Saskia C. M. Van Wees

Utrecht University

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Corné M. J. Pieterse

Utrecht University

J.A. van Pelt

Utrecht University

L.C. van Loon

Utrecht University

Jurriaan Ton

University of Sheffield

Marcel C. Van Verk

Utrecht University

Richard Hickman

Utrecht University

Lotte Caarls

Wageningen University & Research

Dieuwertje van der Does

Sainsbury Laboratory

Peter A. H. M. Bakker

Utrecht University

Robert C. Schuurink

University of Amsterdam

Cooperative Institutions

Utrecht University

Wageningen University & Research

Graduate School Experimental Plant Sciences

Centre for BioSystems Genomics

University of Amsterdam

Leiden University

Netherlands Institute for Neuroscience

University of Tübingen

Consejo Superior de Investigaciones Científicas

Research International (United States)

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Shifting from priming of salicylic acid‐ to jasmonic acid‐regulated defences by Trichoderma protects tomato against the root knot nematode Meloidogyne incognita

New Phytologist (2016)

Ainhoa Martínez‐Medina Iván Fernández Gerrit B. Lok Marı́a J. Pozo Corné M. J. Pieterse

Summary Beneficial root endophytes such as Trichoderma spp. can reduce infections by parasitic nematodes through triggering host defences. Little is currently known about the complex hormone signalling underlying the induction of resistance. In this study, we investigated whether Trichoderma modulates the hormone signalling network in the host to induce resistance to nematodes. We investigated the role and the timing of the jasmonic acid ( JA )‐ and salicylic acid ( SA )‐regulated defensive pathways in Trichoderma ‐induced resistance to the root knot nematode Meloidogyne incognita . A split‐root system of tomato ( Solanum lycopersicum ) was used to study local and systemic induced defences by analysing nematode performance, defence gene expression, responsiveness to exogenous hormone application, and dependence on SA and JA signalling of Trichoderma ‐induced resistance. Root colonization by Trichoderma impeded nematode performance both locally and systemically at multiple stages of the parasitism, that is, invasion, galling and reproduction. First, Trichoderma primed SA ‐regulated defences, which limited nematode root invasion. Then, Trichoderma enhanced JA ‐regulated defences, thereby antagonizing the deregulation of JA ‐dependent immunity by the nematodes, which compromised galling and fecundity. Our results show that Trichoderma primes SA ‐ and JA ‐dependent defences in roots, and that the priming of responsiveness to these hormones upon nematode attack is plastic and adaptive to the parasitism stage.

Jasmonic acid

Root-knot nematode

Trichoderma

Nematode infection

Systemic Acquired Resistance

Abamectin

10.1111/nph.14251

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Citations (301)

European Journal of Plant Pathology (2001)

Corné M. J. Pieterse J.A. van Pelt Saskia C. M. Van Wees Jurriaan Ton Karen M. Léon‐Kloosterziel

Jasmonic acid

Systemic Acquired Resistance

Pseudomonas syringae

NPR1

10.1023/a:1008747926678

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Citations (215)

Enhancement of induced disease resistance by simultaneous activation of salicylate- and jasmonate-dependent defense pathways in Arabidopsis thaliana

Proceedings of the National Academy of Sciences (2000)

Saskia C. M. Van Wees E. Swart J.A. van Pelt L.C. van Loon Corné M. J. Pieterse

The plant-signaling molecules salicylic acid (SA) and jasmonic acid (JA) play an important role in induced disease resistance pathways. Cross-talk between SA- and JA-dependent pathways can result in inhibition of JA-mediated defense responses. We investigated possible antagonistic interactions between the SA-dependent systemic acquired resistance (SAR) pathway, which is induced upon pathogen infection, and the JA-dependent induced systemic resistance (ISR) pathway, which is triggered by nonpathogenic Pseudomonas rhizobacteria. In Arabidopsis thaliana , SAR and ISR are effective against a broad spectrum of pathogens, including the foliar pathogen Pseudomonas syringae pv. tomato ( Pst ). Simultaneous activation of SAR and ISR resulted in an additive effect on the level of induced protection against Pst . In Arabidopsis genotypes that are blocked in either SAR or ISR, this additive effect was not evident. Moreover, induction of ISR did not affect the expression of the SAR marker gene PR-1 in plants expressing SAR. Together, these observations demonstrate that the SAR and the ISR pathway are compatible and that there is no significant cross-talk between these pathways. SAR and ISR both require the key regulatory protein NPR1. Plants expressing both types of induced resistance did not show elevated Npr1 transcript levels, indicating that the constitutive level of NPR1 is sufficient to facilitate simultaneous expression of SAR and ISR. These results suggest that the enhanced level of protection is established through parallel activation of complementary, NPR1-dependent defense responses that are both active against Pst . Therefore, combining SAR and ISR provides an attractive tool for the improvement of disease control.

