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Plant Cell Advance Online Publication
Published on May 26, 2006; 10.1105/tpc.105.039925

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Received December 5, 2005
Returned for revision April 14, 2006
Accepted May 3, 2006

A Network of Local and Redundant Gene Regulation Governs Arabidopsis Seed Maturation

Alexandra To 1, Christiane Valon 1, Gil Savino 1, Jocelyne Guilleminot 2, Martine Devic 2, Jérôme Giraudat 1, and François Parcy 3*

1 Institut des Sciences du Végétal, Unité Propre de Recherche 2355, Centre National de la Recherche Scientifique, 91190 Gif-sur-Yvette, France
2 Laboratoire Génome et Développement des Plantes, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5096, Université de Perpignan, 66860 Perpignan Cedex, France
3 Institut des Sciences du Végétal, Unité Propre de Recherche 2355, Centre National de la Recherche Scientifique, 91190 Gif-sur-Yvette, France; Instituto de Biologia Molecular y Celular de Plantas, Universidad Politécnica de Valencia, Consejo Superior de Investigaciones Científicas, 46022 Valencia, Spain; Physiologie Cellulaire Végétale, Unité Mixte de Recherche, Centre National de la Recherche Scientifique 5168, Commissariat à l'Energie Atomique, Université Joseph Fourier, Institut National de la Recherche Agronomique, 38054 Grenoble Cedex 9, France

* To whom correspondence should be addressed. E-mail: francois.parcy{at}cea.fr.

In Arabidopsis thaliana, four major regulators (ABSCISIC ACID INSENSITIVE3 [ABI3], FUSCA3 [FUS3], LEAFY COTYLEDON1 [LEC1], and LEC2) control most aspects of seed maturation, such as accumulation of storage compounds, cotyledon identity, acquisition of desiccation tolerance, and dormancy. The molecular basis for complex genetic interactions among these regulators is poorly understood. By analyzing ABI3 and FUS3 expression in various single, double, and triple maturation mutants, we have identified multiple regulatory links among all four genes. We found that one of the major roles of LEC2 was to upregulate FUS3 and ABI3. The lec2 mutation is responsible for a dramatic decrease in ABI3 and FUS3 expression, and most lec2 phenotypes can be rescued by ABI3 or FUS3 constitutive expression. In addition, ABI3 and FUS3 positively regulate themselves and each other, thereby forming feedback loops essential for their sustained and uniform expression in the embryo. Finally, LEC1 also positively regulates ABI3 and FUS3 in the cotyledons. Most of the genetic controls discovered were found to be local and redundant, explaining why they had previously been overlooked. This works establishes a genetic framework for seed maturation, organizing the key regulators of this process into a hierarchical network. In addition, it offers a molecular explanation for the puzzling variable features of lec2 mutant embryos.




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