scholarly journals ‘Candidatus Liberibacter asiaticus’-Encoded BCP Peroxiredoxin Suppresses Lipopolysaccharide-Mediated Defense Signaling and Nitrosative Stress in Planta

2021 ◽  
Author(s):  
Mukesh Jain ◽  
Lulu Cai ◽  
Ian Black ◽  
Parastoo Azadi ◽  
Russell Carlson ◽  
...  
Keyword(s):  
Systemic Acquired Resistance ◽  
Nitrosative Stress ◽  
Acquired Resistance ◽  
Primary Source ◽  
In Planta ◽  
Callose Deposition ◽  
Xanthomonas Perforans ◽  
Pathogen Invasion ◽  
Genomic Studies ◽  
Candidatus Liberibacter

The lipopolysaccharides (LPS) of Gram-negative bacteria trigger a nitrosative and oxidative burst in both animals and plants during pathogen invasion. Liberibacter crescens strain BT-1 is a surrogate for functional genomic studies of the uncultured pathogenic ‘Candidatus Liberibacter’ spp. that are associated with severe diseases such as citrus greening and potato zebra chip. Structural determination of L. crescens LPS revealed the presence of a very long chain fatty acid (VLCFA) modification. L. crescens LPS pretreatment suppressed growth of Xanthomonas perforans on non-host tobacco (Nicotiana benthamiana) and X. citri subsp. citri on host citrus (Citrus sinensis, confirming bioactivity of L. crescens LPS in activation of systemic acquired resistance (SAR). L. crescens LPS elicited a rapid burst of nitric oxide (NO) in suspension cultured tobacco cells. Pharmacological inhibitor assays confirmed that arginine-utilizing NO synthase (NOS) activity was the primary source of NO generation elicited by L. crescens LPS. LPS treatment also resulted in biological markers of NO-mediated SAR activation, including an increase in the glutathione (GSH) pool, callose deposition and activation of the salicylic acid (SA) and azelaic acid (AzA) signaling networks. Transient expression of ‘Ca. L. asiaticus’ BCP peroxiredoxin in tobacco compromised AzA signaling, a prerequisite for LPS-triggered SAR. Western blot analyses revealed that ‘Ca. L. asiaticus’ BCP peroxiredoxin prevented peroxynitrite-mediated tyrosine nitration in tobacco. ‘Ca. L. asiaticus’ BCP peroxiredoxin (a) attenuates NO-mediated SAR signaling and (b) scavenges peroxynitrite radicals, which would facilitate repetitive cycles of ‘Ca. L. asiaticus’ acquisition and transmission by fecund psyllids throughout the limited flush period in citrus.

scholarly journals Comparative Efficacy of Systemic Acquired Resistance-Inducing Compounds Against Rust Infection in Sunflower Plants

2007 ◽  
Vol 97 (2) ◽  
pp. 179-186 ◽  
Author(s):  
Esther Amzalek ◽  
Yigal Cohen
Keyword(s):  
Systemic Acquired Resistance ◽  
Acquired Resistance ◽  
Foliar Spray ◽  
Racemic Mixture ◽  
In Planta ◽  
Butanoic Acid ◽  
Defense Compounds ◽  
Rust Infection ◽  
Puccinia Helianthi ◽  
Full Protection

Four inducers of systemic acquired resistance (SAR) were examined for their efficacy in controlling rust infection caused by Puccinia helianthi in sunflower plants. Of the four compounds, DL-3-amino-n-butanoic acid (DL-β-aminobutyric acid [BABA]) was the most effective and sodium salicylate (NaSA) was the least effective in protecting against rust. In leaf disk assays, full protection was obtained with BABA at 25 μg/ml, benzodiathiazol-S-methyl ester (BTH) at 100 μg/ml, 2,6-di-chloroisonicotinic acid (INA) at 100 μg/ml, and NaSA at >200 μg/ml. L-2-amino-n-butanoic acid (AABA) was partially effective, whereas N-methyl-BABA and 4-aminobutnoic acid (GABA) were ineffective. The R-enantiomer of BABA, but not the S-enantiomer, was more effective than the racemic mixture. In intact plants, BABA applied as a foliar spray or a root dip, before or after (up to 48 h) inoculation, provided significant protection for 8 days. BTH, INA, and NaSA were less protective and more phytotoxic compared with BABA. BABA did not affect urediospore germination, germ tube growth, appressorial formation, or initial ingress of P. helianthi, but strongly suppressed mycelial colonization in the mesophyll and, consequently, pustule and urediospore formation. No accumulation of defense compounds (phenolics, lignin, or callose) was detected in BABA-treated inoculated or noninoculated plants. This is the first report on the activity of BABA against an obligate Basidomycete pathogen in planta.

