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First published online December 10, 2008; 10.1104/pp.108.130765

Plant Physiology 149:841-850 (2009)
© 2009 American Society of Plant Biologists

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DEVELOPMENT AND HORMONE ACTION

Tissue Specificity and Evolution of Meristematic WOX3 Function1,[W],[OA]

Rena Shimizu2, Jiabing Ji2, Eric Kelsey, Kazuhiro Ohtsu, Patrick S. Schnable and Michael J. Scanlon*

Department of Plant Biology, Cornell University, Ithaca, New York 14853 (R.S., E.K., M.J.S.); Plant Biology Department, University of Georgia, Athens, Georgia 30602 (J.J.); and Center for Plant Genomics, Iowa State University, Ames, Iowa 50011 (K.O., P.S.S.)

The WUSCHEL-related homeobox (WOX) gene PRESSED FLOWER1 (PRS1) performs a conserved function during lateral organ development in Arabidopsis (Arabidopsis thaliana). Expressed in the periphery of the shoot meristem, PRS1 recruits founder cells that form lateral domains of vegetative and floral organs. Null mutations in PRS1 cause the deletion of lateral stipules from leaves and of lateral sepals and stamens from flowers. Although PRS1 expression is described in the L1 layer, PRS1 recruits founder cells from all meristem layers. The mechanism of non-cell autonomous PRS1 function and the evolution of disparate WOX gene functions are investigated herein. Meristem layer-specific promoters reveal that both L1 and L1-L2 expression of PRS1 fail to fully rescue PRS1 function, and PRS1 protein does not traffic laterally or transversely between shoot meristem layers. PRS1 protein accumulates within all meristematic cell layers (L1-L2-L3) when expressed from the native promoter, presumably due to low-level transcription in the L2 and L3 layers. When driven from the PRS1 promoter, full rescue of vegetative and floral prs1 mutant phenotypes is provided by WUSCHEL1 (WUS1), which is normally expressed in the stem cell organizing center of shoot meristems. The data reveal that WUS1 and PRS1 can engage in equivalent protein-protein interactions and direct transcription of conserved target genes, suggesting that their subfunctionalization has evolved primarily via diverse promoter specificity. Unexpectedly, these results also suggest that meristematic stem cells and lateral organ founder cells are intrinsically similar and formed via equivalent processes such that their ultimate fate is dependent upon stage-specific and domain-specific positional signaling.


1 This work was supported by the National Science Foundation (grant nos. IBN–517070, IBN–0649810, and PGRP–032195 to M.J.S.).

2 These authors contributed equally to the article.

The author responsible for the distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Michael J. Scanlon (mjs298{at}cornell.edu).

[W] The online version of this article contains Web-only data.

[OA] Open access articles can be viewed online without a subscription.

www.plantphysiol.org/cgi/doi/10.1104/pp.108.130765

* Corresponding author; e-mail mjs298{at}cornell.edu.

Received October 3, 2008; accepted December 3, 2008; published December 10, 2008.




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J. Nardmann, P. Reisewitz, and W. Werr
Discrete Shoot and Root Stem Cell-Promoting WUS/WOX5 Functions Are an Evolutionary Innovation of Angiosperms
Mol. Biol. Evol., August 1, 2009; 26(8): 1745 - 1755.
[Abstract] [Full Text] [PDF]




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