The evolution of plant proton pump regulation via the R domain may have facilitated plant terrestrialization

Abstract

Plasma membrane (PM) H+-ATPases are the electrogenic proton pumps that export H+ from plant and fungal cells to acidify the surroundings and generate a membrane potential. Plant PM H+-ATPases are equipped with a C‑terminal autoinhibitory regulatory (R) domain of about 100 amino acid residues, which could not be identified in the PM H+-ATPases of green algae but appeared fully developed in immediate streptophyte algal predecessors of land plants. To explore the physiological significance of this domain, we created in vivo C-terminal truncations of autoinhibited PM H+‑ATPase2 (AHA2), one of the two major isoforms in the land plant Arabidopsis thaliana. As more residues were deleted, the mutant plants became progressively more efficient in proton extrusion, concomitant with increased expansion growth and nutrient uptake. However, as the hyperactivated AHA2 also contributed to stomatal pore opening, which provides an exit pathway for water and an entrance pathway for pests, the mutant plants were more susceptible to biotic and abiotic stresses, pathogen invasion and water loss, respectively. Taken together, our results demonstrate that pump regulation through the R domain is crucial for land plant fitness and by controlling growth and nutrient uptake might have been necessary already for the successful water-to-land transition of plants.

Hypothesis paper: the development of a regulatory layer in P2B autoinhibited Ca 2+ -ATPases may have facilitated plant terrestrialization and animal multicellularization

“…This hypothesis is supported by the fact that the different clades of P2B ATPases from Chlorophyta and Holozoa each include isoforms from the same species (marked by stars in Figure 1A, 2A ). Similar signs of ancient gene duplications were reported previously in P3A, P2A and P5A-ATPases 19 , 29 .…”

“…Chlorophytes live in water or on damp surfaces, while some of the early Streptophytes also appear in soil or on rock surfaces. Interestingly, the appearance of the CaMBD resembles the appearance of the R domain in P3A plasma membrane H + -ATPases that coincided with terrestrialization of plants 19 . Thus, we hypothesize that the CaMBD domain facilitated the survival of plants when facing the harsh conditions on land.…”

“…The search for P-type P2B ATPase sequences was based on the strategy from Stéger et al 19 . In brief, P-type P2B ATPase protein sequences were identified in the following databases using the Basic Local Alignment Search Tool (BLAST) program: the NCBI protein database ( http://blast.ncbi.nlm.nih.gov/ ), the KEGG: Kyoto Encyclopedia of genes and genomes ( https://www.genome.jp/tools/blast/ ), the PhycoCosm Algal Genomics Resource ( https://phycocosm.jgi.doe.gov/phycocosm/home ), the MycoCosm Fungal Genomic Resource ( https://mycocosm.jgi.doe.gov/mycocosm/home ) and the Figshare repository ( https://figshare.com ).…”

“…The phylogenetic analysis of P2B ATPase sequences was based on Stéger et al 19 . In brief, the alignment of the potential amino acid sequences was performed using MUSCLE 20 implemented in MEGA11.…”

“…The aim of this study was to identify the evolutionary history of P2B ATPase regulation with a broader phylogenetic analysis and to hypothesize what initiated it. Our previous paper showed that the appearance of the autoinhibitory regulatory (R) domain of plasma membrane H + -ATPases co-occurred with the water-to-land transition of plants more than 450 million years ago 19 . Such a development might have been necessary for plants to adapt to harsh and changing terrestrial conditions.…”