Plants expressing a miR164-resistant CUC2 gene reveal the importance of post-meristematic maintenance of phyllotaxy in Arabidopsis

In plants, the arrangement of organs along the stem (phyllotaxy) follows a predictable pattern. Recent studies have shown that primordium position at the meristem is governed by local auxin gradients, but little is known about the subsequent events leading to the phyllotaxy along the mature stem. We show here that plants expressing a miR164-resistant CUP-SHAPED COTYLEDON2 (CUC2) gene have an abnormal phyllotactic pattern in the fully grown stem, despite the pattern of organ initiation by the meristem being normal. This implies that abnormal phyllotaxy is generated during stem growth. These plants ectopically express CUC2 in the stem, suggesting that the proper timing of CUC2 expression is required to maintain the pattern initiated in the meristem. Furthermore, by carefully comparing the phyllotaxy in the meristem and along the mature inflorescence in wild types, we show that such deviation also occurs during wild-type development, although to a smaller extent. We therefore suggest that the phyllotactic pattern in a fully grown stem results not only from the organogenetic activity of the meristem, but also from the subsequent growth pattern during stem development.

[1]  E. Coen,et al.  Separable roles of UFO during floral development revealed by conditional restoration of gene function , 2003, Development.

[2]  S. D. de Vries,et al.  The CUP-SHAPED COTYLEDON3 Gene Is Required for Boundary and Shoot Meristem Formation in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.012203. , 2003, The Plant Cell Online.

[3]  P. Prusinkiewicz,et al.  A plausible model of phyllotaxis , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Edwards Allen,et al.  P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA unction. , 2003, Developmental cell.

[5]  G. Jürgens,et al.  Local, Efflux-Dependent Auxin Gradients as a Common Module for Plant Organ Formation , 2003, Cell.

[6]  S. Clark,et al.  The Arabidopsis CLAVATA2 Gene Encodes a Receptor-like Protein Required for the Stability of the CLAVATA1 Receptor-like Kinase , 1999, Plant Cell.

[7]  Daoxiu Zhou,et al.  Arabidopsis Histone Acetyltransferase AtGCN5 Regulates the Floral Meristem Activity through the WUSCHEL/AGAMOUS Pathway* , 2003, Journal of Biological Chemistry.

[8]  C. Kuhlemeier,et al.  Auxin Regulates the Initiation and Radial Position of Plant Lateral Organs , 2000, Plant Cell.

[9]  Steven M. Clark,et al.  CLAVATA3 IS A SPECIFIC REGULATOR OF SHOOT AND FLORAL MERISTEM DEVELOPMENT AFFECTING THE SAME PROCESSES AS CLAVATA1 , 1995 .

[10]  M. Aida,et al.  Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes. , 1999, Development.

[11]  E. Dennis,et al.  amp1 ‐ a mutant with high cytokinin levels and altered embryonic pattern, faster vegetative growth, constitutive photomorphogenesis and precocious flowering , 1993 .

[12]  H Fujisawa,et al.  Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. , 1997, The Plant cell.

[13]  Elliot M. Meyerowitz,et al.  The early extra petals1 Mutant Uncovers a Role for MicroRNA miR164c in Regulating Petal Number in Arabidopsis , 2005, Current Biology.

[14]  G. Jürgens,et al.  Role of the ZWILLE gene in the regulation of central shoot meristem cell fate during Arabidopsis embryogenesis , 1998, The EMBO journal.

[15]  Pierre Barbier de Reuille,et al.  Computer simulations reveal novel properties of the cell-cell signaling network at the shoot apex in /Arabidopsis , 2005 .

[16]  K. Hibara,et al.  The CUP-SHAPED COTYLEDON1 gene of Arabidopsis regulates shoot apical meristem formation. , 2001, Development.

[17]  P. Laufs,et al.  The Balance between the MIR164A and CUC2 Genes Controls Leaf Margin Serration in Arabidopsis[W] , 2006, The Plant Cell Online.

[18]  B. Reinhart,et al.  Prediction of Plant MicroRNA Targets , 2002, Cell.

[19]  R. Simon,et al.  The ethanol switch: a tool for tissue-specific gene induction during plant development. , 2003, The Plant journal : for cell and molecular biology.

[20]  Patrick Laufs,et al.  MicroRNA regulation of the CUC genes is required for boundary size control in Arabidopsis meristems , 2004, Development.

[21]  Alessia Para,et al.  The pleiotropic mutation dar1 affects plant architecture in Arabidopsis thaliana. , 2003, Developmental biology.

[22]  T. Vernoux,et al.  PIN-FORMED 1 regulates cell fate at the periphery of the shoot apical meristem. , 2000, Development.

[23]  E. Meyerowitz,et al.  CLAVATA 3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA 1 , 1995 .

[24]  E. Meyerowitz,et al.  CLAVATA1, a regulator of meristem and flower development in Arabidopsis. , 1993, Development.

[25]  Didier Reinhardt,et al.  Regulation of phyllotaxis. , 2005, The International journal of developmental biology.

[26]  A. Groover,et al.  Phyllotactic pattern and stem cell fate are determined by the Arabidopsis homeobox gene BELLRINGER , 2003, Development.

[27]  M. Bennett,et al.  Regulation of phyllotaxis by polar auxin transport , 2003, Nature.

[28]  S. Hake,et al.  The Interaction of Two Homeobox Genes, BREVIPEDICELLUS and PENNYWISE, Regulates Internode Patterning in the Arabidopsis Inflorescence Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.012856. , 2003, The Plant Cell Online.

[29]  H. Dickinson,et al.  VAAMANA--a BEL1-like homeodomain protein, interacts with KNOX proteins BP and STM and regulates inflorescence stem growth in Arabidopsis. , 2004, Gene.

[30]  Guiliang Tang,et al.  MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5′ region , 2004 .

[31]  E. Mjolsness,et al.  An auxin-driven polarized transport model for phyllotaxis , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[32]  C. Llave,et al.  P 1 / HC-Pro , a Viral Suppressor of RNA Silencing , Interferes with Arabidopsis Development and miRNA , 2003 .