Absence of Cu–Zn superoxide dismutase BCSOD1 reduces Botrytiscinerea virulence in Arabidopsis and tomato plants, revealinginterplay among reactive oxygen species, callose and signallingpathways

Abstract

Plants activate responses against pathogens, including the oxida-tive burst. Necrotrophic pathogens can produce reactive oxygenspecies (ROS) that benefit the colonization process. Previously, wehave demonstrated that tomato plants challenged with Botrytiscinerea accumulate ROS and callose, together with the inductionof genes involved in defence, signalling and oxidative metabolism.Here, we studied the infection phenotype of the Dbcs od1 strain inboth tomato and Arabidopsis plants. This mutant lacks bcsod1,which encodes Cu–Zn superoxide dismutase (SOD). This enzymecatalyses the conversion of superoxide ion (O–2) into hydrogen per-oxide (H2O2). ROS play a protective role and act as signals inplants. Dbcsod1 displayed reduced virulence compared with wild-type B05.10 in both species. Plants infected with Dbcsod1 accu-mulated less H2O2and more O–2than those infected with B05.10,which is associated with an increase in the defensive polymer cal-lose. This supports a major role of fungal SOD in H2O2productionduring the plant–pathogen interaction. The early induction of thecallose synthase gene PMR4 suggested that changes in ROSaltered plant defensive responses at the transcriptional level. Themetabolites and genes involved in signalling and in response tooxidative stress were differentially expressed on Dbcsod1 infec-tion, supporting the notion that plants perceive changes in ROSbalance and activate defence responses. A higher O2–/H2O2ratioseems to be beneficial for plant protection against this necrotroph.Our results highlight the relevance of callose and the oxylipin 12-oxo-phytodienoic acid (OPDA) in the response to changes in theoxidative environment, and clarify the mechanisms that underliethe responses to Botrytis in Arabidopsis and tomato plants.