HISTONE DEACETYLASE 6 suppresses salicylic acid biosynthesis to repress autoimmunity

2021 ◽  
Author(s):  
Zhenjiang Wu ◽  
Lei He ◽  
Ye Jin ◽  
Jing Chen ◽  
Huazhong Shi ◽  
...  
Keyword(s):  
Salicylic Acid ◽  
Histone Deacetylase ◽  
Systemic Acquired Resistance ◽  
Plant Immunity ◽  
Acquired Resistance ◽  
Negative Regulator ◽  
Histone Deacetylase 6 ◽  
Promoter Regions ◽  
Calmodulin Binding ◽  
H3 Acetylation

Abstract Salicylic acid (SA) plays an important role for plant immunity, especially resistance against biotrophic pathogens. SA quickly accumulates after pathogen attack to activate downstream immunity events and is normally associated with a tradeoff in plant growth. Therefore, the SA level in plants has to be strictly controlled when pathogens are absent, but how this occurs is not well understood. Previously we found that in Arabidopsis (Arabidopsis thaliana), HISTONE DEACETYLASE 6 (HDA6), a negative regulator of gene expression, plays an essential role in plant immunity since its mutation allele shining 5 (shi5) exhibits autoimmune phenotypes. Here we report that this role is mainly through suppression of SA biosynthesis: first, the autoimmune phenotypes and higher resistance to Pst DC3000 of shi5 mutants depended on SA; second, SA significantly accumulated in shi5 mutants; third, HDA6 repressed SA biosynthesis by directly controlling the expression of CALMODULIN BINDING PROTEIN 60g (CBP60g) and SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1 (SARD1). HDA6 bound to the chromatin of CBP60g and SARD1 promoter regions, and histone H3 acetylation was highly enriched within these regions. Furthermore, the transcriptome of shi5 mutants mimicked that of plants treated with exogenous SA or attacked by pathogens. All these data suggest that HDA6 is vital for plants in finely controlling the SA level to regulate plant immunity.

scholarly journals Spatial and temporal regulation of biosynthesis of the plant immune signal salicylic acid

2015 ◽  
Vol 112 (30) ◽  
pp. 9166-9173 ◽  
Author(s):  
Xiao-yu Zheng ◽  
Mian Zhou ◽  
Heejin Yoo ◽  
Jose L. Pruneda-Paz ◽  
Natalie Weaver Spivey ◽  
...  
Keyword(s):  
Salicylic Acid ◽  
Systemic Acquired Resistance ◽  
Acquired Resistance ◽  
Signal Transduction Pathway ◽  
Temporal Regulation ◽  
Calmodulin Binding ◽  
Regulation Of Biosynthesis ◽  
Pathogen Entry ◽  
Transcription Activators ◽  
Transcriptional Induction

The plant hormone salicylic acid (SA) is essential for local defense and systemic acquired resistance (SAR). When plants, such as Arabidopsis, are challenged by different pathogens, an increase in SA biosynthesis generally occurs through transcriptional induction of the key synthetic enzyme isochorismate synthase 1 (ICS1). However, the regulatory mechanism for this induction is poorly understood. Using a yeast one-hybrid screen, we identified two transcription factors (TFs), NTM1-LIKE 9 (NTL9) and CCA1 HIKING EXPEDITION (CHE), as activators of ICS1 during specific immune responses. NTL9 is essential for inducing ICS1 and two other SA synthesis-related genes, PHYTOALEXIN-DEFICIENT 4 (PAD4) and ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1), in guard cells that form stomata. Stomata can quickly close upon challenge to block pathogen entry. This stomatal immunity requires ICS1 and the SA signaling pathway. In the ntl9 mutant, this response is defective and can be rescued by exogenous application of SA, indicating that NTL9-mediated SA synthesis is essential for stomatal immunity. CHE, the second identified TF, is a central circadian clock oscillator and is required not only for the daily oscillation in SA levels but also for the pathogen-induced SA synthesis in systemic tissues during SAR. CHE may also regulate ICS1 through the known transcription activators CALMODULIN BINDING PROTEIN 60g (CBP60g) and SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1 (SARD1) because induction of these TF genes is compromised in the che-2 mutant. Our study shows that SA biosynthesis is regulated by multiple TFs in a spatial and temporal manner and therefore fills a gap in the signal transduction pathway between pathogen recognition and SA production.

