Intersection of the tocopherol and plastoquinol metabolic pathways at the plastoglobule

Abstract

Plastoglobules, lipid-protein bodies in the stroma of plant chloroplasts, are enriched in non-polar lipids, in particular prenyl quinols. In the present study we show that, in addition to the thylakoids, plastoglobules also contain a considerable proportion of the plastidial PQ-9 (plastoquinol-9), the redox component of photosystem II, and of the cyclized product of PQ-9, PC-8 (plastochromanol-8), a tocochromanol with a structure similar to gamma-tocopherol and gamma-tocotrienol, but with a C-40 prenyl side chain. PC-8 formation was abolished in the Arabidopsis thaliana tocopherol cyclase mutant vte1, but accumulated in VTE1-overexpressing plants, in agreement with a role of tocopherol cyclase (VTE1) in PC-8 synthesis. VTE1 overexpression resulted in the proliferation of the number of plastoglobules which occurred in the form of clusters in the transgenic lines. Simultaneous overexpression of VTE1 and of the methyltransferase VTE4 resulted in the accumulation of a compound tentatively identified as 5-methyl-PC-8, the methylated form of PC-8. The results of the present study suggest that the existence of a plastoglobular pool of PQ-9, along with the partial conversion of PQ-9 into PC-8, might represent a mechanism for the regulation of the antioxidant content in thylakoids and of the PQ-9 pool that is available for photosynthesis.

A mechanism implicating plastoglobules in thylakoid disassembly during senescence and nitrogen starvation

“…In particular, the important role of PG proteins in prenylquinone metabolism is now well established notably via the characterization of NDC1 and the discovery of new aspects of VTE1 function Szymanska and Kruk 2010;Zbierzak et al 2010;Piller et al 2011Piller et al , 2012.…”

“…VTE1 mediates the conversion of 2,3-dimethyl-5-phytyl-1,4-benzoquinol (DMPBQ) into c-tocopherol. While most of the VTE1 appears to be present in PG, the three enzymes (VTE2, 3, 4) catalyzing the other biosynthetic reactions have been localized to the chloroplast inner envelope membrane (Soll et al 1985;Cheng et al 2003;Vidi et al 2006;Kobayashi and DellaPenna 2008;Zbierzak et al 2010). VTE1 has also been implicated in the recycling of the tocopherol oxidation product, a-tocopherol quinone, that accumulates in response to oxidative stress (Kobayashi and DellaPenna 2008).…”

“…The NADPH dehydrogenase NDC1, localized at plastoglobules, has been implicated in the re-oxidation of the reduced pool of plastoquinol (PQH 2 -9) accumulated in plastoglobules during high light stress (Szymanska and Kruk 2010;Zbierzak et al 2010;Piller et al 2011). This pool can also serve as a substrate for VTE1 to produce plastochromanol-8 (MeneSaffrane et al 2010;Szymanska and Kruk 2010;Zbierzak et al 2010).…”

“…This pool can also serve as a substrate for VTE1 to produce plastochromanol-8 (MeneSaffrane et al 2010;Szymanska and Kruk 2010;Zbierzak et al 2010). A role of NDC1 in the biosynthesis of phylloquinone has also been demonstrated using a non-targeted lipidomic analysis of the ndc1 mutant.…”

“…Plastoquinol (PQH 2 ) and tocopherol (vitamin E) are the major constituents of the prenylquinone lipid family in plastoglobules, whereas phylloquinone (vitamin K) is also present but in minor concentrations (Lichtenthaler and Peveling 1966;Steinmuller and Tevini 1985;Austin et al 2006;Lohmann et al 2006;Gaude et al 2007;Zbierzak et al 2010;Lippold et al 2012).…”