Receptor-mediated yolk uptake is required for oskar mRNA localization and cortical anchorage of germ plasm components in the Drosophila oocyte.

Tsubasa Tanaka,Naoki Tani,Akira Nakamura,Simon Bullock

doi:10.1371/journal.pbio.3001183

Abstract

The Drosophila germ plasm is responsible for germ cell formation. Its assembly begins with localization of oskar mRNA to the posterior pole of the oocyte. The oskar translation produces 2 isoforms with distinct functions: short Oskar recruits germ plasm components, whereas long Oskar remodels actin to anchor the components to the cortex. The mechanism by which long Oskar anchors them remains elusive. Here, we report that Yolkless, which facilitates uptake of nutrient yolk proteins into the oocyte, is a key cofactor for long Oskar. Loss of Yolkless or depletion of yolk proteins disrupts the microtubule alignment and oskar mRNA localization at the posterior pole of the oocyte, whereas microtubule-dependent localization of bicoid mRNA to the anterior and gurken mRNA to the anterior-dorsal corner remains intact. Furthermore, these mutant oocytes do not properly respond to long Oskar, causing defects in the actin remodeling and germ plasm anchoring. Thus, the yolk uptake is not merely the process for nutrient incorporation, but also crucial for oskar mRNA localization and cortical anchorage of germ plasm components in the oocyte.

Highlights

Asymmetric localization of specific RNAs and proteins in developing oocytes is fundamental for body patterning and cell fate determination of future embryos in a variety of organisms
Since long Osk is located on the endosomal surface [10], we proposed that it may contribute to actin remodeling through interaction with proteins that reside on endosomes
In egg-laying animals, the principal nutrient source for embryonic development is yolk proteins, which accumulate in oocytes during oogenesis

Summary

Introduction

Asymmetric localization of specific RNAs and proteins in developing oocytes is fundamental for body patterning and cell fate determination of future embryos in a variety of organisms. In the Drosophila oocyte, specific maternal factors that direct abdominal patterning and germ cell formation are localized in the specialized cytoplasm at the posterior pole, called germ (pole) plasm. The germ plasm is assembled by stepwise targeting of its components to the posterior pole of the oocyte. Germ plasm components are stably maintained at the posterior cortex until their inheritance by germline progenitors (pole cells) in the early embryo [1]. Of the germ plasm begins with localization of oskar (osk) mRNA to the posterior pole of the oocyte [2]. Transport of osk mRNA in the oocyte depends on polarized microtubule arrays whose plus-ends are weakly enriched at the posterior pole [3,4].

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Results

Conclusion