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WIREs Dev Biol

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Morphogenesis of simple leaves: regulation of leaf size and shape

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Ramiro E. Rodriguez, Juan M. Debernardi, Javier F. Palatnik

Published Online: Apr 18 2013

DOI: 10.1002/wdev.115

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Abstract Plants produce new organs throughout their life span. Leaves first initiate as rod‐like structures protruding from the shoot apical meristem, while they need to pass through different developmental stages to become the flat organ specialized in photosynthesis. Leaf morphogenesis is an active process regulated by many genes and pathways that can generate organs with a wide variety of sizes and shapes. Important differences in leaf architecture can be seen among different species, but also in single individuals. A key aspect of leaf morphogenesis is the precise control of cell proliferation. Modification or manipulation of this process may lead to leaves with different sizes and shapes, and changes in the organ margins and curvature. Many genes required for leaf development have been identified in Arabidopsis thaliana, and the mechanisms underlying leaf morphogenesis are starting to be unraveled at the molecular level. WIREs Dev Biol 2014, 3:41–57. doi: 10.1002/wdev.115 This article is categorized under: Plant Development > Vegetative Development Plant Development > Cell Growth and Differentiation

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Dicotyledonous leaves and their variations in size and shape. (a) Arabidopsis thaliana plant showing the three different axes of asymmetries. Bottom left, adult and juvenile leaves. (b) Cross sections of an Arabidopsis leaf blade showing the organization of the different tissues. Two single‐celled layers of epidermis enclose the mesophyll, organized in palisade and spongy parenchyma. (c) Samples for leaf shape and size variations found in nature. The rightmost leaf is a compound or dissected leaf with seven leaflets, while all the others are simple leaves with different shapes, sizes, and margins. From left to right, leaves of Ficus benjamina, Populus nigra, Pyracantha coccinea, Morus nigra, Pelargonium hortorum, Salix babylonica, Hedera helix, and Fraxinus excelsior.

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Variation of leaf shape and size in Arabidopsis natural accessions. (a) Leaf #1 shape and size of 12 Arabidopsis thaliana accessions. The heatmaps represent the leaf area (top) or the length‐to‐width ratio of each accession. (b) A naturally occurring miR164 allele defective in the biogenesis of the miRNA found in the C24 Arabidopsis accession produces deeper serrations when introgressed in Col‐0 plants (Col‐0 × C24 RIL).

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Heteroblasty. (a) Cotyledons, successive true rosette, and cauline leaves in Arabidopsis thaliana. (b) Scheme showing the regulation of vegetative phase change by the miR156‐mediated repression of SPL genes.

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Generation of leaf serrations. Scheme showing the interplay between CUC2 and auxin in the formation of leaf serrations in Arabidopsis leaves. CUC2 promotes the establishment of PIN1 convergence points which in turn generate auxin maxima at the tip of serrations. The auxin maximum represses CUC2 at the serration tip and promotes tooth growth. Note that CUC2 is regulated by miR164.

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Regulation of leaf curvature. (a) Overexpression of miRNA miR319, which negatively regulates TCP transcription factors as seen in the jaw‐D mutant produces an excess of cells in the margins that causes crinkled leaves. (b) Integration of the miR319/TCP and miR396/GRF regulatory nodes in cell proliferation and differentiation.

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Role of the miR396‐GRF‐GIF regulatory network in leaf growth. (a) Scheme showing the expression pattern of CYCLINB1;1 (CYCB1;1), miR396, and KLUH. CYCB1;1 indicates dividing cells; miR396 negatively regulates GRF transcription factors and therefore cell proliferation; and KLUH generates an unknown mobile signal that stimulates cell proliferation. (b) GUS staining in developing leaves #5 of transgenic plants harboring CYCB1;1, wtGRF2, rGRF2, and miR396, reporters. The GRF2 reporter is sensitive to the posttranscriptional regulation by miR396, while rGRF2 has mutations in the miRNA‐binding site, so that it is resistant to miR396 action. (c) GRFs and GIFs promote cell proliferation. Silhouette of first leaves of plants overexpressing miR396 (35S:miR396) or GRF2 (rGRF2) and knock‐outs in GRFs or GIF1 (also known as AN3). Palisade parenchyma cell number and size normalized to wild‐type are indicated below each leaf. (Reprinted with permission from Ref . Copyright 2012 PLOS).

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Cell proliferation and expansion during leaf development. (a) Distribution of the cell proliferation and expansion phases in developing leaves of increasing ages. A CYCLINB1;1, (CYCB1;1:GUS) reporter labels cells in the G2‐M phase of the cell cycle. Note that cell proliferation is restricted to the proximal part of the leaf, while cell expansion occurs in the distal part. (b) Magnitude of the cell expansion process during leaf maturation. Outline of adaxial epidermal pavement cells and paradermal view of palisade parenchyma cells in proliferating and mature leaves (Reprinted with permission from Ref 74. Copyright 2010 The Company of Biologists Ltd).

