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Genetic disruption of Arabidopsis secondary metabolite synthesis leads to microbiome-mediated modulation of nematode invasion

Abstract

In-depth understanding of metabolite-mediated plant-nematode interactions can guide us towards novel nematode management strategies. To improve our understanding of the effects of secondary metabolites on soil nematode communities, we grew Arabidopsis thaliana genetically altered in glucosinolate, camalexin, or flavonoid synthesis pathways, and analyzed their root-associated nematode communities using metabarcoding. To test for any modulating effects of the associated microbiota on the nematode responses, we characterized the bacterial and fungal communities. Finally, as a proxy of microbiome-modulating effects on nematode invasion, we isolated the root-associated microbiomes from the mutants and tested their effect on the ability of the plant parasitic nematode Meloidogyne incognita to penetrate tomato roots. Most mutants had altered relative abundances of several nematode taxa with stronger effects on the plant parasitic Meloidogyne hapla than on other root feeding taxa. This probably reflects that M. hapla invades and remains embedded within root tissues and is thus intimately associated with the host. When transferred to tomato, microbiomes from the flavonoid over-producing pap1-D enhanced M. incognita root-invasion, whereas microbiomes from flavonoid-deficient mutants reduced invasion. This suggests microbiome-mediated effect of flavonoids on Meloidogyne infectivity plausibly mediated by the alteration of the abundances of specific microbial taxa in the transferred microbiomes, although we could not conclusively pinpoint such causative microbial taxa.

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Fig. 1: PCoA plots of Arabidopsis root-associated nematode communities using Bray-Curtis dissimilarity distance matrices.
Fig. 2: Differential abundance of nematode taxa in the roots of the Arabidopsis mutants compared to parental lines.
Fig. 3: Nematode community profile of Arabidopsis roots.
Fig. 4: Heatmap showing significant (p < 0.01) Spearman’s rank correlation between nematodes and bacterial / fungal operational taxonomic units (OTUs) in the roots of Arabidopsis mutants and their parental line.
Fig. 5: Effect of the Arabidopsis root-associated microbiota on M. incognita J2 invasion of tomato roots.

Data availability

The paired end sequence reads for the nematode 18 S rRNA gene, bacterial 16 S rRNA gene, and fungal ITS2 region have been deposited in the NCBI SRA database (https://www.ncbi.nlm.nih.gov/sra) under accession code PRJNA698344 (198 samples), and PRJNA698287 (roots of Arabidopsis parental lines only, 12 samples). Raw data are openly available in the public depository Zenodo at https://doi.org/10.5281/zenodo.5115230.

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Acknowledgements

We acknowledge Professor Judith Bender (Brown University, USA), Professor Wendy Ann Peer (University of Maryland, USA), and the Nottingham Arabidopsis Stock Centre (NASC, UK) for kindly providing the Arabidopsis lines. We are grateful to Mathilde Schiøtt Dige and Simone Ena Rasmussen for their laboratory technical assistance.

Funding

This research work was funded by Aarhus University (project number: 27747) and the Independent Research Fund Denmark DFF (grant numbers: 6111-00065B and 9041-00139B).

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MMS, MN, MV, and OT conceived and designed the experiments. MMS and OT executed the experiments. MMS and ENK analyzed the data. MN, TK, and MV supervised the experiments. MMS wrote the original draft, and all authors edited and reviewed the manuscript.

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Correspondence to Mogens Nicolaisen.

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Sikder, M.M., Vestergård, M., Kyndt, T. et al. Genetic disruption of Arabidopsis secondary metabolite synthesis leads to microbiome-mediated modulation of nematode invasion. ISME J (2022). https://doi.org/10.1038/s41396-022-01276-x

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