Plant PIEZO homologs modulate vacuole morphology during tip growth

Abstract

In animals, PIEZOs are plasma membrane–localized cation channels involved in diverse mechanosensory processes. We investigated PIEZO function in tip-growing cells in the moss Physcomitrium patens and the flowering plant Arabidopsis thaliana. PpPIEZO1 and PpPIEZO2 redundantly contribute to the normal growth, size, and cytoplasmic calcium oscillations of caulonemal cells. Both PpPIEZO1 and PpPIEZO2 localized to vacuolar membranes. Loss-of-function, gain-of-function, and overexpression mutants revealed that moss PIEZO homologs promote increased complexity of vacuolar membranes through tubulation, internalization, and/or fission. Arabidopsis PIEZO1 also localized to the tonoplast and is required for vacuole tubulation in the tips of pollen tubes. We propose that in plant cells the tonoplast has more freedom of movement than the plasma membrane, making it a more effective location for mechanosensory proteins.

TMEM120A contains a specific coenzyme A-binding site and might not mediate poking- or stretch-induced channel activities in cells

“…While members of the MscL family are present in bacteria, archaea, or fungi, and those of the MscS family exist in plants or microbes, they are not found in animals ( Booth et al, 2007 ; Pivetti et al, 2003 ; Wilson et al, 2013 ). Piezo channels are involved in cellular mechanosensation processes crucial for touch perception, proprioception, red blood cell volume regulation, and other physiological functions in animals and plants ( Mousavi et al, 2021 ; Murthy et al, 2017 ; Radin et al, 2021 ; Xiao, 2020 ). Moreover, Drosophila NompC from the transient receptor potential (TRP) channel family, OSCA/TMEM63 (found in plants and animals) and TMC1/2 (mainly found in animals) from the TMEM16 superfamily, mammalian TREK/TRAAK channels from the two pore-domain potassium (K2P) channel subfamily, and Caenorhabditis elegans degenerin channels from the epithelial sodium channel (ENaC)/degenerin family also serve as mechanosensitive ion channels with pivotal functions in various mechanotransduction processes of eukaryotic organisms ( Jin et al, 2020 ).…”

Calpain DEK1 acts as a developmental switch gatekeeping cell fate transitions

“…This vector allows expression during the whole moss life cycle and its targeting to the 108 locus does not induce phenotypic change (e.g. Coudert et al 2019 or Radin et al 2021). For transformation purposes the targeting fragment was PCR-amplified using the primer P3 and P4 designed at each end of the targeting sequence.…”

Between Stress and Response: Function and Localization of Mechanosensitive Ca2+ Channels in Herbaceous and Perennial Plants

“…However, in moss (Physcomitrium patens), PpPiezo1 and 2 are localized in the tonoplast and are thought to be involved in the regulation of vacuole shape in apical caulonemal cells [115]. These results raise the question of the role of the vacuole in mechanosensing.…”

“…Within this MSL family, consisting of 10 members in Arabidopsis, some isoforms localize in membranes of different cell compartments (plasma membrane, tonoplast, mitochondrial membrane) and are expressed in a tissue-specific manner. Concerning calcium-permeable channels, MCA and OSCA channels are located in the plasma membrane [97,123], whereas Piezo1 is located in the tonoplast [115]. However, information is incomplete regarding the location of their expression.…”