How selective severing by katanin promotes order in the plant cortical microtubule array

Eva E. Deinum*, Simon H. Tindemans, J. Lindeboom, Bela M. Mulder

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

14 Citations (Scopus)

Abstract

Plant morphogenesis requires differential and often asymmetric growth. A key role in controlling anisotropic expansion of individual cells is played by the cortical microtubule array. Although highly organized, the array can nevertheless rapidly change in response to internal and external cues. Experiments have identified the microtubule-severing enzyme katanin as a central player in controlling the organizational state of the array. Katanin action is required both for normal alignment and the adaptation of array orientation to mechanical, environmental, and developmental stimuli. How katanin fulfills its controlling role, however, remains poorly understood. On the one hand, from a theoretical perspective, array ordering depends on the "weeding out" of discordant microtubules through frequent catastrophe-inducing collisions among microtubules. Severing would reduce average microtubule length and lifetime, and consequently weaken the driving force for alignment. On the other hand, it has been suggested that selective severing at microtubule crossovers could facilitate the removal of discordant microtubules. Here we show that this apparent conflict can be resolved by systematically dissecting the role of all of the relevant interactions in silico. This procedure allows the identification of the sufficient and necessary conditions for katanin to promote array alignment, stresses the critical importance of the experimentally observed selective severing of the "crossing" microtubule at crossovers, and reveals a hitherto not appreciated role for microtubule bundling. We show how understanding the underlying mechanism can aid with interpreting experimental results and designing future experiments.

Original languageEnglish
Pages (from-to)6942-6947
JournalProceedings of the National Academy of Sciences of the United States of America
Volume114
Issue number27
DOIs
Publication statusPublished - 2017

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Microtubules
katanin
Plant Development
Computer Simulation
Cues
Enzymes
Growth

Keywords

  • Cortical microtubule array
  • Katanin
  • Microtubule dynamics
  • Plant cell biology
  • Self-organization

Cite this

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title = "How selective severing by katanin promotes order in the plant cortical microtubule array",
abstract = "Plant morphogenesis requires differential and often asymmetric growth. A key role in controlling anisotropic expansion of individual cells is played by the cortical microtubule array. Although highly organized, the array can nevertheless rapidly change in response to internal and external cues. Experiments have identified the microtubule-severing enzyme katanin as a central player in controlling the organizational state of the array. Katanin action is required both for normal alignment and the adaptation of array orientation to mechanical, environmental, and developmental stimuli. How katanin fulfills its controlling role, however, remains poorly understood. On the one hand, from a theoretical perspective, array ordering depends on the {"}weeding out{"} of discordant microtubules through frequent catastrophe-inducing collisions among microtubules. Severing would reduce average microtubule length and lifetime, and consequently weaken the driving force for alignment. On the other hand, it has been suggested that selective severing at microtubule crossovers could facilitate the removal of discordant microtubules. Here we show that this apparent conflict can be resolved by systematically dissecting the role of all of the relevant interactions in silico. This procedure allows the identification of the sufficient and necessary conditions for katanin to promote array alignment, stresses the critical importance of the experimentally observed selective severing of the {"}crossing{"} microtubule at crossovers, and reveals a hitherto not appreciated role for microtubule bundling. We show how understanding the underlying mechanism can aid with interpreting experimental results and designing future experiments.",
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author = "Deinum, {Eva E.} and Tindemans, {Simon H.} and J. Lindeboom and Mulder, {Bela M.}",
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How selective severing by katanin promotes order in the plant cortical microtubule array. / Deinum, Eva E.; Tindemans, Simon H.; Lindeboom, J.; Mulder, Bela M.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 114, No. 27, 2017, p. 6942-6947.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - How selective severing by katanin promotes order in the plant cortical microtubule array

AU - Deinum, Eva E.

AU - Tindemans, Simon H.

AU - Lindeboom, J.

AU - Mulder, Bela M.

PY - 2017

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N2 - Plant morphogenesis requires differential and often asymmetric growth. A key role in controlling anisotropic expansion of individual cells is played by the cortical microtubule array. Although highly organized, the array can nevertheless rapidly change in response to internal and external cues. Experiments have identified the microtubule-severing enzyme katanin as a central player in controlling the organizational state of the array. Katanin action is required both for normal alignment and the adaptation of array orientation to mechanical, environmental, and developmental stimuli. How katanin fulfills its controlling role, however, remains poorly understood. On the one hand, from a theoretical perspective, array ordering depends on the "weeding out" of discordant microtubules through frequent catastrophe-inducing collisions among microtubules. Severing would reduce average microtubule length and lifetime, and consequently weaken the driving force for alignment. On the other hand, it has been suggested that selective severing at microtubule crossovers could facilitate the removal of discordant microtubules. Here we show that this apparent conflict can be resolved by systematically dissecting the role of all of the relevant interactions in silico. This procedure allows the identification of the sufficient and necessary conditions for katanin to promote array alignment, stresses the critical importance of the experimentally observed selective severing of the "crossing" microtubule at crossovers, and reveals a hitherto not appreciated role for microtubule bundling. We show how understanding the underlying mechanism can aid with interpreting experimental results and designing future experiments.

AB - Plant morphogenesis requires differential and often asymmetric growth. A key role in controlling anisotropic expansion of individual cells is played by the cortical microtubule array. Although highly organized, the array can nevertheless rapidly change in response to internal and external cues. Experiments have identified the microtubule-severing enzyme katanin as a central player in controlling the organizational state of the array. Katanin action is required both for normal alignment and the adaptation of array orientation to mechanical, environmental, and developmental stimuli. How katanin fulfills its controlling role, however, remains poorly understood. On the one hand, from a theoretical perspective, array ordering depends on the "weeding out" of discordant microtubules through frequent catastrophe-inducing collisions among microtubules. Severing would reduce average microtubule length and lifetime, and consequently weaken the driving force for alignment. On the other hand, it has been suggested that selective severing at microtubule crossovers could facilitate the removal of discordant microtubules. Here we show that this apparent conflict can be resolved by systematically dissecting the role of all of the relevant interactions in silico. This procedure allows the identification of the sufficient and necessary conditions for katanin to promote array alignment, stresses the critical importance of the experimentally observed selective severing of the "crossing" microtubule at crossovers, and reveals a hitherto not appreciated role for microtubule bundling. We show how understanding the underlying mechanism can aid with interpreting experimental results and designing future experiments.

KW - Cortical microtubule array

KW - Katanin

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KW - Self-organization

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