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PMID: 25159991 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The microtubule plus-end tracking protein ARMADILLO-REPEAT KINESIN1 promotes microtubule catastrophe in Arabidopsis.

The Plant cell ·Vol. 26 ·No. 8 ·2014-08-00 ·Pages 3372-86

Eng RC, Wasteneys GO

Abstract

Microtubule dynamics are critically important for plant cell development. Here, we show that Arabidopsis thaliana ARMADILLO-REPEAT KINESIN1 (ARK1) plays a key role in root hair tip growth by promoting microtubule catastrophe events. This destabilizing activity appears to maintain adequate free tubulin concentrations in order to permit rapid microtubule growth, which in turn is correlated with uniform tip growth. Microtubules in ark1-1 root hairs exhibited reduced catastrophe frequency and slower growth velocities, both of which were restored by low concentrations of the microtubule-destabilizing drug oryzalin. An ARK1-GFP (green fluorescent protein) fusion protein expressed under its endogenous promoter localized to growing microtubule plus ends and rescued the ark1-1 root hair phenotype. Transient overexpression of ARK1-RFP (red fluorescent protein) increased microtubule catastrophe frequency. ARK1-fusion protein constructs lacking the N-terminal motor domain still labeled microtubules, suggesting the existence of a second microtubule binding domain at the C terminus of ARK1. ARK1-GFP was broadly expressed in seedlings, but mutant phenotypes were restricted to root hairs, indicating that ARK1's function is redundant in cells other than those forming root hairs.

