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 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 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 An engineered pathway for N-hydroxy-pipecolic acid synthesis enhances systemic acquired resistance in tomato

2019 ◽  
Vol 12 (604) ◽  
pp. eaay3066 ◽  
Author(s):  
Eric C. Holmes ◽  
Yun-Chu Chen ◽  
Elizabeth S. Sattely ◽  
Mary Beth Mudgett
Keyword(s):  
Systemic Acquired Resistance ◽  
Acquired Resistance ◽  
Bacterial Pathogen ◽  
Acid Synthesis ◽  
Crop Plants ◽  
Pipecolic Acid ◽  
External Control ◽  
Long Distance ◽  
Engineering Strategy ◽  
Molecular Machinery

Systemic acquired resistance (SAR) is a powerful immune response that triggers broad-spectrum disease resistance throughout a plant. In the model plant Arabidopsis thaliana, long-distance signaling and SAR activation in uninfected tissues occur without circulating immune cells and instead rely on the metabolite N-hydroxy-pipecolic acid (NHP). Engineering SAR in crop plants would enable external control of a plant’s ability to mount a global defense response upon sudden changes in the environment. Such a metabolite-engineering approach would require the molecular machinery for producing and responding to NHP in the crop plant. Here, we used heterologous expression in Nicotiana benthamiana leaves to identify a minimal set of Arabidopsis genes necessary for the biosynthesis of NHP. Local expression of these genes in tomato leaves triggered SAR in distal tissues in the absence of a pathogen, suggesting that the SAR trait can be engineered to enhance a plant’s endogenous ability to respond to pathogens. We also showed tomato produces endogenous NHP in response to a bacterial pathogen and that NHP is present across the plant kingdom, raising the possibility that an engineering strategy to enhance NHP-induced defenses could be possible in many crop plants.

scholarly journals Arabidopsis UGT76B1 glycosylates N-hydroxy-pipecolic acid and inactivates systemic acquired resistance in tomato

2020 ◽  
Author(s):  
Eric C. Holmes ◽  
Yun-Chu Chen ◽  
Mary Beth Mudgett ◽  
Elizabeth S. Sattely
Keyword(s):  
Pseudomonas Syringae ◽  
Systemic Acquired Resistance ◽  
Acquired Resistance ◽  
Bacterial Pathogen ◽  
Defense Responses ◽  
Pipecolic Acid ◽  
Systemic Resistance ◽  
Biosynthetic Genes ◽  
Solanaceous Plants

AbstractSystemic acquired resistance (SAR) is a mechanism that plants utilize to connect a local pathogen infection to global defense responses. N-hydroxy-pipecolic acid (NHP) and a glycosylated derivative are produced during SAR, yet their individual roles in the response have not yet been elucidated. Here we report that Arabidopsis thaliana UGT76B1 can generate glycosylated NHP (NHP-Glc) in vitro and when transiently expressed alongside Arabidopsis NHP biosynthetic genes in two Solanaceous plants. During infection, Arabidopsis ugt76b1 mutants do not accumulate NHP-Glc and accumulate less glycosylated salicylic acid (SA-Glc) than wild type plants. The metabolic changes in ugt76b1 mutant plants are accompanied by enhanced defense to the bacterial pathogen Pseudomonas syringae, suggesting that glycosylation of SAR molecules NHP and SA by UGT76B1 plays an important role in defense modulation. Transient expression of Arabidopsis UGT76B1 with the Arabidopsis NHP biosynthesis genes ALD1 and FMO1 in tomato increases NHP-Glc production and reduces NHP accumulation in local tissue, and abolishes the systemic resistance seen when expressing NHP-biosynthetic genes alone. These findings reveal that the glycosylation of NHP by UGT76B1 alters defense priming in systemic tissue and provide further evidence for the role of the NHP aglycone as the active metabolite in SAR signaling.

scholarly journals Research progress of NPR genes in signal pathway of salicylic acid mediated plant disease resistance

2020 ◽  
Vol 145 ◽  
pp. 01038
Author(s):  
Pan Wang ◽  
Meiqin Xiang
Keyword(s):  
Salicylic Acid ◽  
Disease Resistance ◽  
Plant Disease Resistance ◽  
Plant Disease ◽  
Systemic Acquired Resistance ◽  
Acquired Resistance ◽  
Signal Transduction Pathway ◽  
Research Progress ◽  
Signal Molecule ◽  
Pathogenesis Related

