Directional cell expansion requires NIMA-related kinase 6 (NEK6)-mediated cortical microtubule destabilization

Shogo Takatani, Shinichiro Ozawa, Noriyoshi Yagi, Takashi Hotta, Takashi Hashimoto, Yuichiro Takahashi, Taku Takahashi, Hiroyasu Motose

Research output: Contribution to journalArticle

4 Citations (Scopus)

Abstract

Plant cortical microtubules align perpendicular to the growth axis to determine the direction of cell growth. However, it remains unclear how plant cells form well-organized cortical microtubule arrays in the absence of a centrosome. In this study, we investigated the functions of Arabidopsis NIMA-related kinase 6 (NEK6), which regulates microtubule organization during anisotropic cell expansion. Quantitative analysis of hypocotyl cell growth in the nek6-1 mutant demonstrated that NEK6 suppresses ectopic outgrowth and promotes cell elongation in different regions of the hypocotyl. Loss of NEK6 function led to excessive microtubule waving and distortion, implying that NEK6 suppresses the aberrant cortical microtubules. Live cell imaging showed that NEK6 localizes to the microtubule lattice and to the shrinking plus and minus ends of microtubules. In agreement with this observation, the induced overexpression of NEK6 reduced and disorganized cortical microtubules and suppressed cell elongation. Furthermore, we identified five phosphorylation sites in β-tubulin that serve as substrates for NEK6 in vitro. Alanine substitution of the phosphorylation site Thr166 promoted incorporation of mutant β-tubulin into microtubules. Taken together, these results suggest that NEK6 promotes directional cell growth through phosphorylation of β-tubulin and the resulting destabilization of cortical microtubules.

Original languageEnglish
Article number7826
JournalScientific Reports
Volume7
Issue number1
DOIs
Publication statusPublished - Dec 1 2017

Fingerprint

Microtubules
Tubulin
Hypocotyl
Phosphorylation
Growth
NIMA-related kinase 6
Centrosome
Plant Cells
Arabidopsis
Alanine

ASJC Scopus subject areas

  • General

Cite this

Directional cell expansion requires NIMA-related kinase 6 (NEK6)-mediated cortical microtubule destabilization. / Takatani, Shogo; Ozawa, Shinichiro; Yagi, Noriyoshi; Hotta, Takashi; Hashimoto, Takashi; Takahashi, Yuichiro; Takahashi, Taku; Motose, Hiroyasu.

In: Scientific Reports, Vol. 7, No. 1, 7826, 01.12.2017.

Research output: Contribution to journalArticle

@article{9f7d3bc9cd8c4cb4a1cd89b77d251e37,
title = "Directional cell expansion requires NIMA-related kinase 6 (NEK6)-mediated cortical microtubule destabilization",
abstract = "Plant cortical microtubules align perpendicular to the growth axis to determine the direction of cell growth. However, it remains unclear how plant cells form well-organized cortical microtubule arrays in the absence of a centrosome. In this study, we investigated the functions of Arabidopsis NIMA-related kinase 6 (NEK6), which regulates microtubule organization during anisotropic cell expansion. Quantitative analysis of hypocotyl cell growth in the nek6-1 mutant demonstrated that NEK6 suppresses ectopic outgrowth and promotes cell elongation in different regions of the hypocotyl. Loss of NEK6 function led to excessive microtubule waving and distortion, implying that NEK6 suppresses the aberrant cortical microtubules. Live cell imaging showed that NEK6 localizes to the microtubule lattice and to the shrinking plus and minus ends of microtubules. In agreement with this observation, the induced overexpression of NEK6 reduced and disorganized cortical microtubules and suppressed cell elongation. Furthermore, we identified five phosphorylation sites in β-tubulin that serve as substrates for NEK6 in vitro. Alanine substitution of the phosphorylation site Thr166 promoted incorporation of mutant β-tubulin into microtubules. Taken together, these results suggest that NEK6 promotes directional cell growth through phosphorylation of β-tubulin and the resulting destabilization of cortical microtubules.",
author = "Shogo Takatani and Shinichiro Ozawa and Noriyoshi Yagi and Takashi Hotta and Takashi Hashimoto and Yuichiro Takahashi and Taku Takahashi and Hiroyasu Motose",
year = "2017",
month = "12",
day = "1",
doi = "10.1038/s41598-017-08453-5",
language = "English",
volume = "7",
journal = "Scientific Reports",
issn = "2045-2322",
publisher = "Nature Publishing Group",
number = "1",

