Extracellular Spermine Triggers a Rapid Intracellular Phosphatidic Acid Response in Arabidopsis, Involving PLDδ Activation and Stimulating Ion Flux
Polyamines, such as putrescine (Put), spermidine (Spd), and spermine (Spm), are low-molecular-weight polycationic molecules found in all living organisms. Despite the fact that they have been implicated in various important developmental and adaptative processes, their mode of action is still largel...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-05-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fpls.2019.00601/full |
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| author | Xavier Zarza Xavier Zarza Lana Shabala Miki Fujita Sergey Shabala Michel A. Haring Antonio F. Tiburcio Teun Munnik Teun Munnik |
| author_facet | Xavier Zarza Xavier Zarza Lana Shabala Miki Fujita Sergey Shabala Michel A. Haring Antonio F. Tiburcio Teun Munnik Teun Munnik |
| author_sort | Xavier Zarza |
| collection | DOAJ |
| description | Polyamines, such as putrescine (Put), spermidine (Spd), and spermine (Spm), are low-molecular-weight polycationic molecules found in all living organisms. Despite the fact that they have been implicated in various important developmental and adaptative processes, their mode of action is still largely unclear. Here, we report that Put, Spd, and Spm trigger a rapid increase in the signaling lipid, phosphatidic acid (PA) in Arabidopsis seedlings but also mature leaves. Using time-course and dose-response experiments, Spm was found to be the most effective; promoting PA responses at physiological (low μM) concentrations. In seedlings, the increase of PA occurred mainly in the root and partly involved the plasma membrane polyamine-uptake transporter (PUT), RMV1. Using a differential 32Pi-labeling strategy combined with transphosphatidylation assays and T-DNA insertion mutants, we found that phospholipase D (PLD), and in particular PLDδ was the main contributor of the increase in PA. Measuring non-invasive ion fluxes (MIFE) across the root plasma membrane of wild type and pldδ-mutant seedlings, revealed that the formation of PA is linked to a gradual- and transient efflux of K+. Potential mechanisms of how PLDδ and the increase of PA are involved in polyamine function is discussed. |
| first_indexed | 2024-12-13T12:23:00Z |
| format | Article |
| id | doaj.art-449b85930f574a44ba44e39bdefe558d |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-12-13T12:23:00Z |
| publishDate | 2019-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-449b85930f574a44ba44e39bdefe558d2022-12-21T23:46:32ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2019-05-011010.3389/fpls.2019.00601458425Extracellular Spermine Triggers a Rapid Intracellular Phosphatidic Acid Response in Arabidopsis, Involving PLDδ Activation and Stimulating Ion FluxXavier Zarza0Xavier Zarza1Lana Shabala2Miki Fujita3Sergey Shabala4Michel A. Haring5Antonio F. Tiburcio6Teun Munnik7Teun Munnik8Plant Cell Biology, Swammerdam Institute for Life Sciences, University of Amsterdam, Amsterdam, NetherlandsPlant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, Amsterdam, NetherlandsTasmanian Institute of Agriculture, University of Tasmania, Hobart, TAS, AustraliaGene Discovery Research Group, RIKEN Plant Science Center, Tsukuba, JapanTasmanian Institute of Agriculture, University of Tasmania, Hobart, TAS, AustraliaPlant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, Amsterdam, NetherlandsDepartment of Biology, Healthcare and the Environment, Faculty of Pharmacy, University of Barcelona, Barcelona, SpainPlant Cell Biology, Swammerdam Institute for Life Sciences, University of Amsterdam, Amsterdam, NetherlandsPlant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, Amsterdam, NetherlandsPolyamines, such as putrescine (Put), spermidine (Spd), and spermine (Spm), are low-molecular-weight polycationic molecules found in all living organisms. Despite the fact that they have been implicated in various important developmental and adaptative processes, their mode of action is still largely unclear. Here, we report that Put, Spd, and Spm trigger a rapid increase in the signaling lipid, phosphatidic acid (PA) in Arabidopsis seedlings but also mature leaves. Using time-course and dose-response experiments, Spm was found to be the most effective; promoting PA responses at physiological (low μM) concentrations. In seedlings, the increase of PA occurred mainly in the root and partly involved the plasma membrane polyamine-uptake transporter (PUT), RMV1. Using a differential 32Pi-labeling strategy combined with transphosphatidylation assays and T-DNA insertion mutants, we found that phospholipase D (PLD), and in particular PLDδ was the main contributor of the increase in PA. Measuring non-invasive ion fluxes (MIFE) across the root plasma membrane of wild type and pldδ-mutant seedlings, revealed that the formation of PA is linked to a gradual- and transient efflux of K+. Potential mechanisms of how PLDδ and the increase of PA are involved in polyamine function is discussed.https://www.frontiersin.org/article/10.3389/fpls.2019.00601/fullphospholipase D (PLD)phosphatidic acid (PA)lipid signalingpolyamines (putrescinespermidinespermine) |
| spellingShingle | Xavier Zarza Xavier Zarza Lana Shabala Miki Fujita Sergey Shabala Michel A. Haring Antonio F. Tiburcio Teun Munnik Teun Munnik Extracellular Spermine Triggers a Rapid Intracellular Phosphatidic Acid Response in Arabidopsis, Involving PLDδ Activation and Stimulating Ion Flux Frontiers in Plant Science phospholipase D (PLD) phosphatidic acid (PA) lipid signaling polyamines (putrescine spermidine spermine) |
| title | Extracellular Spermine Triggers a Rapid Intracellular Phosphatidic Acid Response in Arabidopsis, Involving PLDδ Activation and Stimulating Ion Flux |
| title_full | Extracellular Spermine Triggers a Rapid Intracellular Phosphatidic Acid Response in Arabidopsis, Involving PLDδ Activation and Stimulating Ion Flux |
| title_fullStr | Extracellular Spermine Triggers a Rapid Intracellular Phosphatidic Acid Response in Arabidopsis, Involving PLDδ Activation and Stimulating Ion Flux |
| title_full_unstemmed | Extracellular Spermine Triggers a Rapid Intracellular Phosphatidic Acid Response in Arabidopsis, Involving PLDδ Activation and Stimulating Ion Flux |
| title_short | Extracellular Spermine Triggers a Rapid Intracellular Phosphatidic Acid Response in Arabidopsis, Involving PLDδ Activation and Stimulating Ion Flux |
| title_sort | extracellular spermine triggers a rapid intracellular phosphatidic acid response in arabidopsis involving pldδ activation and stimulating ion flux |
| topic | phospholipase D (PLD) phosphatidic acid (PA) lipid signaling polyamines (putrescine spermidine spermine) |
| url | https://www.frontiersin.org/article/10.3389/fpls.2019.00601/full |
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