Apyrase in horticultural crops: insights into growth, stress adaptation and quality regulation

Abstract

Apyrases are a kind of nucleoside triphosphate diphosphohydrolases that catalyze the removal of the terminal phosphate group from nucleoside triphosphate (NTP) or nucleoside diphosphate (NDP). They also function either intracellularly or extracellularly in mediating the NTP/NDP homeostasis critical for plant growth, development, senescence, stress response and adaptation. Initial studies elucidated the biochemistry, structure and function of plant apyrases, while the recent progresses include the crystallography, newly discovered interaction partners and downstream targets for diverse apyrases. Furthermore, these apyrases play diverse roles in horticultural crops with the new recognition of extracellular ATP (eATP) receptors. This review summarized the types, structures, biochemical and physiological functions of plant apyrases and highlighted their roles in plant growth, development, biotic/abiotic stress responses and adaptation. The physiological activities among the apyrases, eATP with its receptor and eATP/iATP homeostasis, were reviewed. In particular, the quality formation / deterioration of postharvest horticultural crops caused by apyrases was emphasized. This paper reviewed the recent advances in the multiple roles of apyrases in horticultural crops and provided insights into the regulation of physiological activities by the enzyme from molecular network perspectives.

Keywords: Apyrase; Energy; Extracellular ATP; Horticultural crops; Physiological activities; Signal transduction.

Fig. 1

Overview of this review (by Figdraw). Apyrases play multiple roles in plants, such as the regulation of growth and development, abiotic stress response including chilling and salt stresses, biotic stress response including pathogen attack, and the regulation of postharvest quality

Fig. 2

Schematic representation of the pivotal amino acid residues within banana MaAPY6 involved in the dephosphorylation of nucleoside triphosphates (NTPs) including ATP (A), UTP (B), GTP (C), and CTP (D). The precise three-dimensional structural model of MaAPY6 protein was derived from the trRosetta server through direct energy minimization by utilizing a constrained Rosetta version (Du et al. 2021). The NTP-MaAPY6 binding interaction was predicted using Autodock4.2 and Vina4 softwares (Trott and Olson 2010). The final outcomes were visualized using Chimera (Pettersen et al. 2004) and LigPLot (Laskowski and Swindells 2011)

Fig. 3

Differences in apyrase localization by Figdraw. Soybean (Glycine soja) apyrase GS52 and legume (Dolichos biflorus) apyrase named DbLNP were located in cell membrane (Etzler et al. ; Govindarajulu et al. 2009). AtAPY1/2 in Arabidopsis existed in the Glogi (Chiu et al. 2012), while potato (Solanum tuberosum) apyrase StAPY3 was located in the apoplast (Riewe et al. 2008)

Fig. 4

Secondary and tertiary structural analyses of the ten MaAPYs. A Full-length apyrase sequences of Arabidopsis and banana were aligned by jalviewg tool (Waterhouse et al. 2009). Five ACRs were labeled with red color box. B The secondary structure was made by submitting the amino acid sequence to the analysis tool NPS @ SOPMA (https://npsa-pbil.ibcp.fr/) (Deléage 2017). The corresponding membrane-spanning motif was identified by utilizing the online tool TMHMM server v.2.0 according to the default parameters (http://www.cbs.dtu.dk/services/TMHMM/) (Krogh et al. 2001) and then marked with a yellow color box. Alpha helix in blue, beta sheet in red, beta turn in green and random coil in purple were shown. C The structure models were constructed via the web server SWISS-MODEL (https://swissmodel.expasy.org/) (Waterhouse et al. 2018). D The relative sizes and locations of the GDA1-CD39 domains and transmembrane domains (TM) were visualized by IBS2.0 (https://ibs.renlab.org/) (Xie et al. 2022)

