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Chlamydomonas reinhardtii formin and profilin are optimized for acute rapid actin filament assembly

View ORCID ProfileJenna R. Christensen, Michael J. Glista, David M. Mueller, Yujie Li, Jennifer A. Sees, Colleen T. Skau, Laurens J. Mets, View ORCID ProfilePrachee Avasthi, David R. Kovar
doi: https://doi.org/10.1101/096008
Jenna R. Christensen
aDepartment of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, IL 60637, USA
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  • ORCID record for Jenna R. Christensen
Michael J. Glista
aDepartment of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, IL 60637, USA
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David M. Mueller
bDepartment of Anatomy and Cell Biology, University of Kansas Medical Center, Kansas City, KS 66103
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Yujie Li
aDepartment of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, IL 60637, USA
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Jennifer A. Sees
aDepartment of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, IL 60637, USA
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Colleen T. Skau
aDepartment of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, IL 60637, USA
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Laurens J. Mets
aDepartment of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, IL 60637, USA
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Prachee Avasthi
bDepartment of Anatomy and Cell Biology, University of Kansas Medical Center, Kansas City, KS 66103
cDepartment of Ophthalmology, University of Kansas Medical Center, Kansas City, KS 66103
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  • For correspondence: pavasthi@kumc.edu drkovar@uchicago.edu
David R. Kovar
aDepartment of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, IL 60637, USA
dDepartment of Biochemistry and Molecular Biology, The University of Chicago, Chicago, IL 60637, USA
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  • For correspondence: pavasthi@kumc.edu drkovar@uchicago.edu
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ABSTRACT

Chlamydomonas reinhardtii is a unicellular green alga that appears less dependent upon its actin cytoskeleton than other cell types for fundamental processes like division and polarization. Null mutants of actin in Chlamydomonas, as well as treatment with actin depolymerizing drugs, have only mild defects. The reduced dependence on the actin cytoskeleton is now known to be due to the expression of a non-conventional actin in these cells which has both overlapping and unique functions. One structure that contains almost exclusively conventional F-actin is the mating fertilization tubule of gametes as actin depolymerizing drugs and conventional actin mutants have impaired fertilization tubule formation. Therefore, Chlamydomonas provides an excellent system to investigate regulation of the actin cytoskeleton, and in particular, how actin polymerization occurs at a very specific place and time. Interestingly, while it may contain a functionally minimal actin cytoskeleton, Chlamydomonas expresses both a profilin (CrPRF) and a formin (CrFor1). We have found that unlike typical profilins, CrPRF inhibits both F-actin nucleation and barbed end elongation at equimolar concentrations to actin. However, CrFor1 overcomes the low polymerizability of CrPRFbound actin and stimulates rapid actin filament assembly. CrPRF further favors CrFor1mediated actin assembly by potently inhibiting Arp2/3 complex-mediated actin assembly. Together, these findings suggest that CrFor1 and CrPRF work together to selectively and rapidly assemble F-actin at the right time and place. In vivo results demonstrate that this rapid actin assembly by CrFor1 is important specifically for fertilization tubule formation during mating, as formin inhibitor SMIFH2 inhibits formation of fertilization tubules in Chlamydomonas gametes.

  • Abbreviations

    PRM
    proline rich motif
    TIRF
    total internal reflection fluorescence
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    Posted December 21, 2016.
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    Chlamydomonas reinhardtii formin and profilin are optimized for acute rapid actin filament assembly
    Jenna R. Christensen, Michael J. Glista, David M. Mueller, Yujie Li, Jennifer A. Sees, Colleen T. Skau, Laurens J. Mets, Prachee Avasthi, David R. Kovar
    bioRxiv 096008; doi: https://doi.org/10.1101/096008
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    Chlamydomonas reinhardtii formin and profilin are optimized for acute rapid actin filament assembly
    Jenna R. Christensen, Michael J. Glista, David M. Mueller, Yujie Li, Jennifer A. Sees, Colleen T. Skau, Laurens J. Mets, Prachee Avasthi, David R. Kovar
    bioRxiv 096008; doi: https://doi.org/10.1101/096008

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