An Arabidopsis thaliana leucine-rich repeat protein harbors an adenylyl cyclase catalytic center and affects responses to pathogens

Bianchet, Chantal; Wong, Aloysius; Quaglia, Mara; Alqurashi, May; Gehring, Chris; Ntoukakis, Vardis; Pasqualini, Stefania

doi:10.1016/j.jplph.2018.10.025

Cited by 59 publications

(72 citation statements)

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“…By contrast, the decrease in cAMP content in cAS plants led to a reduced resistance of the transgenic lines to the avirulent pathogen PstAvrB , associated with an impairment in hypersensitive cell death. More recently, a leucine‐rich repeat protein with adenylyl cyclase activity (AtLRRAC1) has been identified in Arabidopsis thaliana (Bianchet et al ., ). Interestingly, and in line with our results, knockout mutants of AtLRRAC1 showed compromised immune responses to Pseudomonas syringae (Bianchet et al ., ).…”

Section: Discussionmentioning

confidence: 97%

“…More recently, a leucine‐rich repeat protein with adenylyl cyclase activity (AtLRRAC1) has been identified in Arabidopsis thaliana (Bianchet et al ., ). Interestingly, and in line with our results, knockout mutants of AtLRRAC1 showed compromised immune responses to Pseudomonas syringae (Bianchet et al ., ). The inoculation of Arabidopsis plants with avirulent strains of Pseudomonas syringae pv.…”

Section: Discussionmentioning

confidence: 97%

“…This situation is firstly due to its low cellular concentration (typically between 40 and 170 pmol g −1 fresh weight (FW)) and secondly to the technical difficulties related to its detection (Gehring, ; Gehring and Turek, ). Moreover, plant adenylyl‐cyclases (AC) and cAMP phosphodiesterases (PDE), responsible for cAMP synthesis and catabolism, respectively, have not been isolated and/or fully characterized, although evidence of their activity has been reported (Gehring and Turek, ; Bianchet et al ., ).…”

Section: Introductionmentioning

confidence: 97%

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Genetic buffering of cyclic AMP in Arabidopsis thaliana compromises the plant immune response triggered by an avirulent strain of Pseudomonas syringae pv. tomato

et al. 2019

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Cyclic AMP plays important roles in different physiological processes, including plant defence responses. However, as little information is known on plant enzymes responsible for cAMP production/degradation, studies of cAMP functions have relied, to date, on non-specific pharmacological approaches. We therefore developed a more reliable approach, producing transgenic Arabidopsis thaliana lines overexpressing the 'cAMP-sponge' (cAS), a genetic tool that specifically buffers cAMP levels. In response to an avirulent strain of Pseudomonas syringae pv. tomato (PstAvrB), cAS plants showed a higher bacterial growth and a reduced hypersensitive cell death in comparison with wild-type (WT) plants. The low cAMP availability after pathogen infection delayed cytosolic calcium elevation, as well as hydrogen peroxide increase and induction of redox systems. The proteomic analysis, performed 24 h post-infection, indicated that a core of 49 proteins was modulated in both genotypes, while 16 and 42 proteins were uniquely modulated in WT and cAS lines, respectively. The involvement of these proteins in the impairment of defence response in cAS plants is discussed in this paper. Moreover, in silico analysis revealed that the promoter regions of the genes coding for proteins uniquely accumulating in WT plants shared the CGCG motif, a target of the calcium-calmodulinbinding transcription factor AtSR1 (Arabidopsis thaliana signal responsive1). Therefore, following pathogen perception, the low free cAMP content, altering timing and levels of defence signals, and likely acting in part through the mis-regulation of AtSR1 activity, affected the speed and strength of the immune response. Role of cAMP in plant immune response 597Generation of Arabidopsis cAS-mCherry plants expressing the NES-YC3.6 probeThe Arabidopsis Col-0 cAS-transgenic lines were crossed with the Col-0 pUBQ10-NES-YC3.6 line reported in Krebs et al. (2012). Seeds from cross-pollinated flowers were surface sterilized by vapour-

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Section: Discussionmentioning

confidence: 97%

Section: Discussionmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 97%

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Genetic buffering of cyclic AMP in Arabidopsis thaliana compromises the plant immune response triggered by an avirulent strain of Pseudomonas syringae pv. tomato

et al. 2019

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“…The C2 clade includes the Arabidopsis NLR gene called Resistance to Pseudomonas Syringae 2 (RPS2), whose protein product acts as a guard detecting pathogen effector triggered modification to RPM1-INTERACTING PROTEIN 4 (RIN4) (47,48). The C3 clade includes Arabidopsis LRRAC1 (49). The C3 clade is characterised by a large expansion of monocot NLRs including 7 NLRs with known defence functions (S4 Table).…”

Section: Aquatic Plants Have Lost Most Of the Nlr Plant Immune Receptorsmentioning

confidence: 99%

Convergent loss of an EDS1/PAD4 signalling pathway in several plant lineages predicts new components of plant immunity and drought response

