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

Jamil Samsatly,Suha H Jabaji,Tanya R Copley,Rita Grosch

doi:10.1371/journal.pone.0192682

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.

Highlights

The nectrotrophic fungus Rhizoctonia solani Kuhn is an economically devastating plant pathogen with a wide host range
S. cerevisiae strains defective in either snz1 or sno1 and unable to grow in media lacking vitamin B6 [31, 32]
We confirmed that R. solani AG3 PDX1 and PDX2 are functionally exchangeable with yeast SNZ1 and SNO1, respectively, and are involved in the de novo vitamin B6 biosynthesis via successful complementation of the S. cerevisiae null mutant Δsnz1 phenotype with RsolAG3-PDX1, and the null mutant Δsno1 with RsolAG3-PDX2

Summary

Introduction

The nectrotrophic fungus Rhizoctonia solani Kuhn (teleomorph Thanatephorus cucumeris, Frank, Donk) is an economically devastating plant pathogen with a wide host range. Isolates of the R. solani AG1-IA complex can infect aerial portions of the plant as in the case of soybean leaves causing rhizocotnia foliar blight (RFB) [3, 6, 7]. The common elements in disease development of R. solani isolates are the close association of fungal hyphae with the host epidermis forming branches known as infection cushions or aggregates, penetration of the epidermis, inter- and intracellular colonization and breakage of plant tissue by the production of hydrolytic enzymes, which eventually leads to the development of browning and necrosis associated with oxidative burst and death of tissue [4, 8]. Resistance to R. solani in any plant species does not exist

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