Plant cortical microtubule dynamics and cell division plane orientation

Chakrabortty, Bandan

doi:10.18174/413054

Cited by 2 publications

(5 citation statements)

References 114 publications

(225 reference statements)

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“…The "group A" TPX2/TPXL proteins are ideal, though currently speculative, candidates for supporting preprophase band formation this way, as they are indicated in the recruitment of nucleation complexes to microtubules [69] and contain a nuclear importin domain [70], which could provide the correct perinuclear positioning of a high nucleation zone upon release. Simulations show that concentrating microtubule nucleation to the future band region can indeed reproduce a preprophase band-like structure [71].…”

Section: Discussionmentioning

confidence: 94%

Nucleation complex behaviour is critical for cortical microtubule array homogeneity and patterning

Jacobs¹,

Schneider

Molenaar³

et al. 2022

Preprint

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Plant cell walls are versatile materials that can adopt a wide range of mechanical properties through controlled deposition of cellulose fibrils. Wall integrity requires a sufficiently homogeneous fibril distribution to cope effectively with wall stresses. Additionally, specific conditions, such as the negative pressure in water transporting xylem vessels, may require more complex wall patterns, e.g., bands in protoxylem. The orientation and patterning of cellulose fibrils is guided by dynamic cortical microtubules. New microtubules are predominantly nucleated from parent microtubules causing positive feedback on local microtubule density with the potential to yield highly inhomogeneous patterns. Inhomogeneity indeed appears in all current cortical array simulations that include microtubule-based nucleation, suggesting that plant cells must possess an as-yet unknown balancing mechanism to prevent it. Here, in a combined simulation and experimental approach, we show that the naturally limited local recruitment of nucleation complexes to microtubules can counter the positive feedback, whereas local tubulin depletion cannot. We observe that nucleation complexes are preferentially inserted at microtubules. By incorporating our experimental findings in stochastic simulations, we find that the spatial behaviour of nucleation complexes delicately balances the positive feedback, such that differences in local microtubule dynamics -- as in developing protoxylem -- can quickly turn a homogeneous array into a patterned one. Our results provide insight into how the plant cytoskeleton is wired to meet diverse mechanical requirements and greatly increase the predictive power of computational cell biology studies.

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Section: Discussionmentioning

confidence: 94%

Nucleation complex behaviour is critical for cortical microtubule array homogeneity and patterning

Jacobs¹,

Schneider

Molenaar³

et al. 2022

Preprint

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show abstract

“…The "group A" TPX2/TPXL proteins are ideal, though currently speculative, candidates for supporting preprophase band formation this way, as they are indicated in the recruitment of nucleation complexes to microtubules [230] and contain a nuclear importin domain [231], which could provide the correct perinuclear positioning of a high nucleation zone upon release. Simulations show that concentrating microtubule nucleation to the future band region can indeed reproduce a preprophase band-like structure [145].…”

Section: Discussionmentioning

confidence: 94%

“…In that case, katanin severing can become a way of amplifying discordant microtubules, kickstarting the reorientation of the microtubule array [31,[141][142][143][144]. Models have also provided insight into other aspects of microtubule self-organisation, including selection of the cell division plane [42], formation of the preprophase band [145], and feedback from cell shape [125,127].…”

Section: Microtubule Self-organisationmentioning

confidence: 99%

“…This specific localisation suggests involvement of factors from the nucleus in the positioning of the preprophase band. In simulations, a single microtubule band in the right location could be formed by increasing the local nucleation rate at the future band site [145]. Such an increase could be achieved, for example, by a sudden release of nucleation factors from the nucleus.…”

Section: Cortical Array Homogeneity and Nucleationmentioning

confidence: 99%

“…Models of the plant cortical microtubule array have thus far focused on a variety of properties, including alignment [134][135][136][137][138]160], orientation [42,124,126,127], re-orientation [142,143], homogeneity (chapter 4), and the formation of specific structures like the patterned protoxylem array ( [33] and chapters 4 and 5), and the preprophase band [145]. The microtubule densities that are achieved in the process, however, are often disregarded and not explicitly reported.…”

