The effect of rhizosphere microbes outweighs host plant genetics in reducing insect herbivory

Abstract

Rhizosphere microbes affect plant performance, including plant resistance against insect herbivores; yet, a direct comparison of the relative influence of rhizosphere microbes versus plant genetics on herbivory levels and on metabolites related to defence is lacking. In the crucifer Boechera stricta, we tested the effects of rhizosphere microbes and plant population on herbivore resistance, the primary metabolome, and select secondary metabolites. Plant populations differed significantly in the concentrations of six glucosinolates (GLS), secondary metabolites known to provide herbivore resistance in the Brassicaceae. The population with lower GLS levels experienced ~60% higher levels of aphid (Myzus persicae) attack; no association was observed between GLS and damage by a second herbivore, flea beetles (Phyllotreta cruciferae). Rhizosphere microbiome (disrupted vs. intact native microbiome) had no effect on plant GLS concentrations. However, aphid number and flea beetle damage were respectively about three‐ and seven‐fold higher among plants grown in the disrupted versus intact native microbiome treatment. These differences may be attributable to shifts in primary metabolic pathways previously implicated in host defence against herbivores, including increases in pentose and glucoronate interconversion among plants grown with an intact microbiome. Furthermore, native microbiomes with distinct community composition (as estimated from 16s rRNA amplicon sequencing) differed two‐fold in their effect on host plant susceptibility to aphids. The findings suggest that rhizosphere microbes, including distinct native microbiomes, can play a greater role than population in defence against insect herbivores, and act through metabolic mechanisms independent of population.

Importance of plant‐ and microbe‐driven metabolic pathways for plant defence

“…Hubbard et al. () grew Boechera stricta (Figure a) plants in different microbial contexts and measured effects on concentrations of defensive and primary metabolites, and on realized plant defence. The authors used successive filtration to remove soil particles and then microbes from soil–water slurries, and inoculated populations of B. stricta with either fully filtered water (disrupted communities) or water without microbe filtration (intact communities).…”

“…By surveying chemical defence and primary plant metabolites, Hubbard et al. () disentangled pathways to defence that are driven by plant variation from pathways driven by microbial variation. Higher concentrations of induced or constitutive defensive chemicals, such as the glucosinolates previously shown to be important in B. stricta (see Hubbard et al., ), can reduce the ability of insects to feed, survive or grow on plants.…”

“…() disentangled pathways to defence that are driven by plant variation from pathways driven by microbial variation. Higher concentrations of induced or constitutive defensive chemicals, such as the glucosinolates previously shown to be important in B. stricta (see Hubbard et al., ), can reduce the ability of insects to feed, survive or grow on plants. Similar effects may also be achieved by changing the nutritional quality of plant tissues for insects, or the physical barriers to feeding (Agrawal & Fishbein, ).…”

“…Hubbard et al. () found that plant and microbial variation shifted the relative abundances of a number of metabolites, some of which are involved in known herbivore resistance pathways, and that these changes were probably responsible for knock‐on shifts in resistance to herbivory both in the greenhouse and in the field (Figure b). Most intriguingly, microbes and plant genotype shift plant defence via different metabolic pathways.…”

“…Most intriguingly, microbes and plant genotype shift plant defence via different metabolic pathways. Variation in aphid herbivory attributable to plant genotype probably reflects inter‐population differences in glucosinolate compounds, although shifts in ascorbate metabolism may also contribute (further discussed in Hubbard et al., ). However, microbe‐driven shifts in plant defensive phenotypes had almost no effect on glucosinolate production: instead, microbiome disruption appeared to decrease physical defences through greater pentose and glucoronate interconversion and to reduce overall defence allocation by increasing plant stress (citrate cycle upregulation, see Hubbard et al., ).…”