The Microtubule Plus-End Tracking Protein ARMADILLO-REPEAT KINESIN1 Promotes Microtubule Catastrophe in Arabidopsis

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.

An evolutionarily conserved NIMA-related kinase directs rhizoid tip growth in the basal land plant Marchantia polymorpha

“…Treatment of root hairs with microtubule inhibitors has been shown to lead to wavy growth and the formation of multiple growth tips (Bibikova et al, 1999). In addition, genetic analyses have demonstrated that kinesin motor proteins regulate the directionality of tip growth through microtubule organization (Eng and Wasteneys, 2014;Hiwatashi et al, 2014;Eng et al, 2017). Although longitudinal microtubules similar to those present in root hairs were observed in rhizoids (Murata et al, 1987;Corellou et al, 2005;Duckett et al, 2014), microtubule function in rhizoid growth remains to be demonstrated.…”

Novel roles of Kinesin-13 and Kinesin-8 during cell growth and division in the mossPhyscomitrella patens

“…This may be due to the use of the motor-only construct with which we could not recapitulate the plus-end enrichment of Kinesin-13. Alternatively, considering the decrease and increase in catastrophe and rescue frequency of interphase MTs, it is possible the Kinesin-13 regulates growth and shrink rate indirectly via tubulin cycling: reduced catastrophe would result in reduced availability of tubulin in the free tubulin pool, which might affect MT growth and shrink rates, as was proposed in the studies of Arabidopsis ARK proteins (Eng and Wasteneys, 2014) and more recently with plant-specific MT nucleator MACET4 (Schmidt and Smertenko, 2019).…”

A Cycloheximide-Sensitive Step in Transverse Microtubule Array Patterning

“…The interphase microtubules tend to remain laterally attached to the cell's plasma membrane and rely on cortical attachment to form and maintain functional array patterns (Dhonukshe et al, 2003;Shaw et al, 2003). While molecular mechanisms explicitly related to creating transverse patterns have not been identified in hypocotyl cells, a significant number of genes are known to alter the degree of coalignment or affect microtubule dynamics (Ambrose et al, 2007;Bisgrove et al, 2008;Motose et al, 2011;Kirik et al, 2012;Lin et al, 2013;Lindeboom et al, 2013;Oda and Fukuda, 2013;Wightman et al, 2013;Eng and Wasteneys, 2014;Galva et al, 2014;Walia et al, 2014;Takatani et al, 2017). These activities have been used as a basis for modeling the interactions of cortical array polymers that could lead to ordered states (Eren et al, 2012;Deinum and Mulder, 2013).…”