Salicylic Acid: Biosynthesis and Signaling

2021 ◽  
Vol 72 (1) ◽  
Author(s):  
Yujun Peng ◽  
Jianfei Yang ◽  
Xin Li ◽  
Yuelin Zhang
Keyword(s):  
Salicylic Acid ◽  
Systemic Acquired Resistance ◽  
Current Knowledge ◽  
Plant Immunity ◽  
Acquired Resistance ◽  
Annual Review ◽  
Publication Date ◽  
Basal Defense ◽  
Made In ◽  
Key Questions

Salicylic acid (SA) is an essential plant defense hormone that promotes immunity against biotrophic and semibiotrophic pathogens. It plays crucial roles in basal defense and the amplification of local immune responses, as well as the establishment of systemic acquired resistance. During the past three decades, immense progress has been made in understanding the biosynthesis, homeostasis, perception, and functions of SA. This review summarizes the current knowledge regarding SA in plant immunity and other biological processes. We highlight recent breakthroughs that substantially advanced our understanding of how SA is biosynthesized from isochorismate, how it is perceived, and how SA receptors regulate different aspects of plant immunity. Some key questions in SA biosynthesis and signaling, such as how SA is produced via another intermediate benzoic acid and how SA affects the activities of its receptors in the transcriptional regulation of defense genes, remain to be addressed. Expected final online publication date for the Annual Review of Plant Biology, Volume 72 is May 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

scholarly journals Arabidopsis CALMODULIN-BINDING PROTEIN 60b plays dual roles in plant immunity

2021 ◽  
Author(s):  
Weijie Huang ◽  
Zhongshou Wu ◽  
Hainan Tian ◽  
Xin Li ◽  
Yuelin Zhang
Keyword(s):  
Systemic Acquired Resistance ◽  
Binding Protein ◽  
Plant Immunity ◽  
Interleukin 1 ◽  
Constitutive Expression ◽  
Defense Responses ◽  
Negative Regulator ◽  
Loss Of Function ◽  
Constitutive Defense ◽  
Calmodulin Binding

AbstractArabidopsis SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1 (SARD1) and CALMODULIN-BINDING PROTEIN 60g (CBP60g) are two master transcription factors that regulate many defense-related genes in plant immunity. They are required for immunity downstream of the receptor-like protein SUPPRESSOR OF NPR1-1, CONSTITUTIVE 2 (SNC2). Constitutive defense responses in the gain-of-function autoimmune snc2-1D mutant are modestly affected by either sard1 or cbp60g single mutants, but completely suppressed by the sard1 cbp60g double mutant. Here we report that CBP60b, another member of the CBP60 family, also functions as a positive regulator of SNC2-mediated immunity. Loss-of-function mutations of CBP60b suppress the constitutive expression of SARD1 and enhanced disease resistance in cbp60g-1 snc2-1D, whereas over-expression of CBP60b leads to elevated SARD1 expression and constitutive defense responses. In addition, transient expression of CBP60b in Nicotiana benthamiana activates the expression of the pSARD1::luciferase reporter gene. Chromatin immunoprecipitation assay further showed that CBP60b is recruited to the promoter region of SARD1, suggesting that it directly regulates SARD1 expression. Interestingly, knocking out CBP60b in the wild type background leads to ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1)-dependent autoimmunity, suggesting that CBP60b is required for the expression of a guardee/decoy or a negative regulator in immunity mediated by receptors carrying an N-terminal TIR (Toll-interleukin-1 receptor-like) domain.Significance statementArabidopsis SARD1 serves as a master transcription factor in plant immunity. In this study, we showed that CBP60b positively regulates SARD1 expression, and TIR signaling is activated when CBP60b is inactivated.

scholarly journals The plastidial exporter Enhanced Disease Susceptibility 5 is required for the biosynthesis of N-hydroxy pipecolic acid

2019 ◽  
Author(s):  
Dmitrij Rekhter ◽  
Lennart Mohnike ◽  
Kirstin Feussner ◽  
Krzysztof Zienkiewicz ◽  
Yuelin Zhang ◽  
...  
Keyword(s):  
Salicylic Acid ◽  
Strong Evidence ◽  
Systemic Acquired Resistance ◽  
Disease Susceptibility ◽  
Plant Immunity ◽  
Active Form ◽  
Acquired Resistance ◽  
Pipecolic Acid

AbstractPipecolic acid is essential for the establishment of systemic acquired resistance in plants. It is synthesized in the plastid and further processed in the cytosol to its active form N-hydroxy pipecolic acid. Here we provide strong evidence that the exporter Enhanced Disease Susceptibility 5 is required for the biosynthesis of not only salicylic acid, but also N-hydroxy pipecolic acid, suggesting that it represents a convergent point of plant immunity.

