A cyclic lipopeptide from Fusarium graminearum targets plant membranes to promote virulence

Authors: BRAUER, ELIZABETH - Agriculture And Agri-Food Canada; BOSNICH, WHYNN - Agriculture And Agri-Food Canada; HOLY, KIRSTEN - Agriculture And Agri-Food Canada; THAPA, INDIRA - Agriculture And Agri-Food Canada; KRISHNAN, SRINIVASAN - Boyce Thompson Institute; SYED, MOATTER - Agriculture And Agri-Food Canada; BREDOW, MELISSA - Queens University - United Kingdom; SPROULE, AMANDA - Agriculture And Agri-Food Canada; POWER, MONIQUE - Agriculture And Agri-Food Canada; JOHNSTON, ANNE - Agriculture And Agri-Food Canada; CLOUTIER, MICHAEL - Agriculture And Agri-Food Canada; HARIBABU, NAVEEN - Ottawa Hospital; KHAN, IZHAR - Agriculture And Agri-Food Canada; DIALLO, JEAN-SIMON - Ottawa Hospital; MONAGHAN, JACQUELINE - Queens University - United Kingdom; CHABOT, DENISE - Agriculture And Agri-Food Canada; OVERY, DAVID - Agriculture And Agri-Food Canada; SUBRAMANIAM, RAJAGOPAL - Agriculture And Agri-Food Canada; Pineros, Miguel; BLACKWELL, BARBARA - Agriculture And Agri-Food Canada; HARRIS, LINDA - Agriculture And Agri-Food Canada

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/8/2024
Publication Date: 7/23/2024
Citation: Brauer, E., Bosnich, W., Holy, K., Thapa, I., Krishnan, S., Syed, M., Bredow, M., Sproule, A., Power, M., Johnston, A., Cloutier, M., Haribabu, N., Khan, I., Diallo, J., Monaghan, J., Chabot, D., Overy, D., Subramaniam, R., Pineros, M., Blackwell, B., Harris, L. 2024. A cyclic lipopeptide from Fusarium graminearum targets plant membranes to promote virulence. The Plant Cell. Vol. 43, Issue 7. https://doi.org/10.1016/j.celrep.2024.114384.
DOI: https://doi.org/10.1016/j.celrep.2024.114384

Interpretive Summary: Fusarium graminearum, a fungal pathogen, uses different adaptation mechanism to infect a variety of plants. The resulting head blight disease is devastating to crops, thereby threatening food safety. During infection, the plant fungal pathogen deploys gramillin, a peptide that disrupts the cellular integrity and functioning. In this study we demonstrate that these peptides form ion -conducting pores across the cell membranes, causing cells to release their content, thereby promoting virulence. Although the process of events by which plants sense this cell membrane perturbation are not well understood, we demonstrate the involvement of a complex cascade of signaling events as part of the plant’s immune response. Interestingly, the phytotoxicity of these peptides is host specific hosts, affecting barley, but not wheat. Overall, the findings from this work will assist in identify new targets to devise new anti-Fusarium defenses.

Technical Abstract: Microbial pathogens deploy membrane-destabilizing metabolites including ionophores - molecules that transport ions through lipid bilayers - to hinder host cell function and acquire nutrients. Plants can sense microbial-induced membrane perturbation, though the signaling mechanisms involved remain unclear. Here, we identify the gramillin A and B nonribosomal peptide products of Fusarium graminearum as virulence factors in barley enabling infection of the host. We demonstrate that the gramillins form cation-conducting pores in phospholipid membranes and disrupt the plant plasma membrane to release cell contents. The infection-promoting properties and phytotoxicity of the gramillins are limited to specific hosts (maize, barley) but are ineffective in other hosts such as wheat. Gramillin-induced membrane perturbation activates canonical immune signaling responses in Arabidopsis, including the activation of mitogen activated protein kinases, a burst of reactive oxygen and calcium, and the induction of defense genes. Moreover, gramillin-induced responses are dependent on the plasma membrane-associated receptor-like cytosolic kinase BOTRYTIS INDUCED KINASE 1 (BIK1), a key convergent substrate of multiple immune receptors. Together, our work indicates that the gramillins function as ionophores to target plant cell membranes and promote F. graminearum virulence during barley and maize infection.