Peroxisome dynamics during development of the fungus Podospora anserina

Harumi Takano-Rojas,Denise Zickler,Leonardo Peraza-Reyes

doi:10.3852/15-112

Abstract

Peroxisomes are versatile and dynamic organelles that are required for the development of diverse eukaryotic organisms. We demonstrated previously that in the fungus Podospora anserina different peroxisomal functions are required at distinct stages of sexual development, including the initiation and progression of meiocyte (ascus) development and the differentiation and germination of sexual spores (ascospores). Peroxisome assembly during these processes relies on the differential activity of the protein machinery that drives the import of proteins into the organelle, indicating a complex developmental regulation of peroxisome formation and activity. Here we demonstrate that peroxisome dynamics is also highly regulated during development. We show that peroxisomes in P. anserina are highly dynamic and respond to metabolic and environmental cues by undergoing changes in size, morphology and number. In addition, peroxisomes of vegetative and sexual cell types are structurally different. During sexual development peroxisome number increases at two stages: at early ascus differentiation and during ascospore formation. These processes are accompanied by changes in peroxisome structure and distribution, which include a cell-polarized concentration of peroxisomes at the beginning of ascus development, as well as a morphological transition from predominantly spherical to elongated shapes at the end of the first meiotic division. Further, the mostly tubular peroxisomes present from second meiotic division to early ascospore formation again become rounded during ascospore differentiation. Ultimately the number of peroxisomes dramatically decreases upon ascospore maturation. Our results reveal a precise regulation of peroxisome dynamics during sexual development and suggest that peroxisome constitution and function during development is defined by the coordinated regulation of the proteins that control peroxisome assembly and dynamics.

Highlights

Peroxisomes are ubiquitous single membrane-bounded organelles that perform important metabolic functions
Peroxisomes are highly dynamic organelles during the vegetative cycle.—Peroxisome shape, distribution and movements were analyzed in vegetative hyphae on standard dextrin-containing medium, using a peroxisome matrix-targeted GFP (GFP-PTS1; P. anserina life cycle is described (FIG. 1)
These peroxisomes move along the hypha in both directions with velocities similar to those reported for A. nidulans, where peroxisome displacements depend on the microtubule-based molecular motors dynein and kinesin-3/UncA (Egan et al 2012)

Summary

Introduction

Peroxisomes are ubiquitous single membrane-bounded organelles that perform important metabolic functions. Peroxisomes compartmentalize numerous enzymes involved in the oxidative metabolism of distinct metab‐ olites, including lipids, carbohydrates, amino acids and purines, which produce reactive oxygen species (ROS). They contain various antioxidant enzymes and have an active role in regulating ROS in the cell (Wanders and Waterham 2006, Nordgren and Fransen 2013, Sandalio et al 2013). Peroxisomes are versatile organelles performing spe‐ cific metabolic activities that vary among organisms or even among tissues of a single organism (Gabaldon 2010). Peroxisomes are implicated in cell-signaling processes where they participate in the formation of signaling molecules (Corpas et al 2013, León 2013, Spiess and Zolman 2013, Lodhi and Semenkovich 2014) or provide a subcellular platform that orchestrate complex signaling pathways (Dixit et al 2010, Zhang et al 2013)

Methods

Results

Discussion

Conclusion