Mechanisms of Broad Host Range Necrotrophic Pathogenesis in Sclerotinia sclerotiorum

Abstract

Among necrotrophic fungi, Sclerotinia sclerotiorum is remarkable for its extremely broad host range and for its aggressive host tissue colonization. With full genome sequencing, transcriptomic analyses and the increasing pace of functional gene characterization, the factors underlying the basis of this broad host range necrotrophic pathogenesis are now being elucidated at a greater pace. Among these, genes have been characterized that are required for infection via compound appressoria in addition to genes associated with colonization that regulate oxalic acid (OA) production and OA catabolism. Moreover, virulence-related secretory proteins have been identified, among which are candidates for manipulating host activities apoplastically and cytoplasmically. Coupled with these mechanistic studies, cytological observations of the colonization process have blurred the heretofore clear-cut biotroph versus necrotroph boundary. In this review, we reexamine the cytology of S. sclerotiorum infection and put more recent molecular and genomic data into the context of this cytology. We propose a two-phase infection model in which the pathogen first evades, counteracts and subverts host basal defense reactions prior to killing and degrading host cells. Spatially, the pathogen may achieve this via the production of compatibility factors/effectors in compound appressoria, bulbous subcuticular hyphae, and primary invasive hyphae. By examining the nuances of this interaction, we hope to illuminate new classes of factors as targets to improve our understanding of broad host range necrotrophic pathogens and provide the basis for understanding corresponding host resistance.

Transcriptome analysis of the plant pathogen Sclerotinia sclerotiorum interaction with resistant and susceptible canola (Brassica napus) lines

“…In contrast to the widely accepted necrotrophic nature of S. sclerotiorum, recent molecular and cytological evidences suggest a two-phase model involving a brief biotrophic or basic compatibility phase characterized by host suppression and subverting of host defenses following by necrotrophic phase [38]. The temporal differential expression patterns of the effector candidates in our study supports the two-phase infection model [38][39][40] proposed for S. sclerotiorum. Biotrophic effectors like chorismate mutase (SsCm1), chitin binding proteins, LysM, and genes involved in ROS and RNS scavenging are up-regulated at early infection phase.…”

“…In contrast to the widely accepted necrotrophic nature of the pathogen [1], a two-phase infection model involving a brief biotrophic or basic compatibility phase characterized by host resistance suppression and subverting of host defenses followed by a necrotrophic phase was proposed based on cytological and molecular and genomic evidences [38][39][40]. This brief initial phase appears to be partly facilitated by oxalic acid (OA) and by secreted effectors, which help S. sclerotiorum evade host recognition and suppress host defense signaling pathways [23,24,39].…”

Sclerotinia sclerotiorumhijacks copper from its host for infection

“…ROS is associated with the formation of infection cushions and production of oxalic acid in S. sclerotiorum (Liberti et al , 2013; Veluchamy et al , 2012; Kim et al , 2011). Infection cushions are essential for the S. sclerotiorum to penetrate the host cuticle and infect plants (Liang and Rollins, 2018), and oxalic acid (OA) is one of the virulence factors of S. sclerotiorum (Li et al , 2018; Liang and Rollins, 2018). Therefore, we monitored the infection cushions and OA production among the wild-type, silenced and overexpressing strains on B. napus leaves.…”

The Notorious Soilborne Pathogenic Fungus Sclerotinia sclerotiorum: An Update on Genes Studied with Mutant Analysis

“…Much has been unveiled for the pathogen growth, development, and differentiation signaling pathways. Accordingly, more evidence is supporting the two-phase infection model, where the pathogen suppresses host basal defense prior to killing and degrading host cells [11]. In the short biotrophic phase, the pathogen uses well-orchestrated strategies to overcome host immunity.…”

“…It is therefore not surprising that it causes significant economic losses globally every year [13]. For example, in China, oilseed rape yield losses that are caused by SSR (Sclerotinia stem rot) usually S. sclerotiorum has an extremely broad host range, which consists of more than 600 plant species, including almost all dicotyledonous and some monocotyledonous plants [10,11]. It can infect many economically important crops, such as canola; legumes such as soybean and peanut; sunflower; various vegetables such as lettuce and tomato; and monocotyledonous plants such as tulip and onion [10,12].…”