Dual and Opposing Roles of Xanthine Dehydrogenase in Defense-Associated Reactive Oxygen Species Metabolism in Arabidopsis

Abstract

While plants produce reactive oxygen species (ROS) for stress signaling and pathogen defense, they need to remove excessive ROS induced during stress responses in order to minimize oxidative damage. How can plants fine-tune this balance and meet such conflicting needs? Here, we show that XANTHINE DEHYDROGENASE1 (XDH1) in Arabidopsis thaliana appears to play spatially opposite roles to serve this purpose. Through a large-scale genetic screen, we identified three missense mutations in XDH1 that impair XDH1's enzymatic functions and consequently affect the powdery mildew resistance mediated by RESISTANCE TO POWDERY MILDEW8 (RPW8) in epidermal cells and formation of xanthine-enriched autofluorescent objects in mesophyll cells. Further analyses revealed that in leaf epidermal cells, XDH1 likely functions as an oxidase, along with the NADPH oxidases RbohD and RbohF, to generate superoxide, which is dismutated into H 2 O 2 . The resulting enrichment of H 2 O 2 in the fungal haustorial complex within infected epidermal cells helps to constrain the haustorium, thereby contributing to RPW8-dependent and RPW8-independent powdery mildew resistance. By contrast, in leaf mesophyll cells, XDH1 carries out xanthine dehydrogenase activity to produce uric acid in local and systemic tissues to scavenge H 2 O 2 from stressed chloroplasts, thereby protecting plants from stress-induced oxidative damage. Thus, XDH1 plays spatially specified dual and opposing roles in modulation of ROS metabolism during defense responses in Arabidopsis.

Untargeted liquid chromatography coupled with mass spectrometry reveals metabolic changes in nitrogen-deficient Isatis indigotica Fortune

“…An increase in L-tryptophan content in N-deficiency conditions is probably associated with amino acids acting synergically to mitigate N-deficiency damage of plants. Purine metabolism is part of nitrogen metabolism, and the relative metabolites synthesis is closely linked to nitrogen availability (Ma et al, 2016). We found that the abundances of adenosine, deoxyadenosine and hypoxanthine were significantly different both in roots and leaves.…”

The ribokinases of Arabidopsis thaliana and Saccharomyces cerevisiae are required for ribose recycling from nucleotide catabolism, which in plants is not essential to survive prolonged dark stress

“…The following T-DNA mutants of A. thaliana from the SALK collection (Alonso et al, 2003) and from the GABI-Kat collection (Kleinboelting et al, 2012) were used: SALK007531C, rbsk-1 (Riggs et al, 2016); SALK083120, nsh1-1 (Jung et al, 2011), SALK036597C, cda-2 (Chen et al, 2016); GK432D08, gsda-2 (Dahncke & Witte, 2013); GK015E03, hgprt-2 (here); GK049D04, xdh1-2 (Hauck et al, 2014;Ma et al, 2016). The first mentioning and allele assignments in the literature are cited.…”

“…It was previously reported that plants defective in xanthine dehydrogenase (XDH), an enzyme essential for the generation of uric acid and allantoin (Werner & Witte, 2011), are susceptible to prolonged dark stress (Brychkova et al, 2008). A dual role of XDH in ROS production and in ROS protection during biotic stress has been demonstrated recently (Ma et al, 2016). However, another as yet unexplored hypothesis regarding the increased susceptibility of the NSH1 mutant to dark stress is that carbon starvation might be more severe in this mutant background, because ribose from nucleotide catabolism cannot be released to be used as a carbon source.…”

PeCHYR1, a ubiquitin E3 ligase from Populus euphratica, enhances drought tolerance via ABA‐induced stomatal closure by ROS production in Populus

“…ABA‐induced stomatal closure is a defensive action that is usually accompanied by the production of H 2 O 2 (Li et al ., ; Zhang et al ., ). NADPH oxidase (RbohF) can generate H 2 O 2 in guard cells, which crucially modulates ABA‐induced stomatal closure and plant drought tolerance (Gudesblat et al ., ; Kolla et al ., ; Ma et al ., ). Previous studies have indicated that AtRbohF can be phosphorylated by OST1 (an ABA‐induced SnRK2.6 protein kinase) (Joshi‐Saha et al ., ; Sirichandra et al ., ; Wege et al ., ).…”