Unveiling the Virulence Mechanism of Leptosphaeria maculans in the Brassica napus Interaction: The Key Role of Sirodesmin PL in Cell Death Induction

Abstract

Leptosphaeria maculans is the causal agent of blackleg disease in Brassica napus, leading to substantial yield losses. Sirodesmin PL, the principal toxin produced by L. maculans, has been implicated in the infective process in plants. However, the precise molecular and physiological mechanisms governing its effects remain elusive. This study investigates the changes induced by Sirodesmin PL at the transcriptomic, physiological, and morphological levels in B. napus cotyledons. Sirodesmin PL treatment upregulates genes associated with plant defense processes, including response to chitin, sulfur compound biosynthesis, toxin metabolism, oxidative stress response, and jasmonic acid/ethylene synthesis and signaling. Validation of these transcriptomic changes is evidenced by several typical defense response processes, such as the accumulation of reactive oxygen species (ROS) and callose deposition. Concomitantly, oxidized Sirodesmin PL induces concentration- and exposure duration-dependent cell death. This cellular death is likely attributed to diminished activity of photosystem II and a reduction in the number of chloroplasts per cell. In agreement, a down-regulation of genes associated with the photosynthesis process is observed following Sirodesmin PL treatment. Thus, it is plausible that L. maculans exploits Sirodesmin PL as a virulence factor to instigate cell death in B. napus during its necrotrophic stage, favoring the infective process. HighlightSirodesmin PL, the principal toxin produced by Leptosphaeria maculans, induces cell death and defense mechanisms in Brassica napus, disrupting photosynthesis and facilitating the infective process