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Early events in leaf development. (a) Scanning electron microscopy of a vegetative shoot apical meristem. Note the spiral phyllotaxy of leaf primordia (LP) around the meristem. (b) Architecture of the vegetative shoot apical meristem. Cells in the S‐phase of the cell cycle are revealed by the expression of HISTONE H4 detected by in situ hybridization in medial‐longitudinal sections. (c) Genes and hormones involved in meristem maintenance and leaf initiation. (d) Expression and activity patterns of genes and small‐RNAs essential for the establishment of leaf polarity.

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References

Tucker, MR, Laux, T. Connecting the paths in plant stem cell regulation. Trends Cell Biol 2007, 17:403–410.
Hay, A, Tsiantis, M. KNOX genes: versatile regulators of plant development and diversity. Development 2010, 137:3153–3165.
Hamant, O, Pautot, V. Plant development: a TALE story. C R Biol 2010, 333:371–381.
Moon, J, Hake, S. How a leaf gets its shape. Curr Opin Plant Biol 2011, 14:24–30.
Reinhardt, D, Pesce, ER, Stieger, P, Mandel, T, Baltensperger, K, Bennett, M, Traas, J, Friml, J, Kuhlemeier, C. Regulation of phyllotaxis by polar auxin transport. Nature 2003, 426:255–260.
Heisler, MG, Ohno, C, Das, P, Sieber, P, Reddy, GV, Long, JA, Meyerowitz, EM. Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr Biol 2005, 15:1899–1911.
Stieger, PA, Reinhardt, D, Kuhlemeier, C. The auxin influx carrier is essential for correct leaf positioning. Plant J 2002, 32:509–517.
Byrne, ME, Barley, R, Curtis, M, Arroyo, JM, Dunham, M, Hudson, A, Martienssen, RA. Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 2000, 408:967–971.
Byrne, ME, Simorowski, J, Martienssen, RA. ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis. Development 2002, 129:1957–1965.
Semiarti, E, Ueno, Y, Tsukaya, H, Iwakawa, H, Machida, C, Machida, Y. 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 2001, 128:1771–1783.
Guo, M, Thomas, J, Collins, G, Timmermans, MC. Direct repression of KNOX loci by the ASYMMETRIC LEAVES1 complex of Arabidopsis. Plant Cell 2008, 20:48–58.
Aida, M, Ishida, T, Tasaka, M. Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP‐SHAPED COTYLEDON and SHOOT MERISTEMLESS genes. Development 1999, 126:1563–1570.
Takada, S, Hibara, K, Ishida, T, Tasaka, M. The CUP‐SHAPED COTYLEDON1 gene of Arabidopsis regulates shoot apical meristem formation. Development 2001, 128:1127–1135.
Vroemen, CW, Mordhorst, AP, Albrecht, C, Kwaaitaal, MA, de Vries, SC. The CUP‐SHAPED COTYLEDON3 gene is required for boundary and shoot meristem formation in Arabidopsis. Plant Cell 2003, 15:1563–1577.
Aida, M, Ishida, T, Fukaki, H, Fujisawa, H, Tasaka, M. Genes involved in organ separation in Arabidopsis: an analysis of the cup‐shaped cotyledon mutant. Plant Cell 1997, 9:841–857.
Hibara, K, Karim, MR, Takada, S, Taoka, K, Furutani, M, Aida, M, Tasaka, M. Arabidopsis CUP‐SHAPED COTYLEDON3 regulates postembryonic shoot meristem and organ boundary formation. Plant Cell 2006, 18:2946–2957.
Blein, T, Pulido, A, Vialette‐Guiraud, A, Nikovics, K, Morin, H, Hay, A, Johansen, IE, Tsiantis, M, Laufs, P. A conserved molecular framework for compound leaf development. Science 2008, 322:1835–1839.
Aida, M, Vernoux, T, Furutani, M, Traas, J, Tasaka, M. Roles of PIN‐FORMED1 and MONOPTEROS in pattern formation of the apical region of the Arabidopsis embryo. Development 2002, 129:3965–3974.
Spinelli, SV, Martin, AP, Viola, IL, Gonzalez, DH, Palatnik, JF. A mechanistic link between STM and CUC1 during Arabidopsis development. Plant Physiol 2011, 156:1894–1904.
Husbands, AY, Chitwood, DH, Plavskin, Y, Timmermans, MC. Signals and prepatterns: new insights into organ polarity in plants. Genes Dev 2009, 23:1986–1997.
