Tipping the Balance: Sclerotinia sclerotiorum Secreted Oxalic Acid Suppresses Host Defenses by Manipulating the Host Redox Environment

Abstract

Sclerotinia sclerotiorum is a necrotrophic ascomycete fungus with an extremely broad host range. This pathogen produces the non-specific phytotoxin and key pathogenicity factor, oxalic acid (OA). Our recent work indicated that this fungus and more specifically OA, can induce apoptotic-like programmed cell death (PCD) in plant hosts, this induction of PCD and disease requires generation of reactive oxygen species (ROS) in the host, a process triggered by fungal secreted OA. Conversely, during the initial stages of infection, OA also dampens the plant oxidative burst, an early host response generally associated with plant defense. This scenario presents a challenge regarding the mechanistic details of OA function; as OA both suppresses and induces host ROS during the compatible interaction. In the present study we generated transgenic plants expressing a redox-regulated GFP reporter. Results show that initially, Sclerotinia (via OA) generates a reducing environment in host cells that suppress host defense responses including the oxidative burst and callose deposition, akin to compatible biotrophic pathogens. Once infection is established however, this necrotroph induces the generation of plant ROS leading to PCD of host tissue, the result of which is of direct benefit to the pathogen. In contrast, a non-pathogenic OA-deficient mutant failed to alter host redox status. The mutant produced hypersensitive response-like features following host inoculation, including ROS induction, callose formation, restricted growth and cell death. These results indicate active recognition of the mutant and further point to suppression of defenses by the wild type necrotrophic fungus. Chemical reduction of host cells with dithiothreitol (DTT) or potassium oxalate (KOA) restored the ability of this mutant to cause disease. Thus, Sclerotinia uses a novel strategy involving regulation of host redox status to establish infection. These results address a long-standing issue involving the ability of OA to both inhibit and promote ROS to achieve pathogenic success.

Fungal negative-stranded RNA virus that is related to bornaviruses and nyaviruses

“…4F). This result suggests that the two strains can accumulate comparable amounts of oxalic acid, which is an essential pathogenicity determinant for S. sclerotiorum (35). Therefore, SsNSRV-1 is likely to affect other pathogenesis pathways rather than oxalic acid in S. sclerotiorum.…”

Reactive oxygen species and plant resistance to fungal pathogens

“…Paradoxically, OA can also induce ROS formation and attending plant cell death at a later stage of the infection that benefits a necrotrophic pathogen. A study by Williams et al (2011) nicely demonstrates how Sclerotinia mediates the redox environment in the host using real-time redox sensing by GFP, histological staining and reverse fungal genetics. At an early phase, Sclerotinia creates a reducing environment by secreting OA that prevents the ROS-induced localised defences.…”

The Arabidopsis Mediator Complex Subunit16 Is a Key Component of Basal Resistance against the Necrotrophic Fungal Pathogen Sclerotinia sclerotiorum

“…S. sclerotiorum depends on several virulence mechanisms to successfully attack the broad range of host plants. One mechanism is to produce the non-host-selective toxin oxalic acid, which inhibits plant defense responses, modulates host redox environment, suppresses autophagy, and activates cell wall-degrading enzymes (Marciano et al, 1983;Godoy et al, 1990;Cessna et al, 2000;Rollins and Dickman, 2001;Kim et al, 2008;Williams et al, 2011;Kabbage et al, 2013). Secretion of cell wall-degrading enzymes is another virulence mechanism of S. sclerotiorum, which facilitates penetration, tissue maceration, and plant cell wall depolymerization (Lumsden, 1979;Riou et al, 1991Riou et al, , 1992.…”