WRINKLED1, A Ubiquitous Regulator in Oil Accumulating Tissues from Arabidopsis Embryos to Oil Palm Mesocarp

Abstract

WRINKLED1 (AtWRI1) is a key transcription factor in the regulation of plant oil synthesis in seed and non-seed tissues. The structural features of WRI1 important for its function are not well understood. Comparison of WRI1 orthologs across many diverse plant species revealed a conserved 9 bp exon encoding the amino acids “VYL”. Site-directed mutagenesis of amino acids within the ‘VYL’ exon of AtWRI1 failed to restore the full oil content of wri1-1 seeds, providing direct evidence for an essential role of this small exon in AtWRI1 function. Arabidopsis WRI1 is predicted to have three alternative splice forms. To understand expression of these splice forms we performed RNASeq of Arabidopsis developing seeds and queried other EST and RNASeq databases from several tissues and plant species. In all cases, only one splice form was detected and VYL was observed in transcripts of all WRI1 orthologs investigated. We also characterized a phylogenetically distant WRI1 ortholog (EgWRI1) as an example of a non-seed isoform that is highly expressed in the mesocarp tissue of oil palm. The C-terminal region of EgWRI1 is over 90 amino acids shorter than AtWRI1 and has surprisingly low sequence conservation. Nevertheless, the EgWRI1 protein can restore multiple phenotypes of the Arabidopsis wri1-1 loss-of-function mutant, including reduced seed oil, the “wrinkled” seed coat, reduced seed germination, and impaired seedling establishment. Taken together, this study provides an example of combining phylogenetic analysis with mutagenesis, deep-sequencing technology and computational analysis to examine key elements of the structure and function of the WRI1 plant transcription factor.

Ectopic expression of WRI1 affects fatty acid homeostasis in Brachypodium distachyon vegetative tissues

“…The gray box indicates AtWRI1 and its presumed ortholog in B. distachyon. addition, the sequence VYL present in the first AP2 domain of AtWRI1, which is essential for its function (Ma et al, 2013), was also conserved in BdWRI1 (Supplemental Fig. S1).…”

“…The Arabidopsis wri1 mutant has an 80% reduction of seed oil content (Focks and Benning, 1998), whereas overexpression of WRI1 increases seed oil content by 10% to 20% (Cernac and Benning, 2004). WRI1 orthologs from maize (Zea mays), rape (Brassica napus), and oil palm (Elaeis guineensis) have been shown to be involved in TAG production in embryos or fruit mesocarps, and their overexpression leads to increased seed oil content (Liu et al, 2010;Shen et al, 2010;Pouvreau et al, 2011;Ma et al, 2013;van Erp et al, 2014). Ectopic expression of WRI1 has also been used to stimulate oil production in nonseed tissues in both Arabidopsis and tobacco (Nicotiana tabacum; Cernac and Benning, 2004;Sanjaya et al, 2011;Dussert et al, 2013;Kelly et al, 2013;Vanhercke et al, 2014;Grimberg et al, 2015;Ma et al, 2015).…”

Overexpression of Arabidopsis WRI1 enhanced seed mass and storage oil content in Camelina sativa

“…Later, WRI1 orthologs were isolated from several crops including maize (Zea mays), rapeseed (Brassica napus), palm (Elaeis guineensis), and cotton (Gossypium spp.) (Ma et al 2013;Shen et al 2010;Pouvreau et al 2011;Qu et al 2012;Wu et al 2014). It has been reported that the seed oil contents in transgenic Arabidopsis, rapeseed, and maize overexpressing AtWRI1 or WRI1 orthologs increase by approximately 10-30 % (Cernac and Benning 2004;Liu et al 2010;Shen et al 2010;Wu et al 2014).…”

The Mediator Complex MED15 Subunit Mediates Activation of Downstream Lipid-Related Genes by the WRINKLED1 Transcription Factor

“…On the other hand, WRINKLED1 (WRI1), which is known as an important regulator in Arabidopsis seed development, specifies the activities of genes encoding most key enzymes involved in late stages of glycolysis and fatty acid biosynthesis (Focks and Benning, 1998;Baud et al, 2007;Maeo et al, 2009;Ma et al, 2013).…”