The Leaf Adaxial-Abaxial Boundary and Lamina Growth
Abstract
:1. Introduction
2. Histological Aspects of the Adaxial-Abaxial Boundary of the Leaf
3. The Regulators of the Adaxial-Abaxial Patterning of the Leaf
4. Lamina Growth and Its Regulators
5. The Regulation of Lamina Growth and Margin Formation at the Adaxial-Abaxial Boundary
6. Maintenance of the Adaxial-Abaxial Pattern during Lamina Growth
7. Conclusion and Future Perspectives
Acknowledgments
Conflict of Interest
References
- Blair, S.S. Developmental biology: Boundary lines. Nature 2003, 424, 379–381. [Google Scholar] [CrossRef]
- Dahmann, C.; Basler, K. Compartment boundaries: At the edge of development. Trends Genet. 1999, 15, 320–326. [Google Scholar] [CrossRef]
- Dahmann, C.; Oates, A.C.; Brand, M. Boundary formation and maintenance in tissue development. Nat. Rev. Genet. 2011, 12, 43–55. [Google Scholar] [CrossRef]
- Irvine, K.D. Fringe, Notch, and making developmental boundaries. Curr. Opin. Genet. Dev. 1999, 9, 434–441. [Google Scholar] [CrossRef]
- Irvine, K.D.; Rauskolb, C. Boundaries in development: Formation and function. Annu. Rev. Cell. Dev. Biol. 2001, 17, 189–214. [Google Scholar] [CrossRef]
- Kicheva, A.; Pantazis, P.; Bollenbach, T.; Kalaidzidis, Y.; Bittig, T.; Julicher, F.; Gonzalez-Gaitan, M. Kinetics of morphogen gradient formation. Science 2007, 315, 521–525. [Google Scholar] [CrossRef]
- Klein, T. Wing disc development in the fly: The early stages. Curr. Opin. Genet. Dev. 2001, 11, 470–475. [Google Scholar] [CrossRef]
- Wartlick, O.; Mumcu, P.; Kicheva, A.; Bittig, T.; Seum, C.; Julicher, F.; Gonzalez-Gaitan, M. Dynamics of Dpp signaling and proliferation control. Science 2011, 331, 1154–1159. [Google Scholar] [CrossRef]
- Kato, K.; Orii, H.; Watanabe, K.; Agata, K. Dorsal and ventral positional cues required for the onset of planarian regeneration may reside in differentiated cells. Dev. Biol. 2001, 233, 109–121. [Google Scholar] [CrossRef]
- Major, R.J.; Irvine, K.D. Localization and requirement for Myosin II at the dorsal-ventral compartment boundary of the Drosophila wing. Dev. Dyn. 2006, 235, 3051–3058. [Google Scholar] [CrossRef]
- Landsberg, K.P.; Farhadifar, R.; Ranft, J.; Umetsu, D.; Widmann, T.J.; Bittig, T.; Said, A.; Julicher, F.; Dahmann, C. Increased cell bond tension governs cell sorting at the Drosophila anteroposterior compartment boundary. Curr. Biol. 2009, 19, 1950–1955. [Google Scholar] [CrossRef]
- Canela-Xandri, O.; Sagues, F.; Casademunt, J.; Buceta, J. Dynamics and mechanical stability of the developing dorsoventral organizer of the wing imaginal disc. PLoS Comput. Biol. 2011, 7, e1002153. [Google Scholar] [CrossRef] [Green Version]
- Aliee, M.; Roper, J.C.; Landsberg, K.P.; Pentzold, C.; Widmann, T.J.; Julicher, F.; Dahmann, C. Physical mechanisms shaping the Drosophila dorsoventral compartment boundary. Curr. Biol. 2012, 22, 967–976. [Google Scholar] [CrossRef]
- Aida, M.; Tasaka, M. Genetic control of shoot organ boundaries. Curr. Opin. Plant Biol. 2006, 9, 72–77. [Google Scholar] [CrossRef]
- Blein, T.; Hasson, A.; Laufs, P. Leaf development: What it needs to be complex. Curr. Opin. Plant Biol. 2010, 13, 75–82. [Google Scholar] [CrossRef]
- Rast, M.I.; Simon, R. The meristem-to-organ boundary: More than an extremity of anything. Curr. Opin. Genet. Dev. 2008, 18, 287–294. [Google Scholar] [CrossRef]
- Townsley, B.T.; Sinha, N.R. A new development: Evolving concepts in leaf ontogeny. Annu. Rev. Plant Biol. 2012, 63, 535–562. [Google Scholar] [CrossRef]
- Bowman, J.L.; Eshed, Y.; Baum, S.F. Establishment of polarity in angiosperm lateral organs. Trends Genet. 2002, 18, 134–141. [Google Scholar] [CrossRef]
- Chitwood, D.H.; Guo, M.; Nogueira, F.T.S.; Timmermans, M.C.P. Establishing leaf polarity: The role of small RNAs and positional signals in the shoot apex. Development 2007, 134, 813–823. [Google Scholar] [CrossRef]
- Husbands, A.Y.; Chitwood, D.H.; Plavskin, Y.; Timmermans, M.C. Signals and prepatterns: New insights into organ polarity in plants. Genes Dev. 2009, 23, 1986–1997. [Google Scholar] [CrossRef]
- Yamaguchi, T.; Nukazuka, A.; Tsukaya, H. Leaf adaxial-abaxial polarity specification and lamina outgrowth: Evolution and development. Plant Cell Physiol. 2012, 53, 1180–1194. [Google Scholar] [CrossRef]
- Timmermans, M.; Schultes, N.; Jankovsky, J.; Nelson, T. Leafbladeless1 is required for dorsoventrality of lateral organs in maize. Development 1998, 125, 2813–2823. [Google Scholar]
- Waites, R.; Hudson, A. phantastica: A gene required for dorsoventrality of leaves in Antirrhinum majus. Development 1995, 121, 2143. [Google Scholar]
- Poethig, R.; Sussex, I. The developmental morphology and growth dynamics of the tobacco leaf. Planta 1985, 165, 158–169. [Google Scholar] [CrossRef]
- Mchale, N.; Marcotrigiano, M. LAM1 is required for dorsoventrality and lateral growth of the leaf blade in Nicotiana. Development 1998, 125, 4235. [Google Scholar]
