Inducible NAD overproduction in Arabidopsis alters metabolic pools and gene expression correlated with increased salicylate content and resistance to <i>Pst‐AvrRpm1</i>

Pétriacq, Pierre; Bont, Linda de; Hager, Jutta; Didierlaurent, Laure; Mauve, Caroline; Guérard, Florence; Noctor, Graham; Pelletier, Sandra; Renou, Jean-Pierre; Tcherkez, Guillaume; Gakière, Bertrand

doi:10.1111/j.1365-313x.2012.04920.x

Cited by 84 publications

(109 citation statements)

References 72 publications

(155 reference statements)

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“…Transient increase in NAD + pools induced resistance to the avirulent bacterial strain Pst-AvrRpm1 via stimulation of the defense hormone salicylic acid (SA). Transcriptomic analyses of nadC plants also pointed to NAD-dependent up-regulation of pathogen-inducible genes associated with Ca 2+ signaling and various redox targets, including the hypersensitive response (HR; Pétriacq et al, 2012Pétriacq et al, , 2013. In support of these results, Mou (2009, 2012) suggested that exogenous NAD + in the apoplast plays a role in defenserelated Ca 2+ signaling via both SA-dependent and SAindependent signaling pathways.…”

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“…Indeed in Arabidopsis (Arabidopsis thaliana), genetic knockdown of aspartate oxidase (AO) activity (EC 1.4.3.16; the first enzyme of de novo NAD synthesis in the chloroplast; Katoh et al, 2006) hampers stomatal immunity against the hemibiotrophic pathogen Pseudomonas syringae pv tomato (Pst; Macho et al, 2012), while AO transcripts consistently build up in response to bacterial infection, presumably to sustain NAD consumption . Furthermore, we have demonstrated previously a direct role for intracellular NAD + in defense, using an inducible system that is based on overexpression of the nadC gene from Escherichia coli, which encodes the NAD biosynthesis enzyme quinolinate phosphoribosyltransferase (EC 2.4.2.19;Pétriacq et al, 2012). Transgenic nadC Arabidopsis plants accumulate NAD upon treatment with quinolinic acid (Q), thereby allowing one to determine the biochemical and physiological consequences of increased NAD content in leaves.…”

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NAD Acts as an Integral Regulator of Multiple Defense Layers

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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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NAD Acts as an Integral Regulator of Multiple Defense Layers

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“…This agrees with previous results showing an upregulation of genes associated with Ca 2C response and binding. 4 Hence, direct NAD C treatment is able to induce changes in [Ca 2C ] cyt . To get further insights into the specificity of the [Ca 2C ] cyt response, we then conducted pharmacological treatments using pyridine nucleotides and their derivatives at 1 mM (Fig.…”

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“…10 While cytosolic Ca 2C peaks are potentiated by elicitors treatments such as the elicitor peptide PEP1, 11,12 AtPEP1 and Ca 2C -responsive genes are upregulated by higher NAD. 4 In addition, trapping of Ca 2C by EGTA prevents the induction of Pathogen Related (PR) genes after treatment with exogenous NAD(P). 13 Hence, NAD and Ca 2C -mediated signal transductions are possibly related.…”

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“…[1][2][3] Previously, we demonstrated that an inducible accumulation of NAD in Arabidopsis conferred resistance to the hemibiotrophic avirulent bacteria Pst-AvrRpm1 by modulating SA signaling at the transcripts and metabolites level. 4 Recently, we have detailed the NAD-inducible defense responses that are effective against biotrophic and necrotrophic pathogens. 5 Our study reveals that NAD C acts as an elicitor by stimulating basal defenses (i.e.…”

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Pyridine nucleotides induce changes in cytosolic pools of calcium in Arabidopsis

Pétriacq

Tcherkez

Gakière

2016

Plant Signaling & Behavior

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NAD is a pyridine nucleotide that is involved in cell metabolism and signaling of plant growth and stress. Recently, we reported on the multifaceted nature of NAD-inducible immunity in Arabidopsis. We identified NAD as an integral regulator of multiple defense layers such as production of ROS, deposition of callose, stimulation of cell death and modulation of defense metabolism including the defense hormones SA, JA and ABA, and other defense-associated metabolites. Altogether, NAD-induced immune effects confer resistance to diverse pathogenic microbes. Our addendum to this work further demonstrates an impact of NAD on the cytosolic calcium pool, a well-known component of early plant defense response. The redox cofactor NAD is important for plant metabolism and signaling during growth and stress. 1-3 Previously, we demonstrated that an inducible accumulation of NAD in Arabidopsis conferred resistance to the hemibiotrophic avirulent bacteria Pst-AvrRpm1 by modulating SA signaling at the transcripts and metabolites level. 4 Recently, we have detailed the NAD-inducible defense responses that are effective against biotrophic and necrotrophic pathogens. 5 Our study reveals that NAD C acts as an elicitor by stimulating basal defenses (i.e. ROS production, callose deposition, cell death) and influencing hormonal balance. 5 Metabolomics further demonstrated similarities between plants treated with NAD C and the fungal elicitor chitin.Recent data suggest the involvement of a coordinated integration of ROS and calcium (Ca 2C ) waves in plants under pathogen infections. 6 In addition, NAD and Ca 2C signaling potentially interact during stress responses. 3 In fact, NAD C and its phosphate derivative NADP C could trigger the release of intracellular Ca 2C considering its potential role as an ADP ribose (ADPr) donor for cyclic ADPr and nicotinic acid adenine dinucleotide phosphate (NAADP). Thus far, however, direct evidence of effects of NAD C on Ca 2C fluxes are missing.To investigate the Ca 2C -related component of NAD signaling, we tested cytosolic Ca 2C concentrations (denoted as [Ca 2C ] cyt ) in response to NAD C by luminometry using 2 weeks-old transgenic apoaequorin Arabidopsis seedlings (pMAQ2). 7,8 Upon NAD C addition at physiological concentration (1 mM), 2,3 [Ca 2C ] cyt transiently increased as compared to the control (water treatment) in plants incubated for 10 min, 20 min and 40-50 min (Fig. 1A). [Ca 2C ] cyt then dropped after 60 min suggesting either a consumption to replenish noncytoplasmic calcium pools or an important binding of cytoplasmic Ca 2C . This agrees with previous results showing an upregulation of genes associated with Ca 2C response and binding. 4 Hence, direct NAD C treatment is able to induce changes in [Ca 2C ] cyt . To get further insights into the specificity of the [Ca 2C ] cyt response, we then conducted pharmacological treatments using pyridine nucleotides and their derivatives at 1 mM (Fig. 1B). We focused on the decrease in [Ca 2C ] cyt observed after 60 min of incubation (F...

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