Modulating the bicoid gradient in space and time

Xiaoli Cai,Stefan Baumgartner,Inge Rondeel

doi:10.1186/s41065-021-00192-y

Xiaoli Cai, Stefan Baumgartner + Show 1 more

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https://doi.org/10.1186/s41065-021-00192-y

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Abstract

BackgroundThe formation of the Bicoid (Bcd) gradient in the early Drosophila is one of the most fascinating observations in biology and serves as a paradigm for gradient formation, yet its mechanism is still not fully understood. Two distinct models were proposed in the past, the SDD and the ARTS model.ResultsWe define novel cis- and trans-acting factors that are indispensable for gradient formation. The first one is the poly A tail length of the bcd mRNA where we demonstrate that it changes not only in time, but also in space. We show that posterior bcd mRNAs possess a longer poly tail than anterior ones and this elongation is likely mediated by wispy (wisp), a poly A polymerase. Consequently, modulating the activity of Wisp results in changes of the Bcd gradient, in controlling downstream targets such as the gap and pair-rule genes, and also in influencing the cuticular pattern. Attempts to modulate the Bcd gradient by subjecting the egg to an extra nuclear cycle, i.e. a 15th nuclear cycle by means of the maternal haploid (mh) mutation showed no effect, neither on the appearance of the gradient nor on the control of downstream target. This suggests that the segmental anlagen are determined during the first 14 nuclear cycles. Finally, we identify the Cyclin B (CycB) gene as a trans-acting factor that modulates the movement of Bcd such that Bcd movement is allowed to move through the interior of the egg.ConclusionsOur analysis demonstrates that Bcd gradient formation is far more complex than previously thought requiring a revision of the models of how the gradient is formed.

Highlights

The formation of the Bicoid (Bcd) gradient in Drosophila is one of the most fascinating observations in biology that has intrigued scientists for many decades [1]
Wispy and poly A polymerase 2 (PAP2), two poly A polymerases acting on bcd mRNA localization In search of factors that can modulate the formation of the Bcd gradient, we stumbled over the PAP2 and wispy genes, the poly A polymerase orthologues in Drosophila, respectively [41,42,43]
On the other hand, belongs to the family of atypical poly A polymerases of the GLD-2 family which was first identified in C. elegans [44] and subsequently later in most phyla [45, 46]

Summary

Introduction

The formation of the Bicoid (Bcd) gradient in Drosophila is one of the most fascinating observations in biology that has intrigued scientists for many decades [1]. Bcd protein would diffuse uniformly through the entire embryo to form the gradient, followed by uniform degradation. The ARTS model [1, 7] was proposed in 2009 to solve the apparent difficulty of the SDD model in explaining the fast establishment of the gradient. To account for the rapid gradient establishment, a model was proposed that involved active transport of the bcd mRNA along microtubules (MTs) at the cortex. The formation of the Bicoid (Bcd) gradient in the early Drosophila is one of the most fascinating observations in biology and serves as a paradigm for gradient formation, yet its mechanism is still not fully understood. Two distinct models were proposed in the past, the SDD and the ARTS model

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Conclusion