TY - JOUR

T1 - Hypothesis paper

T2 - the development of a regulatory layer in P2B autoinhibited Ca2+-ATPases may have facilitated plant terrestrialization and animal multicellularization

AU - Stéger, Anett

AU - Palmgren, Michael

PY - 2023

Y1 - 2023

N2 - With the appearance of plants and animals, new challenges emerged. These multicellular eukaryotes had to solve for example the difficulties of multifaceted communication between cells and adaptation to new habitats. In this paper, we are looking for one piece of the puzzle that made the development of complex multicellular eukaryotes possible with a focus on regulation of P2B autoinhibited Ca 2+-ATPases. P2B ATPases pump Ca 2+ out of the cytosol at the expense of ATP hydrolysis, and thereby maintain a steep gradient between the extra- and intracytosolic compartments which is utilized for Ca 2+-mediated rapid cell signaling. The activity of these enzymes is regulated by a calmodulin (CaM)-responsive autoinhibitory region, which can be located in either termini of the protein, at the C-terminus in animals and at the N-terminus in plants. When the cytoplasmic Ca 2+ level reaches a threshold, the CaM/Ca 2+ complex binds to a calmodulin-binding domain (CaMBD) in the autoinhibitor, which leads to the upregulation of pump activity. In animals, protein activity is also controlled by acidic phospholipids that bind to a cytosolic portion of the pump. Here, we analyze the appearance of CaMBDs and the phospholipid-activating sequence and show that their evolution in animals and plants was independent. Furthermore, we hypothesize that different causes may have initiated the appearance of these regulatory layers: in animals, it is linked to the appearance of multicellularity, while in plants it co-occurs with their water-to-land transition.

AB - With the appearance of plants and animals, new challenges emerged. These multicellular eukaryotes had to solve for example the difficulties of multifaceted communication between cells and adaptation to new habitats. In this paper, we are looking for one piece of the puzzle that made the development of complex multicellular eukaryotes possible with a focus on regulation of P2B autoinhibited Ca 2+-ATPases. P2B ATPases pump Ca 2+ out of the cytosol at the expense of ATP hydrolysis, and thereby maintain a steep gradient between the extra- and intracytosolic compartments which is utilized for Ca 2+-mediated rapid cell signaling. The activity of these enzymes is regulated by a calmodulin (CaM)-responsive autoinhibitory region, which can be located in either termini of the protein, at the C-terminus in animals and at the N-terminus in plants. When the cytoplasmic Ca 2+ level reaches a threshold, the CaM/Ca 2+ complex binds to a calmodulin-binding domain (CaMBD) in the autoinhibitor, which leads to the upregulation of pump activity. In animals, protein activity is also controlled by acidic phospholipids that bind to a cytosolic portion of the pump. Here, we analyze the appearance of CaMBDs and the phospholipid-activating sequence and show that their evolution in animals and plants was independent. Furthermore, we hypothesize that different causes may have initiated the appearance of these regulatory layers: in animals, it is linked to the appearance of multicellularity, while in plants it co-occurs with their water-to-land transition.

KW - Animals

KW - Adenosine Triphosphatases

KW - Calmodulin/metabolism

KW - Protein Binding

KW - Calcium Signaling

KW - Calcium/metabolism

U2 - 10.1080/15592324.2023.2204284

DO - 10.1080/15592324.2023.2204284

M3 - Journal article

C2 - 37096591

VL - 18

JO - Plant Signalling & Behavior

JF - Plant Signalling & Behavior

SN - 1559-2316

IS - 1

M1 - e2204284

ER -