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First published online May 26, 2006; 10.1105/tpc.105.039925

The Plant Cell 18:1642-1651 (2006)
© 2006 American Society of Plant Biologists

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

Alexandra Toa,1, Christiane Valona,1, Gil Savinoa, Jocelyne Guilleminotb, Martine Devicb, Jérôme Giraudata and François Parcya,c,d,2

a Institut des Sciences du Végétal, Unité Propre de Recherche 2355, Centre National de la Recherche Scientifique, 91190 Gif-sur-Yvette, France
b Laboratoire Génome et Développement des Plantes, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5096, Université de Perpignan, 66860 Perpignan Cedex, France
c Instituto de Biologia Molecular y Celular de Plantas, Universidad Politécnica de Valencia, Consejo Superior de Investigaciones Científicas, 46022 Valencia, Spain
d 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

2 To whom correspondence should be addressed. E-mail francois.parcy{at}cea.fr; fax 33-4-38-50-91.

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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