Removal of soil biota alters soil feedback effects on plant growth and defense chemistry

Abstract

We examined how the removal of soil biota affects plant-soil feedback (PSF) and defense chemistry of Jacobaea vulgaris, an outbreak plant species in Europe containing the defense compounds pyrrolizidine alkaloids (PAs). Macrofauna and mesofauna, as well as fungi and bacteria, were removed size selectively from unplanted soil or soil planted with J. vulgaris exposed or not to above- or belowground insect herbivores. Wet-sieved fractions, using 1000-, 20-, 5- and 0.2-μm mesh sizes, were added to sterilized soil and new plants were grown. Sieving treatments were verified by molecular analysis of the inocula. In the feedback phase, plant biomass was lowest in soils with 1000- and 20-μm inocula, and soils conditioned with plants gave more negative feedback than without plants. Remarkably, part of this negative PSF effect remained present in the 0.2-μm inoculum where no bacteria were present. PA concentration and composition of plants with 1000- or 20-μm inocula differed from those with 5- or 0.2-μm inocula, but only if soils had been conditioned by undamaged plants or plants damaged by aboveground herbivores. These effects correlated with leaf hyperspectral reflectance. We conclude that size-selective removal of soil biota altered PSFs, but that these PSFs were also influenced by herbivory during the conditioning phase.

Exogenous application of plant hormones in the field alters aboveground plant–insect responses and belowground nutrient availability, but does not lead to differences in plant–soil feedbacks

“…The only measurable response we found in the plant was that J. vulgaris invested in root biomass in more productive plots, which is in line with the finding that J. vulgaris strongly responds to competition (e.g., Van de Voorde et al 2012;Jing et al 2015;Bezemer et al 2018). Jacobaea vulgaris has been used as a model system to study biotic soil legacy effects that contribute to plant-soil feedbacks, and is highly responsive to soil conditioning by different plant species (Van de Voorde et al 2012) and these responses have been ascribed to, at least in part, shifts in soil communities (Bezemer et al 2013;Kos et al 2015;Wang et al 2019). This plant species, for example, responds differently to soil conditioning, depending on the presence or absence of aboveground herbivores on the plant that conditioned the soil (Kostenko et al 2012;Bezemer et al 2013).…”

“…We measured soil nutrients and organic matter, and conducted a phytometer plant assay, using Jacobaea vulgaris. This species is known to be highly sensitive to changes in soil microbial communities and plant-soil feedbacks (Wang et al 2019;Van de Voorde et al 2012;Kostenko et al 2012). We hypothesized that (i) exogenous application of JA and SA individually to the plant community, through plant-mediated changes in the soil, will have a positive effect on the growth of phytometer plant J. vulgaris, compared to their growth in control plots that did not receive JA or SA, and that (ii) exogenous application of JA and SA together, would have additive positive effects on growth of the phytometer plant J. vulgaris, compared to their growth in control plots that did not receive JA or SA.…”

Abiotic and Biotic Soil Legacy Effects of Plant Diversity on Plant Performance

“…Hence, we expected a positive relationship between biomass of J. vulgaris and plant diversity. Earlier studies have shown that soil legacy effects on J. vulgaris can be explained by soil fungal composition (Bezemer et al, 2006;Wang et al, 2019). In our study, soil fungal community composition was not strongly affected by the diversity of the plant community but it was significantly related to the biomass of J. vulgaris when the plants were grown in the pure field soil.…”

Conditioning the soil microbiome through plant–soil feedbacks suppresses an aboveground insect pest

“…Several authors have argued that the introduction of more complex soil communities, rather than single species/ strains, is necessary to achieve consistent enhancement of crop protection (Busby et al, 2017;Pineda et al, 2017), but so far, evidence of resistance against herbivores triggered either by such microbiome or by a single microbial strain functioning in a complex microbial community is scarce. Interestingly, studies with Arabidopsis or other wild plant species have shown, using soil sieving or sterilization, that the soil microbiome as a whole plays a significant role in inducing plant resistance to leaf-feeding herbivorous insects (Badri et al, 2013;Hubbard et al, 2019;Wang et al, 2019). Until now, most studies on soil microbiomes have focused on building synthetic communities based on culturable organisms (Santhanam et al, 2015;Herrera Paredes et al, 2018) and the challenge is now how to manipulate those microbiomes to optimize induced resistance in crops.…”