Literature DB >> 28630321

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

Eva E Deinum1,2, Simon H Tindemans2, Jelmer J Lindeboom3, Bela M Mulder2,4.   

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.

Keywords:  cortical microtubule array; katanin; microtubule dynamics; plant cell biology; self-organization

Mesh:

Substances:

Year:  2017        PMID: 28630321      PMCID: PMC5502621          DOI: 10.1073/pnas.1702650114

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  39 in total

1.  Survival of the aligned: ordering of the plant cortical microtubule array.

Authors:  Simon H Tindemans; Rhoda J Hawkins; Bela M Mulder
Journal:  Phys Rev Lett       Date:  2010-02-05       Impact factor: 9.161

Review 2.  Straighten up and fly right: microtubule dynamics and organization of non-centrosomal arrays in higher plants.

Authors:  David W Ehrhardt
Journal:  Curr Opin Cell Biol       Date:  2008-02       Impact factor: 8.382

3.  Developmental patterning by mechanical signals in Arabidopsis.

Authors:  Olivier Hamant; Marcus G Heisler; Henrik Jönsson; Pawel Krupinski; Magalie Uyttewaal; Plamen Bokov; Francis Corson; Patrik Sahlin; Arezki Boudaoud; Elliot M Meyerowitz; Yves Couder; Jan Traas
Journal:  Science       Date:  2008-12-12       Impact factor: 47.728

Review 4.  Modelling the role of microtubules in plant cell morphology.

Authors:  Eva E Deinum; Bela M Mulder
Journal:  Curr Opin Plant Biol       Date:  2013-10-21       Impact factor: 7.834

5.  Microtubule severing at crossover sites by katanin generates ordered cortical microtubule arrays in Arabidopsis.

Authors:  Quan Zhang; Erica Fishel; Tyler Bertroche; Ram Dixit
Journal:  Curr Biol       Date:  2013-10-24       Impact factor: 10.834

Review 6.  Cortical structure and function in euglenoids with reference to trypanosomes, ciliates, and dinoflagellates.

Authors:  G B Bouck; H Ngô
Journal:  Int Rev Cytol       Date:  1996

7.  A transient array of parallel microtubules in frog eggs: potential tracks for a cytoplasmic rotation that specifies the dorso-ventral axis.

Authors:  R P Elinson; B Rowning
Journal:  Dev Biol       Date:  1988-07       Impact factor: 3.582

8.  A three-dimensional computer simulation model reveals the mechanisms for self-organization of plant cortical microtubules into oblique arrays.

Authors:  Ezgi Can Eren; Ram Dixit; Natarajan Gautam
Journal:  Mol Biol Cell       Date:  2010-06-02       Impact factor: 4.138

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

Authors:  Jelmer J Lindeboom; Antonios Lioutas; Eva E Deinum; Simon H Tindemans; David W Ehrhardt; Anne Mie C Emons; Jan W Vos; Bela M Mulder
Journal:  Plant Physiol       Date:  2013-01-08       Impact factor: 8.340

10.  Self-organization of an acentrosomal microtubule network at the basal cortex of polarized epithelial cells.

Authors:  Amy Reilein; Soichiro Yamada; W James Nelson
Journal:  J Cell Biol       Date:  2005-11-28       Impact factor: 10.539

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  8 in total

Review 1.  The microtubule cytoskeleton acts as a sensor for stress response signaling in plants.

Authors:  Huixian Ma; Min Liu
Journal:  Mol Biol Rep       Date:  2019-05-16       Impact factor: 2.316

Review 2.  Katanin: A Sword Cutting Microtubules for Cellular, Developmental, and Physiological Purposes.

Authors:  Ivan Luptovčiak; George Komis; Tomáš Takáč; Miroslav Ovečka; Jozef Šamaj
Journal:  Front Plant Sci       Date:  2017-11-21       Impact factor: 5.753

3.  The self-organization of plant microtubules inside the cell volume yields their cortical localization, stable alignment, and sensitivity to external cues.

Authors:  Vincent Mirabet; Pawel Krupinski; Olivier Hamant; Elliot M Meyerowitz; Henrik Jönsson; Arezki Boudaoud
Journal:  PLoS Comput Biol       Date:  2018-02-20       Impact factor: 4.475

4.  Long-term single-cell imaging and simulations of microtubules reveal principles behind wall patterning during proto-xylem development.

Authors:  René Schneider; Kris Van't Klooster; Kelsey L Picard; Jasper van der Gucht; Taku Demura; Marcel Janson; Arun Sampathkumar; Eva E Deinum; Tijs Ketelaar; Staffan Persson
Journal:  Nat Commun       Date:  2021-01-28       Impact factor: 14.919

5.  A phosphoinositide map at the shoot apical meristem in Arabidopsis thaliana.

Authors:  Thomas Stanislas; Matthieu Pierre Platre; Mengying Liu; Léa E S Rambaud-Lavigne; Yvon Jaillais; Olivier Hamant
Journal:  BMC Biol       Date:  2018-02-07       Impact factor: 7.431

6.  A computational framework for cortical microtubule dynamics in realistically shaped plant cells.

Authors:  Bandan Chakrabortty; Ikram Blilou; Ben Scheres; Bela M Mulder
Journal:  PLoS Comput Biol       Date:  2018-02-02       Impact factor: 4.475

7.  Spastin is a dual-function enzyme that severs microtubules and promotes their regrowth to increase the number and mass of microtubules.

Authors:  Yin-Wei Kuo; Olivier Trottier; Mohammed Mahamdeh; Jonathon Howard
Journal:  Proc Natl Acad Sci U S A       Date:  2019-03-05       Impact factor: 11.205

Review 8.  Cutting, Amplifying, and Aligning Microtubules with Severing Enzymes.

Authors:  Yin-Wei Kuo; Jonathon Howard
Journal:  Trends Cell Biol       Date:  2020-11-09       Impact factor: 21.167

  8 in total

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