A cyclic lipopeptide from Fusarium graminearum targets plant membranes to promote virulence
Elizabeth K. Brauer,
Whynn Bosnich,
Kirsten Holy,
Indira Thapa,
Srinivasan Krishnan,
Moatter Syed,
Melissa Bredow,
Amanda Sproule,
Monique Power,
Anne Johnston,
Michel Cloutier,
Naveen Haribabu,
Izhar U.H. Khan,
Jean-Simon Diallo,
Jacqueline Monaghan,
Denise Chabot,
David P. Overy,
Rajagopal Subramaniam,
Miguel Piñeros,
Barbara Blackwell,
Linda J. Harris
Affiliations
Elizabeth K. Brauer
Ottawa Research and Development Center, Agriculture and Agri-Food Canada, Ottawa, ON K1A 0C6, Canada; Department of Biology, University of Ottawa, Ottawa, ON K1N 9A7, Canada; Corresponding author
Whynn Bosnich
Ottawa Research and Development Center, Agriculture and Agri-Food Canada, Ottawa, ON K1A 0C6, Canada
Kirsten Holy
Ottawa Research and Development Center, Agriculture and Agri-Food Canada, Ottawa, ON K1A 0C6, Canada
Indira Thapa
Ottawa Research and Development Center, Agriculture and Agri-Food Canada, Ottawa, ON K1A 0C6, Canada
Srinivasan Krishnan
Boyce Thompson Institute for Plant Research, Cornell University, Ithaca, NY 14853, USA
Moatter Syed
Ottawa Research and Development Center, Agriculture and Agri-Food Canada, Ottawa, ON K1A 0C6, Canada; Department of Biology, University of Ottawa, Ottawa, ON K1N 9A7, Canada
Ottawa Research and Development Center, Agriculture and Agri-Food Canada, Ottawa, ON K1A 0C6, Canada
Monique Power
Ottawa Research and Development Center, Agriculture and Agri-Food Canada, Ottawa, ON K1A 0C6, Canada; Department of Biology, University of Ottawa, Ottawa, ON K1N 9A7, Canada
Anne Johnston
Ottawa Research and Development Center, Agriculture and Agri-Food Canada, Ottawa, ON K1A 0C6, Canada
Michel Cloutier
Ottawa Research and Development Center, Agriculture and Agri-Food Canada, Ottawa, ON K1A 0C6, Canada
Naveen Haribabu
Ottawa Hospital Research Institute, 501 Smyth Road, Ottawa, ON K1H 8L6, Canada
Izhar U.H. Khan
Ottawa Research and Development Center, Agriculture and Agri-Food Canada, Ottawa, ON K1A 0C6, Canada
Jean-Simon Diallo
Ottawa Hospital Research Institute, 501 Smyth Road, Ottawa, ON K1H 8L6, Canada
Ottawa Research and Development Center, Agriculture and Agri-Food Canada, Ottawa, ON K1A 0C6, Canada
David P. Overy
Ottawa Research and Development Center, Agriculture and Agri-Food Canada, Ottawa, ON K1A 0C6, Canada
Rajagopal Subramaniam
Ottawa Research and Development Center, Agriculture and Agri-Food Canada, Ottawa, ON K1A 0C6, Canada
Miguel Piñeros
Boyce Thompson Institute for Plant Research, Cornell University, Ithaca, NY 14853, USA; Robert W. Holley Center for Agriculture and Health, United States Department of Agriculture–Agricultural Research Service, Cornell University, Ithaca, NY 14853, USA
Barbara Blackwell
Ottawa Research and Development Center, Agriculture and Agri-Food Canada, Ottawa, ON K1A 0C6, Canada
Linda J. Harris
Ottawa Research and Development Center, Agriculture and Agri-Food Canada, Ottawa, ON K1A 0C6, Canada
Summary: Microbial plant pathogens deploy amphipathic cyclic lipopeptides to reduce surface tension in their environment. While plants can detect these molecules to activate cellular stress responses, the role of these lipopeptides or associated host responses in pathogenesis are not fully clear. The gramillin cyclic lipopeptide is produced by the Fusarium graminearum fungus and is a virulence factor and toxin in maize. Here, we show that gramillin promotes virulence and necrosis in both monocots and dicots by disrupting ion balance across membranes. Gramillin is a cation-conducting ionophore and causes plasma membrane depolarization. This disruption triggers cellular signaling, including a burst of reactive oxygen species (ROS), transcriptional reprogramming, and callose production. Gramillin-induced ROS depends on expression of host ILK1 and RBOHD genes, which promote fungal induction of virulence genes during infection and host susceptibility. We conclude that gramillin’s ionophore activity targets plant membranes to coordinate attack by the F. graminearum fungus.
