Peroxisome dynamics during development of the fungus Podospora anserina

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.

• cell differentiation
• fungi
• meiosis
• peroxisome dynamics
• sexual development

Acknowledgments

This research was supported by grants from Universidad Nacional Autónoma de México (DGAPA-PAPIIT grant IA201815), the European Leukodystrophy Association (ELA) Research Foundation, the Agence nationale de la recherche ( ANR-05-BLAN-0385-01), the Centre National de la Recherche Scientifique and the Université Paris-Sud ( UMR 8621). We are much indebted to Fernando Suaste-Olmos (IFC, UNAM) for technical assistance and to Véronique Berteaux-Lecellier (CRIOBE, CNRS) and Robert Debuchy (I2BC, Université Paris-Sud) for assistance and valuable discussions.