Evolution of Plant P-Type ATPases

Christian N. S. Pedersen,Jeffrey F. Harper,Kristian B. Axelsen,Michael G. Palmgren

doi:10.3389/fpls.2012.00031

Christian N. S. Pedersen, Jeffrey F. Harper + Show 2 more

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https://doi.org/10.3389/fpls.2012.00031

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Abstract

Five organisms having completely sequenced genomes and belonging to all major branches of green plants (Viridiplantae) were analyzed with respect to their content of P-type ATPases encoding genes. These were the chlorophytes Ostreococcus tauri and Chlamydomonas reinhardtii, and the streptophytes Physcomitrella patens (a non-vascular moss), Selaginella moellendorffii (a primitive vascular plant), and Arabidopsis thaliana (a model flowering plant). Each organism contained sequences for all five subfamilies of P-type ATPases. Whereas Na+ and H+ pumps seem to mutually exclude each other in flowering plants and animals, they co-exist in chlorophytes, which show representatives for two kinds of Na+ pumps (P2C and P2D ATPases) as well as a primitive H+-ATPase. Both Na+ and H+ pumps also co-exist in the moss P. patens, which has a P2D Na+-ATPase. In contrast to the primitive H+-ATPases in chlorophytes and P. patens, the H+-ATPases from vascular plants all have a large C-terminal regulatory domain as well as a conserved Arg in transmembrane segment 5 that is predicted to function as part of a backflow protection mechanism. Together these features are predicted to enable H+ pumps in vascular plants to create large electrochemical gradients that can be modulated in response to diverse physiological cues. The complete inventory of P-type ATPases in the major branches of Viridiplantae is an important starting point for elucidating the evolution in plants of these important pumps.

Highlights

P-type ATPases are primary transporters energized by hydrolysis of ATP with a wide range of specificities for small cations and apparently phospholipids (Møller et al, 1996; Palmgren and Harper, 1999)
The P-type ATPases are involved in a wide range of fundamental cellular processes such as the efflux or organismal redistribution of micronutrients (P1B Zn2+- and Cu2+-ATPases), cellular signaling and Ca2+ compartmentalization (P2A and P2B Ca2+-ATPases), energizing the electrochemical gradient used as the driving force for the secondary transporters (P3A H+-ATPases in plants and fungi and P2C Na+/K+-ATPases in animals), and being involved in membrane vesicle budding (P4 ATPases)
This study provides an evolutionary framework for considering how P-type ATPases contribute to the biology of all Viridiplantae, from single celled algae to multicellular flowering plants

Summary

Introduction

P-type ATPases are primary transporters energized by hydrolysis of ATP with a wide range of specificities for small cations and apparently phospholipids (Møller et al, 1996; Palmgren and Harper, 1999). Plant P-type ATPases are characterized structurally by having a single catalytic subunit, 8–12 transmembrane segments, N and C termini exposed to the cytoplasm, and a large central cytoplasmic domain including the phosphorylation and ATP binding sites. The P-type ATPases are involved in a wide range of fundamental cellular processes such as the efflux or organismal redistribution of micronutrients (P1B Zn2+- and Cu2+-ATPases), cellular signaling and Ca2+ compartmentalization (P2A and P2B Ca2+-ATPases), energizing the electrochemical gradient used as the driving force for the secondary transporters (P3A H+-ATPases in plants and fungi and P2C Na+/K+-ATPases in animals), and being involved in membrane vesicle budding (P4 ATPases). The function of P5 ATPases is not known but they have been implicated in vesicle budding from the endoplasmic reticulum (Poulsen et al, 2008a)

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