Microtubule flexibility, microtubule-based nucleation and ROP pattern co-alignment enhance protoxylem microtubule patterning

The development of the water transporting xylem tissue in plants involves an intricate interplay of Rho-of-Plants (ROP) proteins and cortical microtubules to generate highly functional secondary cell wall patterns, such as the ringed or spiral patterns in early-developing protoxylem. We study the re...

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Main Authors: Bas Jacobs, Marco Saltini, Jaap Molenaar, Laura Filion, Eva E. Deinum
Format: Article
Language:English
Published: Cambridge University Press 2025-01-01
Series:Quantitative Plant Biology
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Online Access:https://www.cambridge.org/core/product/identifier/S2632882824000171/type/journal_article
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author Bas Jacobs
Marco Saltini
Jaap Molenaar
Laura Filion
Eva E. Deinum
author_facet Bas Jacobs
Marco Saltini
Jaap Molenaar
Laura Filion
Eva E. Deinum
author_sort Bas Jacobs
collection DOAJ
description The development of the water transporting xylem tissue in plants involves an intricate interplay of Rho-of-Plants (ROP) proteins and cortical microtubules to generate highly functional secondary cell wall patterns, such as the ringed or spiral patterns in early-developing protoxylem. We study the requirements of protoxylem microtubule band formation with simulations in CorticalSim, extended to include finite microtubule persistence length and a novel algorithm for microtubule-based nucleation. We find that microtubule flexibility facilitates pattern formation for all realistic degrees of mismatch between array and pattern orientation. At the same time, flexibility leads to more density loss, both from collisions and the microtubule-hostile gap regions, making it harder to maintain microtubule bands. Microtubule-dependent nucleation helps to counteract this effect by gradually shifting nucleation from the gap regions to the bands as microtubules disappear from the gaps. Our results reveal mechanisms that can result in robust protoxylem band formation.
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institution Kabale University
issn 2632-8828
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publishDate 2025-01-01
publisher Cambridge University Press
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series Quantitative Plant Biology
spelling doaj-art-ab6824ce8661427e845cb7bb856c6c702025-01-27T11:46:38ZengCambridge University PressQuantitative Plant Biology2632-88282025-01-01610.1017/qpb.2024.17Microtubule flexibility, microtubule-based nucleation and ROP pattern co-alignment enhance protoxylem microtubule patterningBas Jacobs0Marco Saltini1https://orcid.org/0000-0002-5425-9101Jaap Molenaar2Laura Filion3Eva E. Deinum4https://orcid.org/0000-0001-8564-200XMathematical and Statistical Methods (Biometris), Plant Science Group, Wageningen University & Research, Wageningen, 6708 PB, The NetherlandsMathematical and Statistical Methods (Biometris), Plant Science Group, Wageningen University & Research, Wageningen, 6708 PB, The NetherlandsMathematical and Statistical Methods (Biometris), Plant Science Group, Wageningen University & Research, Wageningen, 6708 PB, The NetherlandsSoft Condensed Matter and Biophysics Group, Debye Institute for Nanomaterials Science, Utrecht University, Utrecht, 3584 CC, The NetherlandsMathematical and Statistical Methods (Biometris), Plant Science Group, Wageningen University & Research, Wageningen, 6708 PB, The NetherlandsThe development of the water transporting xylem tissue in plants involves an intricate interplay of Rho-of-Plants (ROP) proteins and cortical microtubules to generate highly functional secondary cell wall patterns, such as the ringed or spiral patterns in early-developing protoxylem. We study the requirements of protoxylem microtubule band formation with simulations in CorticalSim, extended to include finite microtubule persistence length and a novel algorithm for microtubule-based nucleation. We find that microtubule flexibility facilitates pattern formation for all realistic degrees of mismatch between array and pattern orientation. At the same time, flexibility leads to more density loss, both from collisions and the microtubule-hostile gap regions, making it harder to maintain microtubule bands. Microtubule-dependent nucleation helps to counteract this effect by gradually shifting nucleation from the gap regions to the bands as microtubules disappear from the gaps. Our results reveal mechanisms that can result in robust protoxylem band formation.https://www.cambridge.org/core/product/identifier/S2632882824000171/type/journal_articlemicrotubule nucleationmicrotubule persistence lengthplant cortical microtubulesprotoxylemstochastic simulation
spellingShingle Bas Jacobs
Marco Saltini
Jaap Molenaar
Laura Filion
Eva E. Deinum
Microtubule flexibility, microtubule-based nucleation and ROP pattern co-alignment enhance protoxylem microtubule patterning
Quantitative Plant Biology
microtubule nucleation
microtubule persistence length
plant cortical microtubules
protoxylem
stochastic simulation
title Microtubule flexibility, microtubule-based nucleation and ROP pattern co-alignment enhance protoxylem microtubule patterning
title_full Microtubule flexibility, microtubule-based nucleation and ROP pattern co-alignment enhance protoxylem microtubule patterning
title_fullStr Microtubule flexibility, microtubule-based nucleation and ROP pattern co-alignment enhance protoxylem microtubule patterning
title_full_unstemmed Microtubule flexibility, microtubule-based nucleation and ROP pattern co-alignment enhance protoxylem microtubule patterning
title_short Microtubule flexibility, microtubule-based nucleation and ROP pattern co-alignment enhance protoxylem microtubule patterning
title_sort microtubule flexibility microtubule based nucleation and rop pattern co alignment enhance protoxylem microtubule patterning
topic microtubule nucleation
microtubule persistence length
plant cortical microtubules
protoxylem
stochastic simulation
url https://www.cambridge.org/core/product/identifier/S2632882824000171/type/journal_article
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AT jaapmolenaar microtubuleflexibilitymicrotubulebasednucleationandroppatterncoalignmentenhanceprotoxylemmicrotubulepatterning
AT laurafilion microtubuleflexibilitymicrotubulebasednucleationandroppatterncoalignmentenhanceprotoxylemmicrotubulepatterning
AT evaedeinum microtubuleflexibilitymicrotubulebasednucleationandroppatterncoalignmentenhanceprotoxylemmicrotubulepatterning