Distinct gene expression and secondary metabolite profiles in suppressor of prosystemin-mediated responses2 (spr2) tomato mutants having impaired mycorrhizal colonization

PeerJ. 2020 Apr 16:8:e8888. doi: 10.7717/peerj.8888. eCollection 2020.

Abstract

Arbuscular mycorrhizal fungi (AMF) colonization, sampled at 32-50 days post-inoculation (dpi), was significantly reduced in suppressor of prosystemin-mediated 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, 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 spr2 mutants is probably caused by multiple and interconnected JA-dependent and independent gene expression and metabolomic alterations.

Keywords: Arbuscular mycorrhizal colonization; Ethylene; Fatty acid desaturase; Gibberellins; Jasmonic acid; Salicylic acid; Tomatine.

Grants and funding

Nicole Dabdoub-González (No. 191369), Josaphat Miguel Montero-Vargas (No. 191369) and Kena Casarrubias-Castillo (No. 227935) were supported by postgraduate scholarships granted by The National Council of Science and Technology (Conacyt, México). Hamlet Avilés-Arnaut was supported by a Basic Science grant conceded by Conacyt (No. 239695). The laboratory for biochemical and instrumental analysis (Robert Winkler) was funded by the CONACyT Fronteras project 2015-2/814 and the bilateral grant Conacyt-DFG 2016/277850. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.