Baggs

Thanki

O’Grady

et al. 2019

Preprint

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Drought and immunity pathway reduction in aquatic environments 2 AbstractThe transition of plants from sea to land sparked an arms race with pathogens. The increased susceptibility of land plants is largely thought to be due to their dependence on micro-organisms for nutrients; the ensuing co-evolution has shaped the plant immune system. By profiling the immune receptors across flowering plants, we identified species with low numbers of NLR immune receptors. Interestingly, four of these species represent distinct lineages of monocots and dicots that returned to the aquatic lifestyle. Both aquatic monocot and dicot species lost the same well-known downstream immune signalling complex (EDS1-PAD4). This observation inspired us to look for other genes with a similar loss pattern and allowed us to predict putative new components of plant immunity. Gene expression analyses confirmed that a group of these genes was differentially expressed under pathogen infection. Excitingly, another subset of these genes was differentially expressed upon drought. Collectively, our study reveals the minimal plant immune system required for life under water, and highlights additional components required for the life of land plants.Drought and immunity pathway reduction in aquatic environments 3 Author summaryPlant resistance to pathogens is commonly mediated by a complex gene family, known as NLRs. Upon pathogen infection, changes in the cellular environment trigger NLR activation and subsequent defence responses. Despite the dependence of agricultural practices on NLR genes to control pathogen load, relatively little is known about this gene family outside of model crop species. In this study, we identified a convergent reduction in the NLR gene family among two lineages of aquatic plants. Furthermore, we established that NLR reduction occurred in conjunction with the loss of a common immune signalling pathway. Subsequently, we identified other genes convergently lost in aquatic species and propose these as candidate components of the plant immune signalling pathway. In addition, we revealed components of the agronomically important drought response to be lost in aquatic plants. This study adds to our understanding of the complex interactions between environment and response to biotic stress, widely known as the disease triangle. The pathways identified in this study shed further light on the link between responses to drought and disease.Drought and immunity pathway reduction in aquatic environments

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“…Moreover, the strength of activity of transmembrane adenylate cyclases (TACs) and soluble adenylate cyclases (SACs) was dependent on the infectious agent, despite the non-specific interaction; infection with Rlv led to the most pronounced activation of TACs and SACs in pea root cells compared with the activation following infection with Psp and short-term contact with Cms [1,3]. Possible mechanisms for modulating the activity of both forms of adenylate cyclases (ACs) under biotic stress may include both ligand-receptor interactions [4] and the influence of calcium ions [5]. The latter can act as an intracellular second messenger, and its concentration can change rapidly following infection.…”

Section: Introductionmentioning

confidence: 99%

Regulation of the activity of adenylate cyclases by hydrogen peroxide in pea root cells Infected with pathogens and a mutualist

Kuzakova

Ломоватская

Романенко

et al. 2020

Izvestiâ vuzov. Prikladnaâ himiâ i biotehnologiâ

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This study examines the effect of a range of exogenous concentrations of hydrogen peroxide on the activity of transmembrane and soluble adenylate cyclases (EC 4.6.1.1) contained in root cells of pea seedlings infected with one of the following: Rhizobium leguminosarum bv. Viciae, Pseudomonas syringae pv. Pisi, and Clavibacter michiganensis ssp. sepedonicus. The results showed that the pool of intracellular H2O2 increased when pea roots were infected with bacteria regardless of type. The study analysed the concentration of intracellular cyclic adenosine monophosphate, a product of the adenosine triphosphate cyclization reaction catalyzed by transmembrane and soluble adenylate cyclases. The concentration of intracellular cyclic adenosine monophosphate increased when infected with either Rhizobium leguminosarum bv. viciae or Clavibacter michiganensis ssp. Sepedonicus; however, the concentration decreased by 20% when infected with Pseudomonas syringae pv. Pisi. The in vitro activity of soluble and transmembrane adenylate cyclases from pea root cells inoculated with Rhizobium leguminosarum bv. viciae was H2O2 dose-dependent: 100 nM of H2O2 reduced the activity of soluble and transmembrane adenylate cyclases slightly, while 26 µM inhibited their activity by 50–60%. When infected with Pseudomonas syringae pv. pisi, the reduction in the activity of soluble and transmembrane adenylate cyclases was independent of the concentrations of H2O2 in the range investigated. When infected with Clavibacter michiganensis ssp. sepedonicus, 100 nM of H2O2 inhibited the activity of transmembrane adenylate cyclases, although enhancing the activity of soluble adenylate cyclases. On the contrary, concentrations of H2O2 of 2.6 and 26 µM increased the activity of transmembrane adenylate cyclases and inhibited the activity of soluble adenylate cyclases. It can be concluded that the specific concentration of second messengers in plant cells depends on the specificity of the biotic stressor and forms, inter alia, by their mutual influence on the components of other plant signaling systems.

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An Arabidopsis thaliana leucine-rich repeat protein harbors an adenylyl cyclase catalytic center and affects responses to pathogens

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Cited by 59 publications

References 97 publications

Genetic buffering of cyclic AMP in Arabidopsis thaliana compromises the plant immune response triggered by an avirulent strain of Pseudomonas syringae pv. tomato

Genetic buffering of cyclic AMP in Arabidopsis thaliana compromises the plant immune response triggered by an avirulent strain of Pseudomonas syringae pv. tomato

Convergent loss of an EDS1/PAD4 signalling pathway in several plant lineages predicts new components of plant immunity and drought response

Regulation of the activity of adenylate cyclases by hydrogen peroxide in pea root cells Infected with pathogens and a mutualist

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