Salicylic Acid: A Double-Edged Sword for Programed Cell Death in Plants

Radojičić, Ana; Li, Xin; Zhang, Yuelin

doi:10.3389/fpls.2018.01133

Cited by 102 publications

(80 citation statements)

References 32 publications

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“…The studies in Arabidopsis could not unambiguously determine the role of SA in initiation of pathogeninduced PCD. In some pathosystems PCD can be regulated by SA, but not in all (Huysmans et al, 2017;Radojičić et al, 2018). Here we determined that features of HR PCD are not dependent on SA in our studied pathosystem (Figure 3, Figure 6D).…”

Section: Discussionmentioning

confidence: 57%

Spatial accumulation of salicylic acid is regulated by RBOHD in potato immunity against viruses

Lukan¹,

Pompe-Novak²,

Baebler³

et al. 2020

Preprint

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Corresponding author: Tjaša Lukan (tjasa.lukan@nib.si). SIGNIFICANCETo get towards sustainable resistance in the field, it is important to understand mechanisms of immune signaling. We here show novel aspects of spatial regulation in effector-triggered immunity (ETI) against potato virus Y. A detailed spatiotemporal analysis in and surrounding the foci of viral infection, on ultrastructural, biochemical and gene expression levels revealed that redox state maintenance is tightly spatiotemporally regulated. We also show the interconnection of salicylic acid and RBOHD through a feedback loop, regulated through UDP-glucosyltransferase, revealing the mechanism of this spatial regulation. The proper function of this loop is essential for successful ETI leading to viral arrest. ABSTRACTWhile activation of resistance (R) proteins has been intensively studied, the mechanisms acting downstream of R protein activation remain elusive. We studied effector-triggered immunity (ETI) conditioned by the potato Ny-1 gene against potato virus Y. Transcriptomic, ultrastructural and biochemical analyses of four consecutive tissue sections in and surrounding the foci of viral infection at three different lesion developmental stages revealed processes that are spatiotemporally regulated.The transcriptional response in the cell death zone and surrounding tissue is dependent on SA. For 2 some of the genes, spatiotemporal regulation is completely lost while for others, the regulation is different in SA-deficient line indicating multiple connections between hormonal signaling modules. The induction of RBOHD NADPH oxidase expression, together with expression of Thioredoxin H gene, occurs specifically in the border region of the lesion during ETI. In plants with silenced RBOHD, ETI is perturbed and virus spread is not arrested at the site of infection. Expression of RBOHD is under the control of SA. On the other hand, RBOHD activity is required for spatial regulation of SA accumulation.We identified an UDP-glucosyltransferase, encoding an enzyme involved in feedback activation of SA biosynthesis, that is derepressed at the border of the lesion in RBOHD silenced plants. Altogether, we revealed a novel aspect of viral ETI, the RBOHD-SA feedback loop required for its spatial regulation.

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Section: Discussionmentioning

confidence: 57%

Spatial accumulation of salicylic acid is regulated by RBOHD in potato immunity against viruses

Lukan¹,

Pompe-Novak²,

Baebler³

et al. 2020

Preprint

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“…Particularly, genes involved in the regulation of SA biosynthetic pathways were found to be upregulated in both model systems. It is well-known that SA induces cell death in plants as a defense response [ 32 , 33 ]. In addition to cell death, we also observed ROS production that precedes visible chlorosis in both systems.…”

Section: Discussionmentioning

confidence: 99%

Transcriptome Analysis Shows Activation of Stress and Defense Responses by Silencing of Chlorophyll Biosynthetic Enzyme CHLI in Transgenic Tobacco

