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Separate Pathways Contribute to the Herbivore-Induced Formation of 2-Phenylethanol in Poplar.
Plant Physiol 2019; 180(2):767-782PP

Abstract

Upon herbivory, the tree species western balsam poplar (Populus trichocarpa) produces a variety of Phe-derived metabolites, including 2-phenylethylamine, 2-phenylethanol, and 2-phenylethyl-β-d-glucopyranoside. To investigate the formation of these potential defense compounds, we functionally characterized aromatic l-amino acid decarboxylases (AADCs) and aromatic aldehyde synthases (AASs), which play important roles in the biosynthesis of specialized aromatic metabolites in other plants. Heterologous expression in Escherichia coli and Nicotiana benthamiana showed that all five AADC/AAS genes identified in the P trichocarpa genome encode active enzymes. However, only two genes, PtAADC1 and PtAAS1, were significantly upregulated after leaf herbivory. Despite a sequence similarity of ∼96%, PtAADC1 and PtAAS1 showed different enzymatic functions and converted Phe into 2-phenylethylamine and 2-phenylacetaldehyde, respectively. The activities of both enzymes were interconvertible by switching a single amino acid residue in their active sites. A survey of putative AADC/AAS gene pairs in the genomes of other plants suggests an independent evolution of this function-determining residue in different plant families. RNA interference -mediated-downregulation of AADC1 in gray poplar (Populus × canescens) resulted in decreased accumulation of 2-phenylethylamine and 2-phenylethyl-β-d-glucopyranoside, whereas the emission of 2-phenylethanol was not influenced. To investigate the last step of 2-phenylethanol formation, we identified and characterized two P trichocarpa short-chain dehydrogenases, PtPAR1 and PtPAR2, which were able to reduce 2-phenylacetaldehyde to 2-phenylethanol in vitro. In summary, 2-phenylethanol and its glucoside may be formed in multiple ways in poplar. Our data indicate that PtAADC1 controls the herbivore-induced formation of 2-phenylethylamine and 2-phenylethyl-β-d-glucopyranoside in planta, whereas PtAAS1 likely contributes to the herbivore-induced emission of 2-phenylethanol.

Authors+Show Affiliations

Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany.Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany.Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany.Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany.Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany.Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany.Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany.Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany koellner@ice.mpg.de.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

30846485

Citation

Günther, Jan, et al. "Separate Pathways Contribute to the Herbivore-Induced Formation of 2-Phenylethanol in Poplar." Plant Physiology, vol. 180, no. 2, 2019, pp. 767-782.
Günther J, Lackus ND, Schmidt A, et al. Separate Pathways Contribute to the Herbivore-Induced Formation of 2-Phenylethanol in Poplar. Plant Physiol. 2019;180(2):767-782.
Günther, J., Lackus, N. D., Schmidt, A., Huber, M., Stödtler, H. J., Reichelt, M., ... Köllner, T. G. (2019). Separate Pathways Contribute to the Herbivore-Induced Formation of 2-Phenylethanol in Poplar. Plant Physiology, 180(2), pp. 767-782. doi:10.1104/pp.19.00059.
Günther J, et al. Separate Pathways Contribute to the Herbivore-Induced Formation of 2-Phenylethanol in Poplar. Plant Physiol. 2019;180(2):767-782. PubMed PMID: 30846485.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Separate Pathways Contribute to the Herbivore-Induced Formation of 2-Phenylethanol in Poplar. AU - Günther,Jan, AU - Lackus,Nathalie D, AU - Schmidt,Axel, AU - Huber,Meret, AU - Stödtler,Heike-Jana, AU - Reichelt,Michael, AU - Gershenzon,Jonathan, AU - Köllner,Tobias G, Y1 - 2019/03/07/ PY - 2019/01/23/received PY - 2019/02/26/accepted PY - 2019/3/9/pubmed PY - 2019/3/9/medline PY - 2019/3/9/entrez SP - 767 EP - 782 JF - Plant physiology JO - Plant Physiol. VL - 180 IS - 2 N2 - Upon herbivory, the tree species western balsam poplar (Populus trichocarpa) produces a variety of Phe-derived metabolites, including 2-phenylethylamine, 2-phenylethanol, and 2-phenylethyl-β-d-glucopyranoside. To investigate the formation of these potential defense compounds, we functionally characterized aromatic l-amino acid decarboxylases (AADCs) and aromatic aldehyde synthases (AASs), which play important roles in the biosynthesis of specialized aromatic metabolites in other plants. Heterologous expression in Escherichia coli and Nicotiana benthamiana showed that all five AADC/AAS genes identified in the P trichocarpa genome encode active enzymes. However, only two genes, PtAADC1 and PtAAS1, were significantly upregulated after leaf herbivory. Despite a sequence similarity of ∼96%, PtAADC1 and PtAAS1 showed different enzymatic functions and converted Phe into 2-phenylethylamine and 2-phenylacetaldehyde, respectively. The activities of both enzymes were interconvertible by switching a single amino acid residue in their active sites. A survey of putative AADC/AAS gene pairs in the genomes of other plants suggests an independent evolution of this function-determining residue in different plant families. RNA interference -mediated-downregulation of AADC1 in gray poplar (Populus × canescens) resulted in decreased accumulation of 2-phenylethylamine and 2-phenylethyl-β-d-glucopyranoside, whereas the emission of 2-phenylethanol was not influenced. To investigate the last step of 2-phenylethanol formation, we identified and characterized two P trichocarpa short-chain dehydrogenases, PtPAR1 and PtPAR2, which were able to reduce 2-phenylacetaldehyde to 2-phenylethanol in vitro. In summary, 2-phenylethanol and its glucoside may be formed in multiple ways in poplar. Our data indicate that PtAADC1 controls the herbivore-induced formation of 2-phenylethylamine and 2-phenylethyl-β-d-glucopyranoside in planta, whereas PtAAS1 likely contributes to the herbivore-induced emission of 2-phenylethanol. SN - 1532-2548 UR - https://www.unboundmedicine.com/medline/citation/30846485/Separate_Pathways_Contribute_to_the_Herbivore_Induced_Formation_of_2_Phenylethanol_in_Poplar_ L2 - http://www.plantphysiol.org/cgi/pmidlookup?view=long&pmid=30846485 DB - PRIME DP - Unbound Medicine ER -