Cellular development associated with induced mycotoxin synthesis in the filamentous fungus Fusarium graminearum

PLoS One. 2013 May 7;8(5):e63077. doi: 10.1371/journal.pone.0063077. Print 2013.

Abstract

Several species of the filamentous fungus Fusarium colonize plants and produce toxic small molecules that contaminate agricultural products, rendering them unsuitable for consumption. Among the most destructive of these species is F. graminearum, which causes disease in wheat and barley and often infests the grain with harmful trichothecene mycotoxins. Synthesis of these secondary metabolites is induced during plant infection or in culture in response to chemical signals. Our results show that trichothecene biosynthesis involves a complex developmental process that includes dynamic changes in cell morphology and the biogenesis of novel subcellular structures. Two cytochrome P-450 oxygenases (Tri4p and Tri1p) involved in early and late steps in trichothecene biosynthesis were tagged with fluorescent proteins and shown to co-localize to vesicles we provisionally call "toxisomes." Toxisomes, the inferred site of trichothecene biosynthesis, dynamically interact with motile vesicles containing a predicted major facilitator superfamily protein (Tri12p) previously implicated in trichothecene export and tolerance. The immediate isoprenoid precursor of trichothecenes is the primary metabolite farnesyl pyrophosphate. Changes occur in the cellular localization of the isoprenoid biosynthetic enzyme HMG CoA reductase when cultures non-induced for trichothecene biosynthesis are transferred to trichothecene biosynthesis inducing medium. Initially localized in the cellular endomembrane system, HMG CoA reductase, upon induction of trichothecene biosynthesis, increasingly is targeted to toxisomes. Metabolic pathways of primary and secondary metabolism thus may be coordinated and co-localized under conditions when trichothecene biosynthesis occurs.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Actins / metabolism
  • Biological Transport
  • Biosynthetic Pathways
  • Cytoplasmic Vesicles / metabolism
  • Fluorescence
  • Fungal Proteins / metabolism
  • Fusarium / cytology*
  • Fusarium / enzymology
  • Fusarium / metabolism*
  • Green Fluorescent Proteins / metabolism
  • Models, Biological
  • Mycotoxins / biosynthesis*
  • Secondary Metabolism
  • Trichothecenes / biosynthesis

Substances

  • Actins
  • Fungal Proteins
  • Mycotoxins
  • Trichothecenes
  • Green Fluorescent Proteins

Grants and funding

This work was funded by the United States Department of Agriculture, Agriculture and Food Research Initiative, National Institute of Food and Agriculture award number 2010-65108-20642, as well as the United States Wheat and Barley Scab Initiative awards FY09-KI-016, FY08-KI-118 and FY07-KI-12. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.