Mycorrhizal Symbiosis Triggers Local Resistance in Citrus Plants Against Spider Mites

Abstract

Citrus plants are a highly mycotrophic species with high levels of fungal colonization. Citrus aurantium rootstocks typically show abundant root colonization by Rhizophagus irregularis three weeks after inoculation. Mycorrhizal symbiosis protects plants against multiple biotic stressors, however, such protection against spider mites remains controversial. We examined mycorrhiza-induced resistance (MIR) in citrus against the two-spotted spider mite Tetranychus urticae. Mycorrhized C. aurantium displayed reduced levels of damage in leaves and lower mite oviposition rates, compared to non-mycorrhized controls. Mycorrhization did not affect host choice of mites in Y-tube assays; of note, C. aurantium has innate strong antixenotic resistance against this mite. Analysis of metabolism pathways in mycorrhized citrus plants showed upregulated expression of the oxylipin-related genes LOX-2 and PR-3 early after infestation. Accordingly, jasmonic acid (JA), 12-oxo phytodienoic acid (OPDA), and JA-Ile concentrations were increased by mycorrhization. Non-targeted metabolomic analysis revealed the amino acid, oxocarboxylic acid, and phenylpropanoid metabolism as the three major pathways with more hits at 24 h post infection (hpi) in mycorrhized plants. Interestingly, there was a transition to a priming profile of these pathways at 48 hpi following infestation. Three flavonoids (i.e., malic acid, coumaric acid, and diconiferyl alcohol) were among the priming compounds. A mixture containing all these compounds provided efficient protection against the mite. Unexpectedly, systemic resistance did not improve after 72 h of primary infestation, probably due to the innate strong systemic resistance of C. aurantium. This is the first study to show that MIR is functional against T. urticae in locally infested citrus leaves, which is mediated by a complex pool of secondary metabolites and is likely coordinated by priming of JA-dependent responses.

Plant-Mediated Effects of Beneficial Microbes and a Plant Strengthener against Spider Mites in Tomato

“…With regard to the effects of arbuscular mycorrhizal fungi (AMF), previous studies have shown variable effects on spider mites. Spider mite performance was shown to be enhanced by the AMF Glomus mosseae on bean plants [ 30 , 31 , 32 ], whereas spider mite performance in Lotus japonicus was differentially affected by four different AMF species belonging to different genera depending on the AMF species [ 48 ], and negatively affected in citrus plants [ 49 ]. It is evident that this important group of plant-interacting organisms need a more thorough evaluation as putative biocontrol agents.…”

Mycorrhiza‐induced resistance in citrus against Tetranychus urticae is plant species dependent and inversely correlated to basal immunity

“…Two-month-old C. reshni and C. aurantium seeds were germinated and grown in vermiculite in a climate chamber with a 16:8 h light/dark photoperiod, 24 °C/18 °C day/night temperature and 50-70% relative humidity (RH). Rhizophagus irregularis (BEG121 isolate) (former Glomus intraradices) was maintained in a soil-based inoculum and inoculated as described by Manresa-Grao et al 44 Control plants were watered once with a filtrate of the mycorrhizal (AM) inoculum, without the AMF spores, to replicate the microbiome. All plants were watered with modified Hoagland's solution; the modification involved the use of a commercial microelements mix (Nutrishell®, Agrimor-Zenagro, Spain), 45 and no pesticide was applied.…”

“…RNA extraction from leaves was performed as described by Kiefer et al, 50 with some modifications indicated in Manresa-Grao et al 44 The RNA concentration was adjusted to 1 μg/μL using a NanoDrop--2000 (Thermo Scientific). Following DNase (Thermo Fisher Scientific) treatment, complementary DNA was obtained using the PrimeScript™ RT Reagent Kit (Takara, Valencia, Spain).…”

“…In a previous study with the mite-resistant species C. aurantium, we showed that symbiosis with Rhizophagus irregularis further boosts local resistance by triggering a concomitant increase in JA, LOXD and the phenylpropanoids cinnamic acid and diconiferyl alcohol, as well as several flavonoids. 44 By contrast, MIR was ineffective in triggering antixenosis or systemic resistance. In this study, we performed comparative experiments on both C. aurantium and C. reshni species to determine the differential impact of MIR related to basal immunity.…”

Phosphorus availability drives mycorrhiza induced resistance in tomato

“…Priming is a common mechanism during induced systemic resistance triggered by beneficial microbes, consisting of a stronger and faster activation of plant defense mechanisms, usually dependent on jasmonate signaling ( Pieterse et al., 2014 ; Mora-Romero et al., 2014 ; Gruden et al., 2020 ). Despite priming of plant defenses in response to pathogens and herbivores in mycorrhizal plants is well documented ( Campos-Soriano et al., 2012 ; Song et al., 2013 ; Song et al., 2015 ; Sanchez-Bel et al., 2016 ; Fiorilli et al., 2018 ; Schoenherr et al., 2019 ; Sanmartín et al., 2020 ; Rivero et al., 2021 ; Manresa-Grao et al., 2022 ) consequences of AM symbiosis for insect herbivores are complex to predict. Indeed, the nutritional benefits of the symbiosis may increase food availability or improve the diet quality for the pest, depending on the fungal and insect identity and growing conditions ( Koricheva et al., 2009 ; Frew and Price, 2019 ).…”