Distinct gene expression and secondary metabolite profiles in tomato mutants having impaired mycorrhizal colonization.

Arbuscular mycorrhizal fungi (AMF) colonization, sampled at 32-50 days post-inoculation (dpi), was significantly reduced in mutant tomato plants impaired in the ω-3 () gene that limits the generation of linolenic acid and, consequently, the wound-responsive jasmonic acid (JA) burst. Contrary to wild-type (WT) plants, JA levels in root and leaves of mutants remained unchanged in response to AMF colonization, further supporting its regulatory role in the AM symbiosis. Decreased AMF colonization in plants was also linked to alterations associated with a disrupted FAD7 function, such as enhanced salicylic acid (SA) levels and SA-related defense gene expression and a reduction in fatty acid content in both mycorrhizal roots and leaves. Transcriptomic data revealed that lower mycorrhizal colonization efficiency in mutants coincided with the modified expression of key genes controlling gibberellin and ethylene signaling, brassinosteroid, ethylene, apocarotenoid and phenylpropanoid synthesis, and the wound response. Targeted metabolomic analysis, performed at 45 dpi, revealed augmented contents of L-threonic acid and DL-malic acid in colonized roots which suggested unfavorable conditions for AMF colonization. Additionally, time- and genotype-dependent changes in root steroid glycoalkaloid levels, including tomatine, suggested that these metabolites might positively regulate the AM symbiosis in tomato. Untargeted metabolomic analysis demonstrated that the tomato root metabolomes were distinctly affected by genotype, mycorrhizal colonization and colonization time. In conclusion, reduced AMF colonization efficiency in mutants is probably caused by multiple and interconnected JA-dependent and independent gene expression and metabolomic alterations.