The Mechanosensitive Ion Channel MSL10 Potentiates Responses to Cell Swelling in Arabidopsis Seedlings

Basu, Debarati; Haswell, Elizabeth S.

doi:10.1016/j.cub.2020.05.015

Cited by 73 publications

(46 citation statements)

References 116 publications

(156 reference statements)

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“…In yeast (Saccharomyces cerevisiae), two mechanosensitive channels (Msy1 and Msy2) have been identified to be involved in cell volume regulation following hypo-osmotic shock. Likewise, the mechanosensitive channel MSL10 was recently demonstrated to potentiate responses to hypo-osmotic shock in Arabidopsis thaliana (Basu & Haswell, 2020). P. tricornutum encodes a suite of channels resembling mechanosensitive/stretchactivated channels (including seven small conductance mechanosensitive channels (MscS) and four TRP channels) (Verret et al, 2010).…”

Section: Discussionmentioning

confidence: 99%

Spatiotemporal patterns of intracellular Ca²⁺ signalling govern hypo‐osmotic stress resilience in marine diatoms

et al. 2021

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Summary Diatoms are globally important phytoplankton that dominate coastal and polar‐ice assemblages. These environments exhibit substantial changes in salinity over dynamic spatiotemporal regimes. Rapid sensory systems are vital to mitigate the harmful consequences of osmotic stress. Population‐based analyses have suggested that Ca2+ signalling is involved in diatom osmotic sensing. However, mechanistic insight of the role of osmotic Ca2+ signalling is limited. Here, we show that Phaeodactylum Ca2+ elevations are essential for surviving hypo‐osmotic shock. Moreover, employing novel single‐cell imaging techniques we have characterised real‐time Ca2+ signalling responses in single diatom cells to environmental osmotic perturbations. We observe that intracellular spatiotemporal patterns of osmotic‐induced Ca2+ elevations encode vital information regarding the nature of the osmotic stimulus. Localised Ca2+ signals evoked by mild or gradual hypo‐osmotic shocks are propagated globally from the apical cell tips, enabling fine‐tuned cell volume regulation across the whole cell. Finally, we demonstrate that diatoms adopt Ca2+‐independent and dependent mechanisms for osmoregulation. We find that efflux of organic osmolytes occurs in a Ca2+‐independent manner, but this response is insufficient to mitigate cell damage during hypo‐osmotic shock. By comparison, Ca2+‐dependent signalling is necessary to prevent cell bursting via precise coordination of K+ transport, and therefore is likely to underpin survival in dynamic osmotic environments.

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Section: Discussionmentioning

confidence: 99%

Spatiotemporal patterns of intracellular Ca²⁺ signalling govern hypo‐osmotic stress resilience in marine diatoms

et al. 2021

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“…Only a few mechanosensitive ion channels have been described in plants (8). MSL8 plays a mechanosensory role in pollen (9), MSL10 is involved in cell swelling (8,10), OSCA1 has mainly been characterized for its role in osmosensation (11), and OSCA1.3 regulates stomatal closure during immune signaling (12). It has been proposed that MCA1, expressed in the elongation zone but not the root cap, is a stretch-activated calcium permeable ion channel involved in soil penetration; however, evidence for its being a bona fide ion channel capable of detecting mechanical force is lacking (13)(14)(15).…”

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confidence: 99%

PIEZO ion channel is required for root mechanotransduction in Arabidopsis thaliana

Mousavi

Dubin

Zeng

et al. 2021

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

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Plant roots adapt to the mechanical constraints of the soil to grow and absorb water and nutrients. As in animal species, mechanosensitive ion channels in plants are proposed to transduce external mechanical forces into biological signals. However, the identity of these plant root ion channels remains unknown. Here, we show that Arabidopsis thaliana PIEZO1 (PZO1) has preserved the function of its animal relatives and acts as an ion channel. We present evidence that plant PIEZO1 is expressed in the columella and lateral root cap cells of the root tip, which are known to experience robust mechanical strain during root growth. Deleting PZO1 from the whole plant significantly reduced the ability of its roots to penetrate denser barriers compared to wild-type plants. pzo1 mutant root tips exhibited diminished calcium transients in response to mechanical stimulation, supporting a role of PZO1 in root mechanotransduction. Finally, a chimeric PZO1 channel that includes the C-terminal half of PZO1 containing the putative pore region was functional and mechanosensitive when expressed in naive mammalian cells. Collectively, our data suggest that Arabidopsis PIEZO1 plays an important role in root mechanotransduction and establish PIEZOs as physiologically relevant mechanosensitive ion channels across animal and plant kingdoms.

