PIEZO ion channel is required for root mechanotransduction in Arabidopsis thaliana

Abstract

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.

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 ).…”

Ethylene Signaling Facilitates Plant Adaption to Physical Barriers

“…Mechanosensitive ion channels are a common mechanism for sensing mechanical impedance. In Arabidopsis , the MID1-complementing activity 1 (MCA1) is a Ca 2+ -permeable mechanosensitive channel enabling roots to overcome mechanical barriers ( Okamoto et al, 2021 ), and the piezo1 (PZO1) is another ion channel that affects Ca 2+ transients in response to mechanical stimulation and is required for roots to penetrate hard agar ( Mousavi et al, 2021 ). The ethylene is biosynthesized by two dedicated enzymatic reactions.…”

A Molecular Pinball Machine of the Plasma Membrane Regulates Plant Growth—A New Paradigm

“…Thus, "PIN" proteins supply auxin that activates the proton pump to promote expansion growth. However, the Ca 2+ signal depends not only on AGP-Ca 2+ but also on Ca 2+ channels activated by reactive oxygen species (ROS) [62] and stress transduction from the cell wall to mechanosensitive ion channels [68][69][70] of the plasma membrane. The transmission of the stress vector most likely involves an arabinogalactan protein APAP1 [71] covalently attached to wall pectin and anchored to the plasma membrane by a C-terminal GPI lipid.…”