scholarly journals N-hydroxy-pipecolic acid is a mobile signal that induces systemic disease resistance in Arabidopsis

2018 ◽  
Author(s):  
Yun Chu Chen ◽  
Eric C. Holmes ◽  
Jakub Rajniak ◽  
Jung-Gun Kim ◽  
Sandy Tang ◽  
...  
Keyword(s):  
Disease Resistance ◽  
Systemic Acquired Resistance ◽  
Systemic Disease ◽  
Acquired Resistance ◽  
Bacterial Pathogen ◽  
Pipecolic Acid ◽  
In Planta ◽  
Global Response ◽  
Promising Target ◽  
Pathogenesis Related

AbstractSystemic acquired resistance (SAR) is a global response in plants induced at the site of infection that leads to long-lasting and broad-spectrum disease resistance at distal, uninfected tissues. Despite the importance of this priming mechanism, the identity of the mobile defense signal that moves systemically throughout plants to initiate SAR has remained elusive. In this paper, we describe a new metabolite, N-hydroxy-pipecolic acid (N-OH-Pip), and provide evidence that this molecule is a mobile signal that plays a central role in initiating SAR signal transduction in Arabidopsis thaliana. We demonstrate that FLAVIN-DEPENDENT MONOOXYGENASE 1 (FMO1), a key regulator of SAR-associated defense priming, can synthesize N-OH-Pip from pipecolic acid in planta, and exogenously applied N-OH-PIP moves systemically in Arabidopsis and can rescue the SAR-deficiency of fmo1 mutants. We also demonstrate that N-OH-Pip treatment causes systemic changes in the expression of pathogenesis-related genes and metabolic pathways throughout the plant, and enhances resistance to a bacterial pathogen. This work provides new insight into the chemical nature of a mobile signal for SAR and also suggests that the N-OH-Pip pathway is a promising target for metabolic engineering to enhance disease resistance.

scholarly journals Conservation of N-hydroxy-pipecolic acid-mediated systemic acquired resistance in crop plants

2019 ◽  
Author(s):  
Eric C. Holmes ◽  
Yun-Chu Chen ◽  
Elizabeth Sattely ◽  
Mary Beth Mudgett
Keyword(s):  
Systemic Acquired Resistance ◽  
Acquired Resistance ◽  
Signal Propagation ◽  
Crop Plants ◽  
Pipecolic Acid ◽  
List Type ◽  
In Planta ◽  
Long Distance ◽  
Plant Kingdom ◽  
Promising Strategy

SUMMARYSignal propagation and the coordination of whole-organism responses in plants rely heavily on small molecules. Systemic acquired resistance (SAR) is one such process in which long-distance signaling activates immune responses in uninfected tissue as a way to limit the spread of a primary, localized infection. Recently, N-hydroxy pipecolic acid (NHP) was discovered and shown to coordinate SAR in Arabidopsis. Here, we provide metabolic and biochemical evidence that NHP is conserved across the plant kingdom and demonstrate a role for NHP in mediating SAR responses in tomato and pepper. We reconstituted the NHP biosynthetic pathway in planta and show that transient expression of two NHP biosynthetic genes in tomato induces enhanced resistance to a bacterial pathogen in distal tissue. Our results suggest engineering strategies to induce NHP-mediated SAR are a promising route to improve broad-spectrum pathogen resistance in crops.IN BRIEFEngineering NHP production is a promising strategy to enhance disease resistance in crops.HIGHLIGHTSArabidopsis N-hydroxy-pipecolic acid (NHP) pathway is conserved across the plant kingdomApplication of NHP to tomato and pepper plants induces a robust SAR responseMetabolic engineering of the Arabidopsis NHP pathway in Solanum lycopersicum leads to enhanced NHP production and defense primingGenetic engineering for enhanced NHP production is a promising strategy to protect crop plants from multiple pathogens

scholarly journals A Single Effector Protein, AvrRpt2EA, from Erwinia amylovora Can Cause Fire Blight Disease Symptoms and Induces a Salicylic Acid–Dependent Defense Response

