Manipulation of the Xanthophyll Cycle Increases Plant Susceptibility to <i>Sclerotinia sclerotiorum</i>

<div><p>The xanthophyll cycle is involved in dissipating excess light energy to protect the photosynthetic apparatus in a process commonly assessed from non-photochemical quenching (NPQ) of chlorophyll fluorescence. Here, it is shown that the xanthophyll cycle is modulated by the necrotrophic pathogen <i>Sclerotinia sclerotiorum</i> at the early stage of infection. Incubation of <i>Sclerotinia</i> led to a localized increase in NPQ even at low light intensity. Further studies showed that this abnormal change in NPQ was closely correlated with a decreased pH caused by <i>Sclerotinia</i>-secreted oxalate, which might decrease the ATP synthase activity and lead to a deepening of thylakoid lumen acidification under continuous illumination. Furthermore, suppression (with dithiothreitol) or a defect (in the <i>npq1-2</i> mutant) of violaxanthin de-epoxidase (VDE) abolished the <i>Sclerotinia</i>-induced NPQ increase. HPLC analysis showed that the <i>Sclerotinia</i>-inoculated tissue accumulated substantial quantities of zeaxanthin at the expense of violaxanthin, with a corresponding decrease in neoxanthin content. Immunoassays revealed that the decrease in these xanthophyll precursors reduced <i>de novo</i> abscisic acid (ABA) biosynthesis and apparently weakened tissue defense responses, including ROS induction and callose deposition, resulting in enhanced plant susceptibility to <i>Sclerotinia</i>. We thus propose that <i>Sclerotinia</i> antagonizes ABA biosynthesis to suppress host defense by manipulating the xanthophyll cycle in early pathogenesis. These findings provide a model of how photoprotective metabolites integrate into the defense responses, and expand the current knowledge of early plant-<i>Sclerotinia</i> interactions at infection sites.</p>