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The phenylpropanoid pathway inhibitor piperonylic acid induces broad-spectrum pest and disease resistance in plants
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  • Willem Desmedt,
  • Wim Jonckheere,
  • Viet Ha Nguyen,
  • Maarten Ameye,
  • Noemi De Zutter,
  • Karen De Kock,
  • Jane Debode,
  • Thomas van Leeuven,
  • Kris Audenaert,
  • Bartel Vanholme,
  • Tina Kyndt
Willem Desmedt
Ghent University

Corresponding Author:[email protected]

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Wim Jonckheere
Ghent University
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Viet Ha Nguyen
Ghent University
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Maarten Ameye
Ghent University
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Noemi De Zutter
Ghent University
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Karen De Kock
Ghent University
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Jane Debode
ILVO
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Thomas van Leeuven
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Kris Audenaert
Ghent University
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Bartel Vanholme
Ghent University
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Tina Kyndt
Ghent University
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Abstract

While many phenylpropanoid pathway-derived molecules act as physical and chemical barriers to pests and pathogens, comparatively little is known about their role in regulating plant immunity. To explore this research field, we transiently perturbed the phenylpropanoid pathway through application of the CINNAMIC ACID-4-HYDROXYLASE (C4H) inhibitor piperonylic acid (PA). Using bioassays involving diverse pests and pathogens, we show that transient C4H inhibition triggers systemic, broad-spectrum resistance in higher plant without affecting growth. PA treatment enhances tomato (Solanum lycopersicum) resistance in field and laboratory conditions, thereby illustrating the potential of phenylpropanoid pathway perturbation in crop protection. At the molecular level, transcriptome and metabolome analyses reveal that transient C4H inhibition in tomato reprograms phenylpropanoid and flavonoid metabolism, systemically induces immune signaling and pathogenesis-related genes, and locally affects reactive oxygen species metabolism. Furthermore, C4H inhibition primes cell wall modification and phenolic compound accumulation in response to root-knot nematode infection. Although PA treatment induces local accumulation of the phytohormone salicylic acid, the PA resistance phenotype is preserved in tomato plants expressing the salicylic acid-degrading NahG construct. Together, our results demonstrate that transient phenylpropanoid pathway perturbation is a conserved inducer of plant resistance and thus highlight the crucial regulatory role of this pathway in plant immunity.
30 Apr 2021Submitted to Plant, Cell & Environment
30 Apr 2021Submission Checks Completed
30 Apr 2021Assigned to Editor
30 Apr 2021Reviewer(s) Assigned
16 May 2021Review(s) Completed, Editorial Evaluation Pending
23 May 2021Editorial Decision: Accept