Interconnection between Methyl Salicylate and Lipid-Based Long-Distance Signaling during the Development of Systemic Acquired Resistance in Arabidopsis and Tobacco

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.

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

10.1101/537597 ◽

2019 ◽

Cited By ~ 1

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

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

Science Signaling ◽

10.1126/scisignal.aay3066 ◽

2019 ◽

Vol 12 (604) ◽

pp. eaay3066 ◽

Cited By ~ 10

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.

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SABP2, a methyl salicylate esterase is required for the systemic acquired resistance induced by acibenzolar-S -methyl in plants

FEBS Letters ◽

10.1016/j.febslet.2010.06.046 ◽

2010 ◽

Vol 584 (15) ◽

pp. 3458-3463 ◽

Cited By ~ 46

Author(s):

Diwaker Tripathi ◽

Yu-Lin Jiang ◽

Dhirendra Kumar

Keyword(s):

Methyl Salicylate ◽

Systemic Acquired Resistance ◽

Acquired Resistance

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Components of Arabidopsis Defense- and Ethylene-Signaling Pathways Regulate Susceptibility to Cauliflower mosaic virus by Restricting Long-Distance Movement

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-20-6-0659 ◽

2007 ◽

Vol 20 (6) ◽

pp. 659-670 ◽

Cited By ~ 52

Author(s):

Andrew J. Love ◽

Valérie Laval ◽

Chiara Geri ◽

Janet Laird ◽

A. Deri Tomos ◽

...

Keyword(s):

Mosaic Virus ◽

Systemic Acquired Resistance ◽

Fluorescent Protein ◽

Acquired Resistance ◽

Systemic Infection ◽

Cauliflower Mosaic Virus ◽

Virus Movement ◽

Wild Type ◽

Long Distance ◽

Systemic Spread

We analyzed the susceptibility of Arabidopsis mutants with defects in salicylic acid (SA) and jasmonic acid (JA)/ethylene (ET) signaling to infection by Cauliflower mosaic virus (CaMV). Mutants cpr1-1 and cpr5-2, in which SA-dependent defense signaling is activated constitutively, were substantially more resistant than the wild type to systemic infection, implicating SA signaling in defense against CaMV. However, SA-deficient NahG, sid2-2, eds5-1, and pad4-1 did not show enhanced susceptibility. A cpr5 eds5 double mutant also was resistant, suggesting that resistance in cpr5 may function partially independently of SA. Treatment of cpr5 and cpr5 eds5, but not cpr1, with salicyl-hydroxamic acid, an inhibitor of alternative oxidase, partially restored susceptibility to wild-type levels. Mutants etr1-1, etr1-3, and ein2-1, and two mutants with lesions in ET/JA-mediated defense, eds4 and eds8, also showed reduced virus susceptibility, demonstrating that ET-dependent responses also play a role in susceptibility. We used a green fluorescent protein (GFP)-expressing CaMV recombinant to monitor virus movement. In mutants with reduced susceptibility, cpr1-1, cpr5-2, and etr1-1, CaMV-GFP formed local lesions similar to the wild type, but systemic spread was almost completely absent in cpr1 and cpr5 and was substantially reduced in etr1-1. Thus, mutations with enhanced systemic acquired resistance or compromised ET signaling show diminished long-distance virus movement.

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