- Sawa, S.; Watanabe, K.; Goto, K.; Kanaya, E.; Morita, E.; 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. [Google Scholar] [CrossRef]
- Zgurski, J.M.; Sharma, R.; Bolokoski, D.A.; Schultz, E.A. Asymmetric auxin response precedes asymmetric growth and differentiation of asymmetric leaf1 and asymmetric leaf2 Arabidopsis leaves. Plant Cell 2005, 17, 77–91. [Google Scholar] [CrossRef]
- Tadege, M.; Lin, H.; Bedair, M.; Berbel, A.; Wen, J.; Rojas, C.M.; Niu, L.; Tang, Y.; Sumner, L.; Ratet, P.; et al. STENOFOLIA regulates blade outgrowth and leaf vascular patterning in Medicago truncatula and Nicotiana sylvestris. Plant Cell 2011, 23, 2125–2142. [Google Scholar] [CrossRef]
- Bremer, B.; Bremer, K.; Chase, M. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Plant J. 2009, 161, 105–121. [Google Scholar]
- Kawamura, E.; Horiguchi, G.; Tsukaya, H. Mechanisms of leaf tooth formation in Arabidopsis. Plant J. 2010, 62, 429–441. [Google Scholar] [CrossRef]
- Reinhardt, B.; Nggi, E.H.; Ller, S.M.; Bauch, M.; Wyrzykowska, J.; Kerstetter, R.; Poethig, S.; Fleming, A.J. Restoration of DWF4 expression to the leaf margin of a dwf4 mutant is sufficient to restore leaf shape but not size: The role of the margin in leaf development. Plant J. 2007, 52, 1094–1104. [Google Scholar] [CrossRef]
- Wang, W.; Xu, B.; Wang, H.; Li, J.; Huang, H.; Xu, L. YUCCA Genes are Expressed in Response to Leaf Adaxial-abaxial Juxtaposition and are Required for Leaf Margin Development. Plant Physiol. 2011, 157, 1805–1819. [Google Scholar] [CrossRef]
- McConnell, J.; Barton, M. Leaf polarity and meristem formation in Arabidopsis. Development 1998, 125, 2935–2942. [Google Scholar]
- McConnell, J.R.; Emery, J.; Eshed, Y.; Bao, N.; Bowman, J.; Barton, M.K. Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 2001, 411, 709–713. [Google Scholar] [CrossRef]
- Otsuga, D.; DeGuzman, B.; Prigge, M.J.; Drews, G.N.; Clark, S.E. REVOLUTA regulates meristem initiation at lateral positions. Plant J. 2001, 25, 223–236. [Google Scholar] [CrossRef]
- Prigge, M.J.; Otsuga, D.; Alonso, J.M.; Ecker, J.R.; Drews, G.N.; Clark, S.E. Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 2005, 17, 61–76. [Google Scholar] [CrossRef]
- Iwakawa, H.; Iwasaki, M.; Kojima, S.; Ueno, Y.; Soma, T.; Tanaka, H.; Semiarti, E.; Machida, Y.; Machida, C. Expression of the ASYMMETRIC LEAVES2 gene in the adaxial domain of Arabidopsis leaves represses cell proliferation in this domain and is critical for the development of properly expanded leaves. Plant J. 2007, 51, 173–184. [Google Scholar] [CrossRef]
- Iwakawa, H.; Ueno, Y.; Semiarti, E.; Onouchi, H.; Kojima, S.; Tsukaya, H.; Hasebe, M.; Soma, T.; Ikezaki, M.; Machida, C.; et al. 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. 2002, 43, 467–478. [Google Scholar] [CrossRef]
- Lin, W.-C.; Shuai, B.; Springer, P.S. The Arabidopsis LATERAL ORGAN BOUNDARIES-domain gene ASYMMETRIC LEAVES2 functions in the repression of KNOX gene expression and in adaxial-abaxial patterning. Plant Cell 2003, 15, 2241–2252. [Google Scholar] [CrossRef]
- Xu, L.; Xu, Y.; Dong, A.; Sun, Y.; Pi, L.; Xu, Y.; 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. [Google Scholar] [CrossRef]
- Sarojam, R.; Sappl, P.G.; Goldshmidt, A.; Efroni, I.; Floyd, S.K.; Eshed, Y.; Bowman, J.L. Differentiating Arabidopsis shoots from leaves by combined YABBY activities. Plant Cell 2010, 22, 2113–2130. [Google Scholar] [CrossRef]
- Siegfried, K.R.; Eshed, Y.; Baum, S.F.; Otsuga, D.; Drews, G.N.; Bowman, J.L. Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 1999, 126, 4117–4128. [Google Scholar]
- Eshed, Y.; Baum, S.F.; Perea, J.V.; Bowman, J.L. Establishment of polarity in lateral organs of plants. Curr. Biol. 2001, 11, 1251–1260. [Google Scholar] [CrossRef]
- Eshed, Y.; Izhaki, A.; Baum, S.; Floyd, S.; Bowman, J. Asymmetric leaf development and blade expansion in Arabidopsis are mediated by KANADI and YABBY activities. Development 2004, 131, 2997–3006. [Google Scholar] [CrossRef]
- Kerstetter, R.A.; Bollman, K.; Taylor, R.A.; Bomblies, K.; Poethig, R.S. KANADI regulates organ polarity in Arabidopsis. Nature 2001, 411, 706–709. [Google Scholar] [CrossRef]
- Chitwood, D.H.; Nogueira, F.T.S.; Howell, M.D.; Montgomery, T.A.; Carrington, J.C.; Timmermans, M.C.P. Pattern formation via small RNA mobility. Genes Dev. 2009, 23, 549–554. [Google Scholar] [CrossRef]
- Pekker, I.; Alvarez, J.P.; Eshed, Y. Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 2005, 17, 2899–2910. [Google Scholar] [CrossRef]
- Waites, R.; Selvadurai, H.R.; Oliver, I.R.; Hudson, A. The PHANTASTICA gene encodes a MYB transcription factor involved in growth and dorsoventrality of lateral organs in Antirrhinum. Cell 1998, 93, 779–789. [Google Scholar] [CrossRef]
- Izhaki, A.; Bowman, J.L. KANADI and class III HD-Zip gene families regulate embryo patterning and modulate auxin flow during embryogenesis in Arabidopsis. Plant Cell 2007, 19, 495–508. [Google Scholar] [CrossRef]
