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Science 289 (5480): 779-781

Copyright © 2000 by the American Association for the Advancement of Science

Cell-Cell Signaling and Movement by the Floral Transcription Factors LEAFY and APETALA1

Allen Sessions,12* Martin F. Yanofsky,1 Detlef Weigel2dagger

LEAFY (LFY) and APETALA1 (AP1) encode unrelated transcription factors that activate overlapping sets of homeotic genes in Arabidopsis flowers. Sector analysis and targeted expression in transgenic plants were used to study whether LFY and AP1 can participate in cell-cell signaling between and within different layers of the floral meristem. LFY signaled equally well from all layers and had substantial long-range action within layers. Nonautonomous action of LFY was accompanied by movement of the protein to adjacent cells, where it directly activated homeotic target genes. In contrast, AP1 had only limited nonautonomous effects, apparently mediated by downstream genes because activation of early target genes by AP1 was cell-autonomous.

1 Department of Biology, University of California, San Diego, La Jolla, CA 92093, USA.
2 Plant Biology Laboratory, Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, CA 92037, USA.
*   Present address: Novartis Agricultural Discovery Institute, 3115 Merryfield Row, San Diego, CA 92121, USA.

dagger    To whom correspondence should be addressed. E-mail: marty{at}ucsd.edu, weigel{at}salk.edu


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   Full Text »    PDF »
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   Abstract »    Full Text »    PDF »

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