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“…In addition to the TM4-5 linker, we noted that the cytoplasmic N-terminus of FLYC1 interacts dynamically with the cytoplasmic cage. Interestingly, interaction between the N and C-terminus of AtMSL10 has been proposed to induce cell death, for instance in response to swelling in seedlings 44,45 . Whether this proposed interaction in AtMSL10 corresponds to the one observed in FLYC1 remains unclear.…”

Section: Discussionmentioning

confidence: 99%

Structural Insights into the Venus flytrap Mechanosensitive Ion Channel Flycatcher1

Jojoa-Cruz

Saotome

Tsui

et al. 2021

Preprint

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Flycatcher1 (FLYC1), a MscS homolog, has recently been identified as a candidate mechanosensitive (MS) ion channel involved in Venus flytrap prey recognition. FLYC1 is larger and its sequence diverges from previously studied MscS homologs, suggesting it has unique structural features that contribute to its function. Here, we characterized FLYC1 by cryo-electron microscopy, molecular dynamics simulations, and electrophysiology. Akin to bacterial MscS and plant MSL1 channels, we find that FLYC1 central core includes side portals in the cytoplasmic cage that regulate ion conduction, by identifying critical residues that modulate channel conductance. Topologically unique cytoplasmic flanking regions can adopt 'up' or 'down' conformations, making the channel asymmetric. Disruption of an up conformation-specific interaction severely delays channel deactivation by 40-fold likely due to stabilization of the channel open state. Our results illustrate novel structural features and likely conformational transitions that regulate mechano-gating of FLYC1.

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The Mechanosensitive Ion Channel MSL10 Potentiates Responses to Cell Swelling in Arabidopsis Seedlings

Abstract: overexposure induces programmed cell death in Arabidopsis, which is mediated by Caspase-like Activities and which can be suppressed by Caspase inhibitors, p35 and defender against apoptotic death.

Cited by 73 publications

References 116 publications

Spatiotemporal patterns of intracellular Ca²⁺ signalling govern hypo‐osmotic stress resilience in marine diatoms

Spatiotemporal patterns of intracellular Ca²⁺ signalling govern hypo‐osmotic stress resilience in marine diatoms

PIEZO ion channel is required for root mechanotransduction in Arabidopsis thaliana

Structural Insights into the Venus flytrap Mechanosensitive Ion Channel Flycatcher1

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The Mechanosensitive Ion Channel MSL10 Potentiates Responses to Cell Swelling in Arabidopsis Seedlings

Abstract: overexposure induces programmed cell death in Arabidopsis, which is mediated by Caspase-like Activities and which can be suppressed by Caspase inhibitors, p35 and defender against apoptotic death.

Cited by 73 publications

References 116 publications

Spatiotemporal patterns of intracellular Ca2+ signalling govern hypo‐osmotic stress resilience in marine diatoms

Spatiotemporal patterns of intracellular Ca2+ signalling govern hypo‐osmotic stress resilience in marine diatoms

PIEZO ion channel is required for root mechanotransduction in Arabidopsis thaliana

Structural Insights into the Venus flytrap Mechanosensitive Ion Channel Flycatcher1

Contact Info

Product

Resources

About

Spatiotemporal patterns of intracellular Ca²⁺ signalling govern hypo‐osmotic stress resilience in marine diatoms

Spatiotemporal patterns of intracellular Ca²⁺ signalling govern hypo‐osmotic stress resilience in marine diatoms