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The phenylpropanoid pathway inhibitor piperonylic acid induces broad-spectrum pest and disease resistance in plants

Willem Desmedt (UGent) , Wim Jonckheere (UGent) , Viet Ha Nguyen (UGent) , Maarten Ameye (UGent) , Noémie De Zutter (UGent) , Karen De Kock (UGent) , Jane Debode, Thomas Van Leeuwen (UGent) , Kris Audenaert (UGent) , Bartel Vanholme (UGent) , et al.
(2021) PLANT CELL AND ENVIRONMENT. 44(9). p.3122-3139
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Abstract
Although 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 plants 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 signalling 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.
Keywords
Plant Science, Physiology, flavonoids, induced resistance, metabolomics, plant immunity, salicylic acid, tomato, transcriptomics, ROOT-KNOT NEMATODES, SALICYLIC-ACID, COS-OGA, CINNAMATE 4-HYDROXYLASE, SYSTEMIC RESISTANCE, DEFENSE, TOMATO, LIGNIFICATION, ARABIDOPSIS, IMMUNITY

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MLA
Desmedt, Willem, et al. “The Phenylpropanoid Pathway Inhibitor Piperonylic Acid Induces Broad-Spectrum Pest and Disease Resistance in Plants.” PLANT CELL AND ENVIRONMENT, vol. 44, no. 9, 2021, pp. 3122–39, doi:10.1111/pce.14119.
APA
Desmedt, W., Jonckheere, W., Nguyen, V. H., Ameye, M., De Zutter, N., De Kock, K., … Kyndt, T. (2021). The phenylpropanoid pathway inhibitor piperonylic acid induces broad-spectrum pest and disease resistance in plants. PLANT CELL AND ENVIRONMENT, 44(9), 3122–3139. https://doi.org/10.1111/pce.14119
Chicago author-date
Desmedt, Willem, Wim Jonckheere, Viet Ha Nguyen, Maarten Ameye, Noémie De Zutter, Karen De Kock, Jane Debode, et al. 2021. “The Phenylpropanoid Pathway Inhibitor Piperonylic Acid Induces Broad-Spectrum Pest and Disease Resistance in Plants.” PLANT CELL AND ENVIRONMENT 44 (9): 3122–39. https://doi.org/10.1111/pce.14119.
Chicago author-date (all authors)
Desmedt, Willem, Wim Jonckheere, Viet Ha Nguyen, Maarten Ameye, Noémie De Zutter, Karen De Kock, Jane Debode, Thomas Van Leeuwen, Kris Audenaert, Bartel Vanholme, and Tina Kyndt. 2021. “The Phenylpropanoid Pathway Inhibitor Piperonylic Acid Induces Broad-Spectrum Pest and Disease Resistance in Plants.” PLANT CELL AND ENVIRONMENT 44 (9): 3122–3139. doi:10.1111/pce.14119.
Vancouver
1.
Desmedt W, Jonckheere W, Nguyen VH, Ameye M, De Zutter N, De Kock K, et al. The phenylpropanoid pathway inhibitor piperonylic acid induces broad-spectrum pest and disease resistance in plants. PLANT CELL AND ENVIRONMENT. 2021;44(9):3122–39.
IEEE
[1]
W. Desmedt et al., “The phenylpropanoid pathway inhibitor piperonylic acid induces broad-spectrum pest and disease resistance in plants,” PLANT CELL AND ENVIRONMENT, vol. 44, no. 9, pp. 3122–3139, 2021.
@article{8712615,
  abstract     = {{Although 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 plants 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 signalling 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.}},
  author       = {{Desmedt, Willem and Jonckheere, Wim and Nguyen, Viet Ha and Ameye, Maarten and De Zutter, Noémie and De Kock, Karen and Debode, Jane and Van Leeuwen, Thomas and Audenaert, Kris and Vanholme, Bartel and Kyndt, Tina}},
  issn         = {{0140-7791}},
  journal      = {{PLANT CELL AND ENVIRONMENT}},
  keywords     = {{Plant Science,Physiology,flavonoids,induced resistance,metabolomics,plant immunity,salicylic acid,tomato,transcriptomics,ROOT-KNOT NEMATODES,SALICYLIC-ACID,COS-OGA,CINNAMATE 4-HYDROXYLASE,SYSTEMIC RESISTANCE,DEFENSE,TOMATO,LIGNIFICATION,ARABIDOPSIS,IMMUNITY}},
  language     = {{eng}},
  number       = {{9}},
  pages        = {{3122--3139}},
  title        = {{The phenylpropanoid pathway inhibitor piperonylic acid induces broad-spectrum pest and disease resistance in plants}},
  url          = {{http://dx.doi.org/10.1111/pce.14119}},
  volume       = {{44}},
  year         = {{2021}},
}

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