AUTHOR=Hashemi Maryam , Amiel Aurélien , Zouaoui Mohamed , Adam Kévin , Clemente Hélène San , Aguilar Marielle , Pendaries Rémi , Couzigou Jean-Malo , Marti Guillaume , Gaulin Elodie , Roy Sébastien , Rey Thomas , Dumas Bernard 

TITLE=The mycoparasite Pythium oligandrum induces legume pathogen resistance and shapes rhizosphere microbiota without impacting mutualistic interactions

JOURNAL=Frontiers in Plant Science

VOLUME=14

YEAR=2023

URL=https://www.frontiersin.org/journals/plant-science/articles/10.3389/fpls.2023.1156733

DOI=10.3389/fpls.2023.1156733

ISSN=1664-462X

ABSTRACT=<p><italic>Pythium oligandrum</italic> is a soil-borne oomycete associated with rhizosphere and root tissues. Its ability to enhance plant growth, stimulate plant immunity and parasitize fungal and oomycete preys has led to the development of agricultural biocontrol products. Meanwhile, the effect of <italic>P. oligandrum</italic> on mutualistic interactions and more generally on root microbial communities has not been investigated. Here, we developed a biological system comprising <italic>P. oligandrum</italic> interacting with two legume plants, <italic>Medicago truncatula</italic> and <italic>Pisum sativum. P. oligandrum</italic> activity was investigated at the transcriptomics level through an RNAseq approach, metabolomics and finally metagenomics to investigate the impact of <italic>P. oligandrum</italic> on root microbiota. We found that <italic>P. oligandrum</italic> promotes plant growth in these two species and protects them against infection by the oomycete <italic>Aphanomyces euteiches</italic>, a devastating legume root pathogen. In addition, <italic>P. oligandrum</italic> up-regulated more than 1000 genes in <italic>M. truncatula</italic> roots including genes involved in plant defense and notably in the biosynthesis of antimicrobial compounds and validated the enhanced production of <italic>M. truncatula</italic> phytoalexins, medicarpin and formononetin. Despite this activation of plant immunity, we found that root colonization by <italic>P. oligandrum</italic> did not impaired symbiotic interactions, promoting the formation of large and multilobed symbiotic nodules with <italic>Ensifer meliloti</italic> and did not negatively affect the formation of arbuscular mycorrhizal symbiosis. Finally, metagenomic analyses showed the oomycete modifies the composition of fungal and bacterial communities. Together, our results provide novel insights regarding the involvement of <italic>P. oligandrum</italic> in the functioning of plant root microbiota.</p>