scholarly journals Transcriptional Dynamics of the Salicylic Acid Response and its Interplay with the Jasmonic Acid Pathway

2019 ◽  
Author(s):  
Richard Hickman ◽  
Marciel Pereira Mendes ◽  
Marcel C. Van Verk ◽  
Anja J.H. Van Dijken ◽  
Jacopo Di Sora ◽  
...  

AbstractThe phytohormone salicylic acid (SA) is a central regulator of plant immunity. Antagonistic and synergistic actions between SA and other defense-associated hormones like jasmonic acid (JA) play key roles in determining the outcome of the plant immune response. To obtain a deeper understanding of SA-mediated transcriptional reprogramming and SA/JA crosstalk, we generated a high-resolution time series of gene expression from Arabidopsis leaves treated with SA alone and a combination of SA and methyl JA (MeJA), sampled at 14 time points over a 16-h period. We found that approximately one-third of the Arabidopsis genome was differentially expressed in response to SA, and temporal changes in gene expression could be partitioned into 45 distinct clusters of process-specific coregulated genes, linked to specific cis-regulatory elements and binding of transcription factors (TFs). Integration of our expression data with information on TF-DNA binding allowed us to generate a dynamic gene regulatory network model of the SA response, recovering known regulators and identifying novel ones. We found that 12% of SA-responsive genes and 69% of the MeJA-responsive genes exhibited antagonistic or synergistic expression levels in the combination treatment. Multi-condition co-clustering of the single- and combined-hormone expression profiles predicted underlying regulatory mechanisms in signal integration. Finally, we identified the TFs ANAC061 and ANAC090 as negative regulators of SA pathway genes and defense against biotrophic pathogens. Collectively, our data provide an unprecedented level of detail about transcriptional changes during the SA response and SA/JA crosstalk, serving as a valuable resource for systems-level network studies and functional plant defense studies.

2021 ◽  
Author(s):  
Young Nam Yang ◽  
Youngseong Kim ◽  
Hyeri Kim ◽  
Su Jin Kim ◽  
Kwang-Moon Cho ◽  
...  

Jasmonic acid (JA) and ethylene (ET) signaling modulate plant defense against necrotrophic pathogens. These hormone pathways lead to transcriptional reprogramming, which is a major part of plant immunity and requires the roles of transcription factors. ET response factors are responsible for the transcriptional regulation of JA/ET-responsive defense genes, among which ORA59 functions as a key regulator of this process and has been implicated in the JA-ET crosstalk. Here, we identified the ERELEE4 as an ORA59-binding cis-element, in addition to the well-characterized GCC box, demonstrating that ORA59 regulates JA/ET-responsive genes through direct binding to these elements in the gene promoters. Notably, ORA59 exhibited differential preference for the GCC box and ERELEE4, depending on whether ORA59 activation is achieved by JA and ET, respectively. Our results provide insights into how ORA59 can generate specific patterns of gene expression dynamics through JA and ET hormone pathways.


Plants ◽  
2020 ◽  
Vol 9 (2) ◽  
pp. 136 ◽  
Author(s):  
Loredana Scalschi ◽  
Eugenio Llorens ◽  
Pilar García-Agustín ◽  
Begonya Vicedo

The jasmonic acid pathway has been considered as the backbone of the response against necrotrophic pathogens. However, a hemi-biotrophic pathogen, such as Pseudomonas syringae, has taken advantage of the crosstalk between the different plant hormones in order to manipulate the responses for its own interest. Despite that, the way in which Pseudomonas syringae releases coronatine to activate jasmonic acid-derived responses and block the activation of salicylic acid-mediated responses is widely known. However, the implication of the jasmonic intermediates in the plant-Pseudomonas interaction is not studied yet. In this work, we analyzed the response of both, plant and bacteria using SiOPR3 tomato plants. Interestingly, SiOPR3 plants are more resistant to infection with Pseudomonas. The gene expression of bacteria showed that, in SiOPR3 plants, the activation of pathogenicity is repressed in comparison to wild type plants, suggesting that the jasmonic acid pathway might play a role in the pathogenicity of the bacteria. Moreover, treatments with JA restore the susceptibility as well as activate the expression of bacterial pathogenicity genes. The observed results suggest that a complete jasmonic acid pathway is necessary for the susceptibility of tomato plants to Pseudomonas syringae.


2019 ◽  
Vol 20 (19) ◽  
pp. 4916 ◽  
Author(s):  
Manoharan ◽  
Qi ◽  
Dhandapani ◽  
Chen ◽  
Rutherford ◽  
...  