- Emery, J.F.; Floyd, S.K.; Alvarez, J.; Eshed, Y.; Hawker, N.P.; Izhaki, A.; Baum, S.F.; Bowman, J.L. Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr. Biol. 2003, 13, 1768–1774. [Google Scholar]
- Wu, G.; Lin, W.-C.; Huang, T.; Poethig, R.S.; Springer, P.S.; Kerstetter, R.A. KANADI1 regulates adaxial–abaxial polarity in Arabidopsis by directly repressing the transcription of ASYMMETRIC LEAVES2. Proc. Natl. Acad. Sci. USA 2008, 105, 16392–16397. [Google Scholar]
- Bonaccorso, O.; Lee, J.E.; Puah, L.; Scutt, C.P.; Golz, J.F. FILAMENTOUS FLOWER controls lateral organ development by acting as both an activator and a repressor. BMC Plant Biol. 2012, 12, 176. [Google Scholar] [CrossRef]
- Kelley, D.R.; Arreola, A.; Gallagher, T.L.; Gasser, C.S. ETTIN (ARF3) physically interacts with KANADI proteins to form a functional complex essential for integument development and polarity determination in Arabidopsis. Development 2012, 139, 1105–1109. [Google Scholar] [CrossRef]
- Jun, J.H.; Ha, C.M.; Fletcher, J.C. BLADE-ON-PETIOLE1 coordinates organ determinacy and axial polarity in arabidopsis by directly activating ASYMMETRIC LEAVES2. Plant Cell 2010, 22, 62–76. [Google Scholar] [CrossRef]
- Ha, C.M.; Jun, J.H.; Nam, H.G.; Fletcher, J.C. BLADE-ON-PETIOLE 1 and 2 control Arabidopsis lateral organ fate through regulation of LOB domain and adaxial-abaxial polarity genes. Plant Cell 2007, 19, 1809–1825. [Google Scholar] [CrossRef]
- Nogueira, F.T.; Madi, S.; Chitwood, D.H.; Juarez, M.T.; Timmermans, M.C. Two small regulatory RNAs establish opposing fates of a developmental axis. Genes Dev. 2007, 21, 750–755. [Google Scholar] [CrossRef]
- Chen, X. Small RNAs and their roles in plant development. Annu. Rev. Cell Dev. Biol. 2009, 25, 21–44. [Google Scholar] [CrossRef]
- Voinnet, O. Origin, biogenesis, and activity of plant microRNAs. Cell 2009, 136, 669–687. [Google Scholar] [CrossRef]
- Kidner, C.A.; Martienssen, R.A. Spatially restricted microRNA directs leaf polarity through ARGONAUTE1. Nature 2004, 428, 81–84. [Google Scholar] [CrossRef]
- Mallory, A.; Reinhart, B.; Jones-Rhoades, M.; Tang, G. MicroRNA control of PHABULOSA in leaf development: Importance of pairing to the microRNA 5' region. EMBO J. 2004, 23, 3356–3364. [Google Scholar] [CrossRef]
- Adenot, X.; Elmayan, T.; Lauressergues, D.; Boutet, S.; Bouche, N.; Gasciolli, V.; Vaucheret, H. DRB4-dependent TAS3 trans-acting siRNAs control leaf morphology through AGO7. Curr. Biol. 2006, 16, 927–932. [Google Scholar]
- Allen, E.; Xie, Z.; Gustafson, A.M.; Carrington, J.C. microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 2005, 121, 207–221. [Google Scholar] [CrossRef]
- Fahlgren, N.; Montgomery, T.A.; Howell, M.D.; Allen, E.; Dvorak, S.K.; Alexander, A.L.; Carrington, J.C. Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr. Biol. 2006, 16, 939–944. [Google Scholar] [CrossRef]
- Garcia, D.; Collier, S.A.; Byrne, M.E.; Martienssen, R.A. Specification of leaf polarity in Arabidopsis via the trans-acting siRNA pathway. Curr. Biol. 2006, 16, 933–938. [Google Scholar] [CrossRef]
- Hunter, C.; Willmann, M.R.; Wu, G.; Yoshikawa, M.; de la Luz Gutierrez-Nava, M.; Poethig, S.R. Trans-acting siRNA-mediated repression of ETTIN and ARF4 regulates heteroblasty in Arabidopsis. Development 2006, 133, 2973–2981. [Google Scholar] [CrossRef]
- Lynn, K.; Fernandez, A.; Aida, M.; Sedbrook, J.; Tasaka, M.; Masson, P.; Barton, M.K. The PINHEAD/ZWILLE gene acts pleiotropically in Arabidopsis development and has overlapping functions with the ARGONAUTE1 gene. Development 1999, 126, 469–481. [Google Scholar]
- Zhu, H.; Hu, F.; Wang, R.; Zhou, X.; Sze, S.H.; Liou, L.W.; Barefoot, A.; Dickman, M.; Zhang, X. Arabidopsis Argonaute10 specifically sequesters miR166/165 to regulate shoot apical meristem development. Cell 2011, 145, 242–256. [Google Scholar] [CrossRef]
- Brandt, R.; Xie, Y.; Musielak, T.; Graeff, M.; Stierhof, Y.D.; Huang, H.; Liu, C.M.; Wenkel, S. Control of stem cell homeostasis via interlocking microRNA and microProtein feedback loops. Mech. Dev. 2012, 130, 25–33. [Google Scholar]
- Wenkel, S.; Emery, J.; Hou, B.H.; Evans, M.M.; Barton, M.K. A feedback regulatory module formed by LITTLE ZIPPER and HD-ZIPIII genes. Plant Cell 2007, 19, 3379–3390. [Google Scholar] [CrossRef]
- Ueno, Y.; Ishikawa, T.; Watanabe, K.; Terakura, S.; Iwakawa, H.; Okada, K.; Machida, C.; Machida, Y. Histone deacetylases and ASYMMETRIC LEAVES2 are involved in the establishment of polarity in leaves of Arabidopsis. Plant Cell 2007, 19, 445–457. [Google Scholar] [CrossRef]
- Pinon, V.; Etchells, J.P.; Rossignol, P.; Collier, S.A.; Arroyo, J.M.; Martienssen, R.A.; Byrne, M.E. Three PIGGYBACK genes that specifically influence leaf patterning encode ribosomal proteins. Development 2008, 135, 1315–1324. [Google Scholar] [CrossRef]