Islam

Bhor

Tanaka

et al. 2020

IJMS

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In the present study, we have shown the transcriptional changes in a chlorosis model transgenic tobacco plant, i-amiCHLI, in which an artificial micro RNA is expressed in a chemically inducible manner to silence the expression of CHLI genes encoding a subunit of a chlorophyll biosynthetic enzyme. Comparison to the inducer-treated and untreated control non-transformants and untreated i-amiCHLI revealed that 3568 and 3582 genes were up- and down-regulated, respectively, in the inducer-treated i-amiCHLI plants. Gene Ontology enrichment analysis of these differentially expressed genes indicated the upregulation of the genes related to innate immune responses, and cell death pathways, and the downregulation of genes for photosynthesis, plastid organization, and primary and secondary metabolic pathways in the inducer-treated i-amiCHLI plants. The cell death in the chlorotic tissues with a preceding H2O2 production was observed in the inducer-treated i-amiCHLI plants, confirming the activation of the immune response. The involvement of activated innate immune response in the chlorosis development was supported by the comparative expression analysis between the two transgenic chlorosis model systems, i-amiCHLI and i-hpHSP90C, in which nuclear genes encoding different chloroplast proteins were similarly silenced.

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“…ICS1 is the key enzyme of SA biosynthesis, which is required for both local and systemic acquired resistance, while SA synthesized through this pathway seems to potentiate plant cell death (Nawrath and Métraux, 1999; Gross et al ., 2006; Strawn et al ., 2007; Garcion et al ., 2008; Chen et al ., 2009). It is well known that SA induces cell death in plants as a defense response (Brodersen et al ., 2005; Radojičić et al ., 2018). We observed the H 2 O 2 production in the chloroplast of Dex-treated i-hpHSP90C plants (Fig.…”

Section: Discussionmentioning

confidence: 99%

Impaired expression of chloroplast HSP90C chaperone activates plant defense responses leading to a disease symptom-like phenotype

Shaikhul

Ashok

Tanaka

et al. 2020

Preprint

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Highlight 27 Induced silencing of HSP90C gene caused the upregulation of stress-responsive 28 genes and the activation of innate immune response, which resulted in the 29 chlorosis development accompanying cell death. 30 31 Abstract 32 RNA-seq analysis of a transgenic tobacco plant, i-hpHSP90C, in which 33 chloroplast HSP90C genes can be silenced in an artificially inducible manner 34 resulting in the development of chlorosis, revealed the up-and down-regulation 35 of 2746 and 3490 genes, respectively. Gene Ontology analysis of these 36 differentially expressed genes indicated the upregulation of ROS-responsive 37 genes, the activation of the innate immunity and cell death pathways, and the 38 downregulation of genes involved in photosynthesis, plastid organization, and cell 39 cycle. Cell death was confirmed by trypan blue staining and electrolyte leakage 40 assay and the H2O2 production by diaminobenzidine staining. The upregulation 41 of ER stress-responsive genes suggested the interplay between ER protein 42 quality control and chloroplast or immune response. The results collectively 43 suggest that the reduced levels of HSP90C chaperone leads the plant to develop 44 chlorosis primarily through the global downregulation of chloroplast and 45 photosynthesis-related genes and additionally through the light-dependent 46 production of ROS, followed by the activation of immune responses including the 47 cell death. 48 49 Transcriptome 52 53 Abbreviations 54 CPRGs, Chloroplast and photosynthesis-related genes; DEGs, Differentially 55 expressed genes; Dex, Dexamethasone; hp-RNA, Hairpin RNA; HSP90C, 56 Chloroplast heat shock protein 90; ROS, Reactive oxygen species; siRNA, Small 57 interfering RNA.58 3

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Salicylic Acid: A Double-Edged Sword for Programed Cell Death in Plants

Cited by 102 publications

References 32 publications

Spatial accumulation of salicylic acid is regulated by RBOHD in potato immunity against viruses

Spatial accumulation of salicylic acid is regulated by RBOHD in potato immunity against viruses

Transcriptome Analysis Shows Activation of Stress and Defense Responses by Silencing of Chlorophyll Biosynthetic Enzyme CHLI in Transgenic Tobacco

Impaired expression of chloroplast HSP90C chaperone activates plant defense responses leading to a disease symptom-like phenotype

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