Mon1-Rab7 axis is essential for transport, localization and anchoring of oskar mRNA

Abstract Asymmetric localization of oskar mRNA to the posterior of the oocyte is a complex process driven by autonomous and non-cell autonomous mechanisms. The former includes Oskar protein that reinforces localization and anchoring of its mRNA through activation of endocytosis and regulation of actin cytoskeleton; the latter includes signals from the posterior follicle cells (PFCs) that regulates microtubule orientation for polarized transport. Here we identify Monensin Sensitivity 1 (Mon1), as a novel factor regulating anterior-posterior (A-P) patterning. Mon1 is an evolutionarily conserved activator of Rab7-a key regulator of the endo-lysosomal pathway. Embryos lacking maternal mon1 (mon1m) show mislocalized oskar and bicoid mRNAs leading to loss of patterning and lethality. In the mutant oocyte Staufen appears clumpy and the levels of Oskar protein and Par-1 is significantly reduced. Abnormal actin rings are seen in the ooplasm. Driving expression of mon1 in the germline rescues these phenotypes and restores viability. In contrast, expression in the PFC predominantly rescues the Par-1 phenotype with a modest effect on viability. We demonstrate that oskar mRNA interacts with Rab7 suggesting possible role for the Mon1-Rab7 axis in the transport of oskar. We show that Mon1 in the PFCs, regulates PIP2 levels to influence accumulation of Par-1 in the oocyte. We propose that Mon1 regulates oskar localization in two distinct ways: cell autonomously in the germline by regulating Rab7, and non-cell autonomously through the PFCs by regulating accumulation of Par-1. Summary statement Mon1, an established Rab converter, has roles in embryonic axial patterning, modulating transport, localisation and anchoring of posteriorly localised mRNA during oocyte maturation. Mon1 influence is both cell autonomous, from within the oocyte and non-cell autonomous, through posterior follicle cells. Competing Interest Statement The authors have declared no competing interest.