Abstract
Plant sulfite oxidase [SO; E.C.1.8.3.1] has been shown to be a key player in protecting plants against exogenous toxic sulfite. Recently we showed that SO activity is essential to cope with rising dark-induced endogenous sulfite levels in tomato plants (Lycopersicon esculentum/Solanum lycopersicum Mill. cv. Rheinlands Ruhm). Here we uncover the ramifications of SO impairment on carbon, nitrogen and sulfur (S) metabolites. Current analysis of the wild-type and SO-impaired plants revealed that under controlled conditions, the imbalanced sulfite level resulting from SO impairment conferred a metabolic shift towards elevated reduced S-compounds, namely sulfide, S-amino acids (S-AA), Co-A and acetyl-CoA, followed by non-S-AA, nitrogen and carbon metabolite enhancement, including polar lipids. Exposing plants to dark-induced carbon starvation resulted in a higher degradation of S-compounds, total AA, carbohydrates, polar lipids and total RNA in the mutant plants. Significantly, a failure to balance the carbon backbones was evident in the mutants, indicated by an increase in tricarboxylic acid cycle (TCA) cycle intermediates, whereas a decrease was shown in stressed wild-type plants. These results indicate that the role of SO is not limited to a rescue reaction under elevated sulfite, but SO is a key player in maintaining optimal carbon, nitrogen and sulfur metabolism in tomato plants.
Highlights
It is commonly assumed that sulfur (S), carbon (C) and nitrogen (N) pathways should be well coordinated in order to maintain the production of S-amino acids in plants [1]
A significant reduction of total plant biomass was noticed in the mutant plants as compared to the wild-type plants grown under normal unstressed growth condition, no obvious tissue damage and enhanced expression of stress marker genes were noticed in the mutant plants
2.1%, respectively (Supplementary Table S5)), these results indicate that in the absence of SO activity the biosynthesis or degradation of the amino acids is specific for the S and non-S amino acids, in a C
Summary
It is commonly assumed that sulfur (S), carbon (C) and nitrogen (N) pathways should be well coordinated in order to maintain the production of S-amino acids in plants [1]. Carbon starvation-induced senescence is associated with a increase in free amino acids [8,9,10,11], which could either be a result of protein degradation, or of de-novo amino acid biosynthesis. Another hallmark of senescence is the enhancement of substances with high N/C ratios, such as ureides, allantoin and allantoate [12], as well as amides, which are preferable storage compounds from an energetic point of view [13]. To delay senescence during accelerated catabolism, the over-accumulation of toxic by-products such as ammonia, sulfite, sulfide, reactive oxygen species (ROS) and others, should be prevented by the activation of detoxification/re-assimilation processes [12,14,15]
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