S-Nitrosoglutathione reductase (GSNOR) mediates the biosynthesis of jasmonic acid and ethylene induced by feeding of the insect herbivore Manduca sexta and is important for jasmonate-elicited responses in Nicotiana attenuata

Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Hans-Knoell-Str. 8, D-07745 Jena, Germany.
Journal of Experimental Botany (Impact Factor: 5.79). 05/2011; 62(13):4605-16. DOI: 10.1093/jxb/err171
Source: PubMed

ABSTRACT S-nitrosoglutathione reductase (GSNOR) reduces the nitric oxide (NO) adduct S-nitrosoglutathione (GSNO), an essential reservoir for NO bioactivity. In plants, GSNOR has been found to be important in resistance to bacterial and fungal pathogens, but whether it is also involved in plant-herbivore interactions was not known. Using a virus-induced gene silencing (VIGS) system, the activity of GSNOR in a wild tobacco species, Nicotiana attenuata, was knocked down and the function of GSNOR in defence against the insect herbivore Manduca sexta was examined. Silencing GSNOR decreased the herbivory-induced accumulation of jasmonic acid (JA) and ethylene, two important phytohormones regulating plant defence levels, without compromising the activity of two mitogen-activated protein kinases (MAPKs), salicylic acid-induced protein kinase (SIPK) and wound-induced protein kinase (WIPK). Decreased activity of trypsin proteinase inhibitors (TPIs) were detected in GSNOR-silenced plants after simulated M. sexta feeding and bioassays indicated that GSNOR-silenced plants have elevated susceptibility to M. sexta attack. Furthermore, GSNOR is required for methyl jasmonate (MeJA)-induced accumulation of defence-related secondary metabolites (TPI, caffeoylputrescine, and diterpene glycosides) but is not needed for the transcriptional regulation of JAZ3 (jasmonate ZIM-domain 3) and TD (threonine deaminase), indicating that GSNOR mediates certain but not all jasmonate-inducible responses. This work highlights the important role of GSNOR in plant resistance to herbivory and jasmonate signalling and suggests the potential involvement of NO in plant-herbivore interactions. Our data also suggest that GSNOR could be a target of genetic modification for improving crop resistance to herbivores.

  • [Show abstract] [Hide abstract]
    ABSTRACT: In eukaryotes, bursts of reactive oxygen and nitrogen species mediate cellular responses to the environment by modifying cysteines of signaling proteins. Cysteine reactivity toward nitric oxide (NO) leads to formation of S-nitrosothiols (SNOs) that play important roles in pathogenesis and immunity. However, it remains poorly understood how SNOs are employed as specific, reversible signaling cues. Here we show that in plant immunity the oxidoreductase Thioredoxin-h5 (TRXh5) reverses SNO modifications by acting as a selective protein-SNO reductase. While TRXh5 failed to restore immunity in gsnor1 mutants that display excessive accumulation of the NO donor S-nitrosoglutathione, it rescued immunity in nox1 mutants that exhibit elevated levels of free NO. Rescue by TRXh5 was conferred through selective denitrosylation of excessive protein-SNO, which reinstated signaling by the immune hormone salicylic acid. Our data indicate that TRXh5 discriminates between protein-SNO substrates to provide previously unrecognized specificity and reversibility to protein-SNO signaling in plant immunity.
    Molecular Cell 09/2014; 56(1). DOI:10.1016/j.molcel.2014.08.003 · 14.46 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: The response of plants to the stress caused by herbivores involves several different defense mechanisms. These responses begin at the plant cell plasma membrane, where insect herbivores interact physically by causing mechanical damage and chemically by introducing elicitors or triggering plant-derived signaling molecules. The earliest plant responses to herbivore contact are represented by ion flux unbalances generated in the plant cell plasma membrane at the damaged site. Differences in the charge distribution generate plasma transmembrane potential (Vm) variation, the first event that eventually leads to the initiation of signal transduction pathways and gene expression. Calcium signaling and the generation of reactive oxygen and nitrogen species are early events closely related to Vm variations. This review provides an update on recent developments and advances in plant early signaling in response to herbivory, with particular emphasis on the electrophysiological variations of the plasma membrane potential, calcium signaling, cation channel activity, the production of reactive oxygen and nitrogen species, and the formation of a systemically moving signal from wounded tissues. The roles of calcium dependent protein kinases and calcineurin signaling are also discussed.
    Journal of Experimental Botany 01/2015; 66:435-448. DOI:10.1093/jxb/eru480 · 5.79 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Knowledge of phosphorylation events and their regulation is crucial to understanding the functional biology of plant proteins, but very little is currently known about nitric oxide-responsive phosphorylation in plants. Here, we report the first large-scale, quantitative phosphoproteome analysis of cotton (Gossypium hirsutum) treated with sodium nitroprusside (nitric oxide donor) by utilizing the isobaric tag for relative and absolute quantitation (iTRAQ) method. A total of 1315 unique phosphopeptides, spanning 1528 non-redundant phosphorylation sites, were detected from 1020 cotton phosphoproteins. Among them, 183 phosphopeptides corresponding to 167 phosphoproteins were found to be differentially phosphorylated in response to sodium nitroprusside. Several of the phosphorylation sites that we identified, including RQxS, DSxE, TxxxxSP and SPxT, have not, to our knowledge, been reported to be protein kinase sites in other species. The phosphoproteins identified are involved in a wide range of cellular processes, including signal transduction, RNA metabolism, intracellular transport and so on. This study reveals unique features of the cotton phosphoproteome and provides new insight into the biochemical pathways that are regulated by nitric oxide.
    PLoS ONE 04/2014; 9(4):e94261. DOI:10.1371/journal.pone.0094261 · 3.53 Impact Factor

Full-text (2 Sources)

Available from
Jun 2, 2014