Mycorrhizal plants display enhanced resistance to several pathogens. However, the molecular mechanisms regulating mycorrhiza-induced resistance (MIR) are still elusive. We aim to study the mechanisms underlying MIR against Botrytis cinerea and the role of callose accumulation during this process. Mycorrhizal tomato plants inoculated with Rhizoglomus irregularis displayed callose priming upon B. cinerea infection. The callose inhibitor 2-deoxy-d-glucose abolished MIR, confirming the relevance of callose in the bioprotection phenomena. While studying the mechanisms underlying mycorrhiza-induced callose priming, we found that mycorrhizal plants display an enhanced starch degradation rate that is correlated with increased levels of β-amylase1 transcripts following pathogen infection. Starch mobilization in mycorrhizal plants seems coordinated with the increased transcription of sugar transporter and invertase genes. Moreover, the expression levels of genes encoding the vesicular trafficking proteins ATL31 and SYP121 and callose synthase PMR4 were higher in the mycorrhizal plants and further boosted by subsequent pathogen infection. All these proteins play a key role in the priming of callose accumulation in Arabidopsis, suggesting that callose priming is an induced resistance mechanism conserved in different plant species. This evidence highlights the importance of sugar mobilization and vesicular trafficking in the priming of callose as a defence mechanism in mycorrhiza-induced resistance.

In low nutritive environments, the uptake of N by arbuscular mycorrhizal (AM) fungi may confer competitive advantages for the host. The present study aims to understand how mycorrhizal tomato plants perceive and then prepare for an N depletion in the root environment. Plants colonized by Rhizophagus irregularis displayed improved responses to a lack of N than nonmycorrhizal (NM) plants. These responses were accomplished by a complex metabolic and transcriptional rearrangement that mostly affected the gibberellic acid and jasmonic acid pathways involving DELLA and JAZ1 genes, which were responsive to changes in the C/N imbalance of the plant. N starved mycorrhizal plants showed lower C/N equilibrium in the shoots than starved NM plants and concomitantly a downregulation of the JAZ1 repressor and the increased expression of the DELLA gene, which translated into a more active oxylipin pathway in mycorrhizal plants. In addition, the results support a priorization in AM plants of stress responses over growth. Therefore, these plants were better prepared for an expected stress. Furthermore, most metabolites that were severely reduced in NM plants following the N depletion remained unaltered in starved AM plants compared with those normally fertilized, suggesting that the symbiosis buffered the stress, improving plant development in a stressed environment.

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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.

Peptides are important regulators that participate in the modulation of almost every physiological event in plants, including defense. Recently, many of these peptides have been described as defense elicitors, termed phytocytokines, that are released upon pest or pathogen attack, triggering an amplification of plant defenses. However, little is known about peptides sensing and inducing resistance activities in heterologous plants. In the present study, exogenous peptides from solanaceous species, Systemins and HypSys, are sensed and induce resistance to the necrotrophic fungus Plectosphaerella cucumerina in the taxonomically distant species Arabidopsis thaliana. Surprisingly, other peptides from closer taxonomic clades have very little or no effect on plant protection. In vitro bioassays showed that the studied peptides do not have direct antifungal activities, suggesting that they protect the plant through the promotion of the plant immune system. Interestingly, tomato Systemin was able to induce resistance at very low concentrations (0.1 and 1 nM) and displays a maximum threshold being ineffective above at higher concentrations. Here, we show evidence of the possible involvement of the JA-signaling pathway in the Systemin-Induced Resistance (Sys-IR) in Arabidopsis. Additionally, Systemin treated plants display enhanced BAK1 and BIK1 gene expression following infection as well as increased production of ROS after PAMP treatment suggesting that Systemin sensitizes Arabidopsis perception to pathogens and PAMPs.

Indole-3-carboxylic acid (I3CA) is an indolic compound that induces resistance in Arabidopsis adult plants against the necrotrophic fungus Plectosphaerella cucumerina through primed callose accumulation. In this study, we confirm the relevance of ATL31 and SYP121 genes involved in vesicular trafficking in I3CA priming of defenses and we discard camalexin as a mediator of I3CA-induced resistance (IR) in adult plants. In addition, we observed that an intact I3CA biosynthetic pathway is necessary for I3CA-IR functionality.

The plant immunity system is being revisited more and more and new elements and roles are attributed to participating in the response to biotic stress. The new terminology is also applied in an attempt to identify different players in the whole scenario of immunity: Phytocytokines are one of those elements that are gaining more attention due to the characteristics of processing and perception, showing they are part of a big family of compounds that can amplify the immune response. This review aims to highlight the latest findings on the role of phytocytokines in the whole immune response to biotic stress, including basal and adaptive immunity, and expose the complexity of their action in plant perception and signaling events.

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