Comparative Secretome Analyses of Trichoderma/Arabidopsis Co-cultures Identify Proteins for Salt Stress, Plant Growth Promotion, and Root Colonization

Abstract

Numerous Trichoderma strains are beneficial for plants, promote their growth, and confer stress tolerance. A recently described novel Trichoderma strain strongly promotes the growth of Arabidopsis thaliana seedlings on media with 50 mM NaCl, while 150 mM NaCl strongly stimulated root colonization and induced salt-stress tolerance in the host without growth promotion. To understand the dynamics of plant-fungus interaction, we examined the secretome from both sides and revealed a substantial change under different salt regimes, and during co-cultivation. Stress-related proteins, such as a fungal cysteine-rich Kp4 domain-containing protein which inhibits plant cell growth, fungal WSC- and CFEM-domain-containing proteins, the plant calreticulin, and cell-wall modifying enzymes, disappear when the two symbionts are co-cultured under high salt concentrations. In contrast, the number of lytic polysaccharide monooxygenases increases, which indicates that the fungus degrades more plant lignocellulose under salt stress and its lifestyle becomes more saprophytic. Several plant proteins involved in plant and fungal cell wall modifications and root colonization are only found in the co-cultures under salt stress, while the number of plant antioxidant proteins decreased. We identified symbiosis- and salt concentration-specific proteins for both partners. The Arabidopsis PYK10 and a fungal prenylcysteine lyase are only found in the co-culture which promoted plant growth. The comparative analysis of the secretomes supports antioxidant enzyme assays and suggests that both partners profit from the interaction under salt stress but have to invest more in balancing the symbiosis. We discuss the role of the identified stage- and symbiosis-specific fungal and plant proteins for salt stress, and conditions promoting root colonization and plant growth.

Plant growth-promoting bacteria potentiate antifungal and plant-beneficial responses of Trichoderma atroviride by upregulating its effector functions

“…tritici [83], for example, and several CFEM domain-containing proteins were found in the secretome of Trichoderma spp. in cocultivation with A. thaliana [84]. In our previous work, we found that tacfem1 was upregulated when confronted with the phytopathogen R. solani anastomosis group AG5 during contact and overgrowth of the pathogen, but not when confronted with the anastomosis group AG2, and it was upregulated in the interaction with A. thaliana on days 5 th and 7 th days [23], however, there is little information on CFEM proteins from Trichoderma spp.…”

Impact of Seed Inoculation with Trichoderma afroharzianum Strains on Plant Growth, Root Morphology, and Leaf Phenolic Content in Hemp (Cannabis sativa L.) at Early Growth Stages

“…It can be hypothesized that the interaction of the two strains with the hemp plant, in terms of level of colonization, types of activated pathways and magnitude of the responses triggered in the host plant, may vary according to the environmental conditions. In this regard, evidence has been reported that plant exposure to salinity strongly increased the root colonization by Trichoderma strains and induced stress tolerance in Arabidopsis plants [37], and that seed inoculation with the T-22 strain in certain crops gave greater benefits under stress than under optimal growth conditions [38]. As for the mechanisms activated by the fungus, evidence exists that Trichoderma spp.…”

Molecular interaction between plants and Trichoderma species against soil-borne plant pathogens

“…In addition, under stressed conditions, WSC domain proteins, viz., FGB1 and WSC3, may be involved in b-glucan remodeling in the fungal cell wall (Wawra et al, 2019). A comparative secretome analysis of Trichoderma under salt stress conditions revealed that, in the presence of its plant host, the expression of WSC domain proteins in Trichoderma decreases, which may be indicative of the benefits derived by the fungus from its symbiont (i.e., the plant) through intensified root colonization (Rouina et al, 2022).…”