Glyphosate residues alter the microbiota of a perennial weed with a minimal indirect impact on plant performance

Abstract

Purpose In cold climates, glyphosate residues may linger in soils, with effects on plant–microbe interactions and, consequently, plant performance. Here, we explore the influence of glyphosate residues on the endophytic microbiota (bacteria and fungi) and performance of the perennial nitrogen-fixing weed Lupinus polyphyllus. Methods In a common garden, we grew plants from six populations of L. polyphyllus in glyphosate-treated or untreated control soils, with or without additional phosphorus. We sampled plant microbiota (leaves, roots, nodules) and assessed plant performance based on six traits: height, retrogression probability (i.e. shrinkage), biomass, root:shoot ratio, nodule number, and nodule viability. Results The richness of plant endophytic microbial communities was determined by soil phosphorus level rather than by glyphosate treatment. However, for bacteria, the composition of these communities differed between glyphosate-treated and control soils across plant tissue types; no difference was observed for fungi. The plant bacterial communities in both soil types were dominated by potential nitrogen-fixing bacteria belonging to family Bradyrhizobiaceae, and particularly so in glyphosate-treated soils. Overall, though, these changes in plant bacterial communities had a minor effect on plant performance: the only difference we detected was that the probability of retrogression was occasionally higher in glyphosate-treated soils than in control soils. Conclusion Our findings indicate that glyphosate-based herbicides, when applied at the recommended frequency and concentration, may not have critical effects on the growth of short-lived weeds after the safety period has passed; however, the endophytic microbiota of such weeds may experience longer-lasting shifts in community structure.

Glyphosate residues in soil can modify plant resistance to herbivores through changes in leaf quality.

“…Neither glyphosate nor phosphorus treatment had effects on the performance of the study species. This result is in line with our previous findings for the same study system (Ramula et al ., 2022), confirming that L . polyphyllus is not particularly sensitive to glyphosate residues or phosphorus levels in soil.…”

“…Glyphosate has also been found to reduce nodulation (Reddy & Zablotowicz, 2003; Zobiole et al ., 2010), which can be critical for a plant's nitrogen availability and nutrient balance. Moreover, glyphosate residues in soil or in manure fertilizer reduce the growth and reproduction of crop plants (Helander et al ., 2019; Soares et al ., 2019; Muola et al ., 2021) and indirectly reduce plant performance in non‐crops through changes in the soil microbiota (Ramula et al ., 2022). On the other hand, the opposite result has also been reported: low doses of glyphosate can induce the growth of both crop and non‐crop plants ( e .…”

Soil microbiota explain differences in herbivore resistance between native and invasive populations of a perennial herb

“…In Finland, bacteria in the family Bradyrhizobiaceae are particularly abundant in the nodules of L. polyphyllus (Ramula et al, 2022), but with only a subset of the available rhizobia (Shelby et al, 2016).…”

“…Generalism in rhizobial association predicts the invasive potential of legumes (T. L. Harrison et al, 2018), and although L. polyphyllus is often considered to have a relatively specialized association with species of Bradyrhizobium , it is able to host other genera of rhizobia as well (Stępkowski et al, 2018). In Finland, bacteria in the family Bradyrhizobiaceae are particularly abundant in the nodules of L. polyphyllus (Ramula et al, 2022), but further studies are needed to tease apart differences in the rhizobial associations of plants of different origins.…”

Management practice and soil properties affect plant productivity and root biomass in endophyte‐symbiotic and endophyte‐free meadow fescue grasses

“…In addition to the effects caused by glyphosate directly, glyphosate residues and aminomethyl phosphonic acid (glyphosate's breakdown product) can indirectly affect the health of plants through changes in the rhizosphere microbiome (van Bruggen et al, 2018; Kremer & Means, 2009; Kuklinsky‐Sobral et al, 2005). At the soil microbial level, glyphosate can reduce beneficial rhizosphere symbionts, including mycorrhizal fungi and nitrogen‐fixing bacteria (van Bruggen et al, 2021; Helander et al, 2018; Mohamed et al, 2021; Ramula et al, 2021; Wilkes et al, 2020). Concentrations of pesticide residues in soil under conventional agriculture are ubiquitous, but residues are also found in organic agricultural management soils and may be introduced via animal manure fertilizer (Fuchs, Saikkonen, et al, 2022; Muola et al, 2021; Riedo et al, 2021).…”