2018 ◽  
Vol 31 (11) ◽  
pp. 1179-1191 ◽  
Author(s):  
Susan Schröpfer ◽  
Christoph Böttcher ◽  
Thomas Wöhner ◽  
Klaus Richter ◽  
John Norelli ◽  
...  
Keyword(s):  
Salicylic Acid ◽  
Fire Blight ◽  
Systemic Acquired Resistance ◽  
Erwinia Amylovora ◽  
Acquired Resistance ◽  
Inducible Promoter ◽  
Marker Genes ◽  
Effector Protein ◽  
In Planta ◽  
Natural Fire

The AvrRpt2EA effector protein of Erwinia amylovora is important for pathogen recognition in the fire blight–resistant crabapple Malus × robusta 5; however, little is known about its role in susceptible apples. To study its function in planta, we expressed a plant-optimized version of AvrRpt2EA driven by a heat shock–inducible promoter in transgenic plants of the fire blight–susceptible cultivar Pinova. After induced expression of AvrRpt2EA, transgenic lines showed shoot necrosis and browning of older leaves, with symptoms similar to natural fire blight infections. Transgenic expression of this effector protein resulted in an increase in the expression of the salicylic acid (SA)-responsive PR-1 gene but, also, in the levels of SA and its derivatives, with diverse kinetics in leaves of different ages. In contrast, no increase of expression levels of VSP2 paralogs, used as marker genes for the activation of the jasmonic acid (JA)-dependent defense pathway, could be detected, which is in agreement with metabolic profiling of JA and its derivatives. Our work demonstrates that AvrRpt2EA acts as a virulence factor and induces the formation of SA and SA-dependent systemic acquired resistance.

scholarly journals Elicitin Genes Expressed In Vitro by Certain Tobacco Isolates of Phytophthora parasitica Are Down Regulated During Compatible Interactions

2001 ◽  
Vol 14 (3) ◽  
pp. 326-335 ◽  
Author(s):  
Virginie Colas ◽  
Sandrine Conrod ◽  
Paul Venard ◽  
Harald Keller ◽  
Pierre Ricci ◽  
...  
Keyword(s):  
Hypersensitive Response ◽  
Systemic Acquired Resistance ◽  
Acquired Resistance ◽  
Compatible Interaction ◽  
Phytophthora Parasitica ◽  
In Planta ◽  
Black Shank ◽  
Phytophthora Spp ◽  
Compatible Interactions

Phytophthora spp. secrete proteins called elicitins in vitro that can specifically induce hypersensitive response and systemic acquired resistance in tobacco. In Phytophthora parasitica, the causal agent of black shank, most isolates virulent on tobacco are unable to produce elicitins in vitro. Recently, however, a few elicitin-producing P. parasitica strains virulent on tobacco have been isolated. We investigated the potential diversity of elicitin genes in P. parasitica isolates belonging to different genotypes and with various virulence levels toward tobacco as well as elicitin expression pattern in vitro and in planta. Although elicitins are encoded by a multigene family, parA1 is the main elicitin gene expressed. This gene is highly conserved among isolates, regardless of the elicitin production and virulence levels toward tobacco. Moreover, we show that elicitin-producing P. parasitica isolates virulent on tobacco down regulate parA1 expression during compatible interactions, whichever host plant is tested. Conversely, one elicitin-producing P. parasitica isolate that is pathogenic on tomato and avirulent on tobacco still expresses parA1 in the compatible interaction. Therefore, some P. parasitica isolates may evade tobacco recognition by down regulating parA1 in planta. The in planta down regulation of parA1 may constitute a suitable mechanism for P. parasitica to infect tobacco without deleterious consequences for the pathogen.

scholarly journals Abnormal Callose Response Phenotype and Hypersusceptibility to Peronospora parasitica in Defense-Compromised Arabidopsis nim1-1 and Salicylate Hydroxylase-Expressing Plants

2001 ◽  
Vol 14 (4) ◽  
pp. 439-450 ◽  
Author(s):  
Nicole M. Donofrio ◽  
Terrence P. Delaney
Keyword(s):  
Systemic Acquired Resistance ◽  
Acquired Resistance ◽  
Peronospora Parasitica ◽  
Wild Type ◽  
Chemical Induction ◽  
Callose Deposition ◽  
Type Pattern ◽  
Pathogen Fitness ◽  
Response Phenotype ◽  
The Impact