- Yao, Y.; Ling, Q.; Wang, H.; Huang, H. Ribosomal proteins promote leaf adaxial identity. Development 2008, 135, 1325–1334. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Horiguchi, G.; Molla-Morales, A.; Perez-Perez, J.M.; Kojima, K.; Robles, P.; Ponce, M.R.; Micol, J.L.; Tsukaya, H. Differential contributions of ribosomal protein genes to Arabidopsis thaliana leaf development. Plant J. 2011, 65, 724–736. [Google Scholar]
- Kojima, S.; Iwasaki, M.; Takahashi, H.; Imai, T.; Matsumura, Y.; Fleury, D.; van Lijsebettens, M.; Machida, Y.; Machida, C. Asymmetric leaves2 and Elongator, a histone acetyltransferase complex, mediate the establishment of polarity in leaves of Arabidopsis thaliana. Plant Cell Physiol. 2011, 52, 1259–1273. [Google Scholar] [CrossRef]
- Szakonyi, D.; Byrne, M.E. Ribosomal protein L27a is required for growth and patterning in Arabidopsis thaliana. Plant J. 2011, 65, 269–281. [Google Scholar] [CrossRef]
- Moschopoulos, A.; Derbyshire, P.; Byrne, M.E. The Arabidopsis organelle-localized glycyl-tRNA synthetase encoded by EMBRYO DEFECTIVE DEVELOPMENT1 is required for organ patterning. J. Exp. Bot. 2012, 63, 5233–5243. [Google Scholar] [CrossRef]
- Tsukaya, H.; Byrne, M.E.; Horiguchi, G.; Sugiyama, M.; van Lijsebettens, M.; Lenhard, M. How do “housekeeping” genes control organogenesis?—Unexpected new findings on the role of housekeeping genes in cell and organ differentiation. J. Plant Res. 2013, 126, 3–15. [Google Scholar] [CrossRef]
- Toyokura, K.; Watanabe, K.; Oiwaka, A.; Kusano, M.; Tameshige, T.; Tatematsu, K.; Matsumoto, N.; Tsugeki, R.; Saito, K.; Okada, K. Succinic Semialdehyde Dehydrogenase is Involved in the Robust Patterning of Arabidopsis Leaves along the Adaxial-Abaxial Axis. Plant Cell Physiol. 2011, 52, 1340–1353. [Google Scholar] [CrossRef]
- La Rota, C.; Chopard, J.; Das, P.; Paindavoine, S.; Rozier, F.; Farcot, E.; Godin, C.; Traas, J.; Moneger, F. A data-driven integrative model of sepal primordium polarity in Arabidopsis. Plant Cell 2011, 23, 4318–4333. [Google Scholar] [CrossRef]
- Steeves, T.A.; Sussex, I.M. Patterns in plant development; Cambridge University Press.: New York, NY, USA, 1989. [Google Scholar]
- Poethig, R.; Sussex, I.M. The cellular parameters of leaf development in tobacco: A clonal analysis. Planta 1985, 165, 170–184. [Google Scholar] [CrossRef]
- Donnelly, P.M.; Bonetta, D.; Tsukaya, H.; Dengler, R.E.; Dengler, N.G. Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev. Biol. 1999, 215, 407–419. [Google Scholar] [CrossRef]
- Dengler, N.G.; Tsukaya, H. Leaf morphogenesis in dicotyledons: Current issues. Int. J. Plant Sci. 2001, 162, 459–464. [Google Scholar] [CrossRef]
- Reinhardt, D.; Mandel, T.; Kuhlemeier, C. Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 2000, 12, 507–518. [Google Scholar]
- Reinhardt, D.; Wittwer, F.; Mandel, T.; Kuhlemeier, C. Localized upregulation of a new expansin gene predicts the site of leaf formation in the tomato meristem. Plant Cell 1998, 10, 1427–1437. [Google Scholar]
- Peaucelle, A.; Louvet, R.; Johansen, J.N.; Hofte, H.; Laufs, P.; Pelloux, J.; Mouille, G. Arabidopsis phyllotaxis is controlled by the methyl-esterification status of cell-wall pectins. Curr. Biol. 2008, 18, 1943–1948. [Google Scholar] [CrossRef]
- Peaucelle, A.; Braybrook, S.A.; Le Guillou, L.; Bron, E.; Kuhlemeier, C.; Hofte, H. Pectin-induced changes in cell wall mechanics underlie organ initiation in Arabidopsis. Curr. Biol. 2011, 21, 1720–1726. [Google Scholar] [CrossRef]
- Kierzkowski, D.; Nakayama, N.; Routier-Kierzkowska, A.L.; Weber, A.; Bayer, E.; Schorderet, M.; Reinhardt, D.; Kuhlemeier, C.; Smith, R.S. Elastic domains regulate growth and organogenesis in the plant shoot apical meristem. Science 2012, 335, 1096–1099. [Google Scholar] [CrossRef]
- Schnittger, A.; Grini, P.E.; Folkers, U.; Hulskamp, M. Epidermal fate map of the Arabidopsis shoot meristem. Dev. Biol. 1996, 175, 248–255. [Google Scholar] [CrossRef]
- Irish, V.F.; Sussex, I. A fate map of the Arabidopsis embryonic shoot apical meristem. Development 1992, 115, 745–753. [Google Scholar]
- Lincoln, C.; Long, J.; Yamaguchi, J.; Serikawa, K.; Hake, S. 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 1994, 6, 1859–1876. [Google Scholar]
- Nishimura, A.; Tamaoki, M.; Sato, Y.; Matsuoka, M. The expression of tobacco knotted1-type class 1 homeobox genes correspond to regions predicted by the cytohistological zonation model. Plant J. 1999, 18, 337–347. [Google Scholar] [CrossRef]
- Ori, N.; Eshed, Y.; Chuck, G.; Bowman, J.L.; Hake, S. Mechanisms that control knox gene expression in the Arabidopsis shoot. Development 2000, 127, 5523–5532. [Google Scholar]
- Sinha, N.; Hake, S. Mutant characters of knotted maize leaves are determined in the innermost tissue layers. Dev. Biol. 1990, 141, 203–210. [Google Scholar] [CrossRef]
- Smith, L.G.; Greene, B.; Veit, B.; Hake, S. A dominant mutation in the maize homeobox gene, Knotted-1, causes its ectopic expression in leaf cells with altered fates. Development 1992, 116, 21–30. [Google Scholar]
