Transcriptome and Metabolome Reprogramming in Tomato Plants by Trichoderma harzianum strain T22 Primes and Enhances Defense Responses Against Aphids

Abstract

Beneficial fungi in the genus Trichoderma are among the most widespread biocontrol agents of plant pathogens. Their role in triggering plant defenses against pathogens has been intensely investigated, while, in contrast, very limited information is available on induced barriers active against insects. The growing experimental evidence on this latter topic looks promising, and paves the way toward the development of Trichoderma strains and/or consortia active against multiple targets. However, the predictability and reproducibility of the effects that these beneficial fungi is still somewhat limited by the lack of an in-depth understanding of the molecular mechanisms underlying the specificity of their interaction with different crop varieties, and on how the environmental factors modulate this interaction. To fill this research gap, here we studied the transcriptome changes in tomato plants (cultivar “Dwarf San Marzano”) induced by Trichoderma harzianum (strain T22) colonization and subsequent infestation by the aphid Macrosiphum euphorbiae . A wide transcriptome reprogramming, related to metabolic processes, regulation of gene expression and defense responses, was induced both by separate experimental treatments, which showed a synergistic interaction when concurrently applied. The most evident expression changes of defense genes were associated with the multitrophic interaction Trichoderma -tomato-aphid. Early and late genes involved in direct defense against insects were induced (i.e., peroxidase, GST, kinases and polyphenol oxidase, miraculin, chitinase ), along with indirect defense genes, such as sesquiterpene synthase and geranylgeranyl phosphate synthase . Targeted and untargeted semi-polar metabolome analysis revealed a wide metabolome alteration showing an increased accumulation of isoprenoids in Trichoderma treated plants. The wide array of transcriptomic and metabolomics changes nicely fit with the higher mortality of aphids when feeding on Trichoderma treated plants, herein reported, and with the previously observed attractiveness of these latter toward the aphid parasitoid Aphidius ervi . Moreover, Trichoderma treated plants showed the over-expression of transcripts coding for several families of defense-related transcription factors (bZIP, MYB, NAC, AP2-ERF, WRKY), suggesting that the fungus contributes to the priming of plant responses against pest insects. Collectively, our data indicate that Trichoderma treatment of tomato plants induces transcriptomic and metabolomic changes, which underpin both direct and indirect defense responses.

Trichoderma atroviride P1 Colonization of Tomato Plants Enhances Both Direct and Indirect Defense Barriers Against Insects

“…One of the peculiar aspects of Trichoderma –tomato interaction is the positive effect exerted by the fungus on TFs regulating defense gene expression (Segarra et al, 2009; Pieterse et al, 2014; Conrath et al, 2015; Rubio et al, 2017). In our data, genes coding for several families of defense-related TFs (i.e., ERF, WRKY, MYB, and bZIP) are all up-regulated, similarly to what was observed following the interaction of tomato plants with T. harzianum T22 (Coppola et al, 2019, this issue). These TFs are involved in innate immunity.…”

“…To date, only limited studies have determined the insect control activity by plants exposed to Trichoderma colonization. Namely, the available information is limited to aphids (Coppola et al, 2019), thrips (Muvea et al, 2014), and caterpillars (Contreras-Cornejo et al, 2018). Battaglia et al (2013) registered a growth-stimulation effect of Trichoderma longibrachiatum MK1 treatments, both on tomato plants and on aphids feeding on them.…”

Comparative transcriptomic and metabolic analysis of wild and domesticated wheat genotypes reveals differences in chemical and physical defense responses against aphids

“…Integration between transcriptomic and metabolic datasets is commonly used to expose how insects may modify their host plant to their advantage [32,33]. In this research, we investigated the differences in the transcriptome and metabolome of wheat seedlings, and we studied the effect on the chemical and physical defenses against Rhopalosiphum padi aphids.…”

Appraisal of Combined Applications of Trichoderma virens and a Biopolymer-Based Biostimulant on Lettuce Agronomical, Physiological, and Qualitative Properties under Variable N Regimes

“…These include the fungi metabolites, proven to have auxin and ethylene-like activity, that induce a reorganization of gene expression patterns in shoots and roots with significant changes in the plant metabolic machinery and a consequent improvement in plant resilience and yield [26,[40][41][42]. These released compounds specifically modify plant root architecture, increasing root length, density and branching, and nutrient uptake (P, Fe, Mn, and Zn), in addition to acting as mediators in the plant microbiome for communication, warning signals, and pest management [25][26][27]43,44]. Recently, experiments conducted by Fiorentino and co-workers [25] on lettuce and rocket, grown under three different N fertilization rates and inoculated with two Trichoderma strains, demonstrated that, in particular, one strain of T. virens G41 (ex-Gliocladium virens GV41) was able to enhance NUE in lettuce, also favoring the uptake of native N present in the soil.…”