Evolution of Plant Na+-P-Type ATPases: From Saline Environments to Land Colonization

Abstract

Soil salinity is one of the major factors obstructing the growth and development of agricultural crops. Eukaryotes have two main transport systems involved in active Na+ removal: cation/H+ antiporters and Na+-P-type ATPases. Key transport proteins, Na+/K+-P-ATPases, are widely distributed among the different taxa families of pumps which are responsible for keeping cytosolic Na+ concentrations below toxic levels. Na+/K+-P-ATPases are considered to be absent in flowering plants. The data presented here are a complete inventory of P-type Na+/K+-P-ATPases in the major branches of the plant kingdom. We also attempt to elucidate the evolution of these important membrane pumps in plants in comparison with other organisms. We were able to observe the gradual replacement of the Na+-binding site to the Ca2+-binding site, starting with cyanobacteria and moving to modern land plants. Our results show that the α-subunit likely evolved from one common ancestor to bacteria, fungi, plants, and mammals, whereas the β-subunit did not evolve in green algae. In conclusion, our results strongly suggest the significant differences in the domain architecture and subunit composition of plant Na+/K+-P-ATPases depending on plant taxa and the salinity of the environment. The obtained data clarified and broadened the current views on the evolution of Na+/K+-P-ATPases. The results of this work would be helpful for further research on P-type ATPase functionality and physiological roles.

Na+/K+-ATPase regulates the K+/Na+ homeostasis in the intertidal macroalgae, Neoporphyra haitanensis, in response to salt stress

“…To maintain K + /Na + homeostasis in the cytoplasm under salt stress, plants limit the accumulation of Na + and the loss of K + ( Hussain et al., 2021 ). Eukaryotes have two major Na + efflux systems: the salt overly sensitive (SOS) system, which is a universally conserved salt tolerance pathway in plants; and the Na + /K + -ATPase system in bacteria, fungi, moss, and mammals ( Nakayama et al., 2010 ; Jacobs et al., 2011 ; Dabravolski and Isayenkov, 2021 ). The function of SOS1 relies on the plasma membrane (PM)-localized H + -ATPase that hydrolyzes adenosine triphosphate (ATP) to generate energy and pumps H + out of the cytoplasm to generate an electrochemical gradient ( Qiu et al., 2002 ; Haruta and Sussman, 2012 ; Yang et al., 2019 ).…”

“…In an evolutionary context, Na + /K + -ATPases can be divided into animal and fungal types, flowering plants are generally considered to lack Na + /K + -ATPases ( Pedersen et al., 2012 ; Dabravolski and Isayenkov, 2021 ). Genomic analyses revealed that genes encoding Na + /K + -ATPases were lost during evolution and land settlement, suggesting that Na + /K + -ATPases might exist in eukaryotes living in high-salinity marine environments ( Garciadeblas et al., 2001 ; Pedersen et al., 2012 ).…”