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Alterations in the phenylpropanoid pathway affect poplar ability for ectomycorrhizal colonisation and susceptibility to root-knot nematodes

Abstract

This study investigates the impact of the alteration of the monolignol biosynthesis pathway on the establishment of the in vitro interaction of poplar roots either with a mutualistic ectomycorrhizal fungus or with a pathogenic root-knot nematode. Overall, the five studied transgenic lines downregulated for caffeoyl-CoA O-methyltransferase (CCoAOMT), caffeic acid O-methyltransferase (COMT), cinnamoyl-CoA reductase (CCR), cinnamyl alcohol dehydrogenase (CAD) or both COMT and CAD displayed a lower mycorrhizal colonisation percentage, indicating a lower ability for establishing mutualistic interaction than the wild-type. The susceptibility to root-knot nematode infection was variable in the five lines, and the CAD-deficient line was found to be less susceptible than the wild-type. We discuss these phenotypic differences in the light of the large shifts in the metabolic profile and gene expression pattern occurring between roots of the CAD-deficient line and wild-type. A role of genes related to trehalose metabolism, phytohormones, and cell wall construction in the different mycorrhizal symbiosis efficiency and nematode sensitivity between these two lines is suggested. Overall, these results show that the alteration of plant metabolism caused by the repression of a single gene within phenylpropanoid pathway results in significant alterations, at the root level, in the response towards mutualistic and pathogenic associates. These changes may constrain plant fitness and biomass production, which are of economic importance for perennial industrial crops such as poplar.

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Acknowledgements

We would like to thank Frédéric Guinet for the technical assistance of in vitro poplar inoculation.

Funding

MB (Marie Baucher) and FBC were supported by the Fonds de la Recherche Scientifique (FRS-FNRS) research project T.0004.14, and RVA and WB by the Multidisciplinary Research Partnership Biotechnology for a sustainable economy and by the European Commission’s Directorate-General for Research within the 7th Framework Program (FP7/2007-2013; grant agreement 270,089, MULTIBIOPRO). MB (Marie Baucher) is a Senior Research Associate of the FRS-FNRS. AK and CVF were supported by grants from the French National Agency of Research (ANR) as part of the “Investissement d’Avenir program” (ANR-11_LABX-0002-01) of Labex ARBRE (CFP15) and the US Department of Energy through the Oak Ridge National Laboratory Scientific Focus Area for Genomics Foundational Sciences (Plant Microbe Interfaces Project).

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Conceptualisation: Fabien Baldacci-Cresp, Janice de Almeida Engler, Mondher El Jaziri and Marie Baucher. Methodology: Fabien Baldacci-Cresp, Claire Veneault-Fourrey and Marie Baucher. Formal analysis and investigation: Marc Behr, Fabien Baldacci-Cresp, Annegret Kohler, Kris Morreel, Rebecca Van Acker, Geert Goeminne, Claire Veneault-Fourrey, Adeline Mol and Marie Baucher. Writing - original draft preparation: Marc Behr. Writing - review and editing: Marc Behr, Fabien Baldacci-Cresp, Claire Veneault-Fourrey, Janice de Almeida Engler, Mondher El Jaziri and Marie Baucher. Funding acquisition: Wout Boerjan, Marie Baucher. Resources: Gilles Pilate. Supervision: Marie Baucher.

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Correspondence to Marie Baucher.

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Electronic supplementary material

ESM 1

Complete results of the metabolomic analysis. (XLSX 1695 kb)

ESM 2

Complete list of genes differentially expressed in CAD root compared to wild-type root (P value <0.05, log ratio > 1). (XLSX 299 kb)

ESM 3

Transgenic poplar lines (P. tremula x P. alba clone INRA 717-1B4) used in this study. (PDF 32 kb)

ESM 4

Characterization of the CAD line used in this study. (PDF 74 kb)

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Behr, M., Baldacci-Cresp, F., Kohler, A. et al. Alterations in the phenylpropanoid pathway affect poplar ability for ectomycorrhizal colonisation and susceptibility to root-knot nematodes. Mycorrhiza 30, 555–566 (2020). https://doi.org/10.1007/s00572-020-00976-6

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Keywords

  • Ectomycorrhiza
  • Monolignol
  • Root-knot nematode
  • Secondary metabolites
  • Transcriptomics
  • Transgenic poplar