How selective severing by katanin promotes order in the plant cortical microtubule array
File(s)
Published version
OA Location
Author(s)
Deinum, EE
Tindemans, SH
Lindeboom, JJ
Mulder, BM
Type
Journal Article
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 identi-
fied 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.
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 identi-
fied 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.
Date Issued
2017-07-03
Date Acceptance
2017-05-09
Citation
Proceedings of the National Academy of Sciences of the United States of America, 2017, 114 (27), pp.6942-6947
ISSN
0027-8424
Publisher
National Academy of Sciences
Start Page
6942
End Page
6947
Journal / Book Title
Proceedings of the National Academy of Sciences of the United States of America
Volume
114
Issue
27
Copyright Statement
Freely available online through the PNAS open access option.
Subjects
Science & Technology
Multidisciplinary Sciences
Science & Technology - Other Topics
katanin
cortical microtubule array
microtubule dynamics
self-organization
plant cell biology
SELF-ORGANIZATION
PLASMA-MEMBRANE
IN-VITRO
ARABIDOPSIS
ORIENTATION
DYNAMICS
MECHANISMS
INITIATION
ALIGNMENT
BEHAVIOR
MD Multidisciplinary