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.

Download full-text


Available from: Jianqiang Wu, Jun 17, 2015
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: The defence mechanisms that are activated by methyl jasmonate (MJ) in fruits are not well understood. In this work, we studied the expression of defence genes in papaya fruit that are induced by the exposure to MJ and/or low temperatures. The papaya fruits 'Maradol' were randomly divided into two groups: one group was the untreated control and the other was treated with 10 -4 M of MJ. Half of the fruits from each of the two groups were stored after treatment for 5 days at 5ºC and 2 days at 20ºC. We studied the expression levels of the pdf1.1 and pdf1.2 genes by amplification from expression libraries created from the pulp and skin tissues of the papaya fruit. As a reference, the mRNA level of the 18s ribosomal gene was used. In the skin tissue, the expression levels of the pdf1.1 and pdf1.2 genes were higher immediately after MJ treatment compared to the control. Furthermore, the expression of pdf1.2 remained high after MJ treatment and subsequent storage compared to the control. It was therefore concluded that the activation of the pdf1.1 and pdf1.2 genes forms part of the molecular defence mechanism in fruits that is activated by exposure to MJ. To our knowledge, this is the first study that analyzes the gene expression in papaya fruit that is induced by the exogenous application of methyl jasmonate and cold treatment.
    Electronic Journal of Biotechnology 07/2012; 15(5):717-3458. DOI:10.2225/vol15-issue5-fulltext-7 · 0.65 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
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: The plant hormone jasmonic acid (JA) plays a central role in plant defense against herbivores. Herbivore damage elicits a rapid and transient JA burst in the wounded leaves and JA functions as a signal to mediate the accumulation of various secondary metabolites that confer resistance to herbivores. Nicotiana attenuata is a wild tobacco species that inhabits western North America. More than fifteen years of study and its unique interaction with the specialist herbivore insect Manduca sexta have made this plant one of the best models for studying plant-herbivore interactions. Here we review the recent progress in understanding the elicitation of JA accumulation by herbivore-specific elicitors, the regulation of JA biosynthesis, JA signaling, and the herbivore-defense traits in N. attenuata.
    Journal of Genetics and Genomics 12/2013; DOI:10.1016/j.jgg.2013.10.001 · 2.92 Impact Factor