Distinct Contributions of the Peroxisome-Mitochondria Fission Machinery During Sexual Development of the Fungus Podospora anserina.

Raful Navarro-Espíndola,Fernando Suaste-Olmos,Leonardo Peraza-Reyes,Harumi Takano-Rojas

doi:10.3389/fmicb.2020.00640

Raful Navarro-Espíndola, Fernando Suaste-Olmos + Show 2 more

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https://doi.org/10.3389/fmicb.2020.00640

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Abstract

Mitochondria and peroxisomes are organelles whose activity is intimately associated and that play fundamental roles in development. In the model fungus Podospora anserina, peroxisomes and mitochondria are required for different stages of sexual development, and evidence indicates that their activity in this process is interrelated. Additionally, sexual development involves precise regulation of peroxisome assembly and dynamics. Peroxisomes and mitochondria share the proteins mediating their division. The dynamin-related protein Dnm1 (Drp1) along with its membrane receptors, like Fis1, drives this process. Here we demonstrate that peroxisome and mitochondrial fission in P. anserina depends on FIS1 and DNM1. We show that FIS1 and DNM1 elimination affects the dynamics of both organelles throughout sexual development in a developmental stage-dependent manner. Moreover, we discovered that the segregation of peroxisomes, but not mitochondria, is affected upon elimination of FIS1 or DNM1 during the division of somatic hyphae and at two central stages of sexual development—the differentiation of meiocytes (asci) and of meiotic-derived spores (ascospores). Furthermore, we found that FIS1 and DNM1 elimination results in delayed karyogamy and defective ascospore differentiation. Our findings reveal that sexual development relies on complex remodeling of peroxisomes and mitochondria, which is driven by their common fission machinery.

Highlights

Eukaryotic cell development relies on the regulation of the activity and dynamics of organelles, which involves precise modulation of their composition, abundance, and morphology
These results show that the P. anserina hyphal growth is diminished when there are defects in the peroxisome-mitochondrial fission machinery
We found that elimination of FIS1 or DNM1 resulted in extensive peroxisome elongation (Figures 2A–E, see Supplementary Figure 6), showing that both proteins are required for peroxisome fission

Summary

Introduction

Eukaryotic cell development relies on the regulation of the activity and dynamics of organelles, which involves precise modulation of their composition, abundance, and morphology. Organelle Dynamics During Sexual Development whose activity in the cell is intimately associated (for review, Fransen et al, 2017) These organelles have long been known for their cooperative function in cell metabolism—including the fatty acid beta-oxidation pathway and the glyoxylate cycle (Kunze et al, 2006; Wanders et al, 2015), and both have a prominent role in reactive oxygen species (ROS) homeostasis and redox regulation (Lismont et al, 2015). Both organelles can act as signaling platforms that integrate complex signaling pathways (Dixit et al, 2010; Horner et al, 2011). Mitochondria contribute to peroxisome biogenesis by providing vesicles that produce peroxisome precursors upon fusion with endoplasmic reticulum (ER)-derived vesicles (Sugiura et al, 2017)

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