- Timmermans, M.C.; Hudson, A.; Becraft, P.W.; Nelson, T. ROUGH SHEATH2: A Myb protein that represses knox homeobox genes in maize lateral organ primordia. Science 1999, 284, 151–153. [Google Scholar] [CrossRef]
- Vollbrecht, E.; Veit, B.; Sinha, N.; Hake, S. The developmental gene Knotted-1 is a member of a maize homeobox gene family. Nature 1991, 350, 241–243. [Google Scholar] [CrossRef]
- 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. [Google Scholar]
- 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. [Google Scholar] [CrossRef]
- Ha, C.M.; Kim, G.T.; Kim, B.C.; Jun, J.H.; Soh, M.S.; Ueno, Y.; Machida, Y.; Tsukaya, H.; Nam, H.G. The BLADE-ON-PETIOLE 1 gene controls leaf pattern formation through the modulation of meristematic activity in Arabidopsis. Development 2003, 130, 161–172. [Google Scholar] [CrossRef]
- Ha, C.M.; Jun, J.H.; Fletcher, J.C. Control of Arabidopsis leaf morphogenesis through regulation of the YABBY and KNOX families of transcription factors. Genetics 2010, 186, 197–206. [Google Scholar] [CrossRef]
- Byrne, M.E.; Barley, R.; Curtis, M.; Arroyo, J.M.; Dunham, M.; Hudson, A.; Martienssen, R.A. Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 2000, 408, 967–971. [Google Scholar] [CrossRef]
- Scanlon, M.J. The polar auxin transport inhibitor N-1-naphthylphthalamic acid disrupts leaf initiation, KNOX protein regulation, and formation of leaf margins in maize. Plant Physiol. 2003, 133, 597–605. [Google Scholar] [CrossRef]
- Scanlon, M.J.; Schneeberger, R.G.; Freeling, M. The maize mutant narrow sheath fails to establish leaf margin identity in a meristematic domain. Development 1996, 122, 1683–1691. [Google Scholar]
- Scanlon, M.J. NARROW SHEATH1 functions from two meristematic foci during founder-cell recruitment in maize leaf development. Development 2000, 127, 4573–4585. [Google Scholar]
- Nardmann, J.; Ji, J.; Werr, W.; Scanlon, M.J. The maize duplicate genes narrow sheath1 and narrow sheath2 encode a conserved homeobox gene function in a lateral domain of shoot apical meristems. Development 2004, 131, 2827–2839. [Google Scholar] [CrossRef]
- Zhang, Y.; Wu, R.; Qin, G.; Chen, Z.; Gu, H.; Qu, L.J. Over-expression of WOX1 leads to defects in meristem development and polyamine homeostasis in Arabidopsis. J. Integr. Plant Biol. 2011, 53, 493–506. [Google Scholar] [CrossRef]
- Schiessl, K.; Kausika, S.; Southam, P.; Bush, M.; Sablowski, R. JAGGED controls growth anisotropyand coordination between cell sizeand cell cycle during plant organogenesis. Curr. Biol. 2012, 22, 1739–1746. [Google Scholar] [CrossRef]
- Ohno, C.K.; Reddy, G.V.; Heisler, M.G.; Meyerowitz, E.M. The Arabidopsis JAGGED gene encodes a zinc finger protein that promotes leaf tissue development. Development 2004, 131, 1111–1122. [Google Scholar] [CrossRef]
- Dinneny, J.; Yadegari, R.; Fischer, R.; Yanofsky, M. The role of JAGGED in shaping lateral organs. Development 2004, 131, 1101–1110. [Google Scholar] [CrossRef]
- Dinneny, J.R.; Weigel, D.; Yanofsky, M.F. NUBBIN and JAGGED define stamen and carpel shape in Arabidopsis. Development 2006, 133, 1645–1655. [Google Scholar] [CrossRef]
- Nakata, M.; Matsumoto, N.; Tsugeki, R.; Rikirsch, E.; Laux, T.; Okada, K. Roles of the middle domain-specific WUSCHEL-RELATED HOMEOBOX genes in early development of leaves in Arabidopsis. Plant Cell 2012, 24, 519–535. [Google Scholar] [CrossRef]
- Golz, J.; Roccaro, M.; Kuzoff, R.; Hudson, A. GRAMINIFOLIA promotes growth and polarity of Antirrhinum leaves. Development 2004, 131, 3661. [Google Scholar] [CrossRef]
- Mchale, N. LAM-1 and FAT genes control development of the leaf blade in Nicotiana sylvestris. Plant Cell 1993, 5, 1029. [Google Scholar]
- 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. [Google Scholar] [CrossRef]
- Norberg, M.; Holmlund, M.; Nilsson, O. The BLADE ON PETIOLE genes act redundantly to control the growth and development of lateral organs. Development 2005, 132, 2203–2213. [Google Scholar] [CrossRef]
- Zhuang, L.L.; Ambrose, M.; Rameau, C.; Weng, L.; Yang, J.; Hu, X.H.; Luo, D.; Li, X. 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 2012, 5, 1333–1345. [Google Scholar]
- Vandenbussche, M.; Horstman, A.; Zethof, J.; Koes, R.; Rijpkema, A.; Gerats, T. Differential recruitment of WOX transcription factors for lateral development and organ fusion in Petunia and Arabidopsis. Plant Cell 2009, 21, 2269–2283. [Google Scholar] [CrossRef]
- Matsumoto, N.; Okada, K. A homeobox gene, PRESSED FLOWER, regulates lateral axis-dependent development of Arabidopsis flowers. Genes Dev. 2001, 15, 3355–3364. [Google Scholar] [CrossRef]
- Nath, U.; Crawford, B.C.; Carpenter, R.; Coen, E. Genetic control of surface curvature. Science 2003, 299, 1404–1407. [Google Scholar] [CrossRef]