Chitwood, DH, Guo, M, Nogueira, FT, Timmermans, MC. Establishing leaf polarity: the role of small RNAs and positional signals in the shoot apex. Development 2007, 134:813–823.
McConnell, JR, Emery, J, Eshed, Y, Bao, N, Bowman, J, Barton, MK. Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 2001, 411:709–713.
McConnell, JR, Barton, MK. Leaf polarity and meristem formation in Arabidopsis. Development 1998, 125:2935–2942.
Emery, JF, Floyd, SK, Alvarez, J, Eshed, Y, Hawker, NP, Izhaki, A, Baum, SF, Bowman, JL. Radial patterning of Arabidopsis shoots by class III HD‐ZIP and KANADI genes. Curr Biol 2003, 13:1768–1774.
Xu, L, Xu, Y, Dong, A, Sun, Y, Pi, L, Huang, H. 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 2003, 130:4097–4107.
Eshed, Y, Baum, SF, Perea, JV, Bowman, JL. Establishment of polarity in lateral organs of plants. Curr Biol 2001, 11:1251–1260.
Kerstetter, RA, Bollman, K, Taylor, RA, Bomblies, K, Poethig, RS. KANADI regulates organ polarity in Arabidopsis. Nature 2001, 411:706–709.
Siegfried, KR, Eshed, Y, Baum, SF, Otsuga, D, Drews, GN, Bowman, JL. Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 1999, 126:4117–4128.
Sawa, S, Watanabe, K, Goto, K, Liu, YG, Shibata, D, Kanaya, E, Morita, EH, Okada, K. FILAMENTOUS FLOWER, a meristem and organ identity gene of Arabidopsis, encodes a protein with a zinc finger and HMG‐related domains. Genes Dev 1999, 13:1079–1088.
Pekker, I, Alvarez, JP, Eshed, Y. Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 2005, 17:2899–2910.
Voinnet, O. Origin, biogenesis, and activity of plant microRNAs. Cell 2009, 136:669–687.
Cuperus, JT, Fahlgren, N, Carrington, JC. Evolution and functional diversification of MIRNA genes. Plant Cell 2011, 23:431–442.
Meyers, BC, Axtell, MJ, Bartel, B, Bartel, DP, Baulcombe, D, Bowman, JL, Cao, X, Carrington, JC, Chen, X, Green, PJ, et al. Criteria for annotation of plant microRNAs. Plant Cell 2008, 20:3186–3190.
Mallory, AC, Elmayan, T, Vaucheret, H. MicroRNA maturation and action—the expanding roles of ARGONAUTEs. Curr Opin Plant Biol 2008, 11:560–566.
Laufs, P, Peaucelle, A, Morin, H, Traas, J. MicroRNA regulation of the CUC genes is required for boundary size control in Arabidopsis meristems. Development 2004, 131:4311–4322.
Mallory, AC, Dugas, DV, Bartel, DP, Bartel, B. MicroRNA regulation of NAC‐domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organs. Curr Biol 2004, 14:1035–1046.
Sieber, P, Wellmer, F, Gheyselinck, J, Riechmann, JL, Meyerowitz, EM. Redundancy and specialization among plant microRNAs: role of the MIR164 family in developmental robustness. Development 2007, 134:1051–1060.
Schwab, R, Palatnik, JF, Riester, M, Schommer, C, Schmid, M, Weigel, D. Specific effects of microRNAs on the plant transcriptome. Dev Cell 2005, 8:517–527.
Nikovics, K, Blein, T, Peaucelle, A, Ishida, T, Morin, H, Aida, M, Laufs, P. The balance between the MIR164A and CUC2 genes controls leaf margin serration in Arabidopsis. Plant Cell 2006, 18:2929–2945.
Peaucelle, A, Morin, H, Traas, J, Laufs, P. Plants expressing a miR164‐resistant CUC2 gene reveal the importance of post‐meristematic maintenance of phyllotaxy in Arabidopsis. Development 2007, 134:1045–1050.
Juarez, MT, Kui, JS, Thomas, J, Heller, BA, Timmermans, MC. microRNA‐mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 2004, 428:84–88.
Juarez, MT, Twigg, RW, Timmermans, MC. Specification of adaxial cell fate during maize leaf development. Development 2004, 131:4533–4544.
Kidner, CA, Martienssen, RA. Spatially restricted microRNA directs leaf polarity through ARGONAUTE1. Nature 2004, 428:81–84.
Mallory, AC, Reinhart, BJ, Jones‐Rhoades, MW, Tang, G, Zamore, PD, Barton, MK, Bartel, DP. MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5′ region. EMBO J 2004, 23:3356–3364.
Liu, Q, Yao, X, Pi, L, Wang, H, Cui, X, Huang, H. The ARGONAUTE10 gene modulates shoot apical meristem maintenance and establishment of leaf polarity by repressing miR165/166 in Arabidopsis. Plant J 2009, 58:27–40.