To investigate the impact of induced host defenses on the virulence of a compatible Peronospora parasitica strain on Arabidopsis thaliana, we examined growth and development of this pathogen in nim1-1 mutants and transgenic salicylate hydroxylase plants. These plants are unable to respond to or accumulate salicylic acid (SA), respectively, are defective in expression of systemic acquired resistance (SAR), and permit partial growth of some normally avirulent pathogens. We dissected the P. parasitica life cycle into nine stages and compared its progression through these stages in the defense-compromised hosts and in wild-type plants. NahG plants supported the greatest accumulation of pathogen biomass and conidiophore production, followed by nim1-1 and then wild-type plants. Unlike the wild type, NahG and nim1-1 plants showed little induction of the SAR gene PR-1 after colonization with P. parasitica, which is similar to our previous observations. We examined the frequency and morphology of callose deposits around parasite haustoria and found significant differences between the three hosts. NahG plants showed a lower fraction of haustoria surrounded by thick callose encasements and a much higher fraction of hausto-ria with callose limited to thin collars around haustorial necks compared to wild type, whereas nim1-1 plants were intermediate between NahG and wild type. Chemical induction of SAR in plants colonized by P. parasitica converted the extrahaustorial callose phenotype in NahG to resemble closely the wild-type pattern, but had no effect on nim1-1 plants. These results suggest that extrahausto-rial callose deposition is influenced by the presence or lack of SA and that this response may be sensitive to the NIM1/NPR1 pathway. Additionally, the enhanced susceptibility displayed by nim1-1 and NahG plants shows that even wild-type susceptible hosts exert defense functions that reduce disease severity and pathogen fitness.

scholarly journals Acibenzolar-S-methyl activates stomatal-based defense systemically in Japanese radish by inducing peroxidase-dependent reactive oxygen species production

2020 ◽  
Author(s):  
Nanami Sakata ◽  
Takako Ishiga ◽  
Shizuku Taniguchi ◽  
Yasuhiro Ishiga
Keyword(s):  
Disease Control ◽  
Systemic Acquired Resistance ◽  
Control Strategies ◽  
Second Messengers ◽  
Stomatal Closure ◽  
Acquired Resistance ◽  
Synthetic Analog ◽  
Control Effect ◽  
Pathogen Invasion ◽  
Japanese Radish

AbstractAcibenzolar-S-methyl (ASM) is a well-known plant activator, which is a synthetic analog of salicylic acid (SA). Recently, copper fungicides and antibiotics are major strategies for controlling bacterial diseases. However, resistant strains have already been found. Therefore, there is an increasing demand for sustainable new disease control strategies. We investigated the ASM disease control effect against Pseudomonas cannabina pv. alisalensis (Pcal), which causes bacterial blight on Japanese radish. In this study, we demonstrated that ASM effectively suppressed Pcal disease symptom development associated with reduced bacterial populations on Japanese radish leaves. Interestingly, we also demonstrated that ASM activated systemic acquired resistance (SAR), including stomatal-based defense, not only on ASM treated leaves, but also on untreated upper and lower leaves. Reactive oxidative species (ROS) are essential second messengers in stomatal-based defense. We found that ASM induced stomatal closure by inducing ROS production through peroxidase. These results indicate that stomatal closure induced by ASM treatment is effective for preventing Pcal pathogen invasion into plants, and in turn reduction of disease development.

scholarly journals N-hydroxy-pipecolic acid is a mobile metabolite that induces systemic disease resistance in Arabidopsis

2018 ◽  
Vol 115 (21) ◽  
pp. E4920-E4929 ◽  
Author(s):  
Yun-Chu Chen ◽  
Eric C. Holmes ◽  
Jakub Rajniak ◽  
Jung-Gun Kim ◽  
Sandy Tang ◽  
...  
Keyword(s):  
Disease Resistance ◽  
Systemic Acquired Resistance ◽  
Systemic Disease ◽  
Acquired Resistance ◽  
Bacterial Pathogen ◽  
Pipecolic Acid ◽  
In Planta ◽  
Global Response ◽  
Promising Target ◽  
Pathogenesis Related

Systemic acquired resistance (SAR) is a global response in plants induced at the site of infection that leads to long-lasting and broad-spectrum disease resistance at distal, uninfected tissues. Despite the importance of this priming mechanism, the identity and complexity of defense signals that are required to initiate SAR signaling is not well understood. In this paper, we describe a metabolite, N-hydroxy-pipecolic acid (N-OH-Pip) and provide evidence that this mobile molecule plays a role in initiating SAR signal transduction in Arabidopsis thaliana. We demonstrate that FLAVIN-DEPENDENT MONOOXYGENASE 1 (FMO1), a key regulator of SAR-associated defense priming, can synthesize N-OH-Pip from pipecolic acid in planta, and exogenously applied N-OH-Pip moves systemically in Arabidopsis and can rescue the SAR-deficiency of fmo1 mutants. We also demonstrate that N-OH-Pip treatment causes systemic changes in the expression of pathogenesis-related genes and metabolic pathways throughout the plant and enhances resistance to a bacterial pathogen. This work provides insight into the chemical nature of a signal for SAR and also suggests that the N-OH-Pip pathway is a promising target for metabolic engineering to enhance disease resistance.

