Arbuscular mycorrhizal fungi (AMF) colonization, sampled at 32-50 days post-inoculation (dpi), was significantly reduced in suppressor of prosysteminmediated responses2 (spr2) mutant tomato plants impaired in the ω−3 FATTY ACID DESATURASE7 (FAD7) 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 spr2 mutants remained unchanged in response to AMF colonization, further supporting its regulatory role in the AM symbiosis. Decreased AMF colonization in spr2 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 spr2 roots and leaves. Transcriptomic data revealed that lower mycorrhizal colonization efficiency in spr2 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 spr2 roots which suggested unfavorable conditions for AMF colonization. Additionally, timeand 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 spr2 mutants is probably caused by multiple and interconnected JA-dependent and independent gene expression and metabolomic alterations.How to cite this article Casarrubias-Castillo K, Montero-Vargas JM, Dabdoub-González N, Winkler R, Martinez-Gallardo NA, Zañudo-Hernández J, Avilés-Arnaut H, Délano-Frier JP. 2020. Distinct gene expression and secondary metabolite profiles in suppressor of prosystemin-mediated responses2 (spr2) tomato mutants having impaired mycorrhizal colonization. PeerJ 8:e8888 . 2012. Loss of function of fatty acid desaturase 7 in tomato enhances basal aphid resistance in a salicylate-dependent manner.

A previous study with spr2 mutant tomato plants which are negatively affected in the synthesis of jasmonic acid (JA), suggested that JA regulates the arbuscular mycorrhizal fungi (AMF) colonization via the control of carbon (C) partitioning. Although this and other studies have suggested the important positive role played by JA in the regulation of AMF root colonization in tomato plants, it is currently unclear how different host plant genetic backgrounds affect gene expression and secondary metabolites variation during JA-dependent mycorrhization. In this study, wild type and spr2 mutant tomato plants having “low”, “medium” and “high” mycorrhizal colonization with Rhizophagus irregularis, were analyzed independently using transcriptomic and untargeted metabolomic approaches. The results obtained revealed that the degree of mycorrhizal colonization efficiency could be associated with contrasting expression levels of certain key genes controlling gibberellin signaling, ethylene biosynthesis and signaling, and synthesis of apocarotenoids, phenylpropanoids and tomatine, in roots. Only a few wound responsive genes, including JA signaling and biosynthesis genes, such as Prosystemin and JAZ2 were found to influence AMF colonization. Conversely, a systemic and JA-dependent induction/ repression of genes different from those altered in roots was detected in leaves of mycorrhizal plants. The most significant changes in metabolite abundance were detected in roots with reduced AMF colonization. Included among the latter were metabolites known to be associated with important aspects of AMF symbiosis, such as signaling, nutrient exchange and modulation of pathogen defense response. Αlpha-tomatine levels appeared to be an important factor, whose abundance negatively correlated wit h AMF colonization levels in tomato, suggesting a regulatory role for JA in the synthesis of this metabolite during the AMF symbiosis.

A previous study with spr2 mutant tomato plants which are negatively affected in the synthesis of jasmonic acid (JA), suggested that JA regulates the arbuscular mycorrhizal fungi (AMF) colonization via the control of carbon (C) partitioning. Although this and other studies have suggested the important positive role played by JA in the regulation of AMF root colonization in tomato plants, it is currently unclear how different host plant genetic backgrounds affect gene expression and secondary metabolites variation during JA-dependent mycorrhization. In this study, wild type and spr2 mutant tomato plants having “low”, “medium” and “high” mycorrhizal colonization with Rhizophagus irregularis, were analyzed independently using transcriptomic and untargeted metabolomic approaches. The results obtained revealed that the degree of mycorrhizal colonization efficiency could be associated with contrasting expression levels of certain key genes controlling gibberellin signaling, ethylene biosynthesis and signaling, and synthesis of apocarotenoids, phenylpropanoids and tomatine, in roots. Only a few wound responsive genes, including JA signaling and biosynthesis genes, such as Prosystemin and JAZ2 were found to influence AMF colonization. Conversely, a systemic and JA-dependent induction/ repression of genes different from those altered in roots was detected in leaves of mycorrhizal plants. The most significant changes in metabolite abundance were detected in roots with reduced AMF colonization. Included among the latter were metabolites known to be associated with important aspects of AMF symbiosis, such as signaling, nutrient exchange and modulation of pathogen defense response. Αlpha-tomatine levels appeared to be an important factor, whose abundance negatively correlated wit h AMF colonization levels in tomato, suggesting a regulatory role for JA in the synthesis of this metabolite during the AMF symbiosis.