Zhu, H, Hu, F, Wang, R, Zhou, X, Sze, SH, Liou, LW, Barefoot, A, Dickman, M, Zhang, X. Arabidopsis Argonaute10 specifically sequesters miR166/165 to regulate shoot apical meristem development. Cell 2011, 145:242–256.
Ji, L, Liu, X, Yan, J, Wang, W, Yumul, RE, Kim, YJ, Dinh, TT, Liu, J, Cui, X, Zheng, B, et al. ARGONAUTE10 and ARGONAUTE1 regulate the termination of floral stem cells through two microRNAs in Arabidopsis. PLoS Genet 2011, 7:e1001358.
Allen, E, Xie, Z, Gustafson, AM, Carrington, JC. microRNA‐directed phasing during trans‐acting siRNA biogenesis in plants. Cell 2005, 121:207–221.
Axtell, MJ, Jan, C, Rajagopalan, R, Bartel, DP. A two‐hit trigger for siRNA biogenesis in plants. Cell 2006, 127:565–577.
Montgomery, TA, Howell, MD, Cuperus, JT, Li, D, Hansen, JE, Alexander, AL, Chapman, EJ, Fahlgren, N, Allen, E, Carrington, JC. Specificity of ARGONAUTE7‐miR390 interaction and dual functionality in TAS3 trans‐acting siRNA formation. Cell 2008, 133: 128–141.
Nogueira, FT, Madi, S, Chitwood, DH, Juarez, MT, Timmermans, MC. Two small regulatory RNAs establish opposing fates of a developmental axis. Genes Dev 2007, 21:750–755.
Donnelly, PM, Bonetta, D, Tsukaya, H, Dengler, RE, Dengler, NG. Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev Biol 1999, 215:407–419.
Andriankaja, M, Dhondt, S, De Bodt, S, Vanhaeren, H, Coppens, F, De Milde, L, Muhlenbock, P, Skirycz, A, Gonzalez, N, Beemster, GT, et al. Exit from proliferation during leaf development in Arabidopsis thaliana: a not‐so‐gradual process. Dev Cell 2012, 22:64–78.
Ferjani, A, Horiguchi, G, Yano, S, Tsukaya, H. Analysis of leaf development in fugu mutants of Arabidopsis reveals three compensation modes that modulate cell expansion in determinate organs. Plant Physiol 2007, 144:988–999.
Kazama, T, Ichihashi, Y, Murata, S, Tsukaya, H. 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 2010, 51:1046–1054.
Powell, AE, Lenhard, M. Control of organ size in plants. Curr Biol 2012, 22:R360–367.
White, DW. PEAPOD regulates lamina size and curvature in Arabidopsis. Proc Natl Acad Sci U S A 2006, 103:13238–13243.
Bergmann, DC, Sack, FD. Stomatal development. Annu Rev Plant Biol 2007, 58:163–181.
Yuan, Z, Luo, D, Li, G, Yao, X, Wang, H, Zeng, M, Huang, H, Cui, X. Characterization of the AE7 gene in Arabidopsis suggests that normal cell proliferation is essential for leaf polarity establishment. Plant J 2010, 64:331–342.
Wang, L, Gu, X, Xu, D, Wang, W, Wang, H, Zeng, M, Chang, Z, Huang, H, Cui, X. miR396‐targeted AtGRF transcription factors are required for coordination of cell division and differentiation during leaf development in Arabidopsis. J Exp Bot 2011, 62:761–773.
Horiguchi, G, Nakayama, H, Ishikawa, N, Kubo, M, Demura, T, Fukuda, H, Tsukaya, H. ANGUSTIFOLIA3 plays roles in adaxial/abaxial patterning and growth in leaf morphogenesis. Plant Cell Physiol 2011, 52:112–124.
Mecchia, MA, Debernardi, JM, Rodriguez, RE, Schommer, C, Palatnik, JF. MicroRNA miR396 and RDR6 synergistically regulate leaf development. Mech Dev 2012, 130:2–13.
Beemster, GT, Fiorani, F, Inze, D. Cell cycle: the key to plant growth control? Trends Plant Sci 2003, 8:154–158.
Inze, D, De Veylder, L. Cell cycle regulation in plant development. Annu Rev Genet 2006, 40:77–105.
Marrocco, K, Bergdoll, M, Achard, P, Criqui, MC, Genschik, P. Selective proteolysis sets the tempo of the cell cycle. Curr Opin Plant Biol 2010, 13:631–639.
Gutierrez, C. The Arabidopsis cell division cycle. Arabidopsis Book 2009, 7:e0120.
Eloy, NB, de Freitas Lima, M, Van Damme, D, Vanhaeren, H, Gonzalez, N, De Milde, L, Hemerly, AS, Beemster, GT, Inze, D, Ferreira, PC. The APC/C subunit 10 plays an essential role in cell proliferation during leaf development. Plant J 2011, 68:351–363.
