Chitin and chitosan remodeling defines vegetative development and Trichoderma biocontrol

Abstract

Fungal parasitism depends on the ability to invade host organisms and mandates adaptive cell wall remodeling to avoid detection and defense reactions by the host. All plant and human pathogens share invasive strategies, which aid to escape the chitin-triggered and chitin-targeted host immune system. Here we describe the full spectrum of the chitin/chitosan-modifying enzymes in the mycoparasite Trichoderma atroviride with a central role in cell wall remodeling. Rapid adaption to a variety of growth conditions, environmental stresses and host defense mechanisms such as oxidative stress depend on the concerted interplay of these enzymes and, ultimately, are necessary for the success of the mycoparasitic attack. To our knowledge, we provide the first in class description of chitin and associated glycopolymer synthesis in a mycoparasite and demonstrate that they are essential for biocontrol. Eight chitin synthases, six chitin deacetylases, additional chitinolytic enzymes, including six chitosanases, transglycosylases as well as accessory proteins are involved in this intricately regulated process. Systematic and biochemical classification, phenotypic characterization and mycoparasitic confrontation assays emphasize the importance of chitin and chitosan assembly in vegetative development and biocontrol in T. atroviride. Our findings critically contribute to understanding the molecular mechanism of chitin synthesis in filamentous fungi and mycoparasites with the overarching goal to selectively exploit the discovered biocontrol strategies.

The GPI-Anchored GH76 Protein Dfg5 Affects Hyphal Morphology and Osmoregulation in the Mycoparasite Trichoderma atroviride and Is Interconnected With MAPK Signaling

“…Uneven distribution of cell wall components was also supported by CR staining ( Supplementary Figure 4 ). A similar chitin accumulation in patches at the lateral walls, together with reduced apical growth and isotropic tip swelling, has recently been described for T. atroviride chitin synthase mutants Δ chs5 and Δ chs7 ( Kappel et al, 2020 ).…”

“…Δ och-1 deletion mutants were hypothesized to exhibit a hyphal elongation disorder, which is similar to the phenotype of a Δ dcw1 , Δ dgf5 double mutant of N. crassa ( Maddi et al, 2012b ). Growth reduction and morphological changes including thinner hyphae have also been described for T. atroviride chitin synthase-deficient mutants such as Δ chs1 and Δ chs2 ( Kappel et al, 2020 ). Furthermore, the patchy chitin accumulation in the cell wall of T. atroviride Δ dfg5 mutants is similar to chitin synthase mutants Δ chs5 and Δ chs7 ( Kappel et al, 2020 ).…”

“…Growth reduction and morphological changes including thinner hyphae have also been described for T. atroviride chitin synthase-deficient mutants such as Δ chs1 and Δ chs2 ( Kappel et al, 2020 ). Furthermore, the patchy chitin accumulation in the cell wall of T. atroviride Δ dfg5 mutants is similar to chitin synthase mutants Δ chs5 and Δ chs7 ( Kappel et al, 2020 ). In in vitro antagonistic assays, T. atroviride WT and the dfg5 OE mutant were able to attack and completely overgrow the phytopathogen R. solani , whereas Δ dfg5 mutants had reduced antagonistic activity.…”

Chitosan and Chitin Deacetylase Activity Are Necessary for Development and Virulence of Ustilago maydis

“…Chitosan has been shown to decorate invasive hyphae of rust fungi, where it is considered to protect hyphae from attack by plant chitinases ( 21 ). CDA genes in plant-pathogenic fungi and fungi associated with plants usually exist in gene families ( 22 – 24 ), which has slowed down comprehensive analyses. Members with a GPI anchor are likely to act in concert with chitin synthases on nascent chitin chains.…”

Boosting photosynthetic machinery and defense priming with chitosan application on tomato plants infected withFusarium oxysporumf. sp.lycopersici

“…Chitosan is a linear polymer partially comprising deacetylated N-acetyl glucosamine (GlcNAc) subunits (Orzali et al, 2017;Goy et al, 2009). If more than 50% of the GlcNAc residues are deacetylated at position 2 the heteropolymer is referred to as chitosan (Kappel et al, 2020).…”