MeSH Terms
Arabidopsis/growth & development,metabolism,ultrastructure Arabidopsis Proteins/analysis,metabolism,physiology Binding Sites Dinitrobenzenes/pharmacology Kinesins/analysis,metabolism,physiology Microtubules/metabolism,ultrastructure Plant Roots/growth & development,metabolism,ultrastructure Protein Structure, Tertiary Sulfanilamides/pharmacology
Chemicals
Arabidopsis Proteins Dinitrobenzenes Sulfanilamides oryzalin MRH2 protein, Arabidopsis Kinesins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Eng Ryan Christopher
Department of Botany, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada.
Wasteneys Geoffrey O ORCID
Department of Botany, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada geoffrey.wasteneys@ubc.ca.
References (44)
44 references, click to expand
  1. The Arabidopsis sku6/spiral1 gene encodes a plus end-localized microtubule-interacting protein involved in directional cell expansion.
    Plant Cell. 2004 Jun;16(6):1506-20 PMID: 15155883
  2. Rho of plant GTPase signaling regulates the behavior of Arabidopsis kinesin-13A to establish secondary cell wall patterns.
    Plant Cell. 2013 Nov;25(11):4439-50 PMID: 24280391
  3. Reorganization and in vivo dynamics of microtubules during Arabidopsis root hair development.
    Plant Physiol. 2004 Dec;136(4):3905-19 PMID: 15557102
  4. A tethering mechanism controls the processivity and kinetochore-microtubule plus-end enrichment of the kinesin-8 Kif18A.
    Mol Cell. 2011 Sep 2;43(5):764-75 PMID: 21884977
  5. Yeast kinesin-8 depolymerizes microtubules in a length-dependent manner.
    Nat Cell Biol. 2006 Sep;8(9):957-62 PMID: 16906145
  6. The N-terminal TOG domain of Arabidopsis MOR1 modulates affinity for microtubule polymers.
    J Cell Sci. 2012 Oct 15;125(Pt 20):4812-21 PMID: 22825869
  7. Molecular crowding creates traffic jams of kinesin motors on microtubules.
    Proc Natl Acad Sci U S A. 2012 Apr 17;109(16):6100-5 PMID: 22431622
  8. A class I ADP-ribosylation factor GTPase-activating protein is critical for maintaining directional root hair growth in Arabidopsis.
    Plant Physiol. 2008 Aug;147(4):1659-74 PMID: 18539780
  9. Armadillo repeat-containing kinesins and a NIMA-related kinase are required for epidermal-cell morphogenesis in Arabidopsis.
    Plant J. 2008 Jan;53(1):157-71 PMID: 17971038
  10. Functions of the Arabidopsis kinesin superfamily of microtubule-based motor proteins.
    Protoplasma. 2012 Oct;249(4):887-99 PMID: 22038119
  11. NIMA-related kinases 6, 4, and 5 interact with each other to regulate microtubule organization during epidermal cell expansion in Arabidopsis thaliana.
    Plant J. 2011 Sep;67(6):993-1005 PMID: 21605211
  12. Spatial organization of plant cortical microtubules: close encounters of the 2D kind.
    Trends Cell Biol. 2009 Feb;19(2):62-71 PMID: 19144522
  13. EB1 reveals mobile microtubule nucleation sites in Arabidopsis.
    Nat Cell Biol. 2003 Nov;5(11):967-71 PMID: 14557818
  14. Mechanisms underlying the dual-mode regulation of microtubule dynamics by Kip3/kinesin-8.
    Mol Cell. 2011 Sep 2;43(5):751-63 PMID: 21884976
  15. The FAST technique: a simplified Agrobacterium-based transformation method for transient gene expression analysis in seedlings of Arabidopsis and other plant species.
    Plant Methods. 2009 May 20;5:6 PMID: 19457242
  16. Low concentrations of propyzamide and oryzalin alter microtubule dynamics in Arabidopsis epidermal cells.
    Plant Cell Physiol. 2004 Sep;45(9):1330-4 PMID: 15509858
  17. A novel localization pattern for an EB1-like protein links microtubule dynamics to endomembrane organization.
    Curr Biol. 2003 Nov 11;13(22):1991-7 PMID: 14614826
  18. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  19. The Arabidopsis CLASP gene encodes a microtubule-associated protein involved in cell expansion and division.
    Plant Cell. 2007 Sep;19(9):2763-75 PMID: 17873093
  20. Mitotic spindle positioning in Saccharomyces cerevisiae is accomplished by antagonistically acting microtubule motor proteins.
    J Cell Biol. 1997 Sep 8;138(5):1041-53 PMID: 9281582
  21. Kin I kinesins are microtubule-destabilizing enzymes.
    Cell. 1999 Jan 8;96(1):69-78 PMID: 9989498
  22. Root hair-specific disruption of cellulose and xyloglucan in AtCSLD3 mutants, and factors affecting the post-rupture resumption of mutant root hair growth.
    Planta. 2011 May;233(5):985-99 PMID: 21279381
  23. Overlapping and divergent signaling pathways for ARK1 and AGD1 in the control of root hair polarity in Arabidopsis thaliana.
    Front Plant Sci. 2013 Dec 24;4:528 PMID: 24400013
  24. SPIRAL1 encodes a plant-specific microtubule-localized protein required for directional control of rapidly expanding Arabidopsis cells.
    Plant Cell. 2004 May;16(5):1178-90 PMID: 15084720
  25. An ungrouped plant kinesin accumulates at the preprophase band in a cell cycle-dependent manner.
    Cytoskeleton (Hoboken). 2011 Apr;68(4):247-58 PMID: 21387573
  26. MOR1, the Arabidopsis thaliana homologue of Xenopus MAP215, promotes rapid growth and shrinkage, and suppresses the pausing of microtubules in vivo.
    J Cell Sci. 2008 Dec 15;121(Pt 24):4114-23 PMID: 19033380
  27. Microtubules regulate tip growth and orientation in root hairs of Arabidopsis thaliana.
    Plant J. 1999 Mar;17(6):657-65 PMID: 10230063
  28. A GFP-MAP4 reporter gene for visualizing cortical microtubule rearrangements in living epidermal cells
    Plant Cell. 1998 Nov;10(11):1927-40 PMID: 9811799
  29. A gateway cloning vector set for high-throughput functional analysis of genes in planta.
    Plant Physiol. 2003 Oct;133(2):462-9 PMID: 14555774
  30. Armadillo-repeat protein functions: questions for little creatures.
    Trends Cell Biol. 2010 Aug;20(8):470-81 PMID: 20688255
  31. Building a hair: tip growth in Arabidopsis thaliana root hairs.
    Philos Trans R Soc Lond B Biol Sci. 2002 Jun 29;357(1422):815-21 PMID: 12079677
  32. Kinesins have a dual function in organizing microtubules during both tip growth and cytokinesis in Physcomitrella patens.
    Plant Cell. 2014 Mar;26(3):1256-66 PMID: 24642939
  33. Analysis of the root-hair morphogenesis transcriptome reveals the molecular identity of six genes with roles in root-hair development in Arabidopsis.
    Plant J. 2006 Jan;45(1):83-100 PMID: 16367956
  34. A non-motor microtubule binding site is essential for the high processivity and mitotic function of kinesin-8 Kif18A.
    PLoS One. 2011;6(11):e27471 PMID: 22102900
  35. A mutation in MRH2 kinesin enhances the root hair tip growth defect caused by constitutively activated ROP2 small GTPase in Arabidopsis.
    PLoS One. 2007 Oct 24;2(10):e1074 PMID: 17957256
  36. Plus end-specific depolymerase activity of Kip3, a kinesin-8 protein, explains its role in positioning the yeast mitotic spindle.
    Nat Cell Biol. 2006 Sep;8(9):913-23 PMID: 16906148
  37. Microtubule polymerization dynamics.
    Annu Rev Cell Dev Biol. 1997;13:83-117 PMID: 9442869
  38. Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments.
    Nat Cell Biol. 2009 Jul;11(7):797-806 PMID: 19525940
  39. A ubiquitin-10 promoter-based vector set for fluorescent protein tagging facilitates temporal stability and native protein distribution in transient and stable expression studies.
    Plant J. 2010 Oct;64(2):355-65 PMID: 20735773
  40. A NIMA-related protein kinase suppresses ectopic outgrowth of epidermal cells through its kinase activity and the association with microtubules.
    Plant J. 2008 Jun;54(5):829-44 PMID: 18266916
  41. MOR1 is essential for organizing cortical microtubules in plants.
    Nature. 2001 May 31;411(6837):610-3 PMID: 11385579
  42. Kif18A uses a microtubule binding site in the tail for plus-end localization and spindle length regulation.
    Curr Biol. 2011 Sep 13;21(17):1500-6 PMID: 21885282
  43. A minus-end-directed kinesin with plus-end tracking protein activity is involved in spindle morphogenesis.
    Mol Biol Cell. 2005 Apr;16(4):1584-92 PMID: 15659646
  44. Endoplasmic microtubules configure the subapical cytoplasm and are required for fast growth of Medicago truncatula root hairs.
    Plant Physiol. 2002 Oct;130(2):977-88 PMID: 12376661
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1532-298X
Published
2014-08-00
Epub
2014-00-26
Pages
3372-86
Language
English
Region
England
NLM ID
9208688
PMCID
PMC4176440
Subset
IM
Corrections
CommentIn
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