De Veylder, L, Beeckman, T, Beemster, GT, Krols, L, Terras, F, Landrieu, I, van der Schueren, E, Maes, S, Naudts, M, Inze, D. Functional analysis of cyclin‐dependent kinase inhibitors of Arabidopsis. Plant Cell 2001, 13:1653–1668.
Weinl, C, Marquardt, S, Kuijt, SJ, Nowack, MK, Jakoby, MJ, Hulskamp, M, Schnittger, A. Novel functions of plant cyclin‐dependent kinase inhibitors, ICK1/KRP1, can act non‐cell‐autonomously and inhibit entry into mitosis. Plant Cell 2005, 17:1704–1722.
van der Knaap, E, Kim, JH, Kende, H. A novel gibberellin‐induced gene from rice and its potential regulatory role in stem growth. Plant Physiol 2000, 122:695–704.
Kim, JH, Choi, D, Kende, H. The AtGRF family of putative transcription factors is involved in leaf and cotyledon growth in Arabidopsis. Plant J 2003, 36:94–104.
Choi, D, Kim, JH, Kende, H. Whole genome analysis of the OsGRF gene family encoding plant‐specific putative transcription activators in rice (Oryza sativa L.). Plant Cell Physiol 2004, 45:897–904.
Horiguchi, G, Kim, GT, Tsukaya, H. The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf primordia of Arabidopsis thaliana. Plant J 2005, 43:68–78.
Kim, JH, Kende, H. A transcriptional coactivator, AtGIF1, is involved in regulating leaf growth and morphology in Arabidopsis. Proc Natl Acad Sci U S A 2004, 101:13374–13379.
Lee, BH, Ko, JH, Lee, S, Lee, Y, Pak, JH, Kim, JH. The Arabidopsis GRF‐INTERACTING FACTOR gene family performs an overlapping function in determining organ size as well as multiple developmental properties. Plant Physiol 2009, 151:655–668.
Rodriguez, RE, Mecchia, MA, Debernardi, JM, Schommer, C, Weigel, D, Palatnik, JF. Control of cell proliferation in Arabidopsis thaliana by microRNA miR396. Development 2010, 137:103–112.
Jones‐Rhoades, MW, Bartel, DP. Computational identification of plant microRNAs and their targets, including a stress‐induced miRNA. Mol Cell 2004, 14:787–799.
Axtell, MJ, Bartel, DP. Antiquity of microRNAs and their targets in land plants. Plant Cell 2005, 17:1658–1673.
Liu, D, Song, Y, Chen, Z, Yu, D. Ectopic expression of miR396 suppresses GRF target gene expression and alters leaf growth in Arabidopsis. Physiol Plant 2009, 136:223–236.
Debernardi, JM, Rodriguez, RE, Mecchia, MA, Palatnik, JF. Functional specialization of the plant miR396 regulatory network through distinct microRNA‐target interactions. PLoS Genet 2012, 8:e1002419.
Elliott, RC, Betzner, AS, Huttner, E, Oakes, MP, Tucker, WQ, Gerentes, D, Perez, P, Smyth, DR. AINTEGUMENTA, an APETALA2‐like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 1996, 8:155–168.
Klucher, KM, Chow, H, Reiser, L, Fischer, RL. The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2. Plant Cell 1996, 8:137–153.
Mizukami, Y, Fischer, RL. Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proc Natl Acad Sci U S A 2000, 97:942–947.
Nole‐Wilson, S, Tranby, TL, Krizek, BA. AINTEGUMENTA‐like (AIL) genes are expressed in young tissues and may specify meristematic or division‐competent states. Plant Mol Biol 2005, 57:613–628.
Hu, Y, Xie, Q, Chua, NH. The Arabidopsis auxin‐inducible gene ARGOS controls lateral organ size. Plant Cell 2003, 15:1951–1961.
Feng, G, Qin, Z, Yan, J, Zhang, X, Hu, Y. Arabidopsis ORGAN SIZE RELATED1 regulates organ growth and final organ size in orchestration with ARGOS and ARL. New Phytol 2011, 191:635–646.
Hu, Y, Poh, HM, Chua, NH. The Arabidopsis ARGOS‐LIKE gene regulates cell expansion during organ growth. Plant J 2006, 47:1–9.
Okushima, Y, Mitina, I, Quach, HL, Theologis, A. AUXIN RESPONSE FACTOR 2 (ARF2): a pleiotropic developmental regulator. Plant J 2005, 43:29–46.
Ellis, CM, Nagpal, P, Young, JC, Hagen, G, Guilfoyle, TJ, Reed, JW. AUXIN RESPONSE FACTOR1 and AUXIN RESPONSE FACTOR2 regulate senescence and floral organ abscission in Arabidopsis thaliana. Development 2005, 132:4563–4574.
