Identification of miRNAs Involved in Maize-Induced Systemic Resistance Primed by Trichoderma harzianum T28 against Cochliobolus heterostrophus

Abstract

microRNAs (miRNAs) are known to play important roles in the immune response to pathogen infection in different plants. Further, Trichoderma strains are able to activate plant defense responses against pathogen attacks. However, little is known about the involvement of miRNAs in the defense response primed by Trichoderma strains. To explore the miRNAs sensitive to priming by Trichoderma, we studied the small RNAs and transcriptome changes in maize leaves that were systemically induced by seed treatment with Trichoderma harzianum (strain T28) against Cochliobolus heterostrophus (C. heterostrophus) infection in leaves. Through analysis of the sequencing data, 38 differentially expressed miRNAs (DEMs) and 824 differentially expressed genes (DEGs) were identified. GO and KEGG analyses of DEGs demonstrated that genes involved in the plant hormone signal transduction pathway and oxidation-reduction process were significantly enriched. In addition, 15 miRNA–mRNA interaction pairs were identified through the combined analysis of DEMs and DEGs. These pairs were supposed to play roles in the maize resistance primed by T. harzianum T28 to C. heterostrophus, in which miR390, miR169j, miR408b, miR395a/p, and novel miRNA (miRn5231) were more involved in the induction of maize resistance. This study provided valuable information for understanding the regulatory role of miRNA in the T. harzianum primed defense response.

Identification of Tomato microRNAs in Late Response to Trichoderma atroviride

“…However, under the sRNAs, a plethora of diverse RNA molecules 20-30 nt long that have emerged as major regulators in plants still have little-known roles in plant-Trichoderma interaction. In recent years, miRNAs from Trichoderma-treated plants have begun to be cataloged [35,37,46], although more research is still needed to understand this interaction and the role of the third layer…”

“…However, under the sRNAs, a plethora of diverse RNA molecules 20-30 nt long that have emerged as major regulators in plants still have little-known roles in plant-Trichoderma interaction. In recent years, miRNAs from Trichoderma-treated plants have begun to be cataloged [35,37,46], although more research is still needed to understand this interaction and the role of the third layer of plant immunity in Trichoderma-induced priming. In this study, we aimed to explore the miRNAs in tomato plants for a long time (30 days) after inoculation with T. atroviride, when the phytohormonal signaling of the plant defenses is quiescent [47] and the plant is in a state of transcriptional memory [1].…”

“…Thus, we have performed RNA sequencing with three biological replicas of tomato-leaf samples from untreated plants and plants from seeds coated with T. atroviride T11. Previous works have analyzed the expression profiles of miRNAs in plants at very short times after Trichoderma application [35,37], while we have wanted to explore which miRNAs related to plant defense are differentially expressed when priming is dormant and only a few genes are differentially transcribed in Trichoderma-treated plants compared to the control [40] and at a transcriptional memory state. Thus, we have performed RNA sequencing with three biological replicas of 30-day-old tomato-leaf samples from untreated plants and plants from seeds coated with T. atroviride T11.…”

“…Root and leaf proteomes of Trichoderma-treated plants have shown an overrepresentation of NLR-like proteins [32,33], and NLR genes have also been reported to be upregulated in such an interaction [34]. So, the third layer of immunity gives sRNAs a central role in this task, as recently described in the expression of miRNAs in Arabidopsis, with wheat and maize leaves of Trichoderma-treated plants linked to the induction of systemic defense [35][36][37]. The priming effect activated by Trichoderma in the plant is durable and effective in adapting to pathogen life cycles [38,39], but the Trichoderma-triggered phytohormone-signaling network alert disappears over time, becoming imperceptible several weeks after the plant has been in contact with the fungus, to save energy when not needed [40].…”

Epigenetic weapons of plants against fungal pathogens

“…Analysis of the sequencing data showed that genes involved in the plant hormone signal transduction pathway and the oxidation-reduction process were significantly enriched. In addition, 15 pairs of miRNA-mRNA interactions that played a role in T. harzianum -induced maize resistance to C. heterostrophus were identified; miR390, miR169j, miR408b, miR395a/p and the novel miRNA miRn5231 were most involved in the induction of maize resistance [ 176 ].…”