The Apoplastic Secretome of Trichoderma virens During Interaction With Maize Roots Shows an Inhibition of Plant Defence and Scavenging Oxidative Stress Secreted Proteins

Abstract

In Nature, almost every plant is colonized by fungi. Trichoderma virens is a biocontrol fungus which has the capacity to behave as an opportunistic plant endophyte. Even though many plants are colonized by this symbiont, the exact mechanisms by which Trichoderma masks its entrance into its plant host remain unknown, but likely involve the secretion of different families of proteins into the apoplast that may play crucial roles in the suppression of plant immune responses. In this study, we investigated T. virens colonization of maize roots under hydroponic conditions, evidencing inter- and intracellular colonization by the fungus and modifications in root morphology and coloration. Moreover, we show that upon host penetration, T. virens secretes into the apoplast an arsenal of proteins to facilitate inter- and intracellular colonization of maize root tissues. Using a gel-free shotgun proteomics approach, 95 and 43 secretory proteins were identified from maize and T. virens, respectively. A reduction in the maize secretome (36%) was induced by T. virens, including two major groups, glycosyl hydrolases and peroxidases. Furthermore, T. virens secreted proteins were mainly involved in cell wall hydrolysis, scavenging of reactive oxygen species and secondary metabolism, as well as putative effector-like proteins. Levels of peroxidase activity were reduced in the inoculated roots, suggesting a strategy used by T. virens to manipulate host immune responses. The results provide an insight into the crosstalk in the apoplast which is essential to maintain the T. virens-plant interaction.

The Multiple Facets of Plant–Fungal Interactions Revealed Through Plant and Fungal Secretomics

“…A recent study on the interaction of T. virens with maize roots (Nogueira-Lopez et al, 2018) has identified 95 secretory proteins of maize using a gel-free shotgun proteomics approach. In this study, maize secretome was found to be reduced by 36% upon colonization with T. virens (Nogueira-Lopez et al, 2018). Seven secreted Uaca_Ns effectors from the bean rust pathogen Uromyces appendiculatus were shown to suppress plant host innate immunity, by either dampening pathgogen-triggered immunity or preventing hypersensitive response (Qi et al, 2019).…”

“…For example, Meijer and colleagues have recovered, through mass spectrometry, proteins lacking obvious SP when analyzing proteins exported by P. infestans in different growth media (Meijer et al, 2014). Similarly, Nogueira-Lopez and colleagues have found evidence for non-conventional secretion mechanisms when analyzing the secretomes of T. virens on its own and within infected maize cells (Nogueira-Lopez et al, 2018).…”

Endophytic fungi as biocontrol agents: elucidating mechanisms in disease suppression

“…Enzymes secreted during the infection and colonisation process, such as xylanases, cellulases and chitinases, can be recognised by the host directly or through their degradation products and induce defence responses (Rotblat et al 2002;Belien et al 2006;Druzhinina et al 2011). Fungal effectors, often small cysteine-rich proteins, are secreted during both pathogenic and endophytic colonisation processes to promote compatibility with the host plant, by modulating defence responses and physiology (Bent and Mackey 2007;Rafiqi et al 2013;Hacquard et al 2016;Nogueira-Lopez et al 2018). These small proteins can also induce plant responses when recognised by the host (Djonovic et al 2007;Salas-Marina et al 2015).…”

Plant–Microbe Symbiosis: What Has Proteomics Taught Us?

“…Several studies supported the functions of SSPs as negative regulators of plant defense, which may be essential for maintaining the state of symbiosis. Nogueira‐Lopez et al . provided an insight into the apoplastic proteins from maize root tissues in order to dissect the crosstalk between the host and T. virens in the apoplastic region using shotgun proteomics .…”

“…Nogueira‐Lopez et al . provided an insight into the apoplastic proteins from maize root tissues in order to dissect the crosstalk between the host and T. virens in the apoplastic region using shotgun proteomics . As a result, 95 and 43 putative secreted proteins were identified from maize and T. virens , respectively.…”