- Kuchen, E.E.; Fox, S.; de Reuille, P.B.; Kennaway, R.; Bensmihen, S.; Avondo, J.; Calder, G.M.; Southam, P.; Robinson, S.; Bangham, A.; et al. Generation of leaf shape through early patterns of growth and tissue polarity. Science 2012, 335, 1092–1096. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Narita, N.N.; Moore, S.; Horiguchi, G.; Kubo, M.; Demura, T.; Fukuda, H.; Goodrich, J.; Tsukaya, H. Overexpression of a novel small peptide ROTUNDIFOLIA4 decreases cell proliferation and alters leaf shape in Arabidopsis thaliana. Plant J. 2004, 38, 699–713. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Ichihashi, Y.; Horiguchi, G.; Gleissberg, S.; Tsukaya, H. The bHLH transcription factor SPATULA controls final leaf size in Arabidopsis thaliana. Plant Cell Physiol. 2010, 51, 252–261. [Google Scholar] [CrossRef]
- Mizukami, Y.; Fischer, R.L. Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proc. Natl. Acad. Sci. USA 2000, 97, 942–947. [Google Scholar] [CrossRef]
- Hu, Y.; Xie, Q.; Chua, N.H. The Arabidopsis auxin-inducible gene ARGOS controls lateral organ size. Plant Cell 2003, 15, 1951–1961. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Horiguchi, G.; Kim, G.T.; 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. [Google Scholar] [CrossRef]
- Lee, B.H.; Ko, J.H.; Lee, S.; Lee, Y.; Pak, J.H.; Kim, J.H. 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. [Google Scholar] [CrossRef]
- Kim, J.H.; Kende, H. A transcriptional coactivator, AtGIF1, is involved in regulating leaf growth and morphology in Arabidopsis. Proc. Natl. Acad. Sci. USA 2004, 101, 13374–13379. [Google Scholar] [CrossRef]
- Palatnik, J.F.; Allen, E.; Wu, X.; Schommer, C.; Schwab, R.; Carrington, J.C.; Weigel, D. Control of leaf morphogenesis by microRNAs. Nature 2003, 425, 257–263. [Google Scholar]
- Efroni, I.; Blum, E.; Goldshmidt, A.; Eshed, Y. A protracted and dynamic maturation schedule underlies Arabidopsis leaf development. Plant Cell 2008, 20, 2293–2306. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Autran, D.; Jonak, C.; Belcram, K.; Beemster, G.T.; Kronenberger, J.; Grandjean, O.; Inze, D.; Traas, J. Cell numbers and leaf development in Arabidopsis: A functional analysis of the STRUWWELPETER gene. EMBO J. 2002, 21, 6036–6049. [Google Scholar] [CrossRef]
- Rodriguez, R.E.; Mecchia, M.A.; Debernardi, J.M.; Schommer, C.; Weigel, D.; Palatnik, J.F. Control of cell proliferation in Arabidopsis thaliana by microRNA miR396. Development 2010, 137, 103–112. [Google Scholar] [CrossRef]
- White, D.W. PEAPOD regulates lamina size and curvature in Arabidopsis. Proc. Natl. Acad. Sci. USA 2006, 103, 13238–13243. [Google Scholar] [CrossRef]
- Li, Y.; Zheng, L.; Corke, F.; Smith, C.; Bevan, M.W. Control of final seed and organ size by the DA1 gene family in Arabidopsis thaliana. Genes Dev. 2008, 22, 1331–1336. [Google Scholar] [CrossRef]
- Xu, R.; Li, Y. Control of final organ size by Mediator complex subunit 25 in Arabidopsis thaliana. Development 2011, 138, 4545–4554. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Kawade, K.; Horiguchi, G.; Tsukaya, H. Non-cell-autonomously coordinated organ size regulation in leaf development. Development 2010, 137, 4221–4227. [Google Scholar] [CrossRef]
- Bilsborough, G.D.; Runions, A.; Barkoulas, M.; Jenkins, H.W.; 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. USA 2011, 108, 3424–3429. [Google Scholar] [CrossRef]
- Zhao, Y.; Christensen, S.K.; Fankhauser, C.; Cashman, J.R.; Cohen, J.D.; Weigel, D.; Chory, J. A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 2001, 291, 306–309. [Google Scholar] [CrossRef]
- Won, C.; Shen, X.; Mashiguchi, K.; Zheng, Z.; Dai, X.; Cheng, Y.; Kasahara, H.; Kamiya, Y.; Chory, J.; Zhao, Y. Conversion of tryptophan to indole-3-acetic acid by TRYPTOPHAN AMINOTRANSFERASES OF ARABIDOPSIS and YUCCAs in Arabidopsis. Proc. Natl. Acad. Sci. USA 2011, 108, 18518–18523. [Google Scholar] [CrossRef]
- Mashiguchi, K.; Tanaka, K.; Sakai, T.; Sugawara, S.; Kawaide, H.; Natsume, M.; Hanada, A.; Yaeno, T.; Shirasu, K.; Yao, H.; et al. The main auxin biosynthesis pathway in Arabidopsis. Proc. Natl. Acad. Sci. USA 2011, 108, 18512–18517. [Google Scholar] [CrossRef]
- Cheng, Y.; Dai, X.; Zhao, Y. Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes Dev. 2006, 20, 1790–1799. [Google Scholar] [CrossRef]
- Hu, Y.; Poh, H.M.; Chua, N.H. The Arabidopsis ARGOS-LIKE gene regulates cell expansion during organ growth. Plant J. 2006, 47, 1–9. [Google Scholar] [CrossRef]
- Lincoln, C.; Britton, J.H.; Estelle, M. Growth and development of the axr1 mutants of Arabidopsis. Plant Cell 1990, 2, 1071–1080. [Google Scholar]
- Keller, C.P.; Stahlberg, R.; Barkawi, L.S.; Cohen, J.D. Long-term inhibition by auxin of leaf blade expansion in bean and Arabidopsis. Plant Physiol. 2004, 134, 1217–1226. [Google Scholar] [CrossRef]
- Tsuge, T.; Tsukaya, H.; Uchimiya, H. Two independent and polarized processes of cell elongation regulate leaf blade expansion in Arabidopsis thaliana (L.) Heynh. Development 1996, 122, 1589–1600. [Google Scholar]
