Extracellular AMP Inhibits Pollen Tube Growth in <i>Picea meyeri</i> via Disrupted Calcium Gradient and Disorganized Microfilaments

Adenosine monophosphate (AMP) is a hydrolysis product of adenosine triphosphate (ATP) and adenosine diphosphate (ADP). In mammalian cells, extracellular AMP functions as a signaling molecule by binding to adenosine A1 receptors, thereby activating various intracellular signaling pathways. However, t...

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Main Authors: Junhui Zhou, Haobo Yang, Yue Zhang, Yuan Cao, Yanping Jing
Format: Article
Language:English
Published: MDPI AG 2024-12-01
Series:Plants
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Online Access:https://www.mdpi.com/2223-7747/14/1/72
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author Junhui Zhou
Haobo Yang
Yue Zhang
Yuan Cao
Yanping Jing
author_facet Junhui Zhou
Haobo Yang
Yue Zhang
Yuan Cao
Yanping Jing
author_sort Junhui Zhou
collection DOAJ
description Adenosine monophosphate (AMP) is a hydrolysis product of adenosine triphosphate (ATP) and adenosine diphosphate (ADP). In mammalian cells, extracellular AMP functions as a signaling molecule by binding to adenosine A1 receptors, thereby activating various intracellular signaling pathways. However, the role of extracellular AMP in plant cells remains largely unclear, and homologs of A1 receptors have not been identified. Our previous studies have demonstrated that extracellular ATP (eATP) is crucial for the normal germination and growth of <i>Picea meyeri</i> pollen tubes. In the present study, we observed that the exogenous addition of ATP to a pollen culture medium could be degraded into AMP and adenosine. Furthermore, the addition of AMP and adenosine to the culture medium was found to inhibit pollen germination and tube elongation. Notably, the addition of an AMP receptor inhibitor into the culture medium mitigated the inhibitory effects of AMP on pollen tube growth. Through intracellular staining for Ca<sup>2+</sup> and microfilaments, we discovered that high concentrations of AMP disrupt the Ca<sup>2+</sup> concentration gradient and impair microfilament organization, ultimately resulting in inhibited pollen tube elongation. In conclusion, we propose that extracellular AMP, as a hydrolysis product of eATP, also plays a significant role in regulating <i>P. meyeri</i> pollen germination and tube growth in vitro.
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spelling doaj-art-93a69a26601640e4a8e4cd4ddcb002ef2025-01-10T13:19:40ZengMDPI AGPlants2223-77472024-12-011417210.3390/plants14010072Extracellular AMP Inhibits Pollen Tube Growth in <i>Picea meyeri</i> via Disrupted Calcium Gradient and Disorganized MicrofilamentsJunhui Zhou0Haobo Yang1Yue Zhang2Yuan Cao3Yanping Jing4State Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, ChinaState Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, ChinaState Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, ChinaState Key Laboratory of Tree Genetics and Breeding, Chinese Academy of Forestry, Beijing 100091, ChinaState Key Laboratory of Tree Genetics and Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, ChinaAdenosine monophosphate (AMP) is a hydrolysis product of adenosine triphosphate (ATP) and adenosine diphosphate (ADP). In mammalian cells, extracellular AMP functions as a signaling molecule by binding to adenosine A1 receptors, thereby activating various intracellular signaling pathways. However, the role of extracellular AMP in plant cells remains largely unclear, and homologs of A1 receptors have not been identified. Our previous studies have demonstrated that extracellular ATP (eATP) is crucial for the normal germination and growth of <i>Picea meyeri</i> pollen tubes. In the present study, we observed that the exogenous addition of ATP to a pollen culture medium could be degraded into AMP and adenosine. Furthermore, the addition of AMP and adenosine to the culture medium was found to inhibit pollen germination and tube elongation. Notably, the addition of an AMP receptor inhibitor into the culture medium mitigated the inhibitory effects of AMP on pollen tube growth. Through intracellular staining for Ca<sup>2+</sup> and microfilaments, we discovered that high concentrations of AMP disrupt the Ca<sup>2+</sup> concentration gradient and impair microfilament organization, ultimately resulting in inhibited pollen tube elongation. In conclusion, we propose that extracellular AMP, as a hydrolysis product of eATP, also plays a significant role in regulating <i>P. meyeri</i> pollen germination and tube growth in vitro.https://www.mdpi.com/2223-7747/14/1/72extracellular AMPpollen tube growth<i>Picea meyeri</i>calcium gradientmicrofilament
spellingShingle Junhui Zhou
Haobo Yang
Yue Zhang
Yuan Cao
Yanping Jing
Extracellular AMP Inhibits Pollen Tube Growth in <i>Picea meyeri</i> via Disrupted Calcium Gradient and Disorganized Microfilaments
Plants
extracellular AMP
pollen tube growth
<i>Picea meyeri</i>
calcium gradient
microfilament
title Extracellular AMP Inhibits Pollen Tube Growth in <i>Picea meyeri</i> via Disrupted Calcium Gradient and Disorganized Microfilaments
title_full Extracellular AMP Inhibits Pollen Tube Growth in <i>Picea meyeri</i> via Disrupted Calcium Gradient and Disorganized Microfilaments
title_fullStr Extracellular AMP Inhibits Pollen Tube Growth in <i>Picea meyeri</i> via Disrupted Calcium Gradient and Disorganized Microfilaments
title_full_unstemmed Extracellular AMP Inhibits Pollen Tube Growth in <i>Picea meyeri</i> via Disrupted Calcium Gradient and Disorganized Microfilaments
title_short Extracellular AMP Inhibits Pollen Tube Growth in <i>Picea meyeri</i> via Disrupted Calcium Gradient and Disorganized Microfilaments
title_sort extracellular amp inhibits pollen tube growth in i picea meyeri i via disrupted calcium gradient and disorganized microfilaments
topic extracellular AMP
pollen tube growth
<i>Picea meyeri</i>
calcium gradient
microfilament
url https://www.mdpi.com/2223-7747/14/1/72
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AT haoboyang extracellularampinhibitspollentubegrowthinipiceameyeriiviadisruptedcalciumgradientanddisorganizedmicrofilaments
AT yuezhang extracellularampinhibitspollentubegrowthinipiceameyeriiviadisruptedcalciumgradientanddisorganizedmicrofilaments
AT yuancao extracellularampinhibitspollentubegrowthinipiceameyeriiviadisruptedcalciumgradientanddisorganizedmicrofilaments
AT yanpingjing extracellularampinhibitspollentubegrowthinipiceameyeriiviadisruptedcalciumgradientanddisorganizedmicrofilaments