Schruff, MC, Spielman, M, Tiwari, S, Adams, S, Fenby, N, Scott, RJ. The AUXIN RESPONSE FACTOR 2 gene of Arabidopsis links auxin signalling, cell division, and the size of seeds and other organs. Development 2006, 133:251–261.
Anastasiou, E, Kenz, S, Gerstung, M, MacLean, D, Timmer, J, Fleck, C, Lenhard, M. Control of plant organ size by KLUH/CYP78A5‐dependent intercellular signaling. Dev Cell 2007, 13:843–856.
Adamski, NM, Anastasiou, E, Eriksson, S, O`Neill, CM, Lenhard, M. Local maternal control of seed size by KLUH/CYP78A5‐dependent growth signaling. Proc Natl Acad Sci U S A 2009, 106:20115–20120.
Ikeuchi, M, Yamaguchi, T, Kazama, T, Ito, T, Horiguchi, G, Tsukaya, H. ROTUNDIFOLIA4 regulates cell proliferation along the body axis in Arabidopsis shoot. Plant Cell Physiol 2011, 52:59–69.
Pinon, V, Etchells, JP, Rossignol, P, Collier, SA, Arroyo, JM, Martienssen, RA, Byrne, ME. Three PIGGYBACK genes that specifically influence leaf patterning encode ribosomal proteins. Development 2008, 135:1315–1324.
Horiguchi, G, Molla‐Morales, A, Perez‐Perez, JM, Kojima, K, Robles, P, Ponce, MR, Micol, JL, Tsukaya, H. Differential contributions of ribosomal protein genes to Arabidopsis thaliana leaf development. Plant J 2011, 65:724–736.
Rosado, A, Sohn, EJ, Drakakaki, G, Pan, S, Swidergal, A, Xiong, Y, Kang, BH, Bressan, RA, Raikhel, NV. Auxin‐mediated ribosomal biogenesis regulates vacuolar trafficking in Arabidopsis. Plant Cell 2010, 22:143–158.
Yao, Y, Ling, Q, Wang, H, Huang, H. Ribosomal proteins promote leaf adaxial identity. Development 2008, 135:1325–1334.
Fujikura, U, Horiguchi, G, Ponce, MR, Micol, JL, Tsukaya, H. Coordination of cell proliferation and cell expansion mediated by ribosome‐related processes in the leaves of Arabidopsis thaliana. Plant J 2009, 59:499–508.
Szakonyi, D, Byrne, ME. Ribosomal protein L27a is required for growth and patterning in Arabidopsis thaliana. Plant J 2011, 65:269–281.
Horiguchi, G, Van Lijsebettens, M, Candela, H, Micol, JL, Tsukaya, H. Ribosomes and translation in plant developmental control. Plant Sci 2012, 191–192.
Byrne, ME. A role for the ribosome in development. Trends Plant Sci 2009, 14:512–519.
Nath, U, Crawford, BC, Carpenter, R, Coen, E. Genetic control of surface curvature. Science 2003, 299:1404–1407.
Martin‐Trillo, M, Cubas, P. TCP genes: a family snapshot ten years later. Trends Plant Sci 2010, 15:31–39.
Weigel, D, Ahn, JH, Blazquez, MA, Borevitz, JO, Christensen, SK, Fankhauser, C, Ferrandiz, C, Kardailsky, I, Malancharuvil, EJ, Neff, MM, et al. Activation tagging in Arabidopsis. Plant Physiol 2000, 122:1003–1013.
Palatnik, JF, Allen, E, Wu, X, Schommer, C, Schwab, R, Carrington, JC, Weigel, D. Control of leaf morphogenesis by microRNAs. Nature 2003, 425:257–263.
Schommer, C, Palatnik, JF, Aggarwal, P, Chetelat, A, Cubas, P, Farmer, EE, Nath, U, Weigel, D. Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biol 2008, 6:e230.
Efroni, I, Blum, E, Goldshmidt, A, Eshed, Y. A protracted and dynamic maturation schedule underlies Arabidopsis leaf development. Plant Cell 2008, 20:2293–2306.
Koyama, T, Furutani, M, Tasaka, M, Ohme‐Takagi, M. TCP transcription factors control the morphology of shoot lateral organs via negative regulation of the expression of boundary‐specific genes in Arabidopsis. Plant Cell 2007, 19:473–484.
Koyama, T, Mitsuda, N, Seki, M, Shinozaki, K, Ohme‐Takagi, M. TCP transcription factors regulate the activities of ASYMMETRIC LEAVES1 and miR164, as well as the auxin response, during differentiation of leaves in Arabidopsis. Plant Cell 2010, 22:3574–3588.
Palatnik, JF, Tognetti, VB, Poli, HO, Rodriguez, RE, Blanco, N, Gattuso, M, Hajirezaei, MR, Sonnewald, U, Valle, EM, Carrillo, N. Transgenic tobacco plants expressing antisense ferredoxin‐NADP(H) reductase transcripts display increased susceptibility to photo‐oxidative damage. Plant J 2003, 35:332–341.
