Abstract
WRINKLED1 (WRI1), a member of the APETALA2 (AP2) class of transcription factors regulates fatty acid biosynthesis and triacylglycerol (TAG) accumulation in plants. Among the four known Arabidopsis WRI1 paralogs, only WRI2 was unable to complement and restore fatty acid content in wri1-1 mutant seeds. Avocado (Persea americana) mesocarp, which accumulates 60-70% dry weight oil content, showed high expression levels for orthologs of WRI2, along with WRI1 and WRI3, during fruit development. While the role of WRI1 as a master regulator of oil biosynthesis is well-established, the function of WRI1 paralogs is poorly understood. Comprehensive and comparative in silico analyses of WRI1 paralogs from avocado (a basal angiosperm) with higher angiosperms Arabidopsis (dicot), maize (monocot) revealed distinct features. Predictive structural analyses of the WRI orthologs from these three species revealed the presence of AP2 domains and other highly conserved features, such as intrinsically disordered regions associated with predicted PEST motifs and phosphorylation sites. Additionally, avocado WRI proteins also contained distinct features that were absent in the nonfunctional Arabidopsis ortholog AtWRI2. Through transient expression assays, we demonstrated that both avocado WRI1 and WRI2 are functional and drive TAG accumulation in Nicotiana benthamiana leaves. We predict that the unique features and activities of ancestral PaWRI2 were likely lost in orthologous genes such as AtWRI2 during evolution and speciation, leading to at least partial loss of function in some higher eudicots. This study provides us with new targets to enhance oil biosynthesis in plants.
Highlights
WRINKLED1 (WRI1) belongs to the APETALA2/ethylene-responsive element binding protein (AP2/EREBP) class of transcription factors that play a master role in the developmental regulation of oil biosynthesis in plants (Cernac and Benning, 2004)
Whether the functional role of WRI2 orthologs in oil biosynthesis is conserved in any of the plant species has not been elucidated, except for AtWRI2, where it was shown to be non-functional based on its inability to complement Atwri1-1 mutant (To et al, 2012)
The three WRI2 orthologs analyzed in this study contained only one AP2 domain, reflecting an ancestral feature, an interruption in the domain by a 35 amino acid stretch in AtWRI2 was likely sufficient for loss of its function (Figure 1)
Summary
WRINKLED1 (WRI1) belongs to the APETALA2/ethylene-responsive element binding protein (AP2/EREBP) class of transcription factors that play a master role in the developmental regulation of oil biosynthesis in plants (Cernac and Benning, 2004). The WRI1 transcription factor was first identified in Arabidopsis, where mutant seeds showed 80% reduction in triacylglycerol (TAG). Subsequent studies revealed that WRI1 regulates a number of genes involved in controlling carbon allocation between sucrose and fatty acids in developing seeds (Focks and Benning, 1998). Arabidopsis wri mutant seeds were unable to efficiently convert carbon from sucrose and glucose into fatty acids during seed development. The genes regulated by WRI1 include phosphoglycerate mutase, plastidial pyruvate kinase β-subunit 1 (PI-PKβ1), pyruvate dehydrogenase 1α (PDHE1α), biotin carboxyl carrier protein 2 (BCCP2), acyl carrier protein 1 (ACP1), and keto-ACP synthase 1 (KAS1) (Baud and Lepiniec, 2009; Maeo et al, 2009). BIOTIN ATTACHMENT DOMAIN CONTAINING (BADC) proteins are conditional inhibitors of fatty acid biosynthesis; the genes encoding for BADC1, 2, and 3 were positively regulated by WRI1 (Keereetaweep et al, 2018; Liu et al, 2019) fatty acid and storage lipid biosynthesis mediated through WRI1-induced genes is a complex and tightly regulated process
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