Manipulation of the Xanthophyll Cycle Increases Plant Susceptibility to Sclerotinia sclerotiorum

• Published in: PLoS pathogens 2015-05, Vol.11 (5), p.e1004878-e1004878
• Main Authors: Zhou, Jun, Zeng, Lizhang, Liu, Jian, Xing, Da
• Format: Article
• Language: English
• Subjects: Abscisic acid; Abscisic Acid - metabolism; Arabidopsis - drug effects; Arabidopsis - immunology; Arabidopsis - metabolism; Arabidopsis - microbiology; Ascomycota - drug effects; Ascomycota - immunology; Ascomycota - physiology; Biosynthesis; Cell cycle; Chlorophyll; Crop diseases; Disease susceptibility; Gene expression; Glucans - metabolism; Health aspects; Host-Pathogen Interactions - drug effects; Hydrogen-Ion Concentration; Identification and classification; Infections; Leaves; Light; Mutation; Oxalates - metabolism; Oxidoreductases - genetics; Oxidoreductases - metabolism; Pathogenesis; Pathogenic fungi; Photosynthesis; Photosynthesis - drug effects; Plant Immunity - drug effects; Plant Leaves - drug effects; Plant Leaves - immunology; Plant Leaves - metabolism; Plant Leaves - microbiology; Plant Proteins - genetics; Plant Proteins - metabolism; Plant-pathogen relationships; Plants, Genetically Modified - drug effects; Plants, Genetically Modified - immunology; Plants, Genetically Modified - metabolism; Plants, Genetically Modified - microbiology; R&D; Reactive Oxygen Species - metabolism; Reducing Agents - pharmacology; Research & development; Software; Studies; Thylakoids - drug effects; Thylakoids - metabolism; Xanthophyll; Xanthophylls - metabolism; Zeaxanthins - metabolism
• ISSN: 1553-7374; 1553-7366; 1553-7374
• DOI: 10.1371/journal.ppat.1004878

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 Sclerotinia sclerotiorum at the early stage of infection. Incubation of Sclerotinia 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 Sclerotinia-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 npq1-2 mutant) of violaxanthin de-epoxidase (VDE) abolished the Sclerotinia-induced NPQ increase. HPLC analysis showed that the Sclerotinia-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 de novo abscisic acid (ABA) biosynthesis and apparently weakened tissue defense responses, including ROS induction and callose deposition, resulting in enhanced plant susceptibility to Sclerotinia. We thus propose that Sclerotinia 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-Sclerotinia interactions at infection sites.