Modes of intercellular transcription factor movement in the Arabidopsis apex

A recent and intriguing discovery in plant biology has been that some transcription factors can move between cells. In Arabidopsis thaliana, the floral identity protein LEAFY has strong non-autonomous effects when expressed in the epidermis, mediated by its movement into underlying tissue layers. By contrast, a structurally unrelated floral identity protein, APETALA1, has only limited non-autonomous effects. Using GFP fusions to monitor protein movement in the shoot apical meristem and in floral primordia of Arabidopsis, we found a strong correlation between cytoplasmic localization of proteins and their ability to move to adjacent cells. The graded distribution of several GFP fusions with their highest levels in the cells where they are produced is compatible with the notion that this movement is driven by diffusion. We also present evidence that protein movement is more restricted laterally within layers than it is from L1 into underlying layers of the Arabidopsis apex. Based on these observations, we propose that intercellular movement of transcription factors can occur in a non-targeted fashion as a result of simple diffusion. This hypothesis raises the possibility that diffusion is the default state for many macromolecules in the Arabidopsis apex, unless they are specifically retained.

[1]  D. Weigel,et al.  Signaling in plants by intercellular RNA and protein movement. , 2002, Genes & development.

[2]  D. Weigel,et al.  Regulatory Elements of the Floral Homeotic Gene AGAMOUS Identified by Phylogenetic Footprinting and Shadowing Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.009548. , 2003, The Plant Cell Online.

[3]  D. Weigel,et al.  A genetic framework for floral patterning , 1998, Nature.

[4]  P. Zambryski,et al.  Plasmodesmata signaling: many roles, sophisticated statutes. , 1999, Current opinion in plant biology.

[5]  D. Weigel,et al.  Floral determination and expression of floral regulatory genes in Arabidopsis. , 1997, Development.

[6]  Y. Matsubayashi,et al.  Peptide signals and their receptors in higher plants. , 2001, Trends in plant science.

[7]  E. Coen,et al.  Expression of floricaula in single cell layers of periclinal chimeras activates downstream homeotic genes in all layers of floral meristems. , 1995, Development.

[8]  P. Benfey,et al.  Intercellular movement of the putative transcription factor SHR in root patterning , 2001, Nature.

[9]  W. J. Lucas.  Plasmodesmata: intercellular channels for macromolecular transport in plants. , 1995, Current opinion in cell biology.

[10]  J. Glazebrook,et al.  Arabidopsis : a laboratory manual , 2002 .

[11]  D. Prasher,et al.  Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[12]  S. Hake,et al.  A dominant mutation in the maize homeobox gene, Knotted-1, causes its ectopic expression in leaf cells with altered fates. , 1992, Development.

[13]  W. J. Lucas,et al.  Selective Trafficking of KNOTTED1 Homeodomain Protein and Its mRNA Through Plasmodesmata , 1995, Science.

[14]  D. Weigel,et al.  Cell-cell signaling and movement by the floral transcription factors LEAFY and APETALA1. , 2000, Science.

[15]  P. Zambryski,et al.  Temporal and spatial regulation of symplastic trafficking during development in Arabidopsis thaliana apices. , 1999, Development.

[16]  V. Citovsky.  Tobacco mosaic virus: a pioneer of cell-to-cell movement. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[17]  W. J. Lucas,et al.  Selective Trafficking of Non-Cell-Autonomous Proteins Mediated by NtNCAPP1 , 2003, Science.

[18]  A. Roberts,et al.  Simple, but Not Branched, Plasmodesmata Allow the Nonspecific Trafficking of Proteins in Developing Tobacco Leaves , 1999, Cell.

[19]  D. Weigel,et al.  LEAFY controls floral meristem identity in Arabidopsis , 1992, Cell.

[20]  D. Weigel,et al.  Activation of a floral homeotic gene in Arabidopsis. , 1999, Science.

[21]  R. Simon,et al.  Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. , 1999, Science.

[22]  D. Weigel,et al.  The Arabidopsis thaliana MERISTEM LAYER 1 promoter specifies epidermal expression in meristems and young primordia. , 1999, The Plant journal : for cell and molecular biology.

[23]  W. J. Lucas,et al.  Plasmodesmata Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.000778. , 2002, The Plant Cell Online.

