Cellular transduction of mechanical oscillations in plants by the plasma-membrane mechanosensitive channel MSL10

Tran, Daniel; Girault, Tiffanie; Guichard, Marjorie; Thomine, Sébastien; Leblanc‐Fournier, Nathalie; Moulia, Bruno; Langre, Emmanuel de; Allain, Jean-Marc; Frachisse, Jean‐Marie

doi:10.1073/pnas.1919402118

Cited by 24 publications

(15 citation statements)

References 44 publications

(46 reference statements)

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“…Molecular genetic approaches in Arabidopsis thaliana and other model plants have recently added another dimension to the study of MS ion channels. However, while research on mechanosensitive ion channels in Arabidopsis and other model plants has increased our understanding of these processes ( Basu et al, 2020 ; Tran et al, 2021 ), much remains unknown, especially in non-model plants such as peanuts.…”

Section: Discussionmentioning

confidence: 99%

Analysis of the Transcriptional Dynamics of Regulatory Genes During Peanut Pod Development Caused by Darkness and Mechanical Stress

Cui

Bian²,

Lv³

et al. 2022

Front. Plant Sci.

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Peanut is an oil crop with important economic value that is widely cultivated around the world. It blooms on the ground but bears fruit underground. When the peg penetrates the ground, it enters a dark environment, is subjected to mechanical stress from the soil, and develops into a normal pod. When a newly developed pod emerges from the soil, it turns green and stops growing. It has been reported that both darkness and mechanical stress are necessary for normal pod development. In this study, we investigated changes in gene expression during the reverse process of peg penetration: developmental arrest caused by pod (Pattee 3 pods) excavation. Bagging the aerial pods was used to simulate loss of mechanical pressure, while direct exposure of the aerial pods was used to simulate loss of both mechanical pressure and darkness. After the loss of mechanical stress and darkness, the DEGs were significantly enriched in photosynthesis, photosynthesis–antenna proteins, plant–pathogen interaction, DNA replication, and circadian rhythm pathways. The DNA replication pathway was enriched by down-regulated genes, and the other four pathways were enriched by upregulated genes. Upregulated genes were also significantly enriched in protein ubiquitination and calmodulin-related genes, highlighting the important role of ubiquitination and calcium signaling in pod development. Further analysis of DEGs showed that phytochrome A (Phy A), auxin response factor 9 (IAA9), and mechanosensitive ion channel protein played important roles in geocarpy. The expression of these two genes increased in subterranean pods but decreased in aerial pods. Based on a large number of chloroplast-related genes, calmodulin, kinases, and ubiquitin-related proteins identified in this study, we propose two possible signal transduction pathways involved in peanut geocarpy, namely, one begins in chloroplasts and signals down through phosphorylation, and the other begins during abiotic stress and signals down through calcium signaling, phosphorylation, and ubiquitination. Our study provides valuable information about putative regulatory genes for peanut pod development and contributes to a better understanding of the biological phenomenon of geocarpy.

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Section: Discussionmentioning

confidence: 99%

Analysis of the Transcriptional Dynamics of Regulatory Genes During Peanut Pod Development Caused by Darkness and Mechanical Stress

Cui

Bian²,

Lv³

et al. 2022

Front. Plant Sci.

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“…1B). The Boltzmann law of activation followed by prokaryotic MscS and MscL channels, as well as mammalian Piezo channels was verified for the plant channels MSL10 and Oscas [28], [34].…”

Section: Ms Channels Are Force-gated Channelsmentioning

confidence: 81%

“…(D) The activity profiles of the MS channels of the four families are characterized by a high conductance for MSLs and MCAs and lower conductance for OSCAs and Piezos with rapid activation kinetics followed by inactivation for the latter two. (MSL studied in protoplast [31], [34], Xenopus oocyte [100], HEK cell [65]; OSCA in HEK cell and liposome [28]; Piezo in HEK cell [77], [83]; MCA in lipid bilayer [29])…”

Section: Ms Channels Are Force-gated Channelsmentioning

confidence: 99%

Mechanotransduction in the spotlight of mechano-sensitive channels

Guichard

Thomine²,

Frachisse³

2022

Current Opinion in Plant Biology

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“…A second model variation, the "Decreasing Tension-Inactivation Model", assumed that inactivation occurred as soon as the membrane tension started to decrease (but not necessarily dropping below the closing tension of the channel). MSL10 shows a related behavior in that its threshold tension and open probability are dependent on the rate at which tension is applied to the membrane 58,59 . Incorporating this modification into the Basic Model only required that kflux be set to zero when the change in membrane tension (…”

Section: Adding Channel Inactivation or Msl8-dependent Effects On Cell Wall Stiffness Produce Models That Fit Experimental Datamentioning

confidence: 99%

In vitro experiments and kinetic models of pollen hydration show that MSL8 is not a simple tension-gated osmoregulator

Miller

Strychalski

Nickaeen

et al. 2021

Preprint

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SummaryPollen, a neighbor-less cell that contains the male gametes, undergoes multiple mechanical challenges during plant sexual reproduction, including desiccation and rehydration. It was previously showed that the pollen-specific mechanosensitive ion channel MscS-Like (MSL)8 is essential for pollen survival during hydration and proposed that it functions as a tension-gated osmoregulator. Here we test this hypothesis with a combination of mathematical modeling and laboratory experiments. Time-lapse imaging revealed that wild-type pollen grains swell and then stabilize in volume rapidly during hydration. msl8 mutant pollen grains, however, continue to expand and eventually burst. We found that a mathematical model wherein MSL8 acts as a simple tension-gated osmoregulator does not replicate this behavior. A better fit was obtained from variations of the model wherein MSL8 inactivation is independent of its membrane tension gating threshold or MSL8 strengthens the cell wall without osmotic regulation. Experimental and computational testing of several perturbations, including hydration in an osmolyte-rich solution, hyper-desiccation of the grains, and MSL8-YFP overexpression, indicated that the Cell Wall Strengthening Model best simulated experimental responses. Finally, expression of a non-conducting MSL8 variant did not complement the msl8 overexpansion phenotype. These data indicate that, contrary to our hypothesis and to known MS ion channel function in single-cell systems, MSL8 does not act as a simple membrane tension-gated osmoregulator. Instead, they support a model wherein ion flux through MSL8 is required to alter pollen cell wall properties. These results demonstrate the utility of pollen as a cellular-scale model system and illustrate how mathematical models can correct intuitive hypotheses.

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Cellular transduction of mechanical oscillations in plants by the plasma-membrane mechanosensitive channel MSL10

Cited by 24 publications

References 44 publications

Analysis of the Transcriptional Dynamics of Regulatory Genes During Peanut Pod Development Caused by Darkness and Mechanical Stress

Analysis of the Transcriptional Dynamics of Regulatory Genes During Peanut Pod Development Caused by Darkness and Mechanical Stress

Mechanotransduction in the spotlight of mechano-sensitive channels

In vitro experiments and kinetic models of pollen hydration show that MSL8 is not a simple tension-gated osmoregulator

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