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Common mycelial network modulates neighbour-primed plant defences against foliar pathogens by co-opting distinct inter-plant metabolic and biotic stress responses.

ABSTRACT: Inter-plant communication is key for the successful thriving of plant communities in nature with yet untapped potential for agroecosystem engineering towards more resilient crops and plant defences against pathogens. Arbuscular mycorrhizal fungi (AMF) are ubiquitous root symbionts, well-known to constitute underground common mycelial networks (CMNs) linking multiple plant hosts underground. The wired connection among plants via CMNs are hypothesized to play a key role for information exchange between plants for the neighbour-primed inter-plant defences. However, the key transcriptomic and metabolome responses in receiver plant associated with inter-plant CMN connections remain yet to be elucidated. Moreover, no studies to date have clearly resolved the confounding effects of hyphal damage from the inter-plant network disconnection. To uncover the contribution of CMN integrity to neighbour-primed plant defences, we used model AMF Rhizophagus irregularis to inter-connect two Medicago truncatula plants and explored the effect of sender wounding and flg22 elicitation on receiver plants’ leaf responses and pathogen tolerance. For the first time, we demonstrate that changes in receiver plants’ biotic stress and defence signalling pathways rely on inter-plant signals via the CMN, not on mycelial network damage itself. This response was associated with distinct leaf isoprenoid production, including volatile monoterpenes and triterpene saponins. Furthermore, CMN-mediated signals from stressed senders enhanced receiver resistance to Fusarium sporotrichoides whilst simultaneously increasing susceptibility to Botrytis cinerea. Our findings highlight the critical role of CMNs in inter-plant signalling for pathogen-specific susceptibility and resistance which can be a key for understanding plant community-level defence in nature and agroecosystems.

ORGANISM(S): Medicago truncatula

PROVIDER: GSE325469 | GEO | 2026/06/06

REPOSITORIES: GEO

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Project description:In plants, an increase in resource allocation to growth (primary metabolism) associated with the presence of neighbors is likely to reduce defense-related production (secondary metabolism), making plants more vulnerable to herbivory. Even though there is increasing evidence supporting this “trade-off hypothesis”, the underlying mechanisms are still unclear. Far red (FR) radiation reflected from plant tissues serves as an early warning signal of future competition, triggering a suite of plastic morphological adjustments that improve plant’s ability to compete for light in crowded populations. Recent evidence from our lab showed that, when competition signals are present, plant defenses are severely reduced. Besides direct effects of herbivory and competition signals on target plants, second order effects occurs on neighboring plants through plant volatiles (PVs) communication. PVs play a key role in plant-plant and plant-insect interactions, changing its content and composition in response to environmental conditions. To increase our understanding of the molecular mechanisms underlying those interacting signaling webs, we performed a field study with tomato plants (cv Moneymaker), in which plants of EMITTER plots (six plants plot-1) were subjected to herbivory (nine larvae of Spodoptera eridania plant-1) and competition signals (increased FR radiation) in a factorial design. Light treatment started 28 days after sowing (DAS), and herbivory treatment and volatiles conduction started 34 DAS. Volatiles were conducted from EMITTER to RECEIVER plots (five plants plot-1) using a 5 inch, 1.4 m long tube fitted with a computer-type fan. 40 and 45 DAS, larval performance was measured on EMITTER plots as well as naturally-occurring insect colonization on RECEIVER plots. Finally (46 DAS), samples for bulk phenolic content were taken on every plot, and plant material from 4th and 5th leaves was collected for microarray analysis. There were three real biological replicates. Keywords: Reference design

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Common mycelial network modulates neighbour-primed plant defences against foliar pathogens by co-opting distinct inter-plant metabolic and biotic stress responses.

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