Palatnik, JF, Wollmann, H, Schommer, C, Schwab, R, Boisbouvier, J, Rodriguez, R, Warthmann, N, Allen, E, Dezulian, T, Huson, D, et al. Sequence and expression differences underlie functional specialization of Arabidopsis microRNAs miR159 and miR319. Dev Cell 2007, 13:115–125.
Malinowski, R, Kasprzewska, A, Fleming, AJ. Targeted manipulation of leaf form via local growth repression. Plant J 2011, 66:941–952.
Tsukaya, H. Controlling size in multicellular organs: focus on the leaf. PLoS Biol 2008, 6:e174.
Beemster, GT, De Veylder, L, Vercruysse, S, West, G, Rombaut, D, Van Hummelen, P, Galichet, A, Gruissem, W, Inze, D, Vuylsteke, M. Genome‐wide analysis of gene expression profiles associated with cell cycle transitions in growing organs of Arabidopsis. Plant Physiol 2005, 138:734–743.
Sugimoto‐Shirasu, K, Roberts, K. “Big it up”: endoreduplication and cell‐size control in plants. Curr Opin Plant Biol 2003, 6:544–553.
Dewitte, W, Riou‐Khamlichi, C, Scofield, S, Healy, JM, Jacqmard, A, Kilby, NJ, Murray, JA. Altered cell cycle distribution, hyperplasia, and inhibited differentiation in Arabidopsis caused by the D‐type cyclin CYCD3. Plant Cell 2003, 15:79–92.
Baskin, TI. Anisotropic expansion of the plant cell wall. Annu Rev Cell Dev Biol 2005, 21:203–222.
Sampedro, J, Cosgrove, DJ. The expansin superfamily. Genome Biol 2005, 6:242.
Cho, HT, Cosgrove, DJ. Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana. Proc Natl Acad Sci U S A 2000, 97:9783–9788.
Savaldi‐Goldstein, S, Peto, C, Chory, J. The epidermis both drives and restricts plant shoot growth. Nature 2007, 446:199–202.
Ohnishi, T, Szatmari, AM, Watanabe, B, Fujita, S, Bancos, S, Koncz, C, Lafos, M, Shibata, K, Yokota, T, Sakata, K, et al. C‐23 hydroxylation by Arabidopsis CYP90C1 and CYP90D1 reveals a novel shortcut in brassinosteroid biosynthesis. Plant Cell 2006, 18:3275–3288.
Berger, Y, Harpaz‐Saad, S, Brand, A, Melnik, H, Sirding, N, Alvarez, JP, Zinder, M, Samach, A, Eshed, Y, Ori, N. The NAC‐domain transcription factor GOBLET specifies leaflet boundaries in compound tomato leaves. Development 2009, 136:823–832.
Hasson, A, Plessis, A, Blein, T, Adroher, B, Grigg, S, Tsiantis, M, Boudaoud, A, Damerval, C, Laufs, P. Evolution and diverse roles of the CUP‐SHAPED COTYLEDON genes in Arabidopsis leaf development. Plant Cell 2011, 23:54–68.
Bilsborough, GD, Runions, A, Barkoulas, M, Jenkins, HW, Hasson, A, Galinha, C, Laufs, P, Hay, A, Prusinkiewicz, P, Tsiantis, M. Model for the regulation of Arabidopsis thaliana leaf margin development. Proc Natl Acad Sci U S A 2011, 108:3424–3429.
Hay, A, Barkoulas, M, Tsiantis, M. ASYMMETRIC LEAVES1 and auxin activities converge to repress BREVIPEDICELLUS expression and promote leaf development in Arabidopsis. Development 2006, 133:3955–3961.
Kawamura, E, Horiguchi, G, Tsukaya, H. Mechanisms of leaf tooth formation in Arabidopsis. Plant J 2010, 62:429–441.
Jay, F, Wang, Y, Yu, A, Taconnat, L, Pelletier, S, Colot, V, Renou, JP, Voinnet, O. Misregulation of AUXIN RESPONSE FACTOR 8 underlies the developmental abnormalities caused by three distinct viral silencing suppressors in Arabidopsis. PLoS Pathog 2011, 7:e1002035.
Kerstetter, RA, Poethig, RS. The specification of leaf identity during shoot development. Annu Rev Cell Dev Biol 1998, 14:373–398.
Tsukaya, H, Shoda, K, Kim, GT, Uchimiya, H. Heteroblasty in Arabidopsis thaliana (L.) Heynh. Planta 2000, 210:536–542.
Tsukaya, H. The leaf index: heteroblasty, natural variation, and the genetic control of polar processes of leaf expansion. Plant Cell Physiol 2002, 43:372–378.
Usami, T, Horiguchi, G, Yano, S, Tsukaya, H. 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 2009, 136:955–964.
Wu, G, Poethig, RS. Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 2006, 133:3539–3547.
