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Kinesin-2 from C. reinhardtii is an atypically fast and auto-inhibited motor that is activated by heterotrimerization for intraflagellar transport

Punam Sonar, Wiphu Youyen, Augustine Cleetus, Pattipong Wisanpitayakorn, Iman S. Mousavi, Willi L. Stepp, William O. Hancock, Erkan Tüzel, Zeynep Ökten
doi: https://doi.org/10.1101/855940
Punam Sonar
1Physik Department E22, Technische Universität München, Garching, Germany
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Wiphu Youyen
2Department of Physics, Worcester Polytechnic Institute, 100 Institute Road, Worcester, Massachusetts
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Augustine Cleetus
1Physik Department E22, Technische Universität München, Garching, Germany
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Pattipong Wisanpitayakorn
3Bioengineering Department, College of Engineering, Temple University, Philadelphia, Pennsylvania
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Iman S. Mousavi
2Department of Physics, Worcester Polytechnic Institute, 100 Institute Road, Worcester, Massachusetts
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Willi L. Stepp
1Physik Department E22, Technische Universität München, Garching, Germany
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William O. Hancock
4Department of Biomedical Engineering, Pennsylvania State University, University Park, PA 16802, USA
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Erkan Tüzel
3Bioengineering Department, College of Engineering, Temple University, Philadelphia, Pennsylvania
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Zeynep Ökten
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  • For correspondence: zoekten@ph.tum.de
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Summary

The construction and function of virtually all cilia require the universally conserved process of Intraflagellar Transport (IFT) [1, 2]. During the atypically fast IFT in the green alga C. reinhardtii, up to ten kinesin-2 motors ‘line up’ in a tight assembly on the trains [3], provoking the question of how these motors coordinate their action to ensure smooth and fast transport along the flagellum without standing in each other’s way. Here, we show that the heterodimeric FLA8/10 kinesin-2 alone is responsible for the atypically fast IFT in C. reinhardtii. Notably, in single-molecule studies, FLA8/10 moved at speeds matching those of in vivo IFT [4], but additionally displayed a slow velocity distribution, indicative of auto-inhibition. Addition of the KAP subunit to generate the heterotrimeric FLA8/10/KAP relieved this inhibition, thus providing a mechanistic rationale for heterotrimerization with the KAP subunit in fully activating FLA8/10 for IFT in vivo. Finally, we link fast FLA8/10 and slow KLP11/20 kinesin-2 from C. reinhardtii and C. elegans through a DNA tether to understand the molecular underpinnings of motor coordination during IFT in vivo. For motor pairs from both species, the co-transport velocities very nearly matched the single-molecule velocities, and the complexes both spent roughly 80% of the time with only one of the two motors attached to the microtubule. Thus, irrespective of phylogeny and kinetic properties, kinesin-2 motors prefer to work alone without sacrificing efficiency. Our findings thus offer a simple mechanism for how efficient IFT is achieved across diverse organisms despite being carried out by motors with different properties.

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Posted November 26, 2019.
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Kinesin-2 from C. reinhardtii is an atypically fast and auto-inhibited motor that is activated by heterotrimerization for intraflagellar transport
Punam Sonar, Wiphu Youyen, Augustine Cleetus, Pattipong Wisanpitayakorn, Iman S. Mousavi, Willi L. Stepp, William O. Hancock, Erkan Tüzel, Zeynep Ökten
bioRxiv 855940; doi: https://doi.org/10.1101/855940
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Kinesin-2 from C. reinhardtii is an atypically fast and auto-inhibited motor that is activated by heterotrimerization for intraflagellar transport
Punam Sonar, Wiphu Youyen, Augustine Cleetus, Pattipong Wisanpitayakorn, Iman S. Mousavi, Willi L. Stepp, William O. Hancock, Erkan Tüzel, Zeynep Ökten
bioRxiv 855940; doi: https://doi.org/10.1101/855940

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