Transport of Germ Plasm on Astral Microtubules Directs Germ Cell Development in Drosophila

Abstract

Summary Background In many organisms, germ cells are segregated from the soma through the inheritance of the specialized germ plasm, which contains mRNAs and proteins that specify germ cell fate and promote germline development. Whereas germ plasm assembly has been well characterized, mechanisms mediating germ plasm inheritance are poorly understood. In the Drosophila embryo, germ plasm is anchored to the posterior cortex and nuclei that migrate into this region give rise to the germ cell progenitors, or pole cells. How the germ plasm interacts with these nuclei for pole cell induction and is selectively incorporated into the forming pole cells is not known. Results Live imaging of two conserved germ plasm components, nanos mRNA and Vasa protein, revealed that germ plasm segregation is a dynamic process involving active transport of germ plasm RNA-protein complexes coordinated with nuclear migration. We show that centrosomes accompanying posterior nuclei induce release of germ plasm from the cortex and recruit these components by dynein-dependent transport on centrosome-nucleated microtubules. As nuclei divide, continued transport on astral microtubules partitions germ plasm to daughter nuclei, leading to its segregation into pole cells. Disruption of these transport events prevents incorporation of germ plasm into pole cells and impairs germ cell development. Conclusions Our results indicate that active transport of germ plasm is essential for its inheritance and ensures the production of a discrete population of germ cell progenitors endowed with requisite factors for germline development. Transport on astral microtubules may provide a general mechanism for the effective segregation of cell fate determinants.

Germ Plasm Anchoring Is a Dynamic State that Requires Persistent Trafficking

“…The process of germ cell formation initiates when centrosomes and/or astral microtubules associated with nuclei that migrate to the posterior of the syncytial embryo induce release of germ plasm from the posterior cortex. Recruitment of germ plasm to the centrosomes by dynein-dependent transport on astral microtubules is required for these nuclei to induce germ cell formation and for the inheritance of the germ plasm by the newly formed germ cells (Lerit and Gavis, 2011). The prior coupling of germ plasm RNP particles to dynein in the oocyte may allow their rapid accumulation on astral microtubules upon release from the cortex.…”

Essential elements for translation: the germline factor Vasa functions broadly in somatic cells

“…Further, these factors also appear to have multiple functions within a cell. For Vasa specifically, this includes recently documented functions recruited to the mitotic spindle both in the germ line and in somatic lineages (Rouhana et al, 2010;Lerit and Gavis, 2011;Pek and Kai, 2011;Yajima and Wessel, 2011b,c;Wagner et al, 2012).…”

Gradual recruitment and selective clearing generate germ plasm aggregates in the zebrafish embryo

“…This so-called pole plasm then incorporates into cells that form prematurely at the posterior pole of the egg to generate PGCs. [4][5][6] In C. elegans, germ plasmlike granules, called P-granules, are detectable in the posterior region of the uncleaved zygote as prelocalized, cytoplasmic particles. 7,8 Under the influence of cell polarity PAR factors 9 and the actin cytoskeleton, P-granules become restricted to the germ cell lineage during asymmetric cell division.…”