[24]  E. Truernit,et al.  Cell-to-Cell and Long-Distance Trafficking of the Green Fluorescent Protein in the Phloem and Symplastic Unloading of the Protein into Sink Tissues , 1999, Plant Cell.

[25]  V. Irish,et al.  Nuclear localization of the Arabidopsis APETALA3 and PISTILLATA homeotic gene products depends on their simultaneous expression. , 1996, Genes & development.

[26]  J. Chory,et al.  PKS1, a substrate phosphorylated by phytochrome that modulates light signaling in Arabidopsis. , 1999, Science.

[27]  W. J. Lucas,et al.  Peptide antagonists of the plasmodesmal macromolecular trafficking pathway , 2000, The EMBO journal.

[28]  W. Frommer,et al.  Macromolecular Trafficking Indicated by Localization and Turnover of Sucrose Transporters in Enucleate Sieve Elements , 1997, Science.

[29]  P. Zambryski,et al.  Non-targeted and targeted protein movement through plasmodesmata in leaves in different developmental and physiological states. , 2001, Plant physiology.

[30]  P. Zambryski,et al.  Leaf-to-shoot apex movement of symplastic tracer is restricted coincident with flowering in Arabidopsis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[31]  P. Zambryski,et al.  Subcellular localization determines the availability of non-targeted proteins to plasmodesmatal transport , 2000, Current Biology.

[32]  V. Irish,et al.  The Arabidopsis floral homeotic gene APETALA3 differentially regulates intercellular signaling required for petal and stamen development. , 2001, Development.

[33]  W. J. Lucas,et al.  Phloem long-distance transport of CmNACP mRNA: implications for supracellular regulation in plants. , 1999, Development.

[34]  B. Pickard,et al.  Changing Patterns of Localization of the Tobacco Mosaic Virus Movement Protein and Replicase to the Endoplasmic Reticulum and Microtubules during Infection , 1998, Plant Cell.

[35]  N. Sinha,et al.  Developmental Changes Due to Long-Distance Movement of a Homeobox Fusion Transcript in Tomato , 2001, Science.

[36]  P. Rinne,et al.  Symplasmic fields in the tunica of the shoot apical meristem coordinate morphogenetic events , 1998 .

[37]  Koji Goto,et al.  Complexes of MADS-box proteins are sufficient to convert leaves into floral organs , 2001, Nature.

[38]  I. Sussex,et al.  LEAFY Interacts with Floral Homeotic Genes to Regulate Arabidopsis Floral Development. , 1992, The Plant cell.

[39]  D Weigel,et al.  LEAFY expression and flower initiation in Arabidopsis. , 1997, Development.

[40]  M. Yanofsky,et al.  Activation of the Arabidopsis B Class Homeotic Genes byAPETALA1 , 2001, Plant Cell.

[41]  E. Coen,et al.  Transposon induced chimeras show that floricaula, a meristem identity gene, acts non-autonomously between cell layers. , 1995, Development.

[42]  H. Jäckle,et al.  From gradients to stripes in Drosophila embryogenesis: filling in the gaps. , 1996, Trends in genetics : TIG.

[43]  David Jackson,et al.  Intercellular trafficking of a KNOTTED1 green fluorescent protein fusion in the leaf and shoot meristem of Arabidopsis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[44]  P. Zambryski,et al.  Plasmodesmata: gatekeepers for cell-to-cell transport of developmental signals in plants. , 2000, Annual review of cell and developmental biology.

[45]  Detlef Weigel,et al.  A developmental switch sufficient for flower initiation in diverse plants , 1995, Nature.

[46]  Joanne Chory,et al.  Conservation and Innovation in Plant Signaling Pathways , 2000, Cell.

[47]  Philip N Benfey,et al.  The SHORT-ROOT Gene Controls Radial Patterning of the Arabidopsis Root through Radial Signaling , 2000, Cell.

[48]  H. Saedler,et al.  Non-cell-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking. , 1996, Development.

[49]  Hans Sommer,et al.  Ternary complex formation between the MADS‐box proteins SQUAMOSA, DEFICIENS and GLOBOSA is involved in the control of floral architecture in Antirrhinum majus , 1999, The EMBO journal.

[50]  S. Hake,et al.  Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot , 1994 .