Salicylic acid (SA) is considered to be an endogenous signal molecule in plants, and it is related to many resistances in plants. In Arabidopsis, Non-expressor of pathogenesis-related gene1 (NPR1) mediates the expression of pathogenesis-related genes (PRs) and systemic acquired resistance (SAR) induced by SA. NPR1 is a key factor in SA signaling pathway, and the research shows that NPR1, NPR3 and NPR4 play a key role in SA mediated plant disease resistance. In this review, the interaction between NPR and transcription factors is discussed, and we also describe the progress of NPR in SA mediated SAR signal transduction pathway, likewise, we introduce the relationship between NPR1 and its paralogues NPR3/NPR4. This paper analyzes the research prospect of NPR as the intersection of multiple signal paths.

scholarly journals Pipecolic Acid Is Induced in Barley upon Infection and Triggers Immune Responses Associated with Elevated Nitric Oxide Accumulation

2019 ◽  
Vol 32 (10) ◽  
pp. 1303-1313 ◽  
Author(s):  
Miriam Lenk ◽  
Marion Wenig ◽  
Kornelia Bauer ◽  
Florian Hug ◽  
Claudia Knappe ◽  
...  
Keyword(s):  
Nitric Oxide ◽  
Immune Responses ◽  
Pseudomonas Syringae ◽  
Systemic Acquired Resistance ◽  
Acquired Resistance ◽  
Bacterial Pathogen ◽  
Pipecolic Acid ◽  
Systemic Immunity ◽  
Exogenous Application ◽  
Barley Leaves

Pipecolic acid (Pip) is an essential component of systemic acquired resistance, priming resistance in Arabidopsis thaliana against (hemi)biotrophic pathogens. Here, we studied the potential role of Pip in bacteria-induced systemic immunity in barley. Exudates of barley leaves infected with the systemic immunity–inducing pathogen Pseudomonas syringae pv. japonica induced immune responses in A. thaliana. The same leaf exudates contained elevated Pip levels compared with those of mock-treated barley leaves. Exogenous application of Pip induced resistance in barley against the hemibiotrophic bacterial pathogen Xanthomonas translucens pv. cerealis. Furthermore, both a systemic immunity–inducing infection and exogenous application of Pip enhanced the resistance of barley against the biotrophic powdery mildew pathogen Blumeria graminis f. sp. hordei. In contrast to a systemic immunity-inducing infection, Pip application did not influence lesion formation by a systemically applied inoculum of the necrotrophic fungus Pyrenophora teres. Nitric oxide (NO) levels in barley leaves increased after Pip application. Furthermore, X. translucens pv. cerealis induced the accumulation of superoxide anion radicals and this response was stronger in Pip-pretreated compared with mock-pretreated plants. Thus, the data suggest that Pip induces barley innate immune responses by triggering NO and priming reactive oxygen species accumulation.

scholarly journals Overexpression of (At)NPR1 in Rice Leads to a BTH- and Environment-Induced Lesion-Mimic/Cell Death Phenotype

2004 ◽  
Vol 17 (2) ◽  
pp. 140-151 ◽  
Author(s):  
Heather A. Fitzgerald ◽  
Maw-Sheng Chern ◽  
Roy Navarre ◽  
Pamela C. Ronald
Keyword(s):  
Cell Death ◽  
Broad Spectrum ◽  
Stress Responses ◽  
Systemic Acquired Resistance ◽  
Plant Stress ◽  
Acquired Resistance ◽  
Bacterial Pathogen ◽  
Lesion Mimic ◽  
Pathogenesis Related ◽  
Plant Stress Responses

Systemic acquired resistance (SAR) is an inducible defense response that protects plants against a broad spectrum of pathogens. A central regulator of SAR in Arabidopsis is NPR1 (nonexpresser of pathogenesis-related genes). In rice, overexpression of Arabidopsis NPR1 enhances plant resistance to the bacterial pathogen Xanthomonas oryzae pv. oryzae. This report demonstrates that overexpression of (At)NPR1 in rice also triggers a lesion-mimic/cell death (LMD) phenotype. The LMD phenotype is environmentally regulated and heritable. In addition, the development of lesions and death correlates with the expression of rice defense genes and the accumulation of hydrogen peroxide. Application of the salicylic acid (SA) analog, benzo(1,2,3) thiadiazole-7-carbothioc acid S-methyl ester (BTH), potentiates this phenotype. Endogenous SA levels are reduced in rice overexpressing (At)NPR1 when compared with wild-type plants, supporting the idea that (At)NPR1 may perceive and modulate the accumulation of SA. The association of (At)NPR1 expression in rice with the development of an LMD phenotype suggests that (At)NPR1 has multiple roles in plant stress responses that may affect its efficacy as a transgenic tool for engineering broad-spectrum resistance.