Fig. 5

Overview of the molecular mechanisms of eATP/iATP homeostasis by apyrases by Figdraw. Under the basal condition, apyrases can catalyze the breakdown of ATP and adenosine diphosphate (ADP) to generate adenosine monophosphate (AMP). Subsequently, 5’-nucleotidase (5’NT) hydrolyzes further AMP to extracellular adenosine (eAdo). The latter can be brought into the cytoplasm by the equilibrative nucleoside transporter 3 (ENT3) or further catalyzed by the extracellular purine-specific nucleoside hydrolase 3 (NSH3) to remove sugar moiety and generate adenine (Ade) that could be transported into the cytoplast by a purine permease transporter (PUP). Apyrases in Golgi may decrease the eATP level by reducing the secretory vesicles to transport ATP to the ECM. Enzymatic activities of some apyrases could be enhanced by calmodulin, whose activities would increase when eATP generated. DORN1 is regarded as the receptor for eATP, which could phosphorylate RBOHD and directly or indirectly involve in ROS and Ca²⁺ signaling pathways

Fig. 6

Roles of apyrases in plant growth and development by Figdraw. A Apyrase-mediated eATP to induce stomatal opening at low concentrations and stomatal closure at high concentrations. The heterotrimeric G protein may activate NADPH oxidase to connect ATP signaling with stomatal opening. B Apyrases may act as the downstream of Nod factor receptor (NFR) for both rhizobial and mycorrhizal symbioses. Lectin–nucleotide phosphohydrolase (LNP) contains a substrate specificity characteristic of apyrase and exhibits an ability to bind Nod factor for modulating the rhizobium–legume symbiosis. C Apyrases involve in polar auxin transport to regulate growth. D AtAPY1/2 are necessary for the light-induced growth of root and hook-cotyledon of seedlings. E Apyrases affect tuber morphology by regulating the concentrations of eATP released by growing cells

Fig. 7

Roles of apyrases in chilling tolerance, salt stress response and postharvest quality regulation by Figdraw. The treatment with phytosulfokine α (PSKα) contributed to reduction of apyrase expression and increase of eATP level. Apyrases could accelerate the vesicular trafficking to increase membrane repair and avoid the inhibition of vesicular trafficking by cold-induced ATP accumulation. The expressions of APY genes were upregulated by NaCl treatment. Salt-elicited eATP triggered the transcriptions of ethylene-related genes, such as AtEIN3, AtEIL1 and AtETR1, which further mediated H₂O₂ and cytosolic Ca²⁺ signaling cascades to regulate K⁺/Na⁺ homeostasis. In terms of postharvest quality, nano packaging was beneficial for delaying programmed cell death (PCD) during storage by inhibiting eATP increase and elevating apyrase activity. eATP induced DORN1 expression to regulate ROS while apyrases involved in the iATP/eATP homeostasis, which could ensure cell membrane integrity for improving cold tolerance. Arrows represented promotion, and termination symbols represented suppression. EIN3, Ethylene insensitive 3; ETR1, Ethylene response 1; EIL1, Ethylene insensitive-like 1; DORN1, Does Not Respond to Nucleotides1

Fig. 8

Roles of apyrases in pathogen attack response by Figdraw. The release of eATP caused by cellular damage after pathogen infection could be recognized by the eATP receptor to enhance the interaction between jasmonate ZIM-domain (JAZ) and coronatine-insensitive1 (COI1) proteasome and then to increase plant defense systems. Pathogenic fungi could target ecto-ATPase (PsAPY1) and achieve spore infection by secreting supprescins, an extracellular effector. On one hand, these supprescins participated in jasmonic acid (JA)-mediated signaling to attenuate salicylic acid (SA)-regulated defense. On the other hand, supprescins could inhibit the event that PsAPY1 initiated the apoplastic oxidative burst such as H₂O₂ production by copper amine oxidase and then affect pathogenic susceptibility. Arrows represented promotion, and termination symbols represented suppression

Fig. 9

Multiple functions of plant apyrase by Figdraw. 5’NT, 5’-nucleotidases; Ade, Adenine; Ado, Adenosine; ADP, Adenosine diphosphate; AMP, Adenosine monophosphate; CaM, Calmodulin; COI1, Coronatine-insensitive1; DORN1, Does Not Respond to Nucleotides1; eAde, Extracellular adenine; eAdo, Extracellular adenosine; eATP, Extracellular ATP; ENT3, Nucleoside transporter 3; iATP, Intracellular ATP; JAZ1, Jasmonate ZIM-domain 1; LNP, Lectin nucleotide phosphohydrolase; NDP, Nucleoside diphosphate; NFR, Nod factor receptor; NSH3, Nucleoside hydrolase 3; ROS, Reactive oxygen species