Pseudomonas syringae

Jasmonic acid

NPR1

Systemic Acquired Resistance

Jasmonate

Methyl jasmonate

10.1073/pnas.130425197

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Citations (594)

Rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis: involvement of jasmonate and ethylene

Corné M. J. Pieterse Saskia C. M. Van Wees Jurriaan Ton Karen M. Léon‐Kloosterziel J.A. van Pelt

The capacity of a plant to express a broad-spectrum systemic acquired resistance (SAR) after primary infection is well known and extensively studied. A relatively unknown form of induced disease resistance is triggered by nonpathogenic, root-colonizing rhizobacteria and is commonly referred to as rhizobacteria-mediated induced systemic resistance (ISR). Rhizosphere bacteria are present in large numbers on the root. Certain strains stimulate plant growth and are therefore called plant growth-promoting rhizobacteria (PGPR). Selected strains with biological control activity, mainly fluorescent Pseudomonas spp., reduce plant diseases by suppressing soil-borne pathogens through competition for nutrients, siderophore-mediated competition for iron or antibiosis.

Antibiosis

Jasmonate

Systemic Acquired Resistance

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Citations (6)

Costs and benefits of hormone‐regulated plant defences

Plant Pathology (2013)

I. A. Vos Corné M. J. Pieterse Saskia C. M. Van Wees

Plants activate defence responses to protect themselves against microbial pathogens and herbivorous insects. However, induction of defences comes at a price, as the associated allocation costs, autotoxicity costs and ecological costs form fitness penalties. Upon pathogen or insect attack, resources are allocated to defences instead of to plant growth and reproduction, while above‐ and below‐ground interactions with beneficial organisms may also be disturbed. The phytohormones salicylic acid and jasmonic acid are major players in the regulation of induced defences and their associated fitness costs. Hormone‐controlled signalling pathways cross‐communicate, providing the plant with a finely tuned defence regulatory system that can contribute to a reduction of fitness costs by repressing ineffective defences. However, this sophisticated regulatory system causes ecological costs, because activated resistance to one organism can suppress resistance to another. Moreover, the system can be hijacked by invading organisms that manipulate it for their own benefit. Priming for enhanced defence emerged as a defence mechanism with limited fitness costs. Because priming results in a faster and stronger activation of defence only after pathogen or insect attack, the limited costs of the primed state are often outweighed by the benefits in environments with pathogen or herbivore pressure. The balance between protection and fitness is crucial for a plant's success and is therefore of great interest for plant breeders and farmers. By combining molecular knowledge and ecological relevance of defence mechanisms, one can gain fundamental insight into how and why plants integrate different immune signals to cope with their natural multitrophic environment in a cost‐effective manner.

Jasmonic acid

Defence mechanisms

Priming (agriculture)

10.1111/ppa.12105

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Citations (184)

Elucidating the Gene Regulatory Network that integrates Abscisic Acid and Jasmonic Acid Signaling.

Niels Aerts Marcel C. Van Verk Saskia C. M. Van Wees

Jasmonic acid

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The Arabidopsis ISR1 Locus Controlling Rhizobacteria-Mediated Induced Systemic Resistance Is Involved in Ethylene Signaling

PLANT PHYSIOLOGY (2001)

Jurriaan Ton Sylke Davison Saskia C. M. Van Wees L.C. van Loon Corné M. J. Pieterse

In Arabidopsis, the rhizobacterial strain Pseudomonas fluorescens WCS417r triggers an induced systemic resistance (ISR) response that is effective against different types of pathogens. The ISR signaling pathway functions independent of salicylic acid, but requires responsiveness to jasmonate (JA) and ethylene. Using the genetic variability of ISR inducibility between Arabidopsis accessions, we recently identified a locus (ISR1) on chromosome III that is involved in ISR signaling. Accessions RLD and Wassilewskija (Ws) are recessive at the ISR1 locus and are, therefore, unable to develop ISR. Here we investigated whether the ISR1 locus is involved in JA or ethylene signaling. Compared with the ISR-inducible accession Columbia (Col), accessions RLD and Ws were not affected in JA-induced inhibition of root growth and expression of the JA-responsive gene Atvsp, suggesting that the ISR1 locus is not involved in JA signaling. However, RLD and Ws showed an affected expression of the triple response and a reduced expression of the ethylene responsive genes Hel and Pdf1.2 after exogenous application of the ethylene precursor 1-aminocyclopropane-1-carboxylate. Moreover, in contrast to Col, RLD and Ws did not develop resistance against P. syringae pv. tomato DC3000 after treatment of the leaves with 1-aminocyclopropane-1-carboxylate. Analysis of the F(2) and F(3) progeny of a cross between Col (ISR1/ISR1) and RLD (isr1/isr1) revealed that reduced sensitivity to ethylene cosegregates with the recessive alleles of the ISR1 locus. These results suggest that the ISR1 locus encodes a component of the ethylene response, which is required for the expression of rhizobacteria-mediated ISR.

