P2K1 Receptor, Heterotrimeric Gα Protein and CNGC2/4 Are Involved in Extracellular ATP-Promoted Ion Influx in the Pollen of Arabidopsis thaliana.

Yansheng Wu,Baozhi Qin,Zhonglin Shang,Kaili Feng,Xinyue Liu,Erfang Kang,Jiawei Xu,Hongmin Yin

doi:10.3390/plants10081743

Yansheng Wu, Baozhi Qin + Show 6 more

Open Access

https://doi.org/10.3390/plants10081743

Copy DOI

Abstract

As an apoplastic signal, extracellular ATP (eATP) is involved in plant growth and development. eATP promotes tobacco pollen germination (PG) and pollen tube growth (PTG) by stimulating Ca2+ or K+ absorption. Nevertheless, the mechanisms underlying eATP-stimulated ion uptake and their role in PG and PTG are still unclear. Here, ATP addition was found to modulate PG and PTG in 34 plant species and showed a promoting effect in most of these species. Furthermore, by using Arabidopsis thaliana as a model, the role of several signaling components involved in eATP-promoted ion (Ca2+, K+) uptake, PG, and PTG were investigated. ATP stimulated while apyrase inhibited PG and PTG. Patch-clamping results showed that ATP promoted K+ and Ca2+ influx into pollen protoplasts. In loss-of-function mutants of P2K1 (dorn1-1 and dorn1-3), heterotrimeric G protein α subunit (gpa1-1, gpa1-2), or cyclic nucleotide gated ion channel (cngc2, cngc4), eATP-stimulated PG, PTG, and ion influx were all impaired. Our results suggest that these signaling components may be involved in eATP-promoted PG and PTG by regulating Ca2+ or K+ influx in Arabidopsis pollen grains.

Highlights

The apoplast, including the cell wall and intercellular space, plays essential roles in modulating plant cell growth and development due to the existence of numerous signaling molecules within the apoplastic matrix
In recent years, growing evidence has shown that adenosine triphosphate (ATP) is present in the apoplast and participates in physiological processes such as vegetative growth, development, and stress response [1,2,3,4]. extracellular ATP (eATP) is involved in maintaining cell viability [5] and the growth rate of cultured cells [6], regulating the rate or direction of the growth of roots [7], hypocotyls [8,9], and cotton fibers [10]
We have reported that eATP stimulates the pollen germination (PG) and pollen tube growth (PTG) of Nicotiana tabacum by facilitating K+ or Ca2+ uptake [63]

Summary

Introduction

The apoplast, including the cell wall and intercellular space, plays essential roles in modulating plant cell growth and development due to the existence of numerous signaling molecules within the apoplastic matrix. EATP is involved in maintaining cell viability [5] and the growth rate of cultured cells [6], regulating the rate or direction of the growth of roots [7], hypocotyls [8,9], and cotton fibers [10]. As a component of the cell wall and a cytoplasmic messenger, Ca2+ ions play essential roles in PG and PTG [31,32,42,43,44,45]. We firstly investigated the response of pollen from 34 plant species to ATP addition and elucidated the role of several signaling components in eATP-regulated PG and PTG of Arabidopsis thaliana

ATP Addition Impacts PG and PTG in Pollens from 34 Species

ATP Regulates PG and PTG of Arabidopsis thaliana

Signaling Underlying ATP-Regulated PG and PTG of Arabidopsis thaliana

Plant Materials

In Vitro Pollen Germination