Wu, G, Park, MY, Conway, SR, Wang, JW, Weigel, D, Poethig, RS. The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 2009, 138:750–759.
Chien, JC, Sussex, IM. Differential regulation of trichome formation on the adaxial and abaxial leaf surfaces by gibberellins and photoperiod in Arabidopsis thaliana (L.) Heynh. Plant Physiol 1996, 111:1321–1328.
Telfer, A, Bollman, KM, Poethig, RS. Phase change and the regulation of trichome distribution in Arabidopsis thaliana. Development 1997, 124:645–654.
Chuck, G, Cigan, AM, Saeteurn, K, Hake, S. The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nat Genet 2007, 39:544–549.
Wang, JW, Schwab, R, Czech, B, Mica, E, Weigel, D. Dual effects of miR156‐targeted SPL genes and CYP78A5/KLUH on plastochron length and organ size in Arabidopsis thaliana. Plant Cell 2008, 20:1231–1243.
Wang, JW, Czech, B, Weigel, D. miR156‐regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 2009, 138:738–749.
Schmid, M, Uhlenhaut, NH, Godard, F, Demar, M, Bressan, R, Weigel, D, Lohmann, JU. Dissection of floral induction pathways using global expression analysis. Development 2003, 130:6001–6012.
Wang, JW, Park, MY, Wang, LJ, Koo, Y, Chen, XY, Weigel, D, Poethig, RS. miRNA control of vegetative phase change in trees. PLoS Genet 2011, 7:e1002012.
Shikata, M, Koyama, T, Mitsuda, N, Ohme‐Takagi, M. Arabidopsis SBP‐box genes SPL10, SPL11 and SPL2 control morphological change in association with shoot maturation in the reproductive phase. Plant Cell Physiol 2009, 50:2133–2145.
Perez‐Perez, JM, Serrano‐Cartagena, J, Micol, JL. Genetic analysis of natural variations in the architecture of Arabidopsis thaliana vegetative leaves. Genetics 2002, 162:893–915.
Weigel, D. Natural variation in Arabidopsis: from molecular genetics to ecological genomics. Plant Physiol 2012, 158:2–22.
Juenger, TE, Sen, S, Stowe, KA, Simms, EL. Epistasis and genotype‐environment interaction for quantitative trait loci affecting flowering time in Arabidopsis thaliana. Genetica 2005, 123:87–105.
El‐Lithy, ME, Clerkx, EJ, Ruys, GJ, Koornneef, M, Vreugdenhil, D. Quantitative trait locus analysis of growth‐related traits in a new Arabidopsis recombinant inbred population. Plant Physiol 2004, 135:444–458.
Tisne, S, Reymond, M, Vile, D, Fabre, J, Dauzat, M, Koornneef, M, Granier, C. Combined genetic and modeling approaches reveal that epidermal cell area and number in leaves are controlled by leaf and plant developmental processes in Arabidopsis. Plant Physiol 2008, 148:1117–1127.
Ichihashi, Y, Kawade, K, Usami, T, Horiguchi, G, Takahashi, T, Tsukaya, H. Key proliferative activity in the junction between the leaf blade and leaf petiole of Arabidopsis. Plant Physiol 2011, 157:1151–1162.
Todesco, M, Balasubramanian, S, Cao, J, Ott, F, Sureshkumar, S, Schneeberger, K, Meyer, RC, Altmann, T, Weigel, D. Natural variation in biogenesis efficiency of individual Arabidopsis thaliana microRNAs. Curr Biol 2012, 22:166–170.
Todesco, M, Balasubramanian, S, Hu, TT, Traw, MB, Horton, M, Epple, P, Kuhns, C, Sureshkumar, S, Schwartz, C, Lanz, C, et al. Natural allelic variation underlying a major fitness trade‐off in Arabidopsis thaliana. Nature 2010, 465:632–636.
Stransfeld, L, Eriksson, S, Adamski, NM, Breuninger, H, Lenhard, M. KLUH/CYP78A5 promotes organ growth without affecting the size of the early primordium. Plant Signal Behav 2010, 5:982–984.
Nelissen, H, Rymen, B, Jikumaru, Y, Demuynck, K, Van Lijsebettens, M, Kamiya, Y, Inze, D, Beemster, GT. A local maximum in gibberellin levels regulates maize leaf growth by spatial control of cell division. Curr Biol 2012, 22:1183–1187.
Li, P, Ponnala, L, Gandotra, N, Wang, L, Si, Y, Tausta, SL, Kebrom, TH, Provart, N, Patel, R, Myers, CR, et al. The developmental dynamics of the maize leaf transcriptome. Nat Genet 2010, 42:1060–1067.

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