The study demonstrates protein tyrosine nitration as a functional post-translational modification (PTM) in biology and pathobiology of the oomycete Phytophthora infestans (Mont.) de Bary, the most harmful pathogen of potato ( Solanum tuberosum L.). Using two P. infestans isolates differing in their virulence toward potato cv. Sarpo Mira we found that the pathogen generates reactive nitrogen species (RNS) in hyphae and mature sporangia growing under in vitro and in planta conditions. However, acceleration of peroxynitrite formation and elevation of the nitrated protein pool within pathogen structures were observed mainly during the avr P. infestans MP 946-potato interaction. Importantly, the nitroproteome profiles varied for the pathogen virulence pattern and comparative analysis revealed that vr MP 977 P. infestans represented a much more diverse quality spectrum of nitrated proteins. Abundance profiles of nitrated proteins that were up- or downregulated were substantially different also between the analyzed growth phases. Briefly, in planta growth of avr and vr P. infestans was accompanied by exclusive nitration of proteins involved in energy metabolism, signal transduction and pathogenesis. Importantly, the P. infestans- potato interaction indicated cytosolic RXLRs and Crinklers effectors as potential sensors of RNS. Taken together, we explored the first plant pathogen nitroproteome. The results present new insights into RNS metabolism in P. infestans indicating protein nitration as an integral part of pathogen biology, dynamically modified during its offensive strategy. Thus, the nitroproteome should be considered as a flexible element of the oomycete developmental and adaptive mechanism to different micro-environments, including host cells.
Peroxynitrite (ONOO-) exhibits a well-documented nitration activity in relation to proteins and lipids; however, the interaction of ONOO- with nucleic acids remains unknown in plants. The study uncovers RNA and mRNA nitration as an integral event in plant metabolism intensified during immune response. Using potato-avr/vr Phytophthora infestans systems and immunoassays we documented that potato immunity is accompanied by two waves of boosted ONOO- formation affecting guanine nucleotides embedded in RNA/mRNA and protein tyrosine residues. The early ONOO- generation was orchestrated with an elevated level of protein nitration and a huge accumulation of 8-nitroguanine (8-NO2-G) in RNA and mRNA pools confirmed as a biomarker of nucleic acid nitration. Importantly, potato cells lacking ONOO- due to scavenger treatment and attacked by the avr pathogen exhibited a low level of 8-NO2-G in the mRNA pool correlated with reduced symptoms of programmed cell death (PCD). The second burst of ONOO- coincided both with an enhanced level of tyrosine-nitrated proteins identified as subtilisine-like proteases and diminished protease activity in cells surrounding the PCD zone. Nitration of both RNA/mRNA and proteins via NO/ONOO- may constitute a new metabolic switch in redox regulation of PCD, potentially limiting its range in potato immunity to avr P. infestans.
Heavy metal (HM) contamination of the environment is a major problem worldwide. The rate of global deposition of HMs in soil has dramatically increased over the past two centuries and there of facilitated their rapid accumulation also in living systems. Although the effects of HMs on plants, animals and humans have been extensively studied, yet little is known about their effects on the (patho)biology of the microorganisms belonging to a unique group of filamentous eukaryotic pathogens, i.e., fungi and oomycetes. Much of the literature concerning mainly model species has revealed that HM stress affects their hyphal growth, morphology, and sporulation. Toxicity at cellular level leads to disturbance of redox homeostasis manifested by the formation of nitro-oxidative intermediates and to the induction of antioxidant machinery. Despite such adverse effects, published data is indicative of the fact that fungal and oomycete pathogens have a relatively high tolerance to HMs in comparison to other groups of microbes such as bacteria. Likely, these pathogens may harbor a network of detoxification mechanisms that ensure their survival in a highly HM-polluted (micro)habitat. Such a network may include extracellular HMs immobilization, biosorption to cell wall, and/or their intracellular sequestration to proteins or other ligands. HMs may also induce a hormesis-like phenomenon allowing the pathogens to maintain or even increase fitness against chemical challenges. Different scenarios linking HMs stress and modification of the microorganisms pathogenicity are disscused in this review.
Heavy metal pollution causes many soils to become a toxic environment not only for plants, but also microorganisms; however, little is known how heavy metal contaminated environment affects metabolism of phytopathogens and their capability of infecting host plants. In this study the oomycete Phytophthora infestans (Mont.) de Bary, the most harmful pathogen of potato, growing under moderate cadmium stress (Cd, 5 mg/L) showed nitro-oxidative imbalance associated with an enhanced antioxidant response. Cadmium notably elevated the level of nitric oxide, superoxide and peroxynitrite that stimulated nitrative modifications within the RNA and DNA pools in the phytopathogen structures. In contrast, the protein pool undergoing nitration was diminished confirming that protein tyrosine nitration is a flexible element of the oomycete adaptive strategy to heavy metal stress. Finally, to verify whether Cd is able to modify P. infestans pathogenicity, a disease index and molecular assessment of disease progress were analysed indicating that Cd stress enhanced aggressiveness of vr P. infestans towards various potato cultivars. Taken together, Cd not only affected hyphal growth rate and caused biochemical changes in P. infestans structures, but accelerated the pathogenicity as well. The nitro-oxidative homeostasis imbalance underlies the phytopathogen adaptive strategy and survival in the heavy metal contaminated environment.
Nitroxyl (HNO) is the one-electron reduced and protonated congener of nitric oxide (•NO), owning a distinct chemical profile. Based on real-time detection, we demonstrate that HNO is endogenously formed in Arabidopsis. Senescence and hypoxia induce shifts in the redox balance, triggering HNO decay or formation mediated by non-enzymatic •NO/HNO interconversion with cellular reductants. The stimuli-dependent HNO generation supports or competes with •NO signalling, depending on the local redox environment.
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