Ethylene modulates the role of NPR1 in cross-talk between salicylate and jasmonate signaling

Plant-Microbe Interactions, Department of Biology, Faculty of Science, Utrecht University, 3508 TB Utrecht, The Netherlands.
Plant physiology (Impact Factor: 6.84). 02/2009; 149(4):1797-809. DOI: 10.1104/pp.108.133926
Source: PubMed


The plant hormones salicylic acid (SA), jasmonic acid (JA), and ethylene (ET) play crucial roles in the signaling network that regulates induced defense responses against biotic stresses. Antagonism between SA and JA operates as a mechanism to fine-tune defenses that are activated in response to multiple attackers. In Arabidopsis (Arabidopsis thaliana), NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 (NPR1) was demonstrated to be required for SA-mediated suppression of JA-dependent defenses. Because ET is known to enhance SA/NPR1-dependent defense responses, we investigated the role of ET in the SA-JA signal interaction. Pharmacological experiments with gaseous ET and the ET precursor 1-aminocyclopropane-1-carboxylic acid showed that ET potentiated SA/NPR1-dependent PATHOGENESIS-RELATED1 transcription, while it rendered the antagonistic effect of SA on methyl jasmonate-induced PDF1.2 and VSP2 expression NPR1 independent. This overriding effect of ET on NPR1 function in SA-JA cross talk was absent in the npr1-1/ein2-1 double mutant, demonstrating that it is mediated via ET signaling. Abiotic and biotic induction of the ET response similarly abolished the NPR1 dependency of the SA-JA signal interaction. Furthermore, JA-dependent resistance against biotic attackers was antagonized by SA in an NPR1-dependent fashion only when the plant-attacker combination did not result in the production of high levels of endogenous ET. Hence, the interaction between ET and NPR1 plays an important modulating role in the fine tuning of the defense signaling network that is activated upon pathogen and insect attack. Our results suggest a model in which ET modulates the NPR1 dependency of SA-JA antagonism, possibly to compensate for enhanced allocation of NPR1 to function in SA-dependent activation of PR genes.

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    • "In general, SA and JA/ET are thought to regulate two different signal transduction pathways in plant disease resistance. SA and JA/ET signalling pathways and the cross-talk between them have been studied in various plants [15] [16] [17]. To determine whether exogenous application of these stimuli could induce the expression of MhRAR1 gene, Malus hupehensis were treated with SA, MeJA and ACC. "

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    • "The residual PDF1.2 activity in the tga256 mutant is not suppressed by SA, indicating that the tga256 mutant mimics a permanent SA-ET cross talk. Moreover, the negative effect of SA is independent from NPR1 (Leon-Reyes et al., 2009). Here, we investigated the global role of class II TGAs within the ET pathway and identified the promoter of the key regulatory gene ORA59 as their direct target site in the cascade. "
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    ABSTRACT: Salicylic acid (SA), a hormone essential for defense against biotrophic pathogens, triggers increased susceptibility of plants against necrotrophic attackers by suppressing the jasmonic acid (JA)/ethylene (ET) defense response. Here we show that this disease-promoting SA effect is abolished in plants lacking the three related bZIP transcription factors TGA2, TGA5 and TGA6 (class-II TGAs). After treatment of plants with the ET precursor 1-aminocyclopropane-1-carboxylic acid (ACC), activation of all those genes that are suppressed by SA depended on class-II TGAs. Rather than TGA binding sites, GCC-box motifs were significantly enriched in the corresponding promoters. GCC-box motifs are recognized by members of the superfamily of APETALA2/ETHYLENE RESPONSE FACTORs (AP2/ERFs). Of the eleven activating ACC-induced AP2/ERFs, only ORA59 and ERF96 were strongly suppressed by SA. ORA59 is the master regulator of the JA/ET-induced defense program. ORA59 transcript levels do not reach maximal levels in the tga2 tga5 tga6 triple mutant and this residual activity cannot be suppressed by SA. The ORA59 promoter contains an essential TGA binding site and is a direct target of class-II TGAs as revealed by chromatin immunoprecipitation experiments. We suggest that class-II TGAs at the ORA59 promoter constitute an important regulatory hub for the activation and SA-suppression of ACC-induced genes.
    Full-text · Article · Jul 2014 · Plant physiology
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    • "The presence of this branch might suggest its role in the resistance response. However, in contrast to earlier conclusions (Leon-Reyes et al., [85]), we determined that SA is not involved in resistance to necrotrophic pathogens, such as V. dahliae. Therefore, we deduced that the process by which cotton becomes infected by Verticillium involves both biotrophic and necrotrophic stages. "
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    ABSTRACT: Verticillium wilt, caused by the fungal pathogen Verticillium dahliae, is the most severe disease in cotton (Gossypium spp.), causing great lint losses worldwide. Disease management could be achieved in the field if genetically improved, resistant plants were used. However, the interaction between V. dahliae and cotton is a complicated process, and its molecular mechanism remains obscure. To understand better the defense response to this pathogen as a means for obtaining more tolerant cultivars, we monitored the transcriptome profiles of roots from resistant plants of G. barbadense cv. Pima90-53 that were challenged with V. dahliae. In all, 46,192 high-quality expressed sequence tags (ESTs) were generated from a full-length cDNA library of G. barbadense. They were clustered and assembled into 23126 unigenes that comprised 2661 contigs and 20465 singletons. Those unigenes were assigned Gene Ontology terms and mapped to 289 KEGG pathways. A total of 3027 unigenes were found to be homologous to known defense-related genes in other plants. They were assigned to the functional classification of plant--pathogen interactions, including disease defenses and signal transduction. The branch of "SA[rightwards arrow]NPR1[rightwards arrow]TGA[rightwards arrow]PR-1[rightwards arrow]Disease resistance" was first discovered in the interaction of cotton--V. dahliae, indicating that this wilt process includes both biotrophic and necrotrophic stages. In all, 4936 genes coding for putative transcription factors (TF) were identified in our library. The most abundant TF family was the NAC group (527), followed by G2-like (440), MYB (372), BHLH (331), bZIP (271) ERF, C3H, and WRKY. We also analyzed the expression of genes involved in pathogen-associated molecular pattern (PAMP) recognition, the activation of effector-triggered immunity, TFs, and hormone biosynthesis, as well as genes that are pathogenesis-related, or have roles in signaling/regulatory functions and cell wall modification. Their differential expression patterns were compared among mock-/inoculated- and resistant/susceptible cotton. Our results suggest that the cotton defense response has significant transcriptional complexity and that large accumulations of defense-related transcripts may contribute to V. dahliae resistance in cotton. Therefore, these data provide a resource for cotton improvement through molecular breeding approaches. This study generated a substantial amount of cotton transcript sequences that are related to defense responses against V. dahliae. These genomics resources and knowledge of important related genes contribute to our understanding of host--pathogen interactions and the defense mechanisms utilized by G. barbadense, a non-model plant system. These tools can be applied in establishing a modern breeding program that uses marker-assisted selections and oligonucleotide arrays to identify candidate genes that can be linked to valuable agronomic traits in cotton, including disease resistance.
    Full-text · Article · Sep 2013 · BMC Genomics
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