Armadillo repeat‐containing kinesins and a NIMA‐related kinase are required for epidermal‐cell morphogenesis in Arabidopsis

Abstract

SummaryThe involvement of kinesin motor proteins in both cell-tip growth and cell-shape determination has been well characterized in various organisms. However, the functions of kinesins during cell morphogenesis in higher plants remain largely unknown. In the current study, we demonstrate that an armadillo repeat-containing kinesin-related protein, ARMADILLO REPEAT KINESIN1 (ARK1), is involved in root-hair morphogenesis. Microtubule polymers are more abundant in ark1 null allele root hairs, but analysis shows that these extra microtubules are concentrated in the endoplasm, and not in the cortical array, suggesting that ARK1 regulates tip growth by limiting the assembly and distribution of endoplasmic microtubules. The ARK1 gene has two homologues in the Arabidopsis genome, ARK2 and ARK3, and our results show that ARK2 is involved in rootcell morphogenesis. We further reveal that a NIMA-related protein kinase, NEK6, binds to the ARK family proteins and has pleiotropic effects on epidermal-cell morphogenesis, suggesting that NEK6 is involved in cell morphogenesis in Arabidopsis via microtubule functions associated with these armadillo repeat-containing kinesins. We discuss the function of NIMA-related protein kinases and armadillo repeat-containing kinesins in the cell morphogenesis of eukaryotes.

A Class I ADP-Ribosylation Factor GTPase-Activating Protein Is Critical for Maintaining Directional Root Hair Growth in Arabidopsis

“…2A). Two independent groups had previously identified mutants in this gene (Jones et al, 2006;Yang et al, 2007;Sakai et al, 2008). These mutants were designated mrh2 but were recently renamed ark1 (Sakai et al, 2008).…”

“…Here, we characterize two loss-of-function Arabidopsis mutants with wavy root hair growth. We show that one mutant is disrupted in a gene that encodes a class I ARF-GAP (AGD1; Vernoud et al, 2003) while the other mutant is a new allele of an armadillo repeat-containing kinesin previously designated MRH2 or ARMADILLO RE-PEAT KINESIN1 (ARK1; Jones et al, 2006;Yang et al, 2007;Sakai et al, 2008). AGD1 localized to punctate intracellular compartments that partially associated with the endocytic marker FM4-64, consistent with its function as a mediator of vesicle trafficking.…”

“…Therefore, we renamed wrh2 as ark1-4, since three other ark1 mutants that included the homozygous SALK lines that we identified here have already been described ( Fig. 2A; Jones et al, 2006;Sakai et al, 2008).…”

“…The important role of the cytoskeleton in this process is supported by the observation that exposure to microtubule inhibitors or downregulation of tubulin, the major protein subunit of microtubules, resulted in the formation of root hairs with multiple tips and wavy growth (Bibikova et al, 1999;Bao et al, 2001). Recently, root hairs of Arabidopsis (Arabidopsis thaliana) knockouts to an armadillo repeatcontaining kinesin displayed wavy and branched root hairs, further establishing the link between microtubules and the maintenance of root hair growth direction (Jones et al, 2006;Yang et al, 2007;Sakai et al, 2008). The actin cytoskeleton also is essential for maintaining tip-focused growth.…”

Structure, function, and evolution of plant NIMA-related kinases: implication for phosphorylation-dependent microtubule regulation

“…(Motose et al 2008). In addition, AtNEK6 has been shown to interact with armadillo-repeat-containing kinesins (ARKs) via its C-termini (Sakai et al 2008). Surprisingly, we found that the plant NEK C-terminal (PNC) motif that follows the coiled-coil domain and is conserved in plant NEKs (Fig.…”