Fibrillin 5 Is Essential for Plastoquinone-9 Biosynthesis by Binding to Solanesyl Diphosphate Synthases in Arabidopsis

Abstract

Fibrillins are lipid-associated proteins in plastids and are ubiquitous in plants. They accumulate in chromoplasts and sequester carotenoids during the development of flowers and fruits. However, little is known about the functions of fibrillins in leaf tissues. Here, we identified fibrillin 5 (FBN5), which is essential for plastoquinone-9 (PQ-9) biosynthesis in Arabidopsis thaliana. Homozygous fbn5-1 mutations were seedling-lethal, and XVE:FBN5-B transgenic plants expressing low levels of FBN5-B had a slower growth rate and were smaller than wild-type plants. In chloroplasts, FBN5-B specifically interacted with solanesyl diphosphate synthases (SPSs) 1 and 2, which biosynthesize the solanesyl moiety of PQ-9. Plants containing defective FBN5-B accumulated less PQ-9 and its cyclized product, plastochromanol-8, but the levels of tocopherols were not affected. The reduced PQ-9 content of XVE:FBN5-B transgenic plants was consistent with their lower photosynthetic performance and higher levels of hydrogen peroxide under cold stress. These results indicate that FBN5-B is required for PQ-9 biosynthesis through its interaction with SPS. Our study adds FBN5 as a structural component involved in the biosynthesis of PQ-9. FBN5 binding to the hydrophobic solanesyl moiety, which is generated by SPS1 and SPS2, in FBN5-B/SPS homodimeric complexes stimulates the enzyme activity of SPS1 and SPS2.

Novel Loci Underlie Natural Variation in Vitamin E Levels in Maize Grain

“…Three of the novel loci encode such functions, including two, a fibrillin and a lipid transfer protein, affecting multiple tocopherol and tocotrienol traits. Fibrillins are encoded by moderate-sized gene families, with individual members having diverse functions ranging from storage of xanthophylls in fruit and flower chromoplasts to interaction with enzymes involved in plastoquinone biosynthesis (Deruère et al, 1994;Singh and McNellis, 2011;Kim et al, 2015). Tocopherols were reported as minor constituents of fibrillins isolated from red bell pepper (Capsicum annuum) fruit (Deruère et al, 1994), and several members localize to plastoglobuli along with various lipid-soluble compounds and enzymes, including tocopherol cyclase (Ytterberg et al, 2006;Bréhélin et al, 2007).…”

“…The identified gene in QTL10, affecting five traits, is one of 12 genes in maize encoding plastid-localized fibrillins, structural proteins that bind hydrophobic molecules and play various roles in their biosynthesis and accumulation in other systems (Deruère et al, 1994;Kim et al, 2015). Fibrillins are prominent components of plastoglobules (Ytterberg et al, 2006;Bréhélin et al, 2007), subcompartments of the chloroplast that also contain tocochromanols, carotenoids, lipids, and various biosynthetic enzymes including tocopherol cyclase.…”

Plastoquinone and Ubiquinone in Plants: Biosynthesis, Physiological Function and Metabolic Engineering

“…Overexpression of AtSPS1 resulted in the accumulation of PQ 9 and its derivative plastochromanol-8 (PC 8 ) (Ksas et al, 2015). Moreover, the enzymatic activity of AtSPS1 and AtSPS2 is stimulated by a member of the lipid-associated fibrillin protein family, fibrillin 5 (FNB5-B), which physically binds to the hydrophobic solanesyl moiety and helps to release the moiety from the enzymes in Arabidopsis cells (Kim et al, 2015). AtSPS3 had been shown previously to be targeted to plastids and to contribute to gibberellin biosynthesis (Bouvier et al, 2000).…”

Lack of FIBRILLIN6 in Arabidopsis thaliana affects light acclimation and sulfate metabolism

“…The first role assigned to members of the FBN family was an involvement in fibril structure formation. Reduced PQ-9 levels are also found in Arabidopsis fbn5 knockout mutants, and interaction experiments, together with the seedling-lethal phenotype of fbn5 mutants, suggest that Arabidopsis FBN5 plays a critical role in PQ-9 biosynthesis, is essential for plant development (Kim et al, 2015), and plays a role as a transmitter of singlet oxygen (O) in the chloroplast stroma (Otsubo et al, 2018). Another proposed FBN function is based on the observation that some of the FBNs contain lipocalin domains, suggesting that FBNs may also play a role in metabolite transport (Singh & McNellis, 2011).…”