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Role and mechanisms of callose priming in mycorrhiza-induced resistance.

ABSTRACT: 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 ?-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.

SUBMITTER: Sanmartin N

PROVIDER: S-EPMC7210776 | biostudies-literature | 2020 May

REPOSITORIES: biostudies-literature

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Role and mechanisms of callose priming in mycorrhiza-induced resistance.

Sanmartín Neus N Pastor Victoria V Pastor-Fernández Julia J Flors Victor V Pozo Maria Jose MJ Sánchez-Bel Paloma P

Journal of experimental botany 20200501 9

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 ...[more]

PMID: 31985797

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Project description:Mycorrhizal plants are generally quite efficient in coping with environmental challenges. It has been shown that the symbiosis with arbuscular mycorrhizal fungi (AMF) can confer resistance against root and foliar pathogens, although the molecular mechanisms underlying such mycorrhiza-induced resistance (MIR) are poorly understood. Tomato plants colonized with the AMF Rhizophagus irregularis display enhanced resistance against the necrotrophic foliar pathogen Botrytis cinerea. Leaves from arbuscular mycorrhizal (AM) plants develop smaller necrotic lesions, mirrored also by a reduced levels of fungal biomass. A plethora of metabolic changes takes place in AMF colonized plants upon infection. Certain changes located in the oxylipin pathway indicate that several intermediaries are over-accumulated in the AM upon infection. AM plants react by accumulating higher levels of the vitamins folic acid and riboflavin, indolic derivatives and phenolic compounds such as ferulic acid and chlorogenic acid. Transcriptional analysis support the key role played by the LOX pathway in the shoots associated with MIR against B. cinerea. Interestingly, plants that have suffered a short period of nitrogen starvation appear to react by reprogramming their metabolic and genetic responses by prioritizing abiotic stress tolerance. Consequently, plants subjected to a transient nitrogen depletion become more susceptible to B. cinerea. Under these experimental conditions, MIR is severely affected although still functional. Many metabolic and transcriptional responses which are accumulated or activated by MIR such NRT2 transcript induction and OPDA and most Trp and indolic derivatives accumulation during MIR were repressed or reduced when tomato plants were depleted of N for 48 h prior infection. These results highlight the beneficial roles of AMF in crop protection by promoting induced resistance not only under optimal nutritional conditions but also buffering the susceptibility triggered by transient N depletion.

Project description:Arbuscular mycorrhizal fungi (AMF) is among the most ubiquitous plant mutualists that enhance plant growth and yield by facilitating the uptake of phosphorus and water. The countless interactions that occur in the rhizosphere between plants and its AMF symbionts are mediated through the plant and fungal metabolites that ensure partner recognition, colonization, and establishment of the symbiotic association. The colonization and establishment of AMF reprogram the metabolic pathways of plants, resulting in changes in the primary and secondary metabolites, which is the focus of this review. During initial colonization, plant-AMF interaction is facilitated through the regulation of signaling and carotenoid pathways. After the establishment, the AMF symbiotic association influences the primary metabolism of the plant, thus facilitating the sharing of photosynthates with the AMF. The carbon supply to AMF leads to the transport of a significant amount of sugars to the roots, and also alters the tricarboxylic acid cycle. Apart from the nutrient exchange, the AMF imparts abiotic stress tolerance in host plants by increasing the abundance of several primary metabolites. Although AMF initially suppresses the defense response of the host, it later primes the host for better defense against biotic and abiotic stresses by reprogramming the biosynthesis of secondary metabolites. Additionally, the influence of AMF on signaling pathways translates to enhanced phytochemical content through the upregulation of the phenylpropanoid pathway, which improves the quality of the plant products. These phytometabolome changes induced by plant-AMF interaction depends on the identity of both plant and AMF species, which could contribute to the differential outcome of this symbiotic association. A better understanding of the phytochemical landscape shaped by plant-AMF interactions would enable us to harness this symbiotic association to enhance plant performance, particularly under non-optimal growing conditions.

Dataset Information

Role and mechanisms of callose priming in mycorrhiza-induced resistance.

Publications

Role and mechanisms of callose priming in mycorrhiza-induced resistance.

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