αTubulin 67C and Ncd are essential for establishing a cortical microtubular network and formation of the Bicoid mRNA gradient in Drosophila

PLoS One. 2014 Nov 12;9(11):e112053. doi: 10.1371/journal.pone.0112053. eCollection 2014.

Abstract

The Bicoid (Bcd) protein gradient in Drosophila serves as a paradigm for gradient formation in textbooks. To explain the generation of the gradient, the ARTS model, which is based on the observation of a bcd mRNA gradient, proposes that the bcd mRNA, localized at the anterior pole at fertilization, migrates along microtubules (MTs) at the cortex to the posterior to form a bcd mRNA gradient which is translated to form a protein gradient. To fulfil the criteria of the ARTS model, an early cortical MT network is thus a prerequisite. We report hitherto undiscovered MT activities in the early embryo important for bcd mRNA transport: (i) an early and omnidirectional MT network exclusively at the anterior cortex of early nuclear cycle embryos showing activity during metaphase and anaphase only, (ii) long MTs up to 50 µm extending into the yolk at blastoderm stage to enable basal-apical transport. The cortical MT network is not anchored to the actin cytoskeleton. The posterior transport of the mRNA via the cortical MT network critically depends on maternally-expressed αTubulin67C and the minus-end motor Ncd. In either mutant, cortical transport of the bcd mRNA does not take place and the mRNA migrates along another yet undisclosed interior MT network, instead. Our data strongly corroborate the ARTS model and explain the occurrence of the bcd mRNA gradient.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actin Cytoskeleton / metabolism
  • Anaphase
  • Animals
  • Cell Nucleus / metabolism
  • Drosophila / growth & development
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Embryo, Nonmammalian / drug effects
  • Embryo, Nonmammalian / metabolism
  • Embryonic Development
  • Female
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / metabolism*
  • Kinesins / metabolism*
  • Metaphase
  • Microtubules / metabolism*
  • Models, Biological
  • Paclitaxel / toxicity
  • RNA Transport
  • RNA, Messenger / metabolism
  • Trans-Activators / genetics
  • Trans-Activators / metabolism*
  • Tubulin / genetics
  • Tubulin / metabolism*
  • Tubulin Modulators / toxicity

Substances

  • Drosophila Proteins
  • Homeodomain Proteins
  • RNA, Messenger
  • Trans-Activators
  • Tubulin
  • Tubulin Modulators
  • bcd protein, Drosophila
  • ncd protein, Drosophila
  • Kinesins
  • Paclitaxel

Grants and funding

SB received funding from the Swedish Research Council, the Eric Philipp Sörensen Stiftelse, the Olle Engkvist Foundation, and the Medical Faculty of Lund. KF received funding from the Swedish Research Council and Hereditas. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.