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Genome-wide association identifies a missing hydrolase for tocopherol synthesis in plants
Friday, 2022/06/17 | 08:03:26

Elise Albert, Sungsoo Kim, Maria Magallanes-Lundback,  et al.

PNAS May 31, 2022; 119 (23) e2113488119

Significance

Tocopherols (vitamin E) are plant-synthesized, lipid-soluble antioxidants whose dietary intake, primarily from seed oils, is essential for human health. Tocopherols contain a phytol-derived hydrophobic tail whose in vivo source has been elusive. The most significant genome-wide association signal for Arabidopsis seed tocopherols identified an uncharacterized, seed-specific esterase (VTE7) localized to the chloroplast envelope, where tocopherol synthesis occurs. VTE7 disruption and overexpression had large impacts on tissue tocopherol contents with metabolic phenotypes consistent with release of prenyl alcohols, including phytol, during chlorophyll synthesis, rather than from the bulk degradation of thylakoid chlorophylls as has long been assumed. Understanding the source of phytol for tocopherols will enable breeding and engineering plants for vitamin E biofortification and enhanced stress resilience.

Abstract

The tocopherol biosynthetic pathway, encoded by VTE genes 1 through 6, is highly conserved in plants but most large effect quantitative trait loci for seed total tocopherols (totalT) lack VTE genes, indicating other activities are involved. A genome-wide association study of Arabidopsis seed tocopherols showed five of seven significant intervals lacked VTE genes, including the most significant, which mapped to an uncharacterized, seed-specific, envelope-localized, alpha/beta hydrolase with esterase activity, designated AtVTE7. Atvte7 null mutants decreased seed totalT 55% while a leaky allele of the maize ortholog, ZmVTE7, decreased kernel and leaf totalT 38% and 49%, respectively. Overexpressing AtVTE7 or ZmVTE7 partially or fully complemented the Atvte7 seed phenotype and increased leaf totalT by 3.6- and 6.9-fold, respectively. VTE7 has the characteristics of an esterase postulated to provide phytol from chlorophyll degradation for tocopherol synthesis, but bulk chlorophyll levels were unaffected in vte7 mutants and overexpressing lines. Instead, levels of specific chlorophyll biosynthetic intermediates containing partially reduced side chains were impacted and strongly correlated with totalT. These intermediates are generated by a membrane-associated biosynthetic complex containing protochlorophyllide reductase, chlorophyll synthase, geranylgeranyl reductase (GGR) and light harvesting-like 3 protein, all of which are required for both chlorophyll and tocopherol biosynthesis. We propose a model where VTE7 releases prenyl alcohols from chlorophyll biosynthetic intermediates, which are then converted to the corresponding diphosphates for tocopherol biosynthesis.

 

See https://www.pnas.org/doi/10.1073/pnas.2113488119

 

Figure 1 Summary of genome-wide and pathway-level association results for seed tocopherol traits. (A) Summarized pathways leading to tocopherol synthesis in Arabidopsis thaliana with key genes mentioned in text indicated and (B) table summarizing association results. White letters with black and red backgrounds indicate genome-wide significance, while gray background indicates significance only in pathway-level analysis. VTE7 is indicated by red highlighting. An FDR threshold of 5% was applied to declare significant SNPs in genome-wide and pathway-level analyses. Genomic information for significant SNPs is presented in SI Appendix, Fig. S2 and Datasets S2 and S4. Compound abbreviations: IPP, isopentenyl diphosphate; PDP, phytyl-diphosphate; HGA, homogentisic acid; MPBQ, 2-methyl-6-phytyl-1,4-benzoquinol; DMPBQ, 2,3-dimethyl-6-phytyl-1,4-benzoquinol; MEP, 2-C-methyl-D-erythritol 4-phosphate. Gene abbreviations: VTE1, tocopherol cyclase; VTE2, homogentisate phytyltransferase; VTE3, MPBQ methyltransferase; VTE4, γ-tocopherol methyltransferase; VTE5, phytol kinase; VTE6, phytylphosphate kinase; TAT2, tyrosine aminotransferase 2; GGR, geranylgeranyl reductase; ISPF, 2C-methyl-D-erythritol 2,4-cyclodiphosphate synthase.

 

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