Abstract
Trichoderma atroviride is a mycoparasitic fungus used as biological control agent against fungal plant pathogens. The recognition and appropriate morphogenetic responses to prey-derived signals are essential for successful mycoparasitism. We established microcolony confrontation assays using T. atroviride strains expressing cell division cycle 42 (Cdc42) and Ras-related C3 botulinum toxin substrate 1 (Rac1) interactive binding (CRIB) reporters to analyse morphogenetic changes and the dynamic displacement of localized GTPase activity during polarized tip growth. Microscopic analyses showed that Trichoderma experiences significant polarity stress when approaching its fungal preys. The perception of prey-derived signals is integrated via the guanosine triphosphatase (GTPase) and mitogen-activated protein kinase (MAPK) signalling network, and deletion of the MAP kinases Trichoderma MAPK 1 (Tmk1) and Tmk3 affected T. atroviride tip polarization, chemotropic growth, and contact-induced morphogenesis so severely that the establishment of mycoparasitism was highly inefficient to impossible. The responses varied depending on the prey species and the interaction stage, reflecting the high selectivity of the signalling process. Our data suggest that Tmk3 affects the polarity-stress adaptation process especially during the pre-contact phase, whereas Tmk1 regulates contact-induced morphogenesis at the early-contact phase. Neither Tmk1 nor Tmk3 loss-of-function could be fully compensated within the GTPase/MAPK signalling network underscoring the crucial importance of a sensitive polarized tip growth apparatus for successful mycoparasitism.
Highlights
With the aim to better understand the underlying guanosine triphosphatase (GTPase) and mitogen-activated protein kinase (MAPK)/stress-activated protein kinase (SAPK) signalling pathways that may trigger virulence-related morphogenetic changes of individual hyphae, we aimed to address the following key questions: (1) do CRIB reporters label apical GTPase activity clusters in Trichoderma during hyphal tip growth including chemotropism, (2) do CRIB reporters facilitate the quantification of morphogenetic changes in individual hyphae of Trichoderma during mycoparasitic confrontations, and (3) does the analysis of MAPK
The plant pathogens Botrytis cinerea B05.10, B. cinerea B05.10 dsRed strain [43], Fusarium oxysporum f. sp. lycopersici strain 4287, and Rhizopus microsporus were used as prey fungi
Live-cell imaging confirmed that the CRIB reporter accumulated in the expected crescent shape in 2D in all actively growing tip apices, with the Spitzenkörper standing out at its central subapical position (Figure 1)
Summary
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. Several species of the filamentous fungal genus Trichoderma are facultative plant symbionts in parallel to being highly effective mycoparasites against devastating fungal plant pathogens. T. atroviride is widely used as a general plant growth promoter and biological control agent in modern agriculture [1]. Direct mycoparasitism of phytopathogenic prey fungi is one important feature of biocontrol. The mycoparasitic interaction is characterized by several steps including prey sensing, directional chemotropic approach, pre-contact chemical attack, and direct physical interaction between mycoparasite and prey hyphae. On the other hand, have the potential to counteract mycoparasitic attack with highly effective defence responses [2,3]
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