- Nakaya, M.; Tsukaya, H.; Murakami, N.; Kato, M. Brassinosteroids control the proliferation of leaf cells of Arabidopsis thaliana. Plant Cell Physiol. 2002, 43, 239–244. [Google Scholar] [CrossRef]
- Kim, G.T.; Tsukaya, H.; Uchimiya, H. The ROTUNDIFOLIA3 gene of Arabidopsis thaliana encodes a new member of the cytochrome P-450 family that is required for the regulated polar elongation of leaf cells. Genes Dev. 1998, 12, 2381–2391. [Google Scholar] [CrossRef]
- Kim, G.T.; Tsukaya, H.; Saito, Y.; Uchimiya, H. Changes in the shapes of leaves and flowers upon overexpression of cytochrome P450 in Arabidopsis. Proc. Natl. Acad. Sci. USA 1999, 96, 9433–9437. [Google Scholar] [CrossRef]
- Gonzalez, N.; de Bodt, S.; Sulpice, R.; Jikumaru, Y.; Chae, E.; Dhondt, S.; van Daele, T.; de Milde, L.; Weigel, D.; Kamiya, Y.; et al. Increased leaf size: Different means to an end. Plant Physiol. 2010, 153, 1261–1279. [Google Scholar] [CrossRef]
- Ishiwata, A.; Ozawa, M.; Nagasaki, H.; Kato, M.; Noda, Y.; Yamaguchi, T.; Nosaka, M.; Shimizu-Sato, S.; Nagasaki, A.; Maekawa, M.; et al. Two WUSCHEL-related homeobox Genes, narrow leaf2 and narrow leaf3, Control Leaf Width in Rice. Plant Cell Physiol. 2013. [Google Scholar] [CrossRef]
- Reinhardt, D.; Frenz, M.; Mandel, T.; Kuhlemeier, C. Microsurgical and laser ablation analysis of leaf positioning and dorsoventral patterning in tomato. Development 2005, 132, 15. [Google Scholar]
- Candela, H.; Johnston, R.; Gerhold, A.; Foster, T.; Hake, S. The milkweed pod1 gene encodes a KANADI protein that is required for abaxial/adaxial patterning in maize leaves. Plant Cell 2008, 20, 2073–2087. [Google Scholar] [CrossRef]
- Juarez, M.T.; Kui, J.S.; Thomas, J.; Heller, B.A.; Timmermans, M.C.P. microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 2004, 428, 84–88. [Google Scholar]
- Fu, Y.; Xu, L.; Xu, B.; Yang, L.; Ling, Q.; Wang, H.; Huang, H. Genetic interactions between leaf polarity-controlling genes and ASYMMETRIC LEAVES1 and 2 in Arabidopsis leaf patterning. Plant Cell Physiol. 2007, 48, 724–735. [Google Scholar] [CrossRef]
- McHale, N.A.; Koning, R.E. PHANTASTICA regulates development of the adaxial mesophyll in Nicotiana leaves. Plant Cell 2004, 16, 1251–1262. [Google Scholar] [CrossRef]
- Iwasaki, M.; Nitasaka, E. The FEATHERED gene is required for polarity establishment in lateral organs especially flowers of the Japanese morning glory (I pomoea nil ). Plant Mol. Biol. 2006, 62, 913–925. [Google Scholar] [CrossRef]
- Szakonyi, D.; Moschopoulos, A.; Byrne, M.E. Perspectives on leaf dorsoventral polarity. J. Plant Res. 2010, 123, 281–290. [Google Scholar] [CrossRef]
- Kim, M.; Pham, T.; Hamidi, A.; McCormick, S.; Kuzoff, R.K.; Sinha, N. Reduced leaf complexity in tomato wiry mutants suggests a role for PHAN and KNOX genes in generating compound leaves. Development 2003, 130, 4405–4415. [Google Scholar] [CrossRef]
- Tameshige, T.; Okada, K. National Institute for Basic Biology: Okazaki, Japan, 2013; Unpublished work.
- Tanaka, W.; Toriba, T.; Ohmori, Y.; Yoshida, A.; Kawai, A.; Mayama-Tsuchida, T.; Ichikawa, H.; Mitsuda, N.; Ohme-Takagi, M.; Hirano, H.Y. The YABBY gene TONGARI-BOUSHI1 is involved in lateral organ development and maintenance of meristem organization in the rice spikelet. Plant Cell 2012, 24, 80–95. [Google Scholar] [CrossRef]
- Juarez, M.T.; Twigg, R.W.; Timmermans, M.C. Specification of adaxial cell fate during maize leaf development. Development 2004, 131, 4533–4544. [Google Scholar] [CrossRef]
- Kumaran, M.K.; Bowman, J.L.; Sundaresan, V. YABBY polarity genes mediate the repression of KNOX homeobox genes in Arabidopsis. Plant Cell 2002, 14, 2761–2770. [Google Scholar] [CrossRef]
- Nole-Wilson, S.; Krizek, B.A. AINTEGUMENTA contributes to organ polarity and regulates growth of lateral organs in combination with YABBY genes. Plant Physiol. 2006, 141, 977–987. [Google Scholar] [CrossRef]
- Stahle, M.I.; Kuehlich, J.; Staron, L.; von Arnim, A.G.; Golz, J.F. YABBYs and the transcriptional corepressors LEUNIG and LEUNIG_HOMOLOG maintain leaf polarity and meristem activity in Arabidopsis. Plant Cell 2009, 21, 3105–3118. [Google Scholar] [CrossRef]
- Aloni, R.; Schwalm, K.; Langhans, M.; Ullrich, C.I. Gradual shifts in sites of free-auxin production during leaf-primordium development and their role in vascular differentiation and leaf morphogenesis in Arabidopsis. Planta 2003, 216, 841–853. [Google Scholar]
- Avsian-Kretchmer, O.; Cheng, J.C.; Chen, L.; Moctezuma, E.; Sung, Z.R. Indole acetic acid distribution coincides with vascular differentiation pattern during Arabidopsis leaf ontogeny. Plant Physiol. 2002, 130, 199–209. [Google Scholar] [CrossRef]
- Mattsson, J.; Sung, Z.R.; Berleth, T. Responses of plant vascular systems to auxin transport inhibition. Development 1999, 126, 2979–2991. [Google Scholar]
- Scarpella, E.; Marcos, D.; Friml, J.; Berleth, T. Control of leaf vascular patterning by polar auxin transport. Genes Dev. 2006, 20, 1015–1027. [Google Scholar] [CrossRef]
