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

Abstract

In higher plants, the plastidial NADH dehydrogenase (Ndh) complex supports nonphotochemical electron fluxes from stromal electron donors to plastoquinones. Ndh functions in chloroplasts are not clearly established; however, its activity was linked to the prevention of the overreduction of stroma, especially under stress conditions. Here, we show by the characterization of Orr Ds , a dominant transposon-tagged tomato (Solanum lycopersicum) mutant deficient in the NDH-M subunit, that this complex is also essential for the fruit ripening process. Alteration to the NDH complex in fruit changed the climacteric, ripening-associated metabolites and transcripts as well as fruit shelf life. Metabolic processes in chromoplasts of ripening tomato fruit were affected in Orr Ds , as mutant fruit were yellow-orange and accumulated substantially less total carotenoids, mainly b-carotene and lutein. The changes in carotenoids were largely influenced by environmental conditions and accompanied by modifications in levels of other fruit antioxidants, namely, flavonoids and tocopherols. In contrast with the pigmentation phenotype in mature mutant fruit, Orr Ds leaves and green fruits did not display a visible phenotype but exhibited reduced Ndh complex quantity and activity. This study therefore paves the way for further studies on the role of electron transport and redox reactions in the regulation of fruit ripening and its associated metabolism.

Alteration of the Interconversion of Pyruvate and Malate in the Plastid or Cytosol of Ripening Tomato Fruit Invokes Diverse Consequences on Sugar But Similar Effects on Cellular Organic Acid, Metabolism, and Transitory Starch Accumulation

“…On the other hand, only one line showed changes in the plastidial redox state in the plastidic NADP-ME antisense lines. Consistent with these changes in the plastidial redox status were the alterations in the activities and activation state of AGPase (in PEPCK and ME lines) and plastidial malate dehydrogenase (in ME lines), which are well documented diagnostics of alteration in redox status (Scheible and Stitt, 1988;Tiessen et al, 2002;Nashilevitz et al, 2010). The lack of absolute starch accumulation in both lines was also corroborated with a decrease in the starch biosynthesis flux.…”

“…Another explanation is that reduction in plastidic NADP-ME activity provokes a small reduction in plastidial malate that was not observed in the global malate pool, but it was enough to display a change in redox state to affect the activation state of AGPase. Increasing plastidial malate dehydrogenase corroborated the change in redox state in these plants (Scheible and Stitt, 1988;Tiessen et al, 2002;Nashilevitz et al, 2010).…”

Comprehensive Profiling of Ethylene Response Factor Expression Identifies Ripening-Associated ERF Genes and Their Link to Key Regulators of Fruit Ripening in Tomato

“…On the other hand, SlERF.D1, which displays a typical down-regulation during fruit ripening (Fig. 1), was reported to be strongly down-regulated during ripening of the OrrDs/ORR heterozygous mutant (Nashilevitz et al, 2010), indicating that ERFs from different subclasses might contribute to the ripening process. Taken together, these data suggest that the coordinated expression of some ERFs is central to fruit ripening.…”

Carotenoid Biosynthesis in Arabidopsis: A Colorful Pathway

“…The NADH dehydrogenase complex can also catalyze the reduction of plastoquinone using soluble (stromal) electron donors (Burrows et al, 1998;Endo et al, 2008). Interestingly, tomato plants deficient in this complex through a mutation in its subunit M show highly reduced carotenoid levels specifically in fruit chromoplasts (Nashilevitz et al, 2010). The possible interaction between the NADH dehydrogenase complex and PTOX and its possible effect on modulating the redox state of plastoquinone (and hence carotenoid desaturation) remains unexplored.…”