Chitooligosaccharide sensing and downstream signaling: contrasted outcomes in pathogenic and beneficial plant–microbe interactions

Hamel, Louis-Philippe; Beaudoin, Nathalie

doi:10.1007/s00425-010-1215-9

Cited by 104 publications

(63 citation statements)

References 179 publications

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“…After cellulose, chitin is the second most ubiquitous polysaccharide in fungal cell walls (Sánchez-Vallet et al, 2015;Shinya et al, 2015). In Arabidopsis, chitin perception by CERK1 leads to a burst of ROS (Miya et al, 2007), and chitin, or its derivative chitosan, increases callose deposition and cell death (Hamel and Beaudoin, 2010;Luna et al, 2011;Hadwiger, 2013). These effects of chitin signaling are supported by our data, since NAD is found to be a potent elicitor of ROS (Fig.…”

Section: The Effect Of Nad On Metabolomics Pattern Matches That Of Elsupporting

confidence: 84%

NAD Acts as an Integral Regulator of Multiple Defense Layers

et al. 2016

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(J.T.).Pyridine nucleotides, such as NAD, are crucial redox carriers and have emerged as important signaling molecules in stress responses. Previously, we have demonstrated in Arabidopsis (Arabidopsis thaliana) that the inducible NAD-overproducing nadC lines are more resistant to an avirulent strain of Pseudomonas syringae pv tomato (Pst-AvrRpm1), which was associated with salicylic acid-dependent defense. Here, we have further characterized the NAD-dependent immune response in Arabidopsis. Quinolinate-induced stimulation of intracellular NAD in transgenic nadC plants enhanced resistance against a diverse range of (a)virulent pathogens, including Pst-AvrRpt2, Dickeya dadantii, and Botrytis cinerea. Characterization of the redox status demonstrated that elevated NAD levels induce reactive oxygen species (ROS) production and the expression of redox marker genes of the cytosol and mitochondrion. Using pharmacological and reverse genetics approaches, we show that NAD-induced ROS production functions independently of NADPH oxidase activity and light metabolism but depends on mitochondrial respiration, which was increased at higher NAD. We further demonstrate that NAD primes pathogen-induced callose deposition and cell death. Mass spectrometry analysis reveals that NAD simultaneously induces different defense hormones and that the NAD-induced metabolic profiles are similar to those of defense-expressing plants after treatment with pathogen-associated molecular patterns. We thus conclude that NAD triggers metabolic profiles rather similar to that of pathogen-associated molecular patterns and discuss how signaling cross talk between defense hormones, ROS, and NAD explains the observed resistance to pathogens.

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Section: The Effect Of Nad On Metabolomics Pattern Matches That Of Elsupporting

confidence: 84%

NAD Acts as an Integral Regulator of Multiple Defense Layers

et al. 2016

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“…Therefore, the data are consistent with a role for the GS52 ectoapyrase in maintaining extracellular nucleotide levels to maximize the symbiotic interaction. The key rhizobial signal required for nodulation is the lipochitooligosaccharide Nod factor, which is essential for the induction of many of the early nodulation responses (Oldroyd and Downie, 2008;Hamel and Beaudoin, 2010). A key event triggered by Nod factor addition is calcium spiking in the root hair, whose frequency and amplitude are apparently a crucial, specific signal to initiate downstream intracellular signaling events (Oldroyd and Downie, 2004).…”

Section: Discussionmentioning

confidence: 99%

Enzymatic Activity of the Soybean Ecto-Apyrase GS52 Is Essential for Stimulation of Nodulation

et al. 2011

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Nitrogen is an essential nutrient for plant growth. In the Rhizobium-legume symbiosis, root nodules are the sites of bacterial nitrogen fixation, in which atmospheric nitrogen is converted into a form that plants can utilize. While recent studies suggested an important role for the soybean (Glycine max) ecto-apyrase GS52 in rhizobial root hair infection and root nodule formation, precisely how this protein impacts the nodulation process remains undetermined. In this study, the biochemical characteristics of the GS52 enzyme were investigated. Computer modeling of the GS52 apyrase structure identified key amino acid residues important for catalytic activity, which were subsequently mutagenized. Although the GS52 enzyme exhibited broad substrate specificity, its activity on pyrimidine nucleotides and diphosphate nucleotides was significantly higher than on ATP. This result was corroborated by structural modeling of GS52, which predicted a low specificity for the adenine base within the substratebinding pocket of the enzyme. The wild-type enzyme and its inactive mutant forms were expressed in soybean roots in order to evaluate the importance of GS52 enzymatic activity for nodulation. The results indicated a clear correlation between GS52 enzymatic activity and nodule number. Altogether, our study indicates that the catalytic activity of the GS52 apyrase, likely acting on extracellular nucleotides, is critical for rhizobial infection and nodulation.

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“…CHOS with 2 to 6 degrees of polymerization (DP) were obtained from chitin by chemical or enzymatic depolymerization or metabolic engineering (2,17,30). Most biological activities require CHOS DP of Ն4 (12), but the synthesis of oligomers with Ն6 DP has been a daunting task. The transglycosylation (TG) activity of chitinases has been actively investigated for synthesis of long-chain CHOS.…”

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confidence: 99%

Synthesis of Long-Chain Chitooligosaccharides by a Hypertransglycosylating Processive Endochitinase of Serratia proteamaculans 568

Purushotham

Podile

2012

J Bacteriol

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We describe the heterologous expression and characterization of a 407-residue single-domain glycosyl hydrolase family 18 chitinase (SpChiD) from Gram-negative Serratia proteamaculans 568 that has unprecedented catalytic properties. SpChiD was optimally active at pH 6.0 and 40°C, where it showed a K m of 83 mg ml ؊1 , a k cat of 3.9 ؋ 10 2 h ؊1 , and a k cat /K m of 4.7 h mg ؊1 ml ؊1 on colloidal chitin. On chitobiose, the K m , k cat , and k cat /K m were 203 M, 1.3 ؋ 10 2 h ؊1 , and 0.62 h ؊1 M ؊1 , respectively. Hydrolytic activity on chitooligosaccharides (CHOS) and colloidal chitin indicated that SpChiD was an endo-acting processive enzyme, with the unique ability to convert released chitobiose to N-acetylglucosamine, the major end product. SpChiD showed hyper transglycosylation (TG) with trimer-hexamer CHOS substrates, generating considerable amounts of long-chain CHOS. The TG activity of SpChiD was dependent on both the length and concentration of the oligomeric substrate and also on the enzyme concentration. The length and amount of accumulated TG products increased with increases in the length of the substrate and its concentration and decreased with increases in the enzyme concentration. The SpChiD bound to insoluble and soluble chitin substrates despite the absence of accessory domains. Sequence alignments and structural modeling indicated that SpChiD would have a deep substrate-binding groove lined with aromatic residues, which is characteristic of processive enzymes. SpChiD shows a combination of properties that seems rare among family 18 chitinases and that may resemble the properties of human chitotriosidase.

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Chitooligosaccharide sensing and downstream signaling: contrasted outcomes in pathogenic and beneficial plant–microbe interactions

Cited by 104 publications

References 179 publications

NAD Acts as an Integral Regulator of Multiple Defense Layers

NAD Acts as an Integral Regulator of Multiple Defense Layers

Enzymatic Activity of the Soybean Ecto-Apyrase GS52 Is Essential for Stimulation of Nodulation

Synthesis of Long-Chain Chitooligosaccharides by a Hypertransglycosylating Processive Endochitinase of Serratia proteamaculans 568

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