Cortical microtubule arrays are initiated from a nonrandom prepattern driven by atypical microtubule initiation

J.J. Lindeboom, A. Lioutas, E.E. Deinum, S. Tindemans, D.W. Ehrhardt, A.M.C. Emons, B. Mulder

Research output: Contribution to journalArticleAcademicpeer-review

19 Citations (Scopus)

Abstract

The ordered arrangement of cortical microtubules in growing plant cells is essential for anisotropic cell expansion and, hence, for plant morphogenesis. These arrays are dismantled when the microtubule cytoskeleton is rearranged during mitosis and reassembled following completion of cytokinesis. The reassembly of the cortical array has often been considered as initiating from a state of randomness, from which order arises at least partly through self-organizing mechanisms. However, some studies have shown evidence for ordering at early stages of array assembly. To investigate how cortical arrays are initiated in higher plant cells, we performed live-cell imaging studies of cortical array assembly in tobacco (Nicotiana tabacum) Bright Yellow-2 cells after cytokinesis and drug-induced disassembly. We found that cortical arrays in both cases did not initiate randomly but with a significant overrepresentation of microtubules at diagonal angles with respect to the cell axis, which coincides with the predominant orientation of the microtubules before their disappearance from the cell cortex in preprophase. In Arabidopsis (Arabidopsis thaliana) root cells, recovery from drug-induced disassembly was also nonrandom and correlated with the organization of the previous array, although no diagonal bias was observed in these cells. Surprisingly, during initiation, only about one-half of the new microtubules were nucleated from locations marked by green fluorescent protein-¿-tubulin complex protein2-tagged ¿-nucleation complexes (¿-tubulin ring complex), therefore indicating that a large proportion of early polymers was initiated by a noncanonical mechanism not involving ¿-tubulin ring complex. Simulation studies indicate that the high rate of noncanonical initiation of new microtubules has the potential to accelerate the rate of array repopulation.
LanguageEnglish
Pages1189-1201
JournalPlant Physiology
Volume161
Issue number3
DOIs
Publication statusPublished - 2013

Fingerprint

Microtubules
microtubules
cells
Cytokinesis
Plant Cells
Tubulin
Arabidopsis
Tobacco
cytokinesis
tubulin
Plant Development
Green Fluorescent Proteins
Cytoskeleton
drugs
Mitosis
Pharmaceutical Preparations
Polymers
cytoskeleton
green fluorescent protein
Nicotiana tabacum

Keywords

  • plant-cells
  • nitella-tasmanica
  • self-organization
  • gamma-tubulin
  • arabidopsis
  • nucleation
  • mechanism
  • orientation
  • dynamics
  • reveals

Cite this

Lindeboom, J.J. ; Lioutas, A. ; Deinum, E.E. ; Tindemans, S. ; Ehrhardt, D.W. ; Emons, A.M.C. ; Mulder, B. / Cortical microtubule arrays are initiated from a nonrandom prepattern driven by atypical microtubule initiation. In: Plant Physiology. 2013 ; Vol. 161, No. 3. pp. 1189-1201.
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abstract = "The ordered arrangement of cortical microtubules in growing plant cells is essential for anisotropic cell expansion and, hence, for plant morphogenesis. These arrays are dismantled when the microtubule cytoskeleton is rearranged during mitosis and reassembled following completion of cytokinesis. The reassembly of the cortical array has often been considered as initiating from a state of randomness, from which order arises at least partly through self-organizing mechanisms. However, some studies have shown evidence for ordering at early stages of array assembly. To investigate how cortical arrays are initiated in higher plant cells, we performed live-cell imaging studies of cortical array assembly in tobacco (Nicotiana tabacum) Bright Yellow-2 cells after cytokinesis and drug-induced disassembly. We found that cortical arrays in both cases did not initiate randomly but with a significant overrepresentation of microtubules at diagonal angles with respect to the cell axis, which coincides with the predominant orientation of the microtubules before their disappearance from the cell cortex in preprophase. In Arabidopsis (Arabidopsis thaliana) root cells, recovery from drug-induced disassembly was also nonrandom and correlated with the organization of the previous array, although no diagonal bias was observed in these cells. Surprisingly, during initiation, only about one-half of the new microtubules were nucleated from locations marked by green fluorescent protein-¿-tubulin complex protein2-tagged ¿-nucleation complexes (¿-tubulin ring complex), therefore indicating that a large proportion of early polymers was initiated by a noncanonical mechanism not involving ¿-tubulin ring complex. Simulation studies indicate that the high rate of noncanonical initiation of new microtubules has the potential to accelerate the rate of array repopulation.",
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Cortical microtubule arrays are initiated from a nonrandom prepattern driven by atypical microtubule initiation. / Lindeboom, J.J.; Lioutas, A.; Deinum, E.E.; Tindemans, S.; Ehrhardt, D.W.; Emons, A.M.C.; Mulder, B.

In: Plant Physiology, Vol. 161, No. 3, 2013, p. 1189-1201.

Research output: Contribution to journalArticleAcademicpeer-review

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T1 - Cortical microtubule arrays are initiated from a nonrandom prepattern driven by atypical microtubule initiation

AU - Lindeboom, J.J.

AU - Lioutas, A.

AU - Deinum, E.E.

AU - Tindemans, S.

AU - Ehrhardt, D.W.

AU - Emons, A.M.C.

AU - Mulder, B.

PY - 2013

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N2 - The ordered arrangement of cortical microtubules in growing plant cells is essential for anisotropic cell expansion and, hence, for plant morphogenesis. These arrays are dismantled when the microtubule cytoskeleton is rearranged during mitosis and reassembled following completion of cytokinesis. The reassembly of the cortical array has often been considered as initiating from a state of randomness, from which order arises at least partly through self-organizing mechanisms. However, some studies have shown evidence for ordering at early stages of array assembly. To investigate how cortical arrays are initiated in higher plant cells, we performed live-cell imaging studies of cortical array assembly in tobacco (Nicotiana tabacum) Bright Yellow-2 cells after cytokinesis and drug-induced disassembly. We found that cortical arrays in both cases did not initiate randomly but with a significant overrepresentation of microtubules at diagonal angles with respect to the cell axis, which coincides with the predominant orientation of the microtubules before their disappearance from the cell cortex in preprophase. In Arabidopsis (Arabidopsis thaliana) root cells, recovery from drug-induced disassembly was also nonrandom and correlated with the organization of the previous array, although no diagonal bias was observed in these cells. Surprisingly, during initiation, only about one-half of the new microtubules were nucleated from locations marked by green fluorescent protein-¿-tubulin complex protein2-tagged ¿-nucleation complexes (¿-tubulin ring complex), therefore indicating that a large proportion of early polymers was initiated by a noncanonical mechanism not involving ¿-tubulin ring complex. Simulation studies indicate that the high rate of noncanonical initiation of new microtubules has the potential to accelerate the rate of array repopulation.

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KW - nitella-tasmanica

KW - self-organization

KW - gamma-tubulin

KW - arabidopsis

KW - nucleation

KW - mechanism

KW - orientation

KW - dynamics

KW - reveals

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DO - 10.1104/pp.112.204057

M3 - Article

VL - 161

SP - 1189

EP - 1201

JO - Plant Physiology

T2 - Plant Physiology

JF - Plant Physiology

SN - 0032-0889

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ER -