resequencing in the RIL population of Brassica rapa. PLOS ONE 8:e76059
    [Google Scholar]
  177. 177. 
    Zhang C, Wang J, Wang X, Li C, Ye Z, Zhang J. 2020. UF, a WOX gene, regulates a novel phenotype of un-fused flower in tomato. Plant Science 297:110523
    [Google Scholar]
  178. 178. 
    Zhang Z, Runions A, Mentink RA, Kierzkowski D, Karady M et al. 2020. A WOX/auxin biosynthesis module controls growth to shape leaf form. Curr. Biol. 30:4857–68.e6
    [Google Scholar]
  179. 179. 
    Zhao C, Chan SSF, Cham W-K, Chu LM. 2015. Plant identification using leaf shapes—a pattern counting approach. Pattern Recognit 48:3203–15
    [Google Scholar]
  180. 180. 
    Zhao F, Du F, Oliveri H, Zhou L, Ali O et al. 2020. Microtubule-mediated wall anisotropy contributes to leaf blade flattening. Curr. Biol. 30:3972–85.e6
    [Google Scholar]
  181. 181. 
    Zhuang L-L, Ambrose M, Rameau C, Weng L, Yang J et al. 2012. LATHYROIDES, encoding a WUSCHEL-related Homeobox1 transcription factor, controls organ lateral growth, and regulates tendril and dorsal petal identities in garden pea (Pisum sativum L.). Mol. Plant 5:1333–45
    [Google Scholar]
  182. 182. 
    Zoulias N, Koenig D, Hamidi A, McCormick S, Kim M. 2012. A role for PHANTASTICA in medio-lateral regulation of adaxial domain development in tomato and tobacco leaves. Ann. Bot. 109:407–18
    [Google Scholar]
  183. 183. 
    Zuniga A, Zeller R. 2014. In Turing's hands—the making of digits. Science 345:516–17
    [Google Scholar]
/content/journals/10.1146/annurev-arplant-080720-101613
Loading
/content/journals/10.1146/annurev-arplant-080720-101613
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error