Microtubule Response to Tensile Stress Is Curbed by NEK6 to Buffer Growth Variation in the Arabidopsis Hypocotyl

Takatani, Shogo; Verger, Stéphane; Okamoto, Takashi; Takahashi, Taku; Hamant, Olivier; Motose, Hiroyasu

doi:10.1016/j.cub.2020.02.024

Cited by 41 publications

(51 citation statements)

References 70 publications

(114 reference statements)

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“…Nastic movement of leaves and stems further suggest that variations in the mechanical status of the plant are subcircadian (30). The analysis of hypocotyl growth also suggests that shorter period fluctuations exist in Arabidopsis seedlings, from which our protoplasts were extracted (31). Last, the calcium waves at the shoot apical meristem, every 10-30 min, may indicate that mechanical fluctuations in plant tissues are underestimated (32).…”

Section: Discussionmentioning

confidence: 93%

Cortical tension overrides geometrical cues to orient microtubules in confined protoplasts

Colin

Chevallier

Tsugawa

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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In plant cells, cortical microtubules (CMTs) generally control morphogenesis by guiding cellulose synthesis. CMT alignment has been proposed to depend on geometrical cues, with microtubules aligning with the cell long axis in silico and in vitro. Yet, CMTs are usually transverse in vivo, i.e., along predicted maximal tension, which is transverse for cylindrical pressurized vessels. Here, we adapted a microwell setup to test these predictions in a single-cell system. We confined protoplasts laterally to impose a curvature ratio and modulated pressurization through osmotic changes. We find that CMTs can be longitudinal or transverse in wallless protoplasts and that the switch in CMT orientation depends on pressurization. In particular, longitudinal CMTs become transverse when cortical tension increases. This explains the dual behavior of CMTs in planta: CMTs become longitudinal when stress levels become low, while stable transverse CMT alignments in tissues result from their autonomous response to tensile stress fluctuations.

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Section: Discussionmentioning

confidence: 93%

Cortical tension overrides geometrical cues to orient microtubules in confined protoplasts

Colin

Chevallier

Tsugawa

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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“…To confirm that such shape descriptors are pertinent, and knowing that cortical microtubules are well-known pavement cell shape regulators, we used mutants with microtubule defects as positive controls. We performed the same analysis on mutants with a reported enhanced microtubule response to stress ( nek6 (Takatani et al, 2020)) and a reported reduced response to stress ( bot1 (Uyttewaal et al, 2012). We also included lines with tubulin mutations affecting microtubule dynamics ( tua3 D205N , tua4 S178Δ , and tua6 A281T referred as tua3 , tua4 and tua5 in the following (Ishida et al, 2007)(Matsumoto et al, 2010)) and spr2 with a reported enhanced cortical microtubule response to stress (Hervieux et al, 2016) but also ambivalent regulatory role in microtubule severing depending on tissue (Wightman et al, 2013)(Fan et al, 2018)(Nakamura et al, 2018).…”

Section: Resultsmentioning

confidence: 99%

Turning plants from passive to active material: FERONIA and microtubules independently contribute to mechanical feedback

Malivert

Erguvan

Chevallier

et al. 2021

Preprint

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To survive, cells must constantly resist mechanical stress. In plants, this involves the reinforcement of cell walls, notably through microtubule-dependent cellulose deposition, and thus wall sensing. Several receptor-like kinases have been proposed to act as mechanosensors. Here we tested whether the microtubule response to stress acts downstream of known wall sensors. Using a multi-step screen with eleven mutant lines, we identify FERONIA as the primary candidate for controlling the microtubule response to stress. However, when performing mechanical perturbations, we show that the microtubule response to stress can be independent from FER. We reveal that the feronia phenotype can be partially rescued by reducing tensile stress levels. Conversely, in the absence of both microtubules and FER, cells swell and burst like soap bubbles. Altogether, this shows that the microtubule response to stress acts as an independent pathway to resist stress, in parallel to FER. We propose that both pathways are key components to turn plant cells from passive to active material.

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“…Turgor pressure levels are monitored by two main families of proteins localized in different subcellular compartments, including chloroplasts and the plasma membrane: histidine kinases and channel complexes. Furthermore, new evidence from observations in A. thaliana seedlings points to a third mechanosensitive system, in which microtubules acting as tension sensors regulating developmental processes contribute also to mechanosensing in plant cells [65,66].…”

Section: Perception Of Turgor Pressure and Mechanical Stimuli In The mentioning

confidence: 99%

The Role of Mechanoperception in Plant Cell Wall Integrity Maintenance

Bacete

Hamann

2020

Plants

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The plant cell walls surrounding all plant cells are highly dynamic structures, which change their composition and organization in response to chemical and physical stimuli originating both in the environment and in plants themselves. They are intricately involved in all interactions between plants and their environment while also providing adaptive structural support during plant growth and development. A key mechanism contributing to these adaptive changes is the cell wall integrity (CWI) maintenance mechanism. It monitors and maintains the functional integrity of cell walls by initiating adaptive changes in cellular and cell wall metabolism. Despite its importance, both our understanding of its mode of action and knowledge regarding the molecular components that form it are limited. Intriguingly, the available evidence implicates mechanosensing in the mechanism. Here, we provide an overview of the knowledge available regarding the molecular mechanisms involved in and discuss how mechanoperception and signal transduction may contribute to plant CWI maintenance.

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Microtubule Response to Tensile Stress Is Curbed by NEK6 to Buffer Growth Variation in the Arabidopsis Hypocotyl

Cited by 41 publications

References 70 publications

Cortical tension overrides geometrical cues to orient microtubules in confined protoplasts

Cortical tension overrides geometrical cues to orient microtubules in confined protoplasts

Turning plants from passive to active material: FERONIA and microtubules independently contribute to mechanical feedback

The Role of Mechanoperception in Plant Cell Wall Integrity Maintenance

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