Non-equivalence in old- and new-flagellum daughter cells of a proliferative division in Trypanosoma brucei.

Movin Abeywickrema,Jack D Sunter,De‐Hua Lai,Vladimir Varga,Sue Vaughan,Richard J Wheeler,Hana Vachova,Keith Gull,Timm Mohr,Helen Farr

doi:10.1111/mmi.14345

Abstract

SummaryDifferentiation of Trypanosoma brucei, a flagellated protozoan parasite, between life cycle stages typically occurs through an asymmetric cell division process, producing two morphologically distinct daughter cells. Conversely, proliferative cell divisions produce two daughter cells, which look similar but are not identical. To examine in detail differences between the daughter cells of a proliferative division of procyclic T. brucei we used the recently identified constituents of the flagella connector. These segregate asymmetrically during cytokinesis allowing the new‐flagellum and the old‐flagellum daughters to be distinguished. We discovered that there are distinct morphological differences between the two daughters, with the new‐flagellum daughter in particular re‐modelling rapidly and extensively in early G1. This re‐modelling process involves an increase in cell body, flagellum and flagellum attachment zone length and is accompanied by architectural changes to the anterior cell end. The old‐flagellum daughter undergoes a different G1 re‐modelling, however, despite this there was no difference in G1 duration of their respective cell cycles. This work demonstrates that the two daughters of a proliferative division of T. brucei are non‐equivalent and enables more refined morphological analysis of mutant phenotypes. We suggest all proliferative divisions in T. brucei and related organisms will involve non‐equivalence.

Highlights

Some cells have the ability to undergo proliferative, so-called ‘symmetric’, cell divisions, generating daughters destined to the same fate, as well as asymmetric cell divisions, which generate daughter cells destined to different fates (Morrison and Kimble, 2006; Santoro et al, 2016)
Differentiation of Trypanosoma brucei, a flagellated protozoan parasite, between life cycle stages typically occurs through an asymmetric cell division process, producing two morphologically distinct daughter cells
We discovered that there are distinct morphological differences between the two daughters, with the new-flagellum daughter in particular re-modelling rapidly and extensively in early G1. This re-modelling process involves an increase in cell body, flagellum and flagellum attachment zone length and is accompanied by architectural changes to the anterior cell end

Summary

Introduction

Some cells have the ability to undergo proliferative, so-called ‘symmetric’, cell divisions, generating daughters destined to the same fate, as well as asymmetric cell divisions, which generate daughter cells destined to different fates (Morrison and Kimble, 2006; Santoro et al, 2016). An excellent example are mammary stem cells, which are able to proliferate as well as exploit asymmetric cell division during differentiation; this allows them to simultaneously generate differentiated cells and replenish themselves (Santoro et al, 2016). The balancing of these two modes of division sustains tissue morphogenesis and homeostasis in such mammalian systems. Asymmetric cell division of a single yeast cell produces a larger ‘mother’ cell inheriting the bud scar, and a smaller ‘daughter’ cell with the birth scar This daughter spends longer time growing in G1 to reach a critical cell size for re-entering the cell cycle (Hartwell and Unger, 1977). A budding yeast cell in a pseudohyphal form on the other hand divides into two visually similar cells by symmetric division; these daughter cells are of similar sizes and enter cell cycle synchronously (Kron et al, 1994)

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