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GENETICS, GENOMICS, AND MOLECULAR EVOLUTION

Epistatic Interactions between Opaque2 Transcriptional Activator and Its Target Gene CyPPDK1 Control Kernel Trait Variation in Maize^{1,[C],[W],[OA]}

University Paris-Sud, UMR 0320/UMR 8120 Génétique Végétale, F–91190 Gif sur Yvette, France (D.M.); INRA, UMR 0320/UMR 8120 Génétique Végétale, F–91190 Gif sur Yvette, France (L.C.-K., S.B., A.R., A.C.); Groupe Biogemma, ZI du Brézet, F–63028 Clermont-Ferrand cedex 2, France (M.F., C.A., L.C., L.F., A.M.); Groupe Limagrain, Domaine de Mons, F–63200 Aubiat, France (N.F.); INRA, UMR 0206 Chimie Biologique, F–78850 Thiverval-Grignon, France (V.M.); University Paris-Sud, UMR 8618 Institut de Biotechnologie des Plantes, F–91405 Orsay, France (J.-L.P.); and CNRS, UMR 0320/UMR 8120 Génétique Végétale, F–91190 Gif sur Yvette, France (C.D.)

Association genetics is a powerful method to track gene polymorphisms responsible for phenotypic variation, since it takes advantage of existing collections and historical recombination to study the correlation between large genetic diversity and phenotypic variation. We used a collection of 375 maize (Zea mays ssp. mays) inbred lines representative of tropical, American, and European diversity, previously characterized for genome-wide neutral markers and population structure, to investigate the roles of two functionally related candidate genes, Opaque2 and CyPPDK1, on kernel quality traits. Opaque2 encodes a basic leucine zipper transcriptional activator specifically expressed during endosperm development that controls the transcription of many target genes, including CyPPDK1, which encodes a cytosolic pyruvate orthophosphate dikinase. Using statistical models that correct for population structure and individual kinship, Opaque2 polymorphism was found to be strongly associated with variation of the essential amino acid lysine. This effect could be due to the direct role of Opaque2 on either zein transcription, zeins being major storage proteins devoid of lysine, or lysine degradation through the activation of lysine ketoglutarate reductase. Moreover, we found that a polymorphism in the Opaque2 coding sequence and several polymorphisms in the CyPPDK1 promoter nonadditively interact to modify both lysine content and the protein-versus-starch balance, thus revealing the role in quantitative variation in plants of epistatic interactions between a transcriptional activator and one of its target genes.

The author responsible for 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: Domenica Manicacci (manicacci{at}moulon.inra.fr).

^[C] Some figures in this article are displayed in color online but in black and white in the print edition.

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

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www.plantphysiol.org/cgi/doi/10.1104/pp.108.131888

^* Corresponding author; e-mail manicacci{at}moulon.inra.fr.

Received October 30, 2008; accepted March 23, 2009; published March 27, 2009.

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