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Reconciling the bizarre inheritance of microtubules in complex (euglenid) microeukaryotes

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Abstract

We introduce a hypothetical model that explains how surface microtubules in euglenids are generated, integrated and inherited with the flagellar apparatus from generation to generation. The Euglenida is a very diverse group of single-celled eukaryotes unified by a complex cell surface called the “pellicle”, consisting of proteinaceous strips that run along the longitudinal axis of the cell and articulate with one another along their lateral margins. The strips are positioned beneath the plasma membrane and are reinforced with subtending microtubules. Euglenids reproduce asexually, and the two daughter cells inherit pellicle strips and associate microtubules from the parent cell in a semi-conservative pattern. In preparation for cell division, nascent pellicle strips develop from the anterior end of the cell and elongate toward the posterior end between two parent (mature) strips, so that the total number of pellicle strips and underlying microtubules is doubled in the predivisional cell. Each daughter cell inherits an alternating pattern of strips consisting of half of the nascent strips and half of the parent (mature) strips. This observation combined with the fact that the microtubules underlying the strips are linked to the flagellar apparatus created a cytoskeletal riddle: how do microtubules associated with an alternating pattern of nascent strips and mature strips maintain their physical relationship to the flagellar apparatus when the parent cell divides? The model of microtubular inheritance articulated here incorporates known patterns of cytoskeletal semi-conservatism and two new inferences: (1) a multigenerational “pellicle microtubule organizing center” (pMTOC) extends from the dorsal root of the flagellar apparatus, encircles the flagellar pocket, and underpins the microtubules of the pellicle; and (2) prior to cytokinesis, nascent pellicle microtubules fall within one of two “left/right” constellations that are linked to one of the two new dorsal basal bodies.

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Abbreviations

DB:

Dorsal basal body

DR:

Dorsal root

IR:

Intermediate root

MTOC:

Microtubular organizing center

pMTOC:

Pellicle microtubule organizing center

VB:

Ventral basal body

VR:

Ventral root

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Acknowledgements

This work was supported by grants from the Tula Foundation (Centre for Microbial Diversity and Evolution at the University of British Columbia) and the Canadian Institute for Advanced Research, Program in Integrated Microbial Biodiversity.

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Correspondence to Naoji Yubuki.

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Handling Editor: David Robinson

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Supplementary Fig. 1

Related to Fig. 4. Illustration of the conventional model of cytoskeletal organization in euglenids using an interphase cell with16 pellicle strips and 16 pairs of microtubules. For the sake of clarity, the ventral root has been omitted. In this model, all of the microtubules that support the wall of the flagellar pocket and the pellicle strips originate directly from the dorsal root. This configuration is physically impossible to maintain during cell division because new microtubule pairs that emerge prior to cytokinesis are associated with new dorsal roots on new dorsal basal bodies and the dorsal root of the parent transforms into an intermediate root on a new ventral basal body. Therefore, the semi-conservative inheritance of new microtubules intercalated between parent microtubules requires a different explanatory model than the one illustrated in previous interpretations. (JPG 1.97 mb)

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Yubuki, N., Leander, B.S. Reconciling the bizarre inheritance of microtubules in complex (euglenid) microeukaryotes. Protoplasma 249, 859–869 (2012). https://doi.org/10.1007/s00709-011-0340-z

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