Arabidopsis MSL10 Has a Regulated Cell Death Signaling Activity That Is Separable from Its Mechanosensitive Ion Channel Activity  

Abstract

Members of the MscS superfamily of mechanosensitive ion channels function as osmotic safety valves, releasing osmolytes under increased membrane tension. MscS homologs exhibit diverse topology and domain structure, and it has been proposed that the more complex members of the family might have novel regulatory mechanisms or molecular functions. Here, we present a study of MscS-Like (MSL)10 from Arabidopsis thaliana that supports these ideas. High-level expression of MSL10-GFP in Arabidopsis induced small stature, hydrogen peroxide accumulation, ectopic cell death, and reactive oxygen species-and cell death-associated gene expression. Phosphomimetic mutations in the MSL10 N-terminal domain prevented these phenotypes. The phosphorylation state of MSL10 also regulated its ability to induce cell death when transiently expressed in Nicotiana benthamiana leaves but did not affect subcellular localization, assembly, or channel behavior. Finally, the N-terminal domain of MSL10 was sufficient to induce cell death in tobacco, independent of phosphorylation state. We conclude that the plant-specific N-terminal domain of MSL10 is capable of inducing cell death, this activity is regulated by phosphorylation, and MSL10 has two separable activities-one as an ion channel and one as an inducer of cell death. These findings further our understanding of the evolution and significance of mechanosensitive ion channels.

The plant cell wall integrity maintenance mechanism – A case study of a cell wall plasma membrane signaling network

“…In recent years homologues of the MscS type of bacterial channels, which perceive hypo-osmotic stress and function as pressure valves during environmental adaptation, have been identified in the Arabidopsis genome and functionally characterized (Haswell and Meyerowitz, 2006;Haswell et al, 2008;Wilson et al, 2011Wilson et al, , 2013. The available data suggest that the MscS-LIKE (MSL) channel proteins in Arabidopsis have similar but not identical functions like the MscS proteins in bacteria with MSL10 functioning both as stretch activated channel and regulator of cell death (Wilson et al, 2014;Maksaev and Haswell, 2012;Veley et al, 2014).…”

Genome-Wide Association Mapping Reveals That Specific and Pleiotropic Regulatory Mechanisms Fine-Tune Central Metabolism and Growth in Arabidopsis

“…MSL family members act as osmotic safety valves to release osmolytes under increased membrane tension (Maksaev and Haswell, 2012). These proteins have been implicated in pollen development (Hamilton et al, 2015), osmotic regulation in plastids , redox homeostasis in mitochondria (Lee et al, 2016), and cell death (Veley et al, 2014). The link between MSL10, sugars, and starch metabolism might be related to osmotic and turgor regulation.…”

Gene co-expression analyses: an overview from microarray collections inArabidopsis thaliana

“…Interestingly, all the 14 gene pairs affected by mutant inclusion in the reference data set showed a gene in common, namely AT5G12080. This gene encodes a mechanically sensitive (or stretch-activated) ion channel in the plasma membrane with a moderate preference for anions, and has been reported as involved in anion transport, detection of mechanical stimulus, leaf senescence and programmed cell death in response to reactive oxygen species [43,44]. Such functions could be related to the differential expression levels of AT5G12080 among plant organs and tissues.…”