- Brandt, R.; Salla-Martret, M.; Bou-Torrent, J.; Musielak, T.; Stahl, M.; Lanz, C.; Ott, F.; Schmid, M.; Greb, T.; Schwarz, M.; et al. Genome-wide binding-site analysis of REVOLUTA reveals a link between leaf patterning and light-mediated growth responses. Plant J. 2012, 72, 31–42. [Google Scholar] [CrossRef]
- Nakata, M.; Okada, K. The three-domain model: A new model for the early development of leaves in Arabidopsis thaliana. Plant Signal. Behav. 2012, 7, 1423–1427. [Google Scholar] [CrossRef]
- Leibfried, A.; To, J.P.; Busch, W.; Stehling, S.; Kehle, A.; Demar, M.; Kieber, J.J.; Lohmann, J.U. WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature 2005, 438, 1172–1175. [Google Scholar]
- Ohmori, Y.; Tanaka, W.; Kojima, M.; Sakakibara, H.; Hirano, H.Y. WUSCHEL-RELATED HOMEOBOX4 is involved in meristem maintenance and is negatively regulated by the cle gene FCP1 in rice. Plant Cell 2013, 25, 229–241. [Google Scholar] [CrossRef]
- Ikeda, M.; Mitsuda, N.; Ohme-Takagi, M. Arabidopsis WUSCHEL is a bifunctional transcription factor that acts as a repressor in stem cell regulation and as an activator in floral patterning. Plant Cell 2009, 21, 3493–3505. [Google Scholar] [CrossRef]
- Lin, H.; Niu, L.; McHale, N.A.; Ohme-Takagi, M.; Mysore, K.S.; Tadege, M. Evolutionarily conserved repressive activity of WOX proteins mediates leaf blade outgrowth and floral organ development in plants. Proc. Natl. Acad. Sci. USA 2013, 110, 366–371. [Google Scholar] [CrossRef]
- Shimizu, R.; Ji, J.; Kelsey, E.; Ohtsu, K.; Schnable, P.S.; Scanlon, M.J. Tissue-specificity and evolution of meristematic WOX3 function. Plant Physiol. 2009, 149, 841–850. [Google Scholar]
- Yao, X.; Wang, H.; Li, H.; Yuan, Z.; Li, F.; Yang, L.; Huang, H. Two types of cis-acting elements control the abaxial epidermis-specific transcription of the MIR165a and MIR166a genes. FEBS Lett. 2009, 583, 3711–3717. [Google Scholar] [CrossRef]
- Carlsbecker, A.; Lee, J.Y.; Roberts, C.J.; Dettmer, J.; Lehesranta, S.; Zhou, J.; Lindgren, O.; Moreno-Risueno, M.A.; Vaten, A.; Thitamadee, S.; et al. Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 2010, 465, 316–321. [Google Scholar]
- Marin, E.; Jouannet, V.; Herz, A.; Lokerse, A.S.; Weijers, D.; Vaucheret, H.; Nussaume, L.; Crespi, M.D.; Maizel, A. MiR390, Arabidopsis TAS3 tasiRNAs, and their AUXIN RESPONSE FACTOR targets define an autoregulatory network quantitatively regulating lateral root growth. Plant Cell 2010, 22, 1104–1117. [Google Scholar] [CrossRef]
- Miyashima, S.; Honda, M.; Hashimoto, K.; Tatematsu, K.; Hashimoto, T.; Sato-Nara, K.; Okada, K.; Nakajima, K. A comprehensive expression analysis of the Arabidopsis MICRORNA165/6 gene family during embryogenesis reveals a conserved role in meristem specification and a non-cell-autonomous function. Plant Cell Physiol. 2013, 54, 375–384. [Google Scholar]
- Miyashima, S.; Koi, S.; Hashimoto, T.; Nakajima, K. Non-cell-autonomous microRNA165 acts in a dose-dependent manner to regulate multiple differentiation status in the Arabidopsis root. Development 2011, 138, 2303–2313. [Google Scholar] [CrossRef]
- Yadav, R.K.; Perales, M.; Gruel, J.; Girke, T.; Jonsson, H.; Reddy, G.V. WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes Dev 2011, 25, 2025–2030. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Nole-Wilson, S.; Azhakanandam, S.; Franks, R.G. Polar auxin transport together with aintegumenta and revoluta coordinate early Arabidopsis gynoecium development. Dev. Biol. 2010, 346, 181–195. [Google Scholar] [CrossRef]
- Yamaguchi, T.; Yano, S.; Tsukaya, H. Genetic framework for flattened leaf blade formation in unifacial leaves of Juncus prismatocarpus. Plant Cell 2010, 22, 2141–2155. [Google Scholar] [CrossRef]
- Gleissberg, S.; Groot, E.P.; Schmalz, M.; Eichert, M.; Kolsch, A.; Hutter, S. Developmental events leading to peltate leaf structure in Tropaeolum majus (Tropaeolaceae) are associated with expression domain changes of a YABBY gene. Dev. Genes Evol. 2005, 215, 313–319. [Google Scholar] [CrossRef]
- Toriba, T.; Suzaki, T.; Yamaguchi, T.; Ohmori, Y.; Tsukaya, H.; Hirano, H.Y. Distinct regulation of adaxial-abaxial polarity in anther patterning in rice. Plant Cell 2010, 22, 1452–1462. [Google Scholar] [CrossRef]
© 2013 by the authors; licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution license (http://creativecommons.org/licenses/by/3.0/).
Share and Cite
Nakata, M.; Okada, K. The Leaf Adaxial-Abaxial Boundary and Lamina Growth. Plants 2013, 2, 174-202. https://doi.org/10.3390/plants2020174
Nakata M, Okada K. The Leaf Adaxial-Abaxial Boundary and Lamina Growth. Plants. 2013; 2(2):174-202. https://doi.org/10.3390/plants2020174
Chicago/Turabian StyleNakata, Miyuki, and Kiyotaka Okada. 2013. "The Leaf Adaxial-Abaxial Boundary and Lamina Growth" Plants 2, no. 2: 174-202. https://doi.org/10.3390/plants2020174