TY - JOUR

T1 - The evolution of plant proton pump regulation via the R domain may have facilitated plant terrestrialization

AU - Stéger, Anett

AU - Hayashi, Maki

AU - Lauritzen, Emil Wacenius

AU - Herburger, Klaus

AU - Shabala, Lana

AU - Wang, Cuiwei

AU - Bendtsen, Amalie Kofoed

AU - Nørrevang, Anton Frisgaard

AU - Madriz-Ordeñana, Kenneth

AU - Ren, Shichao

AU - Trinh, Mai Duy Luu

AU - Thordal-Christensen, Hans

AU - Fuglsang, Anja Thoe

AU - Shabala, Sergey

AU - Østerberg, Jeppe Thulin

AU - Palmgren, Michael

N1 - © 2022. The Author(s).

PY - 2022

Y1 - 2022

N2 - 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.

AB - 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.

U2 - 10.1038/s42003-022-04291-y

DO - 10.1038/s42003-022-04291-y

M3 - Journal article

C2 - 36446861

VL - 5

JO - Communications Biology

JF - Communications Biology

SN - 2399-3642

M1 - 1312

ER -