Orlovskis, Z. | bioRxiv Science

bioRxiv2024

Common mycelial network mediated inter-plant signals modulate plant biotic stress responses and defence against foliar pathogens

Arbuscular mycorrhizal fungi (AMF) are ubiquitous root symbionts that form common mycelial networks (CMN), linking multiple plants underground. CMN are hypothesized to play a role for information exchange between plants for neighbour-primed defences. However, the key transcriptomic and metabolome responses in receiver plant associated with inter-plant CMN connections remain yet to be elucidated. Additionally, the confounding effects of hyphal damage from CMN disconnection have not been clearly resolved. 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 receivers biotic stress and defence signalling pathways rely on CMN-mediated inter-plant signals, not on mycelial network damage. 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 CMN 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.

plant biology↗

bioRxiv2024

Phytoplasma Targeting of MADS-Box Factor SVP Suppresses Leaf Responses to Insect Vector Males, Promoting Female Attraction and Colonization

Obligate parasites often trigger significant changes in their hosts to facilitate transmission to new hosts. The molecular mechanisms behind these extended phenotypes - where genetic information of one organism is manifested as traits in another - remain largely unclear. This study explores the role of the virulence protein SAP54, produced by parasitic phytoplasmas, in attracting leafhopper vectors. SAP54 is responsible for the induction of leaf-like flowers in phytoplasma-infected plants. However, we previously demonstrated that the insects were attracted to leaves and the leaf-like flowers were not required. Here we made the surprising discovery that leaf exposure to leafhopper males is required for the attraction phenotype, suggesting a leaf response that distinguishes leafhopper sex in the presence of SAP54. In contrast, this phytoplasma effector alongside leafhopper females discourages further female colonization. We demonstrate that SAP54 effectively suppresses biotic stress response pathways in leaves exposed to the males. Critically, the host plant MADS-box transcription factor SHORT VEGETATIVE PHASE (SVP) emerges as a key element in the female leafhopper preference for plants exposed to males, with SAP54 promoting the degradation of SVP. This preference extends to female colonization of male-exposed svp null mutant plants over those not exposed to males. Our research underscores the dual role of the phytoplasma effector SAP54 in host development alteration and vector attraction - integral to the phytoplasma life cycle. Importantly, we clarify how SAP54, by targeting SVP, heightens leaf vulnerability to leafhopper males, thus facilitating female attraction and subsequent plant colonization by the insects. SAP54 essentially acts as a molecular "matchmaker," helping male leafhoppers more easily locate mates by degrading SVP-containing complexes in leaves. This study not only provides insights into the long reach of single parasite genes in extended phenotypes, but also opens avenues for understanding how transcription factors that regulate plant developmental processes intersect with and influence plant-insect interactions.

plant biology↗