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.

The roles of methyl jasmonate to stress in plants

2019 ◽  
Vol 46 (3) ◽  
pp. 197 ◽  
Author(s):  
Xiaxia Yu ◽  
Wenjin Zhang ◽  
Yu Zhang ◽  
Xiaojia Zhang ◽  
Duoyong Lang ◽  
...  
Keyword(s):  
Methyl Jasmonate ◽  
Systemic Acquired Resistance ◽  
Acquired Resistance ◽  
Heavy Metal Stress ◽  
Antioxidant Systems ◽  
Endogenous Hormones ◽  
Oxygen Species ◽  
Physiological And Biochemical Characteristics ◽  
Pathogenesis Related ◽  
Physiological And Biochemical

Plants are constantly exposed to various stresses, which can degrade their health. The stresses can be alleviated by the application of methyl jasmonate (MeJA), which is a hormone involved in plant signalling. MeJA induces synthesis of defensive compounds and initiates the expression of pathogenesis-related genes involved in systemic acquired resistance and local resistance. Thus, MeJA may be used against pathogens, salt stress, drought stress, low temperature, heavy metal stress and toxicities of other elements. The application of MeJA improves growth, induces the accumulation of active compounds, and affects endogenous hormones levels, and other physiological and biochemical characteristics in stressed plants. Furthermore, MeJA antagonises the adverse effects of osmotic stress by regulating inorganic penetrating ions or organic penetrants to suppress the absorption of toxic ions. MeJA also mitigates oxidative stress by activating antioxidant systems to scavenge reactive oxygen species (ROS) in stressed plants. For these reasons, we reviewed the use of exogenous MeJA in alleviating biotic (pathogens and insects) and abiotic stresses in plants.

scholarly journals NIM1 Overexpression in Arabidopsis Potentiates Plant Disease Resistance and Results in Enhanced Effectiveness of Fungicides

2001 ◽  
Vol 14 (9) ◽  
pp. 1114-1124 ◽  
Author(s):  
Leslie Friedrich ◽  
Kay Lawton ◽  
Robert Dietrich ◽  
Michael Willits ◽  
Rebecca Cade ◽  
...  
Keyword(s):  
Disease Resistance ◽  
Plant Disease Resistance ◽  
Systemic Acquired Resistance ◽  
Control Strategies ◽  
Chemical Activation ◽  
Acquired Resistance ◽  
Wild Type ◽  
Protein Levels ◽  
Rapid Induction ◽  
Dependent Signal

The NIM1 (for noninducible immunity, also known as NPR1) gene is required for the biological and chemical activation of systemic acquired resistance (SAR) in Arabidopsis. Overexpression of NIM1 in wild-type plants (hereafter referred to as NIM1 plants or lines) results in varying degrees of resistance to different pathogens. Experiments were performed to address the basis of the enhanced disease resistance responses seen in the NIM1 plants. The increased resistance observed in the NIM1 lines correlated with increased NIM1 protein levels and rapid induction of PR1 gene expression, a marker for SAR induction in Arabidopsis, following pathogen inoculation. Levels of salicylic acid (SA), an endogenous signaling molecule required for SAR induction, were not significantly increased compared with wild-type plants. SA was required for the enhanced resistance in NIM1 plants, however, suggesting that the effect of NIM1 overexpression is that plants are more responsive to SA or a SA-dependent signal. This hypothesis is supported by the heightened responsiveness that NIM1 lines exhibited to the SAR-inducing compound benzo(1,2,3)-thiadiazole-7-car-bothioic acid S-methyl ester. Furthermore, the increased efficacy of three fungicides was observed in the NIM1 plants, suggesting that a combination of transgenic and chemical approaches may lead to effective and durable disease-control strategies.

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