Cited by 20Microtubule and mitosis dynamicsPlant Molecular Biology ResearchPlant Reproductive Biology

Armadillo repeat-containing kinesin represents the versatile plus-end-directed transporter in Physcomitrella

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Yoshida, Mari W., Hakozaki, Maya, Goshima, Gohta·2023·Nature Plants

Published version of a preprint

Abstract

Kinesin-1, also known as conventional kinesin, is widely used for microtubule plus-end-directed (anterograde) transport of various cargos in animal cells. However, a motor functionally equivalent to the conventional kinesin has not been identified in plants, which lack the kinesin-1 genes. Here we show that plant-specific armadillo repeat-containing kinesin (ARK) is the long sought-after versatile anterograde transporter in plants. In ARK mutants of the moss Physcomitrium patens, the anterograde motility of nuclei, chloroplasts, mitochondria and secretory vesicles was suppressed. Ectopic expression of non-motile or tail-deleted ARK did not restore organelle distribution. Another prominent macroscopic phenotype of ARK mutants was the suppression of cell tip growth. We showed that this defect was attributed to the mislocalization of actin regulators, including RopGEFs; expression and forced apical localization of RopGEF3 partially rescued the growth phenotype of the ARK mutant. The mutant phenotypes were partially rescued by ARK homologues in Arabidopsis thaliana, suggesting the conservation of ARK functions in plants.

