Abstract
ABSTRACTThe endoplasmic reticulum (ER) is an elaborate organelle composed of distinct structural and functional domains. ER structure and dynamics involve membrane-shaping proteins of the reticulon and Yop1/DP1 families, which promote membrane curvature and regulate ER shaping and remodeling. Here, we analyzed the function of the reticulon (RTN1) and Yop1 proteins (YOP1 and YOP2) of the model fungus Podospora anserina and their contribution to sexual development. We found that RTN1 and YOP2 localize to the peripheral ER and are enriched in the dynamic apical ER domains of the polarized growing hyphal region. We discovered that the formation of these domains is diminished in the absence of RTN1 or YOP2 and abolished in the absence of YOP1 and that hyphal growth is moderately reduced when YOP1 is deleted in combination with RTN1 and/or YOP2. In addition, we found that RTN1 associates with the Spitzenkörper. Moreover, RTN1 localization is regulated during meiotic development, where it accumulates at the apex of growing asci (meiocytes) during their differentiation and at their middle region during the subsequent meiotic progression. Furthermore, we discovered that loss of RTN1 affects ascospore (meiotic spore) formation, in a process that does not involve YOP1 or YOP2. Finally, we show that the defects in ascospore formation of rtn1 mutants are associated with defective nuclear segregation and spindle dynamics throughout meiotic development. Our results show that sexual development in P. anserina involves a developmental remodeling of the ER that implicates the reticulon RTN1, which is required for meiotic nucleus segregation.
Highlights
The endoplasmic reticulum (ER) is an elaborate organelle composed of distinct structural and functional domains
ER-Shaping Proteins during Meiotic Development ectopically expressed ER-targeted green fluorescent protein (ER-GFP), which consisted of enhanced GFP (EGFP) flanked by the ER targeting and retention signals of the putative P. anserina ER chaperone BiP/Kar2 [47]
This ER subdomain consists of a number of dynamic and pleomorphic ER subcompartments (Fig. 1A), which are interconnected with the peripheral ER strands and which undergo fusion and division events accompanied by directional displacements along hyphae [47]
Summary
The endoplasmic reticulum (ER) is an elaborate organelle composed of distinct structural and functional domains. ER structure and dynamics rely on a number of proteins that shape the organelle membranes, facilitate their homotypic fusion, and mediate their association with the cytoskeleton [1] Central to these processes are two conserved families of proteins—the reticulon and Yop1/DP1/REEP proteins—which form oligomers in the ER membrane that promote high membrane curvature [13, 14]. The reticulon and Yop proteins facilitate the formation of the peripheral ER tubules and stabilize the edges of ER sheets [14, 20,21,22] They have been proposed to stabilize the sites of fusion between the inner and outer membranes of the NE at the nuclear pores [23], and they participate in ER membrane constriction and fission [24]. The reticulons participate in the formation of the contact sites that the ER establishes with mitochondria [30, 31], peroxisomes [32], and the plasma membrane [33], as well as in the selective elimination of the ER via autophagy [34,35,36,37]
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