Section: Microtubule Densitymentioning

confidence: 99%

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Exploring mechanisms of xylem cell wall patterning with dynamic models

Jacobs

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Contents 1 General introduction 1.1 Xylem cell wall patterning 1.2 Pattern formation mechanisms 1.2.1 Reaction-diffusion mechanisms 1.2.2 Not every pattern is a Turing pattern 1.3 Small GTPases 1.3.1 Small GTPases in reaction-diffusion systems 1.3.2 Mass conservation 1.4 Microtubules 1.4.1 Microtubule properties 1.4.2 Microtubules and cell wall structure 1.4.3 Microtubule self-organisation 1.5 ROPs and microtubules in xylem patterning 1.6 Aim and thesis outline 3.7.3 Effect of alternative anisotropic diffusion scenarios 3.7.4 Diffusion tensor rotation 3.7.5 Preferred spiral angles 3.7.6 Diffusion term decomposition 3.7.7 Parameters of models with ROP-dependent ROP diffusion 4 The role of nucleation complexes in cortical microtubule array homogeneity and patterning 4.1 Introduction 4.2 Results 4.2.1 A simplified model of transversely oriented microtubules reproduces the inhomogeneity problem 4.2.2 Tubulin diffusion is too fast for sufficient local variation in microtubule growth velocities 4.2.3 Nucleation complexes are preferentially inserted at microtubules 4.2.4 Local limitation of nucleation complexes can solve the inhomogeneity problem 4.3 Discussion 4.4 Methods 4.4.1 Simulation setup 4.4.2 Core microtubule dynamics 4.4.3 Protoxylem band and gap regions 4.4.4 Basic nucleation modes 4.4.5 Tubulin dynamics 4.4.6 Nucleation complexes 4.4.7 Model parameters 4.4.8 Measures of heterogeneity 4.4.9 Experimental measurements 4.5 Supplementary figures 4.6 Supplementary tables 4.7 Appendices 4.7.1 Steady state densities for non-interacting microtubules 4.7.2 Calculating maximal total microtubule length and initial growth speed 4.7.3 Estimation of nucleation complex parameters 5 Protoxylem microtubule patterning requires ROP pattern co-alignment, realistic microtubule-based nucleation, and sufficient microtubule flexibility 5.1 Introduction 5.2 Results 5.2.1 Model outline 5.2.2 Strong co-alignment of the microtubule array with a pre-existing band pattern facilitates rapid microtubule band formation 5.2.3 Microtubule flexibility can lead to density loss from bands 5.2.4 Locally saturating nucleation helps to keep bands populated with semiflexible microtubules, even for misaligned starting arrays viii CONTENTS 5.2.5 Array patterning must be robust against large variations in observed microtubule dynamics 5.2.6 Band-gap separation factors outside the measured parameter differences 5.3 Discussion 5.4 Methods 5.4.1 Simulation setup 5.4.2 Nucleation modes 5.4.3 Expected mismatch angles 5.4.4 Semiflexible microtubules 5.4.5 Cell data simulations 5.4.6 Summary statistics 5.5 Supplementary figures 5.6 Appendices 5.6.1 Parameters for locally saturating nucleation 5.6.2 Persistence length calculations 6 General discussion 6.1 Insights into mechanisms of xylem patterning 6.1.1 A ROP-based Turing pattern as the basis of xylem patterning 6.1.2 Protoxylem ROP pattern orientation 6.1.3 Coexistence in ROP and microtubule patterns 6.1.4 ROP-microtubule interplay 6.2 Insights into non-xylem membrane patterning 6.2.1 Coexistence in non-xyle...

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Plant cortical microtubule dynamics and cell division plane orientation

Cited by 2 publications

References 114 publications

Nucleation complex behaviour is critical for cortical microtubule array homogeneity and patterning

Nucleation complex behaviour is critical for cortical microtubule array homogeneity and patterning

Exploring mechanisms of xylem cell wall patterning with dynamic models

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