Invasive plants are a huge burden on the environment, and modify local ecosystems by affecting the indigenous biodiversity. Invasive plants are generally less affected by pathogens, although the underlying molecular mechanisms responsible for their enhanced resistance are unknown. We investigated expression profiles of three defense hormones (salicylic acid, jasmonic acid, and ethylene) and their associated genes in the invasive weed, Alternanthera philoxeroides, and its native congener, A. sessilis, after inoculation with Rhizoctonia solani. Pathogenicity tests showed significantly slower disease progression in A. philoxeroides compared to A. sessilis. Expression analyses revealed jasmonic acid (JA) and ethylene (ET) expressions were differentially regulated between A. philoxeroides and A. sessilis, with the former having prominent antagonistic cross-talk between salicylic acid (SA) and JA, and the latter showing weak or no cross-talk during disease development. We also found that JA levels decreased and SA levels increased during disease development in A. philoxeroides. Variations in hormonal gene expression between the invasive and native species (including interspecific differences in the strength of antagonistic cross-talk) were identified during R. solani pathogenesis. Thus, plant hormones and their cross-talk signaling may improve the resistance of invasive A. philoxeroides to pathogens, which has implications for other invasive species during the invasion process.


Biomolecules ◽  
2019 ◽  
Vol 9 (1) ◽  
pp. 12 ◽  
Author(s):  
Jie Luo ◽  
Wenxiu Xia ◽  
Pei Cao ◽  
Zheng’ang Xiao ◽  
Yan Zhang ◽  
...  

Plants have evolved a sophisticated system to respond to various stresses. Fungal attack or infection is one of the most important biotic stresses for most plants. During the defense response to fungal infection, the plant hormones jasmonic acid (JA) and salicylic acid (SA) play critical roles. Here, gene expression data on JA/SA treatments and Melampsora larici-populina (MLP) infection were generated. Integrated transcriptome analyses of these data were performed, and 943 genes in total were identified as common responsive genes (CRG). Gene ontology (GO) term analysis revealed that the genes from CRG are generally involved in the processes of stress responses, metabolism, and growth and development. The further cluster analysis of the CRG identified a set of core genes that are involved in the JA/SA-mediated response to fungal defense with distinct gene expression profiles upon JA/SA treatment, which highlighted the different effects of these two hormones on plant fungal defenses. The modifications of several pathways relative to metabolism, biotic stress, and plant hormone signal pathways suggest the possible roles of JA/SA on the regulation of growth and defense responses. Co-expression modules (CMs) were also constructed using the poplar expression data on JA, SA, M. larici-populina, Septoria musiva, and Marssonina brunnea treatment or infection. A total of 23 CMs were constructed, and different CMs clearly exhibited distinct biological functions, which conformably regulated the concerted processes in response to fungal defense. Furthermore, the GO term analysis of different CMs confirmed the roles of JA and SA in regulating growth and defense responses, and their expression profiles suggested that the growth ability was reduced when poplar deployed defense responses. Several transcription factors (TFs) among the CRG in the co-expression network were proposed as hub genes in regulating these processes. According to this study, our data finely uncovered the possible roles of JA/SA in regulating the balance between growth and defense responses by integrating multiple hormone signaling pathways. We were also able to provide more knowledge on how the plant hormones JA/SA are involved in the regulation of the balance between growth and plant defense.


Author(s):  
Huaming He ◽  
Jordi Denecker ◽  
Katrien Van Der Kelen ◽  
Patrick Willems ◽  
Robin Pottie ◽  
...  

Abstract Signaling events triggered by hydrogen peroxide (H2O2) regulate plant growth and defense by orchestrating a genome-wide transcriptional reprogramming. However, the specific mechanisms that govern H2O2-dependent gene expression are still poorly understood. Here, we identify the Arabidopsis Mediator complex subunit MED8 as a regulator of H2O2 responses. The introduction of the med8 mutation in a constitutive oxidative stress genetic background (catalase-deficient, cat2) was associated with enhanced activation of the salicylic acid pathway and accelerated cell death. Interestingly, med8 seedlings were more tolerant to oxidative stress generated by the herbicide methyl viologen (MV) and exhibited transcriptional hyperactivation of defense signaling, in particular salicylic acid- and jasmonic acid-related pathways. The med8-triggered tolerance to MV was manipulated by the introduction of secondary mutations in salicylic acid and jasmonic acid pathways. In addition, analysis of the Mediator interactome revealed interactions with components involved in mRNA processing and microRNA biogenesis, hence expanding the role of Mediator beyond transcription. Notably, MED8 interacted with the transcriptional regulator NEGATIVE ON TATA-LESS, NOT2, to control the expression of H2O2-inducible genes and stress responses. Our work establishes MED8 as a component regulating oxidative stress responses and demonstrates that it acts as a negative regulator of H2O2-driven activation of defense gene expression.


