Antioxidant genes of plants and fungal pathogens are distinctly regulated during disease development in different Rhizoctonia solani pathosystems

Abstract

Biotic stress, as a result of plant-pathogen interactions, induces the accumulation of reactive oxygen species in the cells, causing severe oxidative damage to plants and pathogens. To overcome this damage, both the host and pathogen have developed antioxidant systems to quench excess ROS and keep ROS production and scavenging systems under control. Data on ROS-scavenging systems in the necrotrophic plant pathogen Rhizoctonia solani are just emerging. We formerly identified vitamin B6 biosynthetic machinery of R. solani AG3 as a powerful antioxidant exhibiting a high ability to quench ROS, similar to CATALASE (CAT) and GLUTATHIONE S-TRANSFERASE (GST). Here, we provide evidence on the involvement of R. solani vitamin B6 biosynthetic pathway genes; RsolPDX1 (KF620111.1), RsolPDX2 (KF620112.1), and RsolPLR (KJ395592.1) in vitamin B6 de novo biosynthesis by yeast complementation assays. Since gene expression studies focusing on oxidative stress responses of both the plant and the pathogen following R. solani infection are very limited, this study is the first coexpression analysis of genes encoding vitamin B6, CAT and GST in plant and fungal tissues of three pathosystems during interaction of different AG groups of R. solani with their respective hosts. The findings indicate that distinct expression patterns of fungal and host antioxidant genes were correlated in necrotic tissues and their surrounding areas in each of the three R. solani pathosystems: potato sprout-R. solani AG3; soybean hypocotyl-R. solani AG4 and soybean leaves-R. solani AG1-IA interactions. Levels of ROS increased in all types of potato and soybean tissues, and in fungal hyphae following infection of R. solani AGs as determined by non-fluorescence and fluorescence methods using H2DCF-DA and DAB, respectively. Overall, we demonstrate that the co-expression and accumulation of certain plant and pathogen ROS-antioxidant related genes in each pathosystem are highlighted and might be critical during disease development from the plant’s point of view, and in pathogenicity and developing of infection structures from the fungal point of view.

Vitamin B6 Is Under a Tight Balance During Disease Development by Rhizoctonia solani on Different Cultivars of Potato and on Arabidopsis thaliana Mutants

“…In a preceding research, we provided evidence that genes of vitamin B6 biosynthetic machinery are implicated as antioxidants in response to oxidative stress formed during potato-R. solani interaction and that VB6 genes are co-expressed in both the potato and R. solani during their interaction. We also provided evidence that the differential transcription of genes in infected necrotic tissues and their surrounding areas is spatially regulated (Samsatly et al, 2018). These results indicate that VB6 antioxidant genes are critical during disease development from the host's viewpoint, and are crucial for detoxification and pathogenicity from the pathogen's perspective.…”

“…ROS molecules are highly reactive and toxic to biological molecules, and are not only essential regulators of plant growth, but are involved in limiting pathogen spread, induction of cell death and signal transduction in host-plant interactions (Torres, 2010;Barna et al, 2012). There is also increasing evidence that fungi also produce ROS during pathogenic interactions (Daub and Ehrenshaft, 2000;Samsatly et al, 2018). Therefore, the regulation of ROS in fungal cells and tolerance to external ROS produced by the host plant represent a balanced control and detoxification by both partners which can govern the fate of disease progression of necrotrophic pathogens (Heller and Tudzynski, 2011).…”

Single‐marker and haplotype‐based association analysis of anthracnose (Colletotrichum dematium)resistance in spinach (Spinacia oleracea)

“…FAD synthase 2 is a chloroplastic protein known for its crucial role in defence signalling against oxidative stress (Sandoval et al, ). Similarly, antioxidant vitamin tocopherols, including α‐tocopherol, β‐tocopherol, γ‐tocopherol and δ‐tocopherol (Cheng et al, ; Porfirova, Bergmuller, Tropf, Lemke, & Dormann, ), have been ubiquitously identified in co‐expression analysis during fungal and plant–host interactions (Samsatly, Copley, & Jabaji, ). The strong signal associated with these antioxidant genes may suggest similar defence signalling in C. dematium and S. oleracea L. interactions.…”

Viruses Infecting the Plant Pathogenic Fungus Rhizoctonia solani

“…and Waitea spp.). Rhizoctonia solani Kühn (teleomorph: Thanatephorus cucumeris) is the most widely known species within the group of multinucleate Rhizoctonia and is classified into fourteen anastomosis groups (AGs) based on hyphal fusion experiments (Table 1) [2][3][4][5][6]. R. solani is a soil-borne plant pathogen with widespread geographical distribution and a wide host range, known to cause various important crop diseases, leading to significant agricultural and economic losses.…”