}

TY - JOUR

T1 - Directional cell expansion requires NIMA-related kinase 6 (NEK6)-mediated cortical microtubule destabilization

AU - Takatani, Shogo

AU - Ozawa, Shinichiro

AU - Yagi, Noriyoshi

AU - Hotta, Takashi

AU - Hashimoto, Takashi

AU - Takahashi, Yuichiro

AU - Takahashi, Taku

AU - Motose, Hiroyasu

PY - 2017/12/1

Y1 - 2017/12/1

N2 - Plant cortical microtubules align perpendicular to the growth axis to determine the direction of cell growth. However, it remains unclear how plant cells form well-organized cortical microtubule arrays in the absence of a centrosome. In this study, we investigated the functions of Arabidopsis NIMA-related kinase 6 (NEK6), which regulates microtubule organization during anisotropic cell expansion. Quantitative analysis of hypocotyl cell growth in the nek6-1 mutant demonstrated that NEK6 suppresses ectopic outgrowth and promotes cell elongation in different regions of the hypocotyl. Loss of NEK6 function led to excessive microtubule waving and distortion, implying that NEK6 suppresses the aberrant cortical microtubules. Live cell imaging showed that NEK6 localizes to the microtubule lattice and to the shrinking plus and minus ends of microtubules. In agreement with this observation, the induced overexpression of NEK6 reduced and disorganized cortical microtubules and suppressed cell elongation. Furthermore, we identified five phosphorylation sites in β-tubulin that serve as substrates for NEK6 in vitro. Alanine substitution of the phosphorylation site Thr166 promoted incorporation of mutant β-tubulin into microtubules. Taken together, these results suggest that NEK6 promotes directional cell growth through phosphorylation of β-tubulin and the resulting destabilization of cortical microtubules.

AB - Plant cortical microtubules align perpendicular to the growth axis to determine the direction of cell growth. However, it remains unclear how plant cells form well-organized cortical microtubule arrays in the absence of a centrosome. In this study, we investigated the functions of Arabidopsis NIMA-related kinase 6 (NEK6), which regulates microtubule organization during anisotropic cell expansion. Quantitative analysis of hypocotyl cell growth in the nek6-1 mutant demonstrated that NEK6 suppresses ectopic outgrowth and promotes cell elongation in different regions of the hypocotyl. Loss of NEK6 function led to excessive microtubule waving and distortion, implying that NEK6 suppresses the aberrant cortical microtubules. Live cell imaging showed that NEK6 localizes to the microtubule lattice and to the shrinking plus and minus ends of microtubules. In agreement with this observation, the induced overexpression of NEK6 reduced and disorganized cortical microtubules and suppressed cell elongation. Furthermore, we identified five phosphorylation sites in β-tubulin that serve as substrates for NEK6 in vitro. Alanine substitution of the phosphorylation site Thr166 promoted incorporation of mutant β-tubulin into microtubules. Taken together, these results suggest that NEK6 promotes directional cell growth through phosphorylation of β-tubulin and the resulting destabilization of cortical microtubules.

UR - http://www.scopus.com/inward/record.url?scp=85040692601&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85040692601&partnerID=8YFLogxK

U2 - 10.1038/s41598-017-08453-5

DO - 10.1038/s41598-017-08453-5

M3 - Article

VL - 7

JO - Scientific Reports

JF - Scientific Reports

SN - 2045-2322

IS - 1

M1 - 7826

ER -