WRINKLED1 specifies the regulatory action of LEAFY COTYLEDON2 towards fatty acid metabolism during seed maturation in Arabidopsis

Abstract

SummaryThe WRINKLED1 (WRI1) transcription factor has been shown to play a role of the utmost importance during oil accumulation in maturing seeds of Arabidopsis thaliana. However, little is known about the regulatory processes involved. In this paper, comprehensive functional analyses of three new mutants corresponding to null alleles of wri1 confirm that the induction of WRI1 is a prerequisite for fatty acid synthesis and is important for normal embryo development. The strong expression of WRI1 specifically detected at the onset of the maturation phase in oil-accumulating tissues of A. thaliana seeds is fully consistent with this function. Complementation experiments carried out with various seed-specific promoters emphasized the importance of a tight regulation of WRI1 expression for proper oil accumulation, raising the question of the factors controlling WRI1 transcription. Interestingly, molecular and genetic analyses using an inducible system demonstrated that WRI1 is a target of LEAFY COTYLEDON2 and is necessary for the regulatory action of LEC2 towards fatty acid metabolism. In addition to this, quantitative RT-PCR experiments suggested that several genes encoding enzymes of late glycolysis, the fatty acid synthesis pathway, and the biotin and lipoic acid biosynthetic pathways are targets of WRI1. Taken together, these results indicate new relationships in the regulatory model for the control of oil synthesis in maturing A. thaliana seeds. In addition, they exemplify how metabolic and developmental processes affecting the developing embryo can be coordinated at the molecular level.

Enhanced Seed Oil Production in Canola by Conditional Expression of Brassica napus LEAFY COTYLEDON1 and LEC1-LIKE in Developing Seeds

“…S6). Consistent with these results, expression of canola WRI1 (BnWRI1), an ortholog of the Arabidopsis WRI1 gene that plays a critical role in regulating glycolysis and lipid biosynthesis (Focks and Benning, 1998;Cernac and Benning, 2004;Baud et al, 2007), was also increased in developing seeds of the BnLEC1 transgenic plants (Fig. 5).…”

“…AtLEC1, encoding an NF-YBtype transcription factor and acting in a pathway independent from that of LEC2 (Lotan et al, 1998;Cernac et al, 2006), positively regulates WRI1 and a large repertoire of FA synthetic genes and several glycolytic genes (Baud et al, 2007;Mu et al, 2008). Overexpression of these genes results in an increased level of FAs in the transgenic Arabidopsis plants, accompanied by up-regulated expression of key FA synthetic genes as well as glycolytic genes (Stone et al, 2001;Kwong et al, 2003;Cernac and Benning, 2004;Baud et al, 2007;Mu et al, 2008). However, in most, if not all cases, overexpression of these transcription factor genes causes a variety of developmental abnormalities and even lethality (Lotan et al, 1998;Stone et al, 2001;Cernac and Benning, 2004;Wang et al, 2007;Mu et al, 2008;Shen et al, 2010).…”

“…WRI1, encoding an AP2/EREBP transcription factor, regulates a subset of genes involved in glycolysis and the incorporation of Suc into TAG (Focks and Benning, 1998;Cernac and Benning, 2004). LEC2 encodes a plant-specific B3-type transcription factor and directly regulates WRI1, which, in turn controls a subset of late glycolytic genes and FA synthetic genes (Stone et al, 2001;Baud et al, 2007). AtLEC1, encoding an NF-YBtype transcription factor and acting in a pathway independent from that of LEC2 (Lotan et al, 1998;Cernac et al, 2006), positively regulates WRI1 and a large repertoire of FA synthetic genes and several glycolytic genes (Baud et al, 2007;Mu et al, 2008).…”

“…LEC2 encodes a plant-specific B3-type transcription factor and directly regulates WRI1, which, in turn controls a subset of late glycolytic genes and FA synthetic genes (Stone et al, 2001;Baud et al, 2007). AtLEC1, encoding an NF-YBtype transcription factor and acting in a pathway independent from that of LEC2 (Lotan et al, 1998;Cernac et al, 2006), positively regulates WRI1 and a large repertoire of FA synthetic genes and several glycolytic genes (Baud et al, 2007;Mu et al, 2008). Overexpression of these genes results in an increased level of FAs in the transgenic Arabidopsis plants, accompanied by up-regulated expression of key FA synthetic genes as well as glycolytic genes (Stone et al, 2001;Kwong et al, 2003;Cernac and Benning, 2004;Baud et al, 2007;Mu et al, 2008).…”

Predictive Modeling of Biomass Component Tradeoffs in Brassica napus Developing Oilseeds Based on in Silico Manipulation of Storage Metabolism

“…In addition to FUS3 and ABI3, LEC2 appears to have control over WRINKLED1 (WRI1), which has been studied in great detail and has been shown to regulate storage lipid synthesis specifically at late glycolytic steps and early lipid biosynthesis (Focks and Benning, 1998;Ruuska et al, 2002;Cernac and Benning, 2004;Baud and Graham, 2006;Baud et al, 2007Baud et al, , 2009Maeo et al, 2009). Overexpression of rapeseed homologs of WRI1 in Arabidopsis resulted in increased oil content and enlarged seed size (Liu et al, 2010).…”