Arbuscular Mycorrhizal Symbiosis Leads to Differential Regulation of Genes and miRNAs Associated with the Cell Wall in Tomato Leaves

SIMPLE SUMMARY: Tomato can interact with arbuscular mycorrhizal fungi (AMF) to form a symbiotic association called arbuscular mycorrhiza. This symbiosis, in addition to providing nutritional benefits to plants, induces a plant defense response against biotic and abiotic stresses locally in the roots, and systemically throughout the entire plant. However, the mechanisms underlying these conferred systemic resistance-induced responses are largely unknown. This work aimed to identify which regulatory molecules could be involved in the response mechanisms elicited during priming. The findings presented here provide valuable information on the molecules that could participate in these responses, with the aim of elucidating the whole mechanism. ABSTRACT: Arbuscular mycorrhizal symbiosis is an association that provides nutritional benefits to plants. Importantly, it induces a physiological state allowing plants to respond to a subsequent pathogen attack in a more rapid and intense manner. Consequently, mycorrhiza-colonized plants become less susceptible to root and shoot pathogens. This study aimed to identify some of the molecular players and potential mechanisms related to the onset of defense priming by mycorrhiza colonization, as well as miRNAs that may act as regulators of priming genes. The upregulation of cellulose synthases, pectinesterase inhibitors, and xyloglucan endotransglucosylase/hydrolase, as well as the downregulation of a pectinesterase, suggest that the modification and reinforcement of the cell wall may prime the leaves of mycorrhizal plants to react faster and stronger to subsequent pathogen attack. This was confirmed by the findings of miR164a-3p, miR164a-5p, miR171e-5p, and miR397, which target genes and are also related to the biosynthesis or modification of cell wall components. Our findings support the hypothesis that the reinforcement or remodeling of the cell wall and cuticle could participate in the priming mechanism triggered by mycorrhiza colonization, by strengthening the first physical barriers upstream of the pathogen encounter.