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  1. Encalada, S. E. & Goldstein, L. S. B. Biophysical Challenges to Axonal Transport: Motor-Cargo Deficiencies and Neurodegeneration. Annual Review of Biophysics 43, 141-169 (2014).
  2. Nakata, T. & Hirokawa, N. Microtubules provide directional cues for polarized axonal transport through interaction with kinesin motor head. The Journal of cell biology 162, 1045-1055 (2003).
  3. Splinter, D. et al. Bicaudal D2, Dynein, and Kinesin-1 Associate with Nuclear Pore Complexes and Regulate Centrosome and Nuclear Positioning during Mitotic Entry. PLOS Biology 8, e1000350 (2010).
  4. Kong, S.-G. & Wada, M. Molecular basis of chloroplast photorelocation movement. Journal of plant research 129, 159-166 (2016).
  5. Frey, N., Klotz, J. & Nick, P. A kinesin with calponin-homology domain is involved in premitotic nuclear migration. Journal of Experimental Botany 61, 3423- 3437 (2010).
  6. Katsuta, J., Hashiguchi, Y. & Shibaoka, H. The role of the cytoskeleton in positioning of the nucleus in premitotic tobacco BY-2 cells. Journal of cell science 95, 413-422 (1990).
  7. Zonia, L., Tupý, J. & Staiger, C. J. Unique actin and microtubule arrays co- ordinate the differentiation of microspores to mature pollen in Nicotiana tabacum. Journal of Experimental Botany 50, 581-594 (1999).
  8. Yamada, M., Tanaka-Takiguchi, Y., Hayashi, M., Nishina, M. & Goshima, G. Multiple kinesin-14 family members drive microtubule minus end-directed transport in plant cells. Journal of Cell Biology 216, 1705-1714 (2017).
  9. Sun, J., Zhang, M., Qi, X., Doyle, C. & Zheng, H. Armadillo-repeat kinesin1 interacts with Arabidopsis atlastin RHD3 to move ER with plus-end of microtubules. Nat Commun 11, 5510 (2020).
  10. Tran, P. T., Marsh, L., Doye, V., Inoué, S. & Chang, F. A Mechanism for Nuclear Positioning in Fission Yeast Based on Microtubule Pushing. Journal of Cell Biology 153, 397-412 (2001).
  11. Kanda, A., Otani, K., Takahashi, T. & Motose, H. Plant specific armadillo repeat kinesin directs organelle transport and microtubule convergence to promote tip growth. 2022.07.08.499237 Preprint at https://doi.org/10.1101/2022.07.08.499237 (2022). (bioRxiv) · DOI · Paper page
  12. Yi, P. & Goshima, G. Transient cotransformation of CRISPR/Cas9 and oligonucleotide templates enables efficient editing of target loci in Physcomitrella patens. Plant Biotechnology Journal 18, 599-601 (2020).
  13. Nakata, T. & Hirokawa, N. Point mutation of adenosine triphosphate-binding motif generated rigor kinesin that selectively blocks anterograde lysosome membrane transport. Journal of Cell Biology 131, 1039-1053 (1995).
  14. Furt, F., Lemoi, K., Tüzel, E. & Vidali, L. Quantitative analysis of organelle distribution and dynamics in Physcomitrella patens protonemal cells. BMC Plant Biology 12, 70 (2012).
  15. Hunt, A. J., Gittes, F. & Howard, J. The force exerted by a single kinesin molecule against a viscous load. Biophysical Journal 67, 766-781 (1994).
  16. Doonan, J. H., Cove, D. J. & Lloyd, C. W. Microtubules and microfilaments in tip growth: evidence that microtubules impose polarity on protonemal growth in Physcomitrella patens. Journal of Cell Science 89, 533-540 (1988).
  17. Wu, S.-Z. & Bezanilla, M. Actin and microtubule cross talk mediates persistent polarized growth. Journal of Cell Biology 217, 3531-3544 (2018).
  18. Vidali, L. et al. Rapid formin-mediated actin-filament elongation is essential for polarized plant cell growth. Proceedings of the National Academy of Sciences 106, 13341-13346 (2009).
  19. Reddy, A. S. N. Molecular motors and their functions in plants. in International Review of Cytology vol. 204 97-178 (Elsevier, 2001).
  20. Maney, T., Wagenbach, M. & Wordeman, L. Molecular Dissection of the Microtubule Depolymerizing Activity of Mitotic Centromere-associated Kinesin*. Journal of Biological Chemistry 276, 34753-34758 (2001).
  21. Riquelme, M. Tip Growth in Filamentous Fungi: A Road Trip to the Apex. Annual Review of Microbiology 67, 587-609 (2013).
  22. Shirae-Kurabayashi, M., Edzuka, T., Suzuki, M. & Goshima, G. Cell tip growth underlies injury response of marine macroalgae. PLOS ONE 17, e0264827 (2022).
  23. Browning, H. et al. Tea2p Is a Kinesin-like Protein Required to Generate Polarized Growth in Fission Yeast. Journal of Cell Biology 151, 15-28 (2000).
  24. Kreitzer, G. & Myat, M. M. Microtubule Motors in Establishment of Epithelial Cell Polarity. Cold Spring Harb Perspect Biol 10, a027896 (2018).
  25. Sakai, T. et al. Armadillo repeat-containing kinesins and a NIMA-related kinase are required for epidermal-cell morphogenesis in Arabidopsis. The Plant Journal 53, 157-171 (2008).
  26. Lan, M., Kang, E., Liu, X., Fu, Y. & Zhu, L. Stable ARMADILLO REPEAT KINESIN 2 in light inhibits hypocotyl elongation and facilitates light-induced cortical microtubule reorientation in Arabidopsis. Journal of Experimental Botany erac473 (2022) doi:10.1093/jxb/erac473. · DOI
  27. Collonnier, C. et al. CRISPR-Cas9-mediated efficient directed mutagenesis and RAD 51-dependent and RAD 51-independent gene targeting in the moss Physcomitrella patens. Plant Biotechnology Journal 15, 122-131 (2017).
  28. Chang, P. & Ohi, R.) 263-282 (Springer, 2016). doi:10.1007/978-1-4939-3542-0_17. · DOI · Paper page

Cited by

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Authors
Yoshida, M. W., Hakozaki, M., & Goshima, G.
Affiliations
Nagoya University (JP)
Corresponding author
Goshima, Gohta
Venue
Nature Plants
Published
2023-05-04
Volume
9
Issue
5
Pages
733-748
ISSN
  • 2055-026X (ISSN-L)
  • 2055-0278
OpenAlex
W4368374050
Cited by
20
References
4
Citations by year
2026: 2 · 2025: 7 · 2024: 7 · 2023: 3 · 2022: 1
FWCI
2.65
Type
journal article
Language
en
Open access
Locations
  • Nature Plants (publishedVersion)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • Institutional Repositories DataBase (IRDB) (acceptedVersion)
  • Nagoya University Repository (NAGOYA Repository) (submittedVersion, cc-by-nc-nd)
Funders
MEXT | Japan Society for the Promotion of Science (18KK0202, 22H02644, 17H06471)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant Reproductive Biology
Keywords
Physcomitrella patens, bryophytes, organelle motility, secretory vesicle transport, cell polarity, actin regulators, kinesin-1
MeSH terms
Protein Domains, Kinesins, Arabidopsis, Bryopsida

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