scholarly journals Salicylic Acid Induces Resistance to Alternaria solani in Hydroponically Grown Tomato

1999 ◽  
Vol 89 (9) ◽  
pp. 722-727 ◽  
Author(s):  
Matthew E. Spletzer ◽  
Alexander J. Enyedi
Keyword(s):  
Salicylic Acid ◽  
Systemic Acquired Resistance ◽  
Critical Role ◽  
Acquired Resistance ◽  
Alternaria Solani ◽  
Economic Losses ◽  
Signal Molecule ◽  
Challenge Inoculation ◽  
Tomato Plants ◽  
Pathogen Invasion

Alternaria solani is the causal agent of early blight disease in tomato and is responsible for significant economic losses sustained by tomato producers each year. Because salicylic acid (SA) is an important signal molecule that plays a critical role in plant defense against pathogen invasion, we investigated if the exogenous application of SA would activate systemic acquired resistance (SAR) against A. solani in tomato leaves. The addition of 200 μM SA to the root system significantly increased the endogenous SA content of leaves. Free SA levels increased 65-fold over basal levels to 5.85 μg g-1 fresh weight (FW) after 48 h. This level of SA had no visible phytotoxic effects. Total SA content (free SA + SA-glucose conjugate) increased to 108 μg g-1 FW after 48 h. Concomitant with elevated SA levels, expression of the tomato pathogenesis-related (PR)-1B gene was strongly induced within 24 h of the addition of 200 μM SA. PR-1B expression was still evident after 48 h; however, PR-1B induction was not observed in plants not receiving SA treatment. Challenge inoculation of SA-treated tomato plants using conidia of A. solani resulted in 83% fewer lesions per leaf and a 77% reduction in blighted leaf area as compared with control plants not receiving SA. Our data indicate that root feeding 200 μM SA to tomato plants can (i) significantly elevate foliar SA levels, (ii) induce PR-1B gene expression, and (iii) activate SAR that is effective against A. solani.

scholarly journals Arabidopsismlo3mutant plants exhibit spontaneous callose deposition and signs of early leaf senescence

2019 ◽  
Author(s):  
Stefan Kusch ◽  
Susanne Thiery ◽  
Anja Reinstädler ◽  
Katrin Gruner ◽  
Krzysztof Zienkiewicz ◽  
...  
Keyword(s):  
Salicylic Acid ◽  
Powdery Mildew ◽  
Pseudomonas Syringae ◽  
Systemic Acquired Resistance ◽  
Acquired Resistance ◽  
Bacterial Pathogen ◽  
Resistance Locus ◽  
Callose Deposition ◽  
Powdery Mildew Fungi ◽  
Hyaloperonospora Arabidopsidis

The family of Mildew resistance Locus O (MLO) proteins is best known for its profound effect on the outcome of powdery mildew infections: when the appropriate MLO protein is absent, the plant is fully resistant to otherwise virulent powdery mildew fungi. However, most members of the MLO protein family remain functionally unexplored. Here, we investigateArabidopsis thaliana MLO3, the closest relative ofAtMLO2, AtMLO6andAtMLO12, which are the ArabidopsisMLOgenes implicated in the powdery mildew interaction. The co-expression network ofAtMLO3suggests association of the gene with plant defense-related processes such as salicylic acid homeostasis. Our extensive analysis shows thatmlo3mutants are unaffected regarding their infection phenotype upon challenge with the powdery mildew fungiGolovinomyces orontiiandErysiphe pisi, the oomyceteHyaloperonospora arabidopsidis, and the bacterial pathogenPseudomonas syringae(the latter both in terms of basal and systemic acquired resistance), indicating that the protein does not play a major role in the response to any of these pathogens. However,mlo3genotypes display spontaneous callose deposition as well as signs of early senescence in six-or seven-week-old rosette leaves in the absence of any pathogen challenge, a phenotype that is reminiscent ofmlo2mutant plants. We hypothesize that de-regulated callose deposition inmlo3genotypes is the result of a subtle transient aberration of salicylic acid-jasmonic acid homeostasis during development.

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