Proteinaceous effector discovery and characterization in filamentous plant pathogens

Abstract

The complicated interplay of plant–pathogen interactions occurs on multiple levels as pathogens evolve to constantly evade the immune responses of their hosts. Many economically important crops fall victim to filamentous pathogens that produce small proteins called effectors to manipulate the host and aid infection/colonization. Understanding the effector repertoires of pathogens is facilitating an increased understanding of the molecular mechanisms underlying virulence as well as guiding the development of disease control strategies. The purpose of this review is to give a chronological perspective on the evolution of the methodologies used in effector discovery from physical isolation and in silico predictions, to functional characterization of the effectors of filamentous plant pathogens and identification of their host targets.

Turning Inside Out: Filamentous Fungal Secretion and Its Applications in Biotechnology, Agriculture, and the Clinic

“…Disease causing fungi secrete an arsenal of proteins, acids, and secondary metabolites which can initiate infection, perturb or disrupt host immune responses, cause tissue death, and acquire nutrients from the host (see Section 3 and Section 4 ), among numerous other functions. Proteins which facilitate infection are secreted via the classical pathway [ 24 , 25 ], in EVs [ 87 ], via unconventional routes [ 26 ], and, in some plant infecting fungi, via a newly discovered host derived structure termed the biotrophic interface complex (see [ 24 ]). Secretion routes for the diverse repertoire of secondary metabolites during infection are less comprehensively understood, but presumably include secretion by plasma membrane transporters (e.g., siderophores [ 28 ]), EVs [ 88 ], and possibly the vesicle based route (recently reviewed in [ 29 ]).…”

“…More recently, the role of secreted polyunsaturated fatty acids (PUFAs) during infection has gained attention in mediating both plant and mammalian infection (reviewed in [ 135 ]). While the precise roles of extracellular fungal molecules during host–pathogen interactions and disease are extremely diverse and multifaceted (reviewed in [ 25 , 26 , 29 , 135 , 136 ]), some broad aspects are summarized here, and their applications discussed in the subsequent section.…”

“…Similar functions of secreted LysM proteins have recently been confirmed during fungal infection of insects [ 140 ]. These proteins are part of the extremely diverse fungal ‘effector’ arsenal, whereby many small molecular weight proteins are secreted to manipulate and attack the host (recently reviewed in [ 25 ]).…”

Genomic Approaches to Identify Molecular Bases of Crop Resistance to Diseases and to Develop Future Breeding Strategies

“…Among “omics” technologies that have provided new insights into the understanding and managing of pathogenesis, effectoromics is a novel approach that allows the identification of candidate pathogen effectors ( Avr ) and their use as functional markers to define corresponding host resistance (R) and susceptibility (S) genes. A review has been recently released on the evolution of methods used in effector discovery, from physical isolation and in silico predictions to functional characterization of the effectors of plant pathogens and identification of their host targets [ 145 ]. Few examples are so far reported in the literature on crops.…”

Transcription factor control of virulence in phytopathogenic fungi

“…Nevertheless, most fungi are nonpathogenic and most plants are resistant to all but a few species, begging the question, what is it that allows a disease to develop? Recent advances have shed light on various aspects of fungal virulence by highlighting the role of microbial effector-host receptor interactions (Han & Kahmann, 2019;Kanja & Hammond-Kosack, 2020;de Wit et al, 2017), secondary metabolite (SM) biosynthesis (Chooi et al, 2014;Collemare et al, 2019;Macheleidt et al, 2016), signal transduction/ cellular metabolism (Bielska et al, 2014;Ikeda et al, 2019), cellular trafficking/secretion systems (Le Marquer et al, 2019;Park et al, 2018;Rascle et al, 2018), and the channelling of noncoding RNAs (Cai et al, 2019;Hua et al, 2018;Sesma, 2016). However, a universal strategy does not appear to exist.…”