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Microbiota responses to mutations affecting NO homeostasis in Arabidopsis thaliana

Antoine Berger, Eduardo Pérez-Valera, Manuel Blouin, Marie-Christine Breuil, Klaus Butterbach-Bahl, Michael Dannenmann, Angelique Besson-Bard, Sylvain Jeandroz, Josep Valls, Aymé Spor, Logapragasan Subramaniam, Pierre Pétriacq, David Wendehenne and Laurent Philippot

Data

The raw data for this study are available in the NCBI SRA under Bio-Projects PRJNA1086445 for the 16S rRNA sequences and PRJNA1086460 for the ITS sequences.

To cite this work

Berger, A., Pérez-Valera, E., Blouin, M., Breuil, M.-C., Butterbach-Bahl, K., Dannenmann, M., Besson-Bard, A., Jeandroz, S., Valls, J., Spor, A., Subramaniam, L., Pétriacq, P., Wendehenne, D., Philippot, L., 2024. Microbiota responses to mutations affecting NO homeostasis in Arabidopsis thaliana. New Phytologist 2008–2023. doi:10.1111/nph.20159

Summary

• Interactions between plants and microorganisms are pivotal for plant growth and productivity. Several plant molecular mechanisms that shape these microbial communities have been identified. However, the importance of nitric oxide (NO) produced by plants for the associated microbiota remains elusive.
• Using Arabidopsis thaliana isogenic mutants overproducing NO (nox1, NO overexpression) or down-producing NO (i.e. nia1nia2 impaired in the expression of both nitrate reductases NR1/NIA1 and NR2/NIA2; the 35s::GSNOR1 line overexpressing nitrosoglutathione reductase (GSNOR) and 35s::AHB1 line overexpressing haemoglobin 1 (AHB1)), we investigated how altered NO homeostasis affects microbial communities in the rhizosphere and in the roots, soil microbial activity and soil metabolites.
• We show that the rhizosphere microbiome was affected by the mutant genotypes, with the nox1 and nia1nia2 mutants causing opposite shifts in bacterial and fungal communities compared with the wild-type (WT) Col-0 in the rhizosphere and roots, respectively. These mutants also exhibited distinctive soil metabolite profiles than those from the other genotypes while soil microbial activity did not differ between the mutants and the WT Col-0.
• Our findings support our hypothesis that changes in NO production by plants can influence the plant microbiome composition with differential effects between fungal and bacterial communities.

Funding

This work was co-funded by the French ANR and German DFG under contract number ANR-20-CE92-0004 and DFG BU 1173/25-1. The authors are grateful for financial support from MetaboHUB (ANR-11-INBS-0010) and PHENOME (ANR-11-INBS-0012) projects.