Deciphering the role of mechanosensitive channels in plant root biology: perception, signaling, and adaptive responses.

ABSTRACT

MAIN CONCLUSION: Mechanosensitive channels are integral membrane proteins that rapidly translate extrinsic or intrinsic mechanical tensions into biological responses. They can serve as potential candidates for developing smart-resilient crops with efficient root systems. Mechanosensitive (MS) calcium channels are molecular switches for mechanoperception and signal transduction in all living organisms. Although tremendous progress has been made in understanding mechanoperception and signal transduction in bacteria and animals, this remains largely unknown in plants. However, identification and validation of MS channels such as Mid1-complementing activity channels (MCAs), mechanosensitive-like channels (MSLs), and Piezo channels (PIEZO) has been the most significant discovery in plant mechanobiology, providing novel insights into plant mechanoperception. This review summarizes recent advances in root mechanobiology, focusing on MS channels and their related signaling players, such as calcium ions (Ca2+), reactive oxygen species (ROS), and phytohormones. Despite significant advances in understanding the role of Ca2+ signaling in root biology, little is known about the involvement of MS channel-driven Ca2+ and ROS signaling. Additionally, the hotspots connecting the upstream and downstream signaling of MS channels remain unclear. In light of this, we discuss the present knowledge of MS channels in root biology and their role in root developmental and adaptive traits. We also provide a model highlighting upstream (cell wall sensors) and downstream signaling players, viz., Ca2+, ROS, and hormones, connected with MS channels. Furthermore, we highlighted the importance of emerging signaling molecules, such as nitric oxide (NO), hydrogen sulfide (H2S), and neurotransmitters (NTs), and their association with root mechanoperception. Finally, we conclude with future directions and knowledge gaps that warrant further research to decipher the complexity of root mechanosensing.