Ectomycorrhizal fungi induce systemic resistance against insects on a non-mycorrhizal plant in a CERK1-dependent manner

Abstract

20Below-ground microbes can induce systemic resistance (ISR) against foliar pests and 21 pathogens on diverse plant hosts. The prevalence of ISR among plant-microbe-pest systems 22 raises the question of host specificity in microbial induction of ISR. To test whether ISR is 23 limited by plant host range, we tested the ISR-inducing ectomycorrhizal (ECM) fungus 24 Laccaria bicolor on the non-mycorrhizal plant Arabidopsis. We found that root inoculation 25 with L. bicolor triggered ISR against the insect herbivore Trichoplusia ni and induced systemic 26 susceptibility (ISS) against the bacterial pathogen Pseudomonas syringae pv. tomato DC3000 27 (Pto). We found that L. bicolor-triggered ISR against T. ni was dependent on jasmonic acid 28 (JA) signaling and salicylic acid (SA) biosynthesis and signaling. We found that heat killed L. 29 bicolor and chitin are sufficient to trigger ISR against T. ni and ISS against Pto and that the 30 chitin receptor CERK1 is necessary for L. bicolor-mediated effects on systemic immunity. 31Collectively our findings suggest that some ISR responses might not require intimate co-32 evolution of host and microbe, but rather might be the result of root perception of conserved 33 microbial signals. 34 35 Plants associate with complex communities of microorganisms. Interplay of host and 36 microbial genotype determine whether the outcome of specific plant-microbe interactions is 37 beneficial or detrimental to plant health 1-3 . Plants possess receptors to sense potential 38 pathogens including transmembrane pattern-recognition receptors that recognize conserved 39 microbe-associated molecular patterns (MAMPs), and intracellular receptors that directly or 40 indirectly recognize effectors to help limit pathogen growth 4,5 . MAMP perception by plant 41 receptors triggers pattern-triggered immunity (PTI) responses including a reactive oxygen 42 species (ROS) burst, Mitogen-Activated Protein Kinase (MAPK) signaling, ion influx and 43 callose deposition 6-9 . In addition to local immune mechanisms, root-associated microbes can 44 induce systemic resistance (ISR) against a diverse spectrum of above-ground threats 2,10 . While 45 the mechanisms by which plants perceive MAMPs and effectors are well understood, there is 46 a more limited understanding of the mechanisms by which plant perceive the microbes that 47 trigger ISR. 48 In response to perception of microbes or pathogens, plants activate systemic defense 49 mechanisms including commensal-triggered ISR and pathogen-triggered systemic acquired 50 resistance (SAR) 11,12 . While both SAR and ISR confer resistance to pests and pathogens, they 51 promote resistance through distinct mechanisms 2 . SAR occurs upon local perception of a 52 pathogen, MAMP, or effector and results in systemic induction of SA-dependent gene 53 expression and accumulation of secondary metabolites 13,14 . Unlike SAR, ISR is associated with 54 small or no changes in systemic gene expression and phytohormone levels 15,16 . Additionally, 55while SAR is dependent...

Impact of Nitrogen Nutrition and Ectomycorrhizal Interaction on Populus x canescens Xylem Sap Composition and Defense

“…Taken together, these results indicate a pivotal role of JA in L. bicolor induced systemic defense responses. Additionally, SA-related responses were involved in the systemic reaction, supporting the findings of and Vishwanathan et al (2020).…”

“…The expression of genes involved in the response to jasmonic acid (JA) was increased in the new leaf transcriptome data, which is contradictory to what we published before . A dependence on JA signaling in L. bicolormediated defense responses was shown in the non-host Arabidopsis (Vishwanathan et al, 2020).…”

“…In recent years, it was recognized that beneficial microbes can strengthen plant defenses (Pieterse et al, 2014). In contrast to SAR, this response was denominated as "induced systemic resistance (ISR)" describing processes that trigger aboveground defenses when plants interact with growth promoting rhizobacteria (PGPR) (van Loon, 2007), arbuscular (Jung et al, 2012) or ectomycorrhizal fungi Szuba et al, 2019;Vishwanathan et al, 2020). The fitness improvement of plants resulting from the interaction of symbiotic fungi and plants is also termed mycorrhiza-induced resistance (MIR) (Jung et al, 2012).…”

“…This observation was underpinned when the influence of L. bicolor was studied in Arabidopsis. Although Arabidopsis -like all Brassicaceae (Fernández et al, 2019)cannot form mycorrhizal associations, the presence of L. bicolor enhances resistance against caterpillar (Trichoplusia ni) feeding (Vishwanathan et al, 2020). This response requires CERK1, JA signaling via COI1 and repression of SA signaling via NPR3/4 (Vishwanathan et al, 2020).…”

Microbiota-root-shoot axis modulation by MYC2 favoursArabidopsisgrowth over defence under suboptimal light

“…Induction of systemic defence responses, including pathogen-triggered systemic acquired resistance (SAR, SA-dependent) and commensal-triggered induced systemic resistance (ISR, JA- and ET-dependent), has been extensively reported in response to specific commensal or pathogenic microbes ( Chanda et al 2011; Cecchini et al 2015; Zamioudis et al, 2015; Vishwanathan et al 2020; Wenig et al, 2019 ). Here, we showed that root colonization by a multi-kingdom consortium of microbes originally isolated from roots of healthy plants, triggered aboveground induction of defence responses effective against Bc and Pst .…”