Regulation of Vacuole Morphology by PIEZO Channels in Spreading Earth Moss

Abstract

The perception of mechanical force is a fundamental property of most, if not all cells. PIEZO channels are plasma membrane-embedded mechanosensitive calcium channels that play diverse and essential roles in mechanobiological processes in animals1,2. PIEZO channel homologs are found in plants3,4, but their role(s) in the green lineage are almost completely unknown. Plants and animals diverged approximately 1.5 billion years ago, independently evolved multicellularity, and have vastly different cellular mechanics5. Here, we investigate PIEZO channel function in the moss Physcomitrium patens, a representative of one of the first land plant lineages. PpPIEZO1 and PpPIEZO2 were redundantly required for normal growth, size, and shape of tip-growing caulonema cells. Both were localized to vacuolar membranes and facilitated the release of calcium into the cytosol in response to hypoosmotic shock. Loss-of-function (ΔPppiezo1/2) and gain-of-function (PpPIEZO2-R2508K and -R2508H) mutants revealed a role for moss PIEZO homologs in regulating vacuole morphology. Our work here shows that plant and animal PIEZO homologs have diverged in both subcellular localization and in function, likely co-opted to serve different needs in each lineage. The plant homologs of PIEZO channels thus provide a compelling lens through which to study plant mechanobiology and the evolution of mechanoperceptive strategies in multicellular eukaryotes.

A voltage‐dependent Ca2+ homeostat operates in the plant vacuolar membrane

“…Members of the cyclic nucleotide gated channel (CNGCs), hyperosmolarity‐induced [Ca 2+ ] channels (OSCAs) and glutamate receptor‐like channels (GLRs) families were shown to be involved in several physiological processes such as auxin signalling (Shih et al, 2015; Dindas et al, 2018), plant immunity (Yuan et al, 2014; Tian et al, 2019; Thor et al, 2020), reproduction (Frietsch et al, 2007; Michard et al, 2011; Tunc‐Ozdemir et al, 2013; Wudick et al, 2018; Pan et al, 2019) and long distance systemic signalling (Nguyen et al, 2018; Toyota et al, 2018). In addition, several classes of mechanically activated Ca 2+ ‐permeable PM channels in plants are likely to be encoded by the mid1 ‐complementing activity (MCAs), piezos and MSL1 channels (Kurusu et al, 2013; Hou et al, 2014; Hamilton et al, 2015; Li et al, 2020; Mousavi et al, 2020; Radin et al, 2020).…”