The fungal NADPH oxidase is an essential element for the molecular dialog between Trichoderma and Arabidopsis

Abstract

SUMMARY Members of the fungal genus Trichoderma stimulate growth and reinforce plant immunity. Nevertheless, how fungal signaling elements mediate the establishment of a successful Trichoderma−plant interaction is largely unknown. In this work, we analyzed growth, root architecture and defense in an Arabidopsis−Trichoderma co‐cultivation system, including the wild‐type (WT) strain of the fungus and mutants affected in NADPH oxidase. Global gene expression profiles were assessed in both the plant and the fungus during the establishment of the interaction. Trichoderma atroviride WT improved root branching and growth of seedling as previously reported. This effect diminished in co‐cultivation with the ∆nox1, ∆nox2 and ∆noxR null mutants. The data gathered of the Arabidopsis interaction with the ∆noxR strain showed that the seedlings had a heightened immune response linked to jasmonic acid in roots and shoots. In the fungus, we observed repression of genes involved in complex carbohydrate degradation in the presence of the plant before contact. However, in the absence of NoxR, such repression was lost, apparently due to a poor ability to adequately utilize simple carbon sources such as sucrose, a typical plant exudate. Our results unveiled the critical role played by the Trichoderma NoxR in the establishment of a fine‐tuned communication between the plant and the fungus even before physical contact. In this dialog, the fungus appears to respond to the plant by adjusting its metabolism, while in the plant, fungal perception determines a delicate growth−defense balance.

Plant recognition byTrichoderma harzianumelicits upregulation of a novel secondary metabolite cluster required for colonization

“…Considering the NADPH oxidase domain of PCA1, a relevance of an NADPH oxidase involved in ROS production for plant-fungus interaction was previously shown for T. atroviride [82]. For F. oxysporum , NADPH oxidase was found to be essential for chemotropic response to the presence of a plant [33].…”

Alteration of plant immunity in the interaction of roots with the endophytic fungus Phomopsis liquidambaris in response to external nitrogen conditions

“…liquidambaris ‐enhanced oxidative signals of rice are highly conditional upon particular environmental conditions, for example, the amount of soil N availability. Although plant oxidative signals are generally produced at the early stages after microbe infection (Jedelská et al, 2021; Villalobos‐Escobedo et al, 2020), these signals could also be induced in host plantlets at a later stage by fungal endophytes (Cui et al, 2017). In the present study, Ph.…”

Trichoderma atroviride‐emitted volatiles improve growth of Arabidopsis seedlings through modulation of sucrose transport and metabolism

“…atroviride has an intracellular invertase (Triat51014) and two putative sucrose transporters (Triat226844 and Triat83012) to be able to use plant‐derived carbon. Recently, Villalobos‐Escobedo et al (2020) demonstrated that T . atroviride represses its genes encoding enzymes involved in complex carbohydrate degradation prior to root colonization of Arabidopsis , suggesting that its saprophytic behaviour changes to acquire and use the simple sugars available in root exudates.…”

“…The genus Trichoderma includes opportunistic avirulent fungal species with a versatile lifestyle, which rely on plant‐derived sugars for fast growth and root colonization. They also thrive as decomposers of decaying plant residues or parasitize other fungi when nutrients are limiting (Ramírez‐Valdespino, Casas‐Flores, & Olmedo‐Monfil, 2019; Vargas, Crutcher, & Kenerley, 2011; Vargas, Mandawe, & Kenerley, 2009; Villalobos‐Escobedo et al, 2020). Upon root colonization, Trichoderma influences shoot performance through long distance, systemic signalling relying on oxylipins that strengthen photosynthesis, sugar homeostasis and exudation patterns (Coppola et al, 2019; Doni et al, 2019; Macías‐Rodríguez, Guzmán‐Gómez, García‐Juárez, & Contreras‐Cornejo, 2018; Wang, Borrego, Kenerley, & Kolomiets, 2020).…”