[MIC-Advanced pub] Organelle activity organized by the endoplasmic reticulum-mitochondria encounter structure –ERMES– is essential for Podospora anserina development

Research Articles:

Microbial Cell, Vol. 12, No. 1, pp. 255 - 273; doi: 10.15698/mic2025.09.860

Melisa Álvarez-Sánchez1, Matías Ramírez-Noguez1, Beatriz Aguirre-López1 and Leonardo Peraza-Reyes1

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Eucaryotic cell functioning and development depend on the concerted activity of its organelles. In the model fungus Podospora anserina, sexual development involves a dynamic regulation of mitochondria, peroxisomes and the endoplasmic reticulum (ER), suggesting that their activity during this process is coordinated. The ER-Mitochondria Encounter Structure (ERMES) is a tether complex composed of the ER protein Mmm1 and the mitochondrial proteins Mdm10, Mdm12 and Mdm34, which mediates membrane contact-site formation between these organelles. This complex also mediates interactions between mitochondria and peroxisomes. Here we analyzed the role of the ERMES complex during P. anserina development. By studying a thermosensitive MDM10 mutant, we show that MDM10 is required for mitochondrial morphology and distribution, as well as for peroxisome membrane-remodeling and motility. We discovered that lipid droplets exhibit a subapical hyphal localization, which depends on MDM10. MDM10 is also required for ER shaping and dynamics, notably of the apical ER domains of the polarized-growing hyphal region, in a process that involves the activity of the protein YOP1. We also show that apical ER shaping involves a Spitzenkörper-associated membrane traffic, which implicates MDM10, and that the mycelial growth defect of mdm10 mutants is exacerbated when the ER-shaping proteins YOP1 or RTN1 are loss. Finaly, we show that MMM1 is strictly required for mycelial growth and sexual development, suggesting that its activity is essential. Our results show that the activity of distinct organelles depends on the ERMES complex, and that the function of this complex is critical for P. anserina growth and development.

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ACKNOWLEDGMENTS

This work was supported by grants from CONACYT, Mexico (grant CONACYT-DFG 277869) and from PAPIIT-DGAPA, UNAM, Mexico (grant IN227823). Melisa Álvarez-Sánchez and Matías Ramírez-Noguez were supported by scholarships from CONACYT and PAPIIT-DGAPA, UNAM, respectively. We are much indebted to Véronique Contamine and Robert Debuchy for their generous gift of strains. We thank Ruth Rincón Heredia, Nicolás Jiménez Pérez and Abraham Rosas Arellano (IFC Imaging Facility, UNAM) for assistance on microscopy.

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Organelle activity organized by the endoplasmic reticulum-mitochondria encounter structure –ERMES– is essential for Podospora anserina development by Álvarez-Sánchez et al. is licensed under a Creative Commons Attribution 4.0 International License.

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