A Molecular Pinball Machine of the Plasma Membrane Regulates Plant Growth—A New Paradigm

Novel molecular pinball machines of the plasma membrane control cytosolic Ca<sup>2+</sup> levels that regulate plant metabolism. The essential components involve: 1. an auxin-activated proton pump; 2. arabinogalactan glycoproteins (AGPs); 3. Ca<sup>2+</sup> channels; 4. auxin...

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Main Authors: Derek T. A. Lamport, Li Tan, Marcia J. Kieliszewski
Format: Article
Language:English
Published: MDPI AG 2021-07-01
Series:Cells
Subjects:
Online Access:https://www.mdpi.com/2073-4409/10/8/1935
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author Derek T. A. Lamport
Li Tan
Marcia J. Kieliszewski
author_facet Derek T. A. Lamport
Li Tan
Marcia J. Kieliszewski
author_sort Derek T. A. Lamport
collection DOAJ
description Novel molecular pinball machines of the plasma membrane control cytosolic Ca<sup>2+</sup> levels that regulate plant metabolism. The essential components involve: 1. an auxin-activated proton pump; 2. arabinogalactan glycoproteins (AGPs); 3. Ca<sup>2+</sup> channels; 4. auxin-efflux “PIN” proteins. Typical pinball machines release pinballs that trigger various sound and visual effects. However, in plants, “proton pinballs” eject Ca<sup>2+</sup> bound by paired glucuronic acid residues of numerous glycomodules in periplasmic AGP-Ca<sup>2+</sup>. Freed Ca<sup>2+</sup> ions flow down the electrostatic gradient through open Ca<sup>2+</sup> channels into the cytosol, thus activating numerous Ca<sup>2+</sup>-dependent activities. Clearly, cytosolic Ca<sup>2+</sup> levels depend on the activity of the proton pump, the state of Ca<sup>2+</sup> channels and the size of the periplasmic AGP-Ca<sup>2+</sup> capacitor; proton pump activation is a major regulatory focal point tightly controlled by the supply of auxin. Auxin efflux carriers conveniently known as “PIN” proteins (null mutants are pin-shaped) pump auxin from cell to cell. Mechanosensitive Ca<sup>2+</sup> channels and their activation by reactive oxygen species (ROS) are yet another factor regulating cytosolic Ca<sup>2+</sup>. Cell expansion also triggers proton pump/pinball activity by the mechanotransduction of wall stress via Hechtian adhesion, thus forming a Hechtian oscillator that underlies cycles of wall plasticity and oscillatory growth. Finally, the Ca<sup>2+</sup> homeostasis of plants depends on cell surface external storage as a source of dynamic Ca<sup>2+</sup>, unlike the internal ER storage source of animals, where the added regulatory complexities ranging from vitamin D to parathormone contrast with the elegant simplicity of plant life. This paper summarizes a sixty-year Odyssey.
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spelling doaj.art-e3517b87ef544b62a14bde7361ca4fce2023-11-22T07:09:24ZengMDPI AGCells2073-44092021-07-01108193510.3390/cells10081935A Molecular Pinball Machine of the Plasma Membrane Regulates Plant Growth—A New ParadigmDerek T. A. Lamport0Li Tan1Marcia J. Kieliszewski2School of Life Sciences, University of Sussex, Falmer, Brighton BN1 9QG, UKComplex Carbohydrate Research Center, University of Georgia, Athens, GA 30602, USADepartment of Chemistry and Biochemistry, Ohio University, Athens, OH 45701, USANovel molecular pinball machines of the plasma membrane control cytosolic Ca<sup>2+</sup> levels that regulate plant metabolism. The essential components involve: 1. an auxin-activated proton pump; 2. arabinogalactan glycoproteins (AGPs); 3. Ca<sup>2+</sup> channels; 4. auxin-efflux “PIN” proteins. Typical pinball machines release pinballs that trigger various sound and visual effects. However, in plants, “proton pinballs” eject Ca<sup>2+</sup> bound by paired glucuronic acid residues of numerous glycomodules in periplasmic AGP-Ca<sup>2+</sup>. Freed Ca<sup>2+</sup> ions flow down the electrostatic gradient through open Ca<sup>2+</sup> channels into the cytosol, thus activating numerous Ca<sup>2+</sup>-dependent activities. Clearly, cytosolic Ca<sup>2+</sup> levels depend on the activity of the proton pump, the state of Ca<sup>2+</sup> channels and the size of the periplasmic AGP-Ca<sup>2+</sup> capacitor; proton pump activation is a major regulatory focal point tightly controlled by the supply of auxin. Auxin efflux carriers conveniently known as “PIN” proteins (null mutants are pin-shaped) pump auxin from cell to cell. Mechanosensitive Ca<sup>2+</sup> channels and their activation by reactive oxygen species (ROS) are yet another factor regulating cytosolic Ca<sup>2+</sup>. Cell expansion also triggers proton pump/pinball activity by the mechanotransduction of wall stress via Hechtian adhesion, thus forming a Hechtian oscillator that underlies cycles of wall plasticity and oscillatory growth. Finally, the Ca<sup>2+</sup> homeostasis of plants depends on cell surface external storage as a source of dynamic Ca<sup>2+</sup>, unlike the internal ER storage source of animals, where the added regulatory complexities ranging from vitamin D to parathormone contrast with the elegant simplicity of plant life. This paper summarizes a sixty-year Odyssey.https://www.mdpi.com/2073-4409/10/8/1935arabinogalactan proteinproton pumpcalcium signallingauxinPIN proteinsmorphogenesis
spellingShingle Derek T. A. Lamport
Li Tan
Marcia J. Kieliszewski
A Molecular Pinball Machine of the Plasma Membrane Regulates Plant Growth—A New Paradigm
Cells
arabinogalactan protein
proton pump
calcium signalling
auxin
PIN proteins
morphogenesis
title A Molecular Pinball Machine of the Plasma Membrane Regulates Plant Growth—A New Paradigm
title_full A Molecular Pinball Machine of the Plasma Membrane Regulates Plant Growth—A New Paradigm
title_fullStr A Molecular Pinball Machine of the Plasma Membrane Regulates Plant Growth—A New Paradigm
title_full_unstemmed A Molecular Pinball Machine of the Plasma Membrane Regulates Plant Growth—A New Paradigm
title_short A Molecular Pinball Machine of the Plasma Membrane Regulates Plant Growth—A New Paradigm
title_sort molecular pinball machine of the plasma membrane regulates plant growth a new paradigm
topic arabinogalactan protein
proton pump
calcium signalling
auxin
PIN proteins
morphogenesis
url https://www.mdpi.com/2073-4409/10/8/1935
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