Kinesin-4 Functions in Vesicular Transport on Cortical Microtubules and Regulates Cell Wall Mechanics during Cell Elongation in Plants

Zhaosheng Kong, Motohide Ioki, Siobhan Braybrook, Shundai Li, Zheng Hua Ye, Yuh Ru Julie Lee, Takashi Hotta, Anny Chang, Juan Tian, Guangda Wang, Bo Liu

Research output: Contribution to journalArticle

35 Citations (Scopus)

Abstract

In plants, anisotropic cell expansion depends on cortical microtubules that serve as tracks along which macromolecules and vesicles are transported by the motor kinesins of unknown identities. We used cotton (Gossypium hirsutum) fibers that underwent robust elongation to discover kinesins that are involved in cell elongation and found Gh KINESIN-4A expressed abundantly. The motor was detected by immunofluorescence on vesicle-like structures that were associated with cortical microtubules. In Arabidopsis thaliana, the orthologous motor At KINESIN-4A/FRA1, previously implicated in cellulose deposition during secondary growth in fiber cells, was examined by live-cell imaging in cells expressing the fluorescently tagged functional protein. The motor decorated vesicle-like particles that exhibit a linear movement along cortical microtubules with an average velocity of 0.89 μm/min, which was significantly different from those linked to cellulose biosynthesis. We also discovered that At KINESIN-4A/FRA1 and the related At KINESIN-4C play redundant roles in cell wall mechanics, cell elongation, and the axial growth of various vegetative and reproductive organs, as the loss of At KINESIN-4C greatly enhanced the defects caused by a null mutation at the KINESIN-4A/FRA1 locus. The double mutant displayed a lack of cell wall softening at normal stages of rapid cell elongation. Furthermore, enhanced deposition of arabinose-containing carbohydrate was detected in the kinesin-4 mutants. Our findings established a connection between the Kinesin-4-based transport of cargoes containing non-cellulosic components along cortical microtubules and cell wall mechanics and cell elongation in flowering plants.

Original languageEnglish (US)
Article number67
Pages (from-to)1011-1023
Number of pages13
JournalMolecular plant
Volume8
Issue number7
DOIs
StatePublished - Jul 6 2015

Fingerprint

Kinesin
kinesin
Mechanics
mechanics
Microtubules
Cell Wall
microtubules
cell growth
cell walls
cellulose
fiber cells
mutants
Cellulose
cells
arabinose
Gossypium hirsutum
fluorescent antibody technique
vegetative growth
Angiospermae
cotton

All Science Journal Classification (ASJC) codes

  • Molecular Biology
  • Plant Science

Cite this

Kong, Zhaosheng ; Ioki, Motohide ; Braybrook, Siobhan ; Li, Shundai ; Ye, Zheng Hua ; Julie Lee, Yuh Ru ; Hotta, Takashi ; Chang, Anny ; Tian, Juan ; Wang, Guangda ; Liu, Bo. / Kinesin-4 Functions in Vesicular Transport on Cortical Microtubules and Regulates Cell Wall Mechanics during Cell Elongation in Plants. In: Molecular plant. 2015 ; Vol. 8, No. 7. pp. 1011-1023.
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abstract = "In plants, anisotropic cell expansion depends on cortical microtubules that serve as tracks along which macromolecules and vesicles are transported by the motor kinesins of unknown identities. We used cotton (Gossypium hirsutum) fibers that underwent robust elongation to discover kinesins that are involved in cell elongation and found Gh KINESIN-4A expressed abundantly. The motor was detected by immunofluorescence on vesicle-like structures that were associated with cortical microtubules. In Arabidopsis thaliana, the orthologous motor At KINESIN-4A/FRA1, previously implicated in cellulose deposition during secondary growth in fiber cells, was examined by live-cell imaging in cells expressing the fluorescently tagged functional protein. The motor decorated vesicle-like particles that exhibit a linear movement along cortical microtubules with an average velocity of 0.89 μm/min, which was significantly different from those linked to cellulose biosynthesis. We also discovered that At KINESIN-4A/FRA1 and the related At KINESIN-4C play redundant roles in cell wall mechanics, cell elongation, and the axial growth of various vegetative and reproductive organs, as the loss of At KINESIN-4C greatly enhanced the defects caused by a null mutation at the KINESIN-4A/FRA1 locus. The double mutant displayed a lack of cell wall softening at normal stages of rapid cell elongation. Furthermore, enhanced deposition of arabinose-containing carbohydrate was detected in the kinesin-4 mutants. Our findings established a connection between the Kinesin-4-based transport of cargoes containing non-cellulosic components along cortical microtubules and cell wall mechanics and cell elongation in flowering plants.",
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Kong, Z, Ioki, M, Braybrook, S, Li, S, Ye, ZH, Julie Lee, YR, Hotta, T, Chang, A, Tian, J, Wang, G & Liu, B 2015, 'Kinesin-4 Functions in Vesicular Transport on Cortical Microtubules and Regulates Cell Wall Mechanics during Cell Elongation in Plants', Molecular plant, vol. 8, no. 7, 67, pp. 1011-1023. https://doi.org/10.1016/j.molp.2015.01.004

Kinesin-4 Functions in Vesicular Transport on Cortical Microtubules and Regulates Cell Wall Mechanics during Cell Elongation in Plants. / Kong, Zhaosheng; Ioki, Motohide; Braybrook, Siobhan; Li, Shundai; Ye, Zheng Hua; Julie Lee, Yuh Ru; Hotta, Takashi; Chang, Anny; Tian, Juan; Wang, Guangda; Liu, Bo.

In: Molecular plant, Vol. 8, No. 7, 67, 06.07.2015, p. 1011-1023.

Research output: Contribution to journalArticle

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AU - Kong, Zhaosheng

AU - Ioki, Motohide

AU - Braybrook, Siobhan

AU - Li, Shundai

AU - Ye, Zheng Hua

AU - Julie Lee, Yuh Ru

AU - Hotta, Takashi

AU - Chang, Anny

AU - Tian, Juan

AU - Wang, Guangda

AU - Liu, Bo

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