Leaf polarity establishment and the two sets of regulators
DOI:
https://doi.org/10.14456/tjg.2012.8Keywords:
adaxial, abaxial, leaf polarity, leaf development, ArabidopsisAbstract
Proper leaf morphogenesis is evolutionarily important for higher plants in enabling them the maximum photosynthesis capacity. This complex developmental process comprises of several stages. The establishment of leaf polarity along the adaxial (doral)-abaxial (ventral) axis occurs in young leaf primordia and is critically required for subsequent leaf blade expansion. This polar patterning results in distinct anatomical and morphological structures between the upper and the lower sides of the leaf. The first recognition of leaf polarity began with a classical microsurgical study on potato shoot tips over 50 years ago. Subsequently, important leaf polarity regulators have been identified through genetic and molecular studies. This review is mainly focused on characterization of Arabidopsis key determinants that regulate leaf polarity establishment at various levels including transcription, post-transcription, translation and post-translation. Recent development in leaf polarity study is also provided.
References
Allen, E., Xie, Z., Gustafson, A.M., Carrington, J.C. 2005. microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121: 207–221.
Bailey-Serres, J. 1998. A Look Beyond Transcription: Mechanisms Determining mRNA Stability and Translation in Plants, American Society of Plant Physiologists, Rockville.
Baima, S., Possenti, M., Matteucci, A., Wisman, E., Altamura, M.M., Ruberti, I., Morelli, G. 2001. The Arabidopsis ATHB-8 HD-ZIP protein acts as a differentiation-promoting transcription factor of the vascular meristems. Plant Physiol 126: 643–655.
Barakat, A., Szick-Miranda, K., Chang, I.F., Guyot, R., Blanc, G., Cooke, R., Delseny, M., Bailey-Serres, J. 2001. The organization of cytoplasmic ribosomal protein genes in the Arabidopsis genome. Plant Physiol 127: 398–415.
Byrne, M.E., Barley, R., Curtis, M., Arroyo, J.M., Dunham, M., Hudson, A., Martienssen, R.A. 2000. Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 408: 967–971.
Emery, J.F., Floyd, S.K., Alvarez, J., Eshed, Y., Hawker, N.P., Izhaki, A., Baum, S.F., Bowman, J.L. 2003. Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr Biol 13: 1768–1774.
Eshed, Y., Baum, S.F., Perea, J.V., Bowman, J.L. 2001. Establishment of polarity in lateral organs of plants. Curr Biol 11: 1251–1260.
Eshed, Y., Izhaki, A., Baum, S.F., Floyd, S.K., Bowman, J.L. 2004. Asymmetric leaf development and blade expansion in Arabidopsis are mediated by KANADI and YABBY activities. Development 131: 2997–3006.
Franks, R.G., Wang, C., Levin, J.Z., Liu, Z. 2006. SEUSS and LEUNIG regulate cell proliferation, vascular development and organ polarity in Arabidopsis petals. Planta 224: 801–811.
Hunter, C., Willmann, M.R., Wu, G., Yoshikawa, M., de la Luz Gutiérrez-Nava, M., Poethig, S.R. 2006. trans-acting siRNA-mediated repression of ETTIN and ARF4 regulates heteroblasty in Arabidopsis. Development 133: 2973–2981.
Husbands, A.Y., Chitwood, D.H., Plavskin, Y., Timmermans, M.C.P. 2009. Signals and prepatterns: new insights into organ polarity in plants. Genes Dev 23: 1986–1997.
Kerstetter, R.A., Bollman, K., Taylor, R.A., Bomblies, K., Poethig, R.S. 2001. KANADI regulates organ polarity in Arabidopsis. Nature 411: 706–709.
Kidner, C.A. and Martienssen, R.A. 2004. Spatially restricted microRNA directs leaf polarity through ARGONAUTE1. Nature 428: 81–84.
Kim, Y.-S., Kim, S.-G., Lee, M., Lee, I., Park, H.-Y., Seo, P.J., Jung, J.-H., Kwon, E.-J., Suh, S.W., Paek, K.-H., Park, C.-M. 2008. HD-ZIP III activity is modulated by competitive inhibitors via a feedback loop in Arabidopsis shoot apical meristem development. Plant Cell 20: 920–933.
Li, H., Xu, L., Wang, H., Yuan, Z., Cao, X., Yang, Z., Zhang, D., Xu, Y., Huang, H. 2005. The putative RNA-dependent RNA polymerase RDR6 acts synergistically with ASYMMETRIC LEAVES1 and 2 to repress BREVIPEDICELLUS and microRNA165/166 in Arabidopsis Leaf Development. Plant Cell 17: 2157–2171.
