Dual Role of the Plastid Terminal Oxidase in Tomato

Abstract

The plastid terminal oxidase (PTOX) is a plastoquinol oxidase whose absence in tomato (Solanum lycopersicum) results in the ghost (gh) phenotype characterized by variegated leaves (with green and bleached sectors) and by carotenoid-deficient ripe fruit. We show that PTOX deficiency leads to photobleaching in cotyledons exposed to high light primarily as a consequence of reduced ability to synthesize carotenoids in the gh mutant, which is consistent with the known role of PTOX as a phytoene desaturase cofactor. In contrast, when entirely green adult leaves from gh were produced and submitted to photobleaching high light conditions, no evidence for a deficiency in carotenoid biosynthesis was obtained. Rather, consistent evidence indicates that the absence of PTOX renders the tomato leaf photosynthetic apparatus more sensitive to light via a disturbance of the plastoquinone redox status. Although gh fruit are normally bleached (most likely as a consequence of a deficiency in carotenoid biosynthesis at an early developmental stage), green adult fruit could be obtained and submitted to photobleaching high light conditions. Again, our data suggest a role of PTOX in the regulation of photosynthetic electron transport in adult green fruit, rather than a role principally devoted to carotenoid biosynthesis. In contrast, ripening fruit are primarily dependent on PTOX and on plastid integrity for carotenoid desaturation. In summary, our data show a dual role for PTOX. Its activity is necessary for efficient carotenoid desaturation in some organs at some developmental stages, but not all, suggesting the existence of a PTOX-independent pathway for plastoquinol reoxidation in association with phytoene desaturase. As a second role, PTOX is implicated in a chlororespiratory mechanism in green tissues.

An Orange Ripening Mutant Links Plastid NAD(P)H Dehydrogenase Complex Activity to Central and Specialized Metabolism during Tomato Fruit Maturation

“…These observations in Orr Ds resemble the effects seen in fruits of the tomato ghost (gh) mutant when averted from light (Shahbazi et al, 2007). This mutant is impaired in the plastid terminal oxidase gene (PTOX).…”

Effects of n-propyl gallate on photosynthesis and physiological parameters in Dunaliella salina are affected by stressful conditions

“…Since it has been confirmed that PTOX plays a role as a terminal oxidase and the carotenoid biosynthesis process is dependent on re-oxidation of the reduced PQ pool (Carol and Kuntz, 2001;Morstadt et al, 2002), the suggested role for PTOX in the latter process is not incompatible. Thus, inhibition of PTOX in both molecular (by mutation) and biochemical (by inhibitor) levels affects plant photosynthesis apparatus, and consequently, plants tolerance under environmental stress conditions (Shahbazi et al, 2007;Gamboa et al, 2009). However, although PTOX in the photosynthetic electron transport chain probably does not play a major role during photosynthesis under optimal conditions (Gamboa et al, 2009), it likely participates to the required flexibility of photosynthetic electron transfer reactions, when photosynthesis operates under unstable environmental conditions.…”

Conserved Active Site Sequences in Arabidopsis Plastid Terminal Oxidase (PTOX)

“…during stress (20 -23). Consistent with this view, studies in tomato ghost (the ortholog of the Arabidopsis im mutant) reveal that lack of PTOX in young seedlings as well as in mature tomato leaves results in increased sensitivity to high light stress due to disturbances in the redox status of the plastoquinone pool (23). In contrast, in vivo chlorophyll fluorescence measurements reveal that modulating IMMUTANS expression and/or protein accumulation does not alter the flux of intersystem electrons during steady state photosynthesis in Arabidopsis nor does it afford photoprotection (17).…”

“…However, in contrast to early development, studies with im and with Arabidopsis PTOX overexpressor lines show that alterations in IMMUTANS expression and/or protein accumulation have no effect on electron flow during steady state photosynthesis in mature leaves (17). Interestingly, this does not appear to be the case in tomato, where recent studies in the ghost variegation mutant have demonstrated that PTOX activity is necessary in mature leaves, especially under high light conditions (23).…”

“…We hypothesize that a lack of PTOX (as in immutans) results in over-reduction of the PQ pool under restrictive conditions (e.g. high light); this has been demonstrated (21,23). This over-reduction prevents further transfer of electrons to the PQ pool and, consequently, an inhibition of the carotenoid pathway at the PDS step.…”