Sulfite oxidase controls sulfur metabolism under SO₂ exposure in Arabidopsis thaliana

Abstract

In the present study, the significance of sulfite oxidase (SO) for sulfite detoxification and sulfur assimilation was investigated. In response to sulfur dioxide (SO2) exposure, a remarkable expansion of sulfate and a significant increase of GSH pool were observed in wild-type and SO-overexpressing Arabidopsis. These metabolic changes were connected with a negative feedback inhibition of adenosine 5Ј-phosphosulfate reductase (APR), but no alterations in gas exchange parameters or visible symptoms of injury. However, Arabidopsis SO-KO mutants were consistently negatively affected upon 600 nL L -1 SO2 exposure for 60 h and showed phenotypical symptoms of injury with small necrotic spots on the leaves. The mean g H O 2 ( ) was reduced by about 60% over the fumigation period, accompanied by a reduction of net CO2 assimilation and SO2 uptake of about 50 and 35%. Moreover, sulfur metabolism was completely distorted. Whereas sulfate pool was kept constant, thiol-levels strongly increased. This demonstrates that SO should be the only protagonist for back-oxidizing and detoxification of sulfite. Based on these results, it is suggested that co-regulation of SO and APR controls sulfate assimilation pathway and stabilizes sulfite distribution into organic sulfur compounds. In conclusion, a sulfate-sulfite cycle driven by APR and SO can be postulated for fine-tuning of sulfur distribution that is additionally used for sulfite detoxification, when plants are exposed to atmospheric SO2.

Sulfite Reductase Protects Plants against Sulfite Toxicity

“…Similarly, a 1.5-to 2-fold increase in SiR activity was recorded in Arabidopsis plants after relatively long-term fumigation with SO 2 for 60 h (Randewig et al, 2012).…”

“…SO, like SiR, has been shown to be constitutively expressed in Arabidopsis plant organs, with relative enrichment in root tips and the vascular system (Brychkova et al, 2007;Lang et al, 2007;Khan et al, 2010;Randewig et al, 2012). Infiltration of sulfite by injection into plant leaves allowed us to demonstrate the rapid (within 30 min) inducibility of both SiR and SO expression.…”

“…SiR transcript up-regulation in Arabidopsis wild-type and SO-impaired plants 2 h after fumigation with toxic levels of SO 2 (2 mL L 21 ) may be indicative of an enhancement of SiR activity as well (Brychkova et al, 2007). An enhancement of SiR activity was recently demonstrated in response to relatively nontoxic SO 2 (0.6 mL L 21 ) fumigation for 60 h (Randewig et al, 2012), possibly representing an adaptation to longterm SO 2 exposure. Employing the technique of sulfite infiltration by injection into the leaves (Wu et al, 2011;Brychkova et al, 2012a), we were able to demonstrate a fast induction of SiR activity in response to sulfite.…”

“…These results show that SiR transcript and activity levels rose within minutes (30-180 min), and this rise extended over a period of a few hours in both plant species, demonstrating the inducible nature of SiR in response to sulfite application. SO localized to the peroxisomes was recently deciphered as the key enzyme in the back oxidation and detoxification of sulfite by oxidation to sulfate (Brychkova et al, 2007;Randewig et al, 2012). Indeed, when SO Ri plants with negligible SO activity (Supplemental Table S2) were used as a positive control, they were found to be highly sensitive to 4 and 8 mM sulfite injections.…”

An Essential Role for Tomato Sulfite Oxidase and Enzymes of the Sulfite Network in Maintaining Leaf Sulfite Homeostasis

“…Their close vicinity to the chloroplasts (Oikawa et al, 2003) and mitochondria (Islam and Takagi, 2010) would enable the generation of a sulfite gradient facilitated by SOdependent sulfite oxidation (Hansch and Mendel, 2008). Indeed, application by fumigation of toxic SO 2 levels to normally grown Arabidopsis and tomato mutants, overexpressing or lacking SO activity, demonstrated the essential role of SO in protecting plant cell components from toxic sulfite (Brychkova et al, 2007;Lang et al, 2007;Randewig et al, 2012). By employing prolonged dark stress to induce the production of endogenous sulfite under conditions in which other sulfite network components are downregulated, we further demonstrated that peroxisomal SO serves as the major conduit of sulfite detoxification (Fig.…”