Glyphosate is a commonly used herbicide with a broad action spectrum. However, at sublethal doses, glyphosate can induce plant growth, a phenomenon known as hormesis. Most glyphosate hormesis studies have been performed under microbe-free or reduced-microbial-diversity conditions; only a few were performed in open systems or agricultural fields, which include a higher diversity of soil microorganisms. Here, we investigated how microbes affect the8 hormesis induced by low doses of glyphosate. To this end, we used Arabidopsis thaliana and a well-characterized synthetic bacterial community of 185 strains (SynCom) that mimics the root-associated microbiome of Arabidopsis. We found that a dose of 3.6 x 10-6 g acid equivalent/liter (low dose of glyphosate, or LDG) produced an ~14% increase in the shoot dry weight (i.e., hormesis) of uninoculated plants. Unexpectedly, in plants inoculated with the SynCom, LDG reduced shoot dry weight by 17%. We found that LDG enriched two Firmicutes and two Burkholderia strains in the roots. These specific strains are known to act as root growth inhibitors (RGI) in monoassociation assays. We tested the link between RGI and shoot dry weight reduction in LDG by assembling a new synthetic community lacking RGI strains. Dropping RGI strains out of the community restored growth induction by LDG. Finally, we showed that individual RGI strains from a few specific phyla were sufficient to switch the response to LDG from growth promotion to growth inhibition. Our results indicate that glyphosate hormesis was completely dependent on the root microbiome composition, specifically on the presence of root growth inhibitor strains.
Bibliographical noteFunding Information:
This work was supported by USFQ Collaboration Grant 2019 to A.L.R., NSF grant IOS-1917270, and the Office of Science (BER), U.S. Department of Energy, grant DESC0014395 to J.L.D. J.L.D. is an Investigator of the Howard Hughes Medical Institute and is supported by the HHMI. O.M.F. was supported by NIH NRSA Fellowship F32-GM117758. C.R.F. was supported by an NSERC postdoctoral fellowship (532852-2019). We also thank the Institute of Geography at Universidad San Francisco de Quito (USFQ) and Galapagos Science Center (GSC-UNC) for the financial support given to A.L.R. and D.X.R. during this project.
© 2020 Ramirez-Villacis et al.