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 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 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 The glycosyltransferase UGT76B1 is critical for plant immunity as it governs the homeostasis of N-hydroxy-pipecolic acid

2020 ◽  
Author(s):  
Lennart Mohnike ◽  
Dmitrij Rekhter ◽  
Weijie Huang ◽  
Kirstin Feussner ◽  
Hainan Tian ◽  
...  
Keyword(s):  
Systemic Acquired Resistance ◽  
Plant Immunity ◽  
Acquired Resistance ◽  
Pipecolic Acid ◽  
Balance Growth ◽  
Loss Of Function ◽  
Long Distance ◽  
Knock Out ◽  
Endogenous Substrates ◽  
Mutant Lines

AbstractThe trade-off between growth and defense is a critical aspect of plant immunity. Therefore, plant immune response needs to be tightly regulated. The hormone regulating plant defense against biotrophic pathogens is salicylic acid (SA). Recently, N-hydroxy-pipecolic acid (NHP) was identified as second regulator for plant innate immunity and systemic acquired resistance. Although the biosynthetic pathway leading to NHP formation has already been identified, the route how NHP is further metabolized was unclear. Here, we present UGT76B1 as a UDP-dependent glycosyltransferase that modifies NHP by catalyzing the formation of 1-O-glucosyl-pipecolic acid (NHP-OGlc). Analysis of T-DNA and CRISPR knock-out mutant lines of UGT76B1 by targeted and non-targeted UHPLC-HRMS underlined NHP and SA as endogenous substrates of this enzyme in response to Pseudomonas infection and UV treatment. UGT76B1 shows similar KM for NHP and SA. ugt76b1 mutant plants have a dwarf phenotype and a constitutive defense response which can be suppressed by loss of function of the NHP biosynthetic enzyme FMO1. This suggests that elevated accumulation of NHP contributes to the enhanced disease resistance in ugt76b1. Externally applied NHP can move to distal tissue in ugt76b1 mutant plants. Although glycosylation is not required for the long distance movement of NHP during systemic acquired resistance, it is crucial to balance growth and defense.

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 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 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.

Using DIR1 to investigate long-distance signal movement during Systemic Acquired Resistance

2016 ◽  
Vol 38 (1) ◽  
pp. 19-24 ◽  
Author(s):  
Robin K. Cameron ◽  
Philip Carella ◽  
Marisa Isaacs ◽  
Marc Champigny ◽  
Juliane Merl-Pham ◽  
...  
Keyword(s):  
Systemic Acquired Resistance ◽  
Acquired Resistance ◽  
Long Distance ◽  
Distance Signal

scholarly journals Long distance movement of DIR1 and investigation of the role of DIR1-like during systemic acquired resistance in Arabidopsis

2013 ◽  
Vol 4 ◽  
Author(s):  
Marc J. Champigny ◽  
Marisa Isaacs ◽  
Philip Carella ◽  
Jennifer Faubert ◽  
Pierre R. Fobert ◽  
...  
Keyword(s):  
Systemic Acquired Resistance ◽  
Acquired Resistance ◽  
Long Distance ◽  
Long Distance Movement
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