Martinez-Medina, A. | bioRxiv Science

bioRxiv2026

Herbivory-triggered assemblage of sunflower rhizosphere microbiome enhances herbivore tolerance through plant-soil feedback

BackgroundMicrobial communities in the rhizosphere are key drivers of plant immunity, mediating plant responses to stress. Under specific stresses plants are capable of recruiting beneficial microorganisms into their rhizosphere with the potential to alleviate these stresses. Among these stresses, herbivorous pests remain a major agricultural challenge. Despite this, the impact of leaf herbivory on root-associated microbiomes, and how this impact can shape plant defense phenotypes are still understudied. In this study, our main objective was to determine the extent to which leaf herbivory affects the rhizosphere microbiome, and whether and how these herbivory-induced changes modulate plant defense phenotypes through plant-soil feedback. To that end, we designed a two-phase assay in which we challenged sunflower (Helianthus annuus L.) with Spodoptera exigua and later tested the effect of the microbial legacy after infestation on sunflower defense phenotype, considering resistance and tolerance as major drivers. ResultsWe found that herbivory triggered significant changes in the bacteriome structure and dynamics, and microbiome functional profile, while effects on mycobiome were comparatively less pronounced. Under herbivory, several bacterial taxa and functional groups were enriched, the bacterial co-occurrence network was more complex and assembly processes were slightly more stochastic. Furthermore, after evaluating the plant-soil feedbacks of herbivory-induced microbiomes we observed no effect on plant resistance proxies such as herbivore growth and survival, and leaf phenolic and flavonoid content. We did observe differences on tolerance proxies, while plants grown on herbivore-challenged microbiome were overall smaller, the biomass loss to herbivory was significantly lower while the elemental nutrient content and photosynthetic pigments content was enhanced. ConclusionsOur study demonstrates that insect herbivory by S.exigua reshapes sunflower rhizosphere microbiome and generates a soil legacy that promotes herbivory tolerance on subsequent plant generations. This highlights the broader potential of microbiome-mediated plant-soil feedbacks in shaping plant adaptation to herbivory.

plant biology↗

bioRxiv2024

Ethylene signaling is essential for mycorrhiza-induced resistance against chewing herbivores in tomato

Root colonization by certain beneficial microbes can prime plant defenses aboveground, modifying plant responses to potential attackers. Arbuscular mycorrhizal (AM) fungi establish mutualistic symbiosis with most plant species, usually enhancing plant resistance to biotic stresses, leading to Mycorrhiza-Induced Resistance (MIR). Still, our knowledge of the complex molecular regulation leading to MIR is very limited. Here we show that the AM fungus Funneliformis mosseae protects tomato plants against two different chewing herbivores, Spodoptera exigua and Manduca sexta, and we explore the underlying molecular mechanism. We explore the impact of AM symbiosis on the plant response to the herbivores through genome-wide transcriptional profiling, followed by bioinformatics network analyses and functional bioassays. Herbivore-triggered JA-regulated defenses were primed in leaves of mycorrhizal plants, while ET biosynthesis and signaling was also higher both before and after herbivory. We hypothesized that fine-tuned ET signaling is required for the primed defensive response leading to MIR in mycorrhizal plants. We followed analytical, functional, and genetic approaches to test this hypothesis and get mechanistic insights into the ET signaling in MIR. ET is a complex regulator of plant responses to stress, and although ET is generally considered a negative regulator of plant defenses against herbivory, tomato lines deficient in ET synthesis or perception could not develop MIR against either herbivore. Thus, we demonstrate that hormone crosstalk is central to the priming of plant immunity by beneficial microbes, with ET fine-tuning being essential for the primed JA biosynthesis and boosted defenses leading to MIR in tomato.

plant biology↗