Pseudomonas syringae

Jasmonate

Methyl jasmonate

10.1104/pp.125.2.652

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Citations (105)

Arabidopsis JASMONATE-INDUCED OXYGENASES down-regulate plant immunity by hydroxylation and inactivation of the hormone jasmonic acid

bioRxiv (Cold Spring Harbor Laboratory) (2017)

Lotte Caarls Joyce Elberse Mo Awwanah Nora R. Ludwig Michèl de Vries

ABSTRACT The phytohormone jasmonic acid (JA) is vital in plant defense and development. Although biosynthesis of JA and activation of JA-responsive gene expression by the bioactive form JA-isoleucine (JA-Ile) have been well-studied, knowledge on JA metabolism is incomplete. In particular, the enzyme that hydroxylates JA to 12-OH-JA, an inactive form of JA that accumulates after wounding and pathogen attack, is unknown. Here, we report the identification of four paralogous 2-oxoglutarate/Fe(II)-dependent oxygenases in Arabidopsis thaliana as JA hydroxylases and show that they down-regulate JA-dependent responses. As they are induced by JA we named them JASMONATE-INDUCED OXYGENASEs ( JOXs ). Concurrent mutation of the four genes in a quadruple Arabidopsis mutant resulted in increased defense gene expression and increased resistance to the necrotrophic fungus Botrytis cinerea and the caterpillar Mamestra brassicae . In addition, root and shoot growth of the plants was inhibited. Metabolite analysis of leaves showed that loss of function of the four JOX enzymes resulted in over-accumulation of JA and in reduced turnover of JA into 12-OH-JA. Transformation of the quadruple mutant with each JOX gene strongly reduced JA levels, demonstrating that all four JOXs inactivate JA in plants. The in vitro catalysis of 12-OH-JA from JA by recombinant enzyme could be confirmed for three JOXs. The identification of the enzymes responsible for hydroxylation of JA reveals a missing step in JA metabolism, which is important for the inactivation of the hormone and subsequent down-regulation of JA-dependent defenses. SIGNIFICANCE STATEMENT In plants, the hormone jasmonic acid (JA) is synthesized in response to attack by pathogens and herbivores, leading to activation of defense responses. Rapidly following JA accumulation, the hormone is metabolized, presumably to prevent inhibitive effects of high JA levels on growth and development. The enzymes that directly inactivate JA were so far unknown. Here, we identify four jasmonate-induced oxygenases (JOXs) in Arabidopsis that hydroxylate jasmonic acid to form inactive 12-OH-JA. A mutant that no longer produces the four enzymes hyperaccumulates JA, exhibits reduced growth, and is highly resistant to attackers that are sensitive to JA-dependent defense. The JOX enzymes thus play an important role in determining the amplitude and duration of JA responses to balance the growth-defense tradeoff.

Jasmonic acid

Jasmonate

Hydroxylation

Plant hormone

10.1101/102103

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Citations (6)

Cross-talk between salicylate- and jasmonate-dependent induced defenses in Arabidopsis

Corné M. J. Pieterse Steven H. Spoel Jurriaan Ton Saskia C. M. Van Wees J.A. van Pelt

Plants possess inducible defense mechanisms to effectively combat invasion by microbial pathogens or attack by herbivorous insects. Research on defense signaling pathways revealed that induced defenses against pathogens and herbivores are regulated by a network of interconnecting signaling pathways in which the plant signal molecules salicylic acid (SA), jasmonic acid (JA) and ethylene (ET) play a dominant role. In many cases, attack by pathogens or herbivores is associated with enhanced production of these hormones and a concomitant activation of distinct sets of defense-related genes. Moreover, exogenous application of SA, JA or ET often results in an enhanced level of resistance.

Jasmonic acid

Jasmonate

Methyl jasmonate

Defence mechanisms

Source

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Citations (1)

A MEMORIAL TO TSUNE KOSUGE

Annual Review of Phytopathology (1988)

Corné M. J. Pieterse Christos Zamioudis Roeland L. Berendsen David M. Weller Saskia C. M. Van Wees

Beneficial microbes in the microbiome of plant roots improve plant health. Induced systemic resistance (ISR) emerged as an important mechanism by which selected plant growth–promoting bacteria and fungi in the rhizosphere prime the whole plant body for ...Read More

10.1146/annurev.py.26.060804.100001

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