scholarly journals Systemic Acquired Resistance in Canola Is Linked with Pathogenesis-Related Gene Expression and Requires Salicylic Acid

2007 ◽  
Vol 97 (7) ◽  
pp. 794-802 ◽  
Author(s):  
Shobha D. Potlakayala ◽  
Darwin W. Reed ◽  
Patrick S. Covello ◽  
Pierre R. Fobert
Keyword(s):  
Salicylic Acid ◽  
Pseudomonas Syringae ◽  
Systemic Acquired Resistance ◽  
Induced Defense ◽  
Acquired Resistance ◽  
Microbial Pathogens ◽  
Broad Host Range ◽  
Avirulent Strain ◽  
Enhanced Resistance ◽  
Pathogenesis Related

Systemic acquired resistance (SAR) is an induced defense response that confers long-lasting protection against a broad range of microbial pathogens. Here we show that treatment of Brassica napus plants with the SAR-inducing chemical benzo-(1,2,3)-thiadiazole-7-carbothioic acid S-methyl ester (BTH) significantly enhanced resistance against virulent strains of the bacterial pathogen Pseudomonas syringae pv. maculicola and the fungal pathogen Leptosphaeria maculans. Localized preinoculation of plants with an avirulent strain of P. syringae pv. maculicola also enhanced resistance to these pathogens but was not as effective as BTH treatment. Single applications of either SAR-inducing pretreatment were effective against P. syringae pv. maculicola, even when given more than 3 weeks prior to the secondary challenge. The pretreatments also led to the accumulation of pathogenesis-related (PR) genes, including BnPR-1 and BnPR-2, with higher levels of transcripts observed in the BTH-treatment material. B. napus plants expressing a bacterial salicylate hydroxylase transgene (NahG) that metabolizes salicylic acid to catechol were substantially compromised in SAR and accumulated reduced levels of PR gene transcripts when compared with untransformed controls. Thus, SAR in B. napus displays many of the hallmarks of classical SAR including long lasting and broad host range resistance, association with PR gene activation, and a requirement for salicylic acid.

scholarly journals Genome-wide identification, evolution, and expression analysis of the NPR1-like gene family in pears

PeerJ ◽  
2021 ◽  
Vol 9 ◽  
pp. e12617
Author(s):  
Yarui Wei ◽  
Shuliang Zhao ◽  
Na Liu ◽  
Yuxing Zhang
Keyword(s):  
Gene Family ◽  
Stress Responses ◽  
Systemic Acquired Resistance ◽  
Acquired Resistance ◽  
Signal Transduction Pathway ◽  
Promoter Regions ◽  
Systematic Analysis ◽  
Genome Wide ◽  
Pathogenesis Related ◽  
Genome Level

The NONEXPRESSOR OF PATHOGENESIS-RELATED GENES 1 (NPR1) plays a master regulatory role in the salicylic acid (SA) signal transduction pathway and plant systemic acquired resistance (SAR). Members of the NPR1-like gene family have been reported to the associated with biotic/abiotic stress in many plants, however the genome-wide characterization of NPR1-like genes has not been carried out in Chinese pear (Pyrus bretschneideri Reld). In this study, a systematic analysis was conducted on the characteristics of the NPR1-like genes in P. bretschneideri Reld at the whole-genome level. A total nine NPR1-like genes were detected which eight genes were located on six chromosomes and one gene was mapped to scaffold. Based on the phylogenetic analysis, the nine PbrNPR1-like proteins were divided into three clades (Clades I–III) had similar gene structure, domain and conserved motifs. We sorted the cis-acting elements into three clades, including plant growth and development, stress responses, and hormone responses in the promoter regions of PbrNPR1-like genes. The result of qPCR analysis showed that expression diversity of PbrNPR1-like genes in various tissues. All the genes were up-regulated after SA treatment in leaves except for Pbrgene8896. PbrNPR1-like genes showed circadian rhythm and significantly different expression levels after inoculation with Alternaria alternata. These findings provide a solid insight for understanding the functions and evolution of PbrNPR1-like genes in Chinese pear.

scholarly journals Identification and Cloning of a Negative Regulator of Systemic Acquired Resistance, SNI1, through a Screen for Suppressors of npr1-1

Cell ◽  
1999 ◽  
Vol 98 (3) ◽  
pp. 329-339 ◽  
Author(s):  
Xin Li ◽  
Yuelin Zhang ◽  
Joseph D Clarke ◽  
Yan Li ◽  
Xinnian Dong
Keyword(s):  
Systemic Acquired Resistance ◽  
Acquired Resistance ◽  
Negative Regulator
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