Lin, W.C., Shuai, B., Springer, P.S. 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: 2241–2252.
McConnell, J.R. and Barton, M.K. 1998. Leaf polarity and meristem formation in Arabidopsis. Development 125: 2935–2942.
McConnell, J.R., Emery, J., Eshed, Y., Bao, N., Bowman, J., Barton, M.K. 2001. Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411: 709–713.
Nakata, M., Matsumoto, N., Tsugeki, R., Rikirsch, 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: 519–535.
Pekker, I., Alvarez, J.P., Eshed, Y. 2005. Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 17: 2899–2910.
Pinon, V., Etchells, J.P., Rossignol, P., Collier, S.A., Arroyo, J.M., Martienssen, R.A., Byrne, M.E. 2008. Three PIGGYBACK genes that specifically influence leaf patterning encode ribosomal proteins. Development 135: 1315–1324.
Prigge, M.J., Otsuga, D., Alonso, J.M., Ecker, J.R., Drews, G.N., Clark, S.E. 2005. Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 17: 61–76.
Reinhardt, D., Frenz, M., Mandel, T., Kuhlemeier, C. 2005. Microsurgical and laser ablation analysis of leaf positioning and dorsoventral patterning in tomato. Development 132: 15–26.
Siegfried, K.R., Eshed, Y., Baum, S.F., Otsuga, D., Drews, G.N., Bowman, J.L. 1999. Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 126: 4117–4128.
Stahle, M., Kuehlich, J., Staron, L., von Amim, A.G., Golz, J. 2009. YABBYs and the transcriptional corepressors LEUNIG and LEUNIG_HOMOLOG maintain leaf polarity and meristem activity in Arabidopsis. Plant Cell 21: 3105–3118.
Sussex, I.M. 1955. Morphogenesis in Solanum tuberosum L.: experimental investigation of leaf dorsoventrality and orientation in the juvenile shoot. Phytomorphology 5: 286–300.
Talbert, P.B., Adler, H.T., Parks, D.W., Comai, L. 1995. The REVOLUTA gene is necessary for apical meristem development and for limiting cell divisions in the leaves and stems of Arabidopsis thaliana. Development 121: 2723–2735.
Tiwari, S.B., Hagen, G., Guilfoyle, T. 2003. The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15: 533–543.
Vaucheret, H., Vazquez, F., Crété, P., Bartel, D.P. 2004. The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev 18: 1187–1197.
Waites, R. and Hudson, A. 1995. phantastica: a gene required for dorsoventrality of leaves in Antirrhinum majus. Development 121: 2143–2154.
Waites, R., Selvadurai, H.R., Oliver, I.R., Hudson, A. 1998. The PHANTASTICA gene encodes a MYB transcription factor involved in growth and dorsoventrality of lateral organs in Antirrhinum. Cell 93: 779–789.
Wenkel, S., Emery, J., Hou, B.H., Evans, M.M., Barton, M.K. 2007. A feedback regulatory module formed by LITTLE ZIPPER and HD-ZIPIII genes. Plant Cell 19: 3379–3390.
Williams, L., Grigg, S.P., Xie, M., Christensen, S., Fletcher, J.C. 2005. Regulation of Arabidopsis shoot apical meristem and lateral organ formation by microRNA miR166g and its AtHD-ZIP target genes. Development 132: 3657–3668.
Wu, G., Lin, W.C., Huang, T., Poethig, R.S., Springer, P.S., Kerstetter, R.A. 2008. KANADI1 regulates adaxial-abaxial polarity in Arabidopsis by directly repressing the transcription of ASYMMETRIC LEAVES2. Proc Natl Acad Sci USA 105: 16392–16397.
Xu, L., Xu, Y., Dong, A., Sun, Y., Pi, L., Huang, H. 2003. Novel as1 and as2 defects in leaf adaxial-abaxial polarity reveal the requirement for ASYMMETRIC LEAVES1 and 2 and ERECTA functions in specifying leaf adaxial identity. Development 130: 4097–4107.
Yao, Y., Ling, Q., Wang, H., Huang, H. 2008. Ribosomal proteins promote leaf adaxial identity. Development 135: 1325–1334.
Yuan, Z., Luo, D., Li, G., Yao, X., Wang, H., Zeng, M., Huang, H., Cui, X. 2010. Characterization of the AE7 gene in Arabidopsis suggests that normal cell proliferation is essential for leaf polarity establishment. Plant J 64: 331–342.