BMC Genomics ◽  
2021 ◽  
Vol 22 (1) ◽  
Author(s):  
E Soltanmohammadi ◽  
Y Zhang ◽  
I Chatzistamou ◽  
H. Kiaris

Abstract Background Genes that belong to the same network are frequently co-expressed, but collectively, how the coordination of the whole transcriptome is perturbed during aging remains unclear. To explore this, we calculated the correlation of each gene in the transcriptome with every other, in the brain of young and older outbred deer mice (P. leucopus and P. maniculatus). Results In about 25 % of the genes, coordination was inversed during aging. Gene Ontology analysis in both species, for the genes that exhibited inverse transcriptomic coordination during aging pointed to alterations in the perception of smell, a known impairment occurring during aging. In P. leucopus, alterations in genes related to cholesterol metabolism were also identified. Among the genes that exhibited the most pronounced inversion in their coordination profiles during aging was THBS4, that encodes for thrombospondin-4, a protein that was recently identified as rejuvenation factor in mice. Relatively to its breadth, abolishment of coordination was more prominent in the long-living P. leucopus than in P. maniculatus but in the latter, the intensity of de-coordination was higher. Conclusions There sults suggest that aging is associated with more stringent retention of expression profiles for some genes and more abrupt changes in others, while more subtle but widespread changes in gene expression appear protective. Our findings shed light in the mode of the transcriptional changes occurring in the brain during aging and suggest that strategies aiming to broader but more modest changes in gene expression may be preferrable to correct aging-associated deregulation in gene expression.


2018 ◽  
Vol 31 (12) ◽  
pp. 1271-1279 ◽  
Author(s):  
Xiaochen Jia ◽  
Haihong Zeng ◽  
Wenxia Wang ◽  
Fuyun Zhang ◽  
Heng Yin

Chitosan oligosaccharide (COS) is an effective plant immunity elicitor; however, its induction mechanism in plants is complex and needs further investigation. In this study, the Arabidopsis–Pseudomonas syringae pv. tomato DC3000 (hereafter called DC3000) interaction was used to investigate the induction effect and the underlying mechanisms of COS. COS is effective in inducing resistance to DC3000 in Arabidopsis, and our results demonstrate that treatment with COS 3 days before DC3000 inoculation provided the most effective resistance. Disease severity in jar1 (jasmonic acid [JA]-deficient mutant), NahG, and sid2 (salicylic acid [SA]-deficient mutants) suggest both the SA and JA pathways are required for the Arabidopsis response to DC3000. COS pretreatment induced resistance in wild type (WT), jar1, and also, although to a lesser degree, in NahG and sid2 plants, implying that the SA and JA pathways play redundant roles in COS-induced resistance to DC3000. In COS-pretreated plants, expression of genes related to the SA pathway (PR1, PR2, and PR5) and SA content increased in both WT and jar1. Moreover, expression of genes related to the JA pathway (PDF1.2 and VSP2) and JA content both increased in WT and NahG. In conclusion, COS induces resistance to DC3000 in Arabidopsis by activating both SA- and JA-mediated pathways, although SA and JA pathways play redundant roles in this COS-induced resistance.


Plants ◽  
2020 ◽  
Vol 9 (5) ◽  
pp. 624 ◽  
Author(s):  
Vicente Montejano-Ramírez ◽  
Ernesto García-Pineda ◽  
Eduardo Valencia-Cantero

Plants face a variety of biotic and abiotic stresses including attack by microbial phytopathogens and nutrient deficiencies. Some bacterial volatile organic compounds (VOCs) activate defense and iron-deficiency responses in plants. To establish a relationship between defense and iron deficiency through VOCs, we identified key genes in the defense and iron-deprivation responses of the legume model Medicago truncatula and evaluated the effect of the rhizobacterial VOC N,N-dimethylhexadecylamine (DMHDA) on the gene expression in these pathways by RT-qPCR. DMHDA increased M. truncatula growth 1.5-fold under both iron-sufficient and iron-deficient conditions compared with untreated plants, whereas salicylic acid and jasmonic acid decreased growth. Iron-deficiency induced iron uptake and defense gene expression. Moreover, the effect was greater in combination with DMHDA. Salicylic acid, Pseudomonas syringae, jasmonic acid, and Botrytis cinerea had inhibitory effects on growth and iron response gene expression but activated defense genes. Taken together, our results showed that the VOC DMHDA activates defense and iron-deprivation pathways while inducing a growth promoting effect unlike conventional phytohormones, highlighting that DMHDA does not mimic jasmonic acid but induces an alternative pathway. This is a novel aspect in the complex interactions between biotic and abiotic stresses.


2020 ◽  
Vol 71 (17) ◽  
pp. 5256-5268 ◽  
Author(s):  
Jian Chen ◽  
Michael Clinton ◽  
Guang Qi ◽  
Daowen Wang ◽  
Fengquan Liu ◽  
...  

Abstract As a plant hormone, salicylic acid (SA) plays essential roles in plant defense against biotrophic and hemibiotrophic pathogens. Significant progress has been made in understanding the SA biosynthesis pathways and SA-mediated defense signaling networks in the past two decades. Plant defense responses involve rapid and massive transcriptional reprogramming upon the recognition of pathogens. Plant transcription factors and their co-regulators are critical players in establishing a transcription regulatory network and boosting plant immunity. A multitude of transcription factors and epigenetic regulators have been discovered, and their roles in SA-mediated defense responses have been reported. However, our understanding of plant transcriptional networks is still limited. As such, novel genomic tools and bioinformatic techniques will be necessary if we are to fully understand the mechanisms behind plant immunity. Here, we discuss current knowledge, provide an update on the SA biosynthesis pathway, and describe the transcriptional and epigenetic regulation of SA-mediated plant immune responses.


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