Phosphatidic acid produced by phospholipase D is required for hyphal cell-cell fusion and fungal-plant symbiosis

Mol Microbiol. 2020 Jun;113(6):1101-1121. doi: 10.1111/mmi.14480. Epub 2020 Feb 12.

Abstract

Although lipid signaling has been shown to serve crucial roles in mammals and plants, little is known about this process in filamentous fungi. Here we analyze the contribution of phospholipase D (PLD) and its product phosphatidic acid (PA) in hyphal morphogenesis and growth of Epichloë festucae and Neurospora crassa, and in the establishment of a symbiotic interaction between E. festucae and Lolium perenne. Growth of E. festucae and N. crassa PLD deletion strains in axenic culture, and for E. festucae in association with L. perenne, were analyzed by light-, confocal- and electron microscopy. Changes in PA distribution were analyzed in E. festucae using a PA biosensor and the impact of these changes on the endocytic recycling and superoxide production investigated. We found that E. festucae PldB, and the N. crassa ortholog, PLA-7, are required for polarized growth and cell fusion and contribute to ascospore development, whereas PldA/PLA-8 are dispensable for these functions. Exogenous addition of PA rescues the cell-fusion phenotype in E. festucae. PldB is also crucial for E. festucae to establish a symbiotic association with L. perenne. This study identifies a new component of the cell-cell communication and cell fusion signaling network for hyphal morphogenesis and growth of filamentous fungi.

Keywords: Epichloë festucae; Neurospora crassa; cell-cell fusion; mutualism; phosphatidic acid; phospholipase D; sexual development.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Biosensing Techniques
  • Cell Communication
  • Cell Fusion
  • Epichloe / growth & development*
  • Epichloe / physiology
  • Gene Deletion
  • Gene Expression Regulation, Fungal / genetics
  • Hyphae / growth & development
  • Lolium / microbiology*
  • Lolium / physiology
  • Neurospora crassa / growth & development*
  • Phosphatidic Acids / metabolism*
  • Phosphatidylcholines / metabolism
  • Phospholipase D / metabolism*
  • Signal Transduction / physiology
  • Spores, Fungal / growth & development
  • Superoxides / metabolism
  • Symbiosis / physiology

Substances

  • Phosphatidic Acids
  • Phosphatidylcholines
  • Superoxides
  • Phospholipase D

Supplementary concepts

  • Epichloe festucae