Si permeability of a deficient Lsi1 aquaporin in tobacco can be enhanced through a conserved residue substitution

Abstract Silicon (Si) is a beneficial substrate for many plants, conferring heightened resilience to environmental stress. A plant's ability to absorb Si is primarily dependent on the presence of a Si‐permeable Lsi1 (NIP2‐1) aquaporin in its roots. Structure‐function analyses of Lsi1 channels f...

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Main Authors: Devrim Coskun, Rupesh Deshmukh, Humira Sonah, Sheelavanta Matha Shivaraj, Rachelle Frenette‐Cotton, Laurence Tremblay, Paul Isenring, Richard R. Bélanger
Format: Article
Language:English
Published: Wiley 2019-08-01
Series:Plant Direct
Subjects:
Online Access:https://doi.org/10.1002/pld3.163
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spelling doaj-b4d388f794404cd79c81ac6f1f237ed22021-05-02T19:25:33ZengWileyPlant Direct2475-44552019-08-0138n/an/a10.1002/pld3.163Si permeability of a deficient Lsi1 aquaporin in tobacco can be enhanced through a conserved residue substitutionDevrim Coskun0Rupesh Deshmukh1Humira Sonah2Sheelavanta Matha Shivaraj3Rachelle Frenette‐Cotton4Laurence Tremblay5Paul Isenring6Richard R. Bélanger7Département de Phytologie, Faculté des Sciences de l’Agriculture et de l’Alimentation (FSAA) Université Laval Québec QC CanadaDépartement de Phytologie, Faculté des Sciences de l’Agriculture et de l’Alimentation (FSAA) Université Laval Québec QC CanadaDépartement de Phytologie, Faculté des Sciences de l’Agriculture et de l’Alimentation (FSAA) Université Laval Québec QC CanadaDépartement de Phytologie, Faculté des Sciences de l’Agriculture et de l’Alimentation (FSAA) Université Laval Québec QC CanadaNephrology Group, Department of Medicine, Faculty of Medicine, L’Hôtel‐Dieu de Québec Institution Université Laval Québec QC CanadaNephrology Group, Department of Medicine, Faculty of Medicine, L’Hôtel‐Dieu de Québec Institution Université Laval Québec QC CanadaNephrology Group, Department of Medicine, Faculty of Medicine, L’Hôtel‐Dieu de Québec Institution Université Laval Québec QC CanadaDépartement de Phytologie, Faculté des Sciences de l’Agriculture et de l’Alimentation (FSAA) Université Laval Québec QC CanadaAbstract Silicon (Si) is a beneficial substrate for many plants, conferring heightened resilience to environmental stress. A plant's ability to absorb Si is primarily dependent on the presence of a Si‐permeable Lsi1 (NIP2‐1) aquaporin in its roots. Structure‐function analyses of Lsi1 channels from higher plants have thus far revealed two key molecular determinants of Si permeability: (a) the amino acid motif GSGR in the aromatic/arginine selectivity filter and (b) 108 amino acids between two highly conserved NPA domains. Curiously, tobacco (Nicotiana sylvestris) stands as a rare exception as it possesses an Lsi1 (NsLsi1) with these molecular signatures but is reported as a low Si accumulator. The aim of this study was therefore to identify whether additional determinants influence Si permeability via Lsi1 channels, focusing on the role of residues that differ uniquely in NsLsi1 relative to functional Lsi1 homologs. We observed tobacco indeed absorbed Si poorly (0.1% dw), despite NsLsi1 being expressed constitutively in planta. Si influx measured in NsLsi1‐expressing Xenopus oocytes was very low (<13% that of OsLsi1 from rice (Oryza sativa) over a 3‐hr time course), which likely explains why tobacco is a low Si accumulator. Interestingly, NsLsi1P125F displayed a significant gain of function (threefold increase in Si influx relative to NsLsi1WT), which coincided with a threefold increase in plasma membrane localization in planta, as measured by transient expression of GFP constructs in Nicotiana benthamiana leaves. These findings thus reveal a novel molecular determinant of Si transport in plants and inform breeding, biotechnological, and agricultural practices to effectively utilize Si in the context of plant resilience to environmental stress.https://doi.org/10.1002/pld3.163aquaporininfluxLsi1molecular determinantsNIP2‐1silicon (Si)
collection DOAJ
language English
format Article
sources DOAJ
author Devrim Coskun
Rupesh Deshmukh
Humira Sonah
Sheelavanta Matha Shivaraj
Rachelle Frenette‐Cotton
Laurence Tremblay
Paul Isenring
Richard R. Bélanger
spellingShingle Devrim Coskun
Rupesh Deshmukh
Humira Sonah
Sheelavanta Matha Shivaraj
Rachelle Frenette‐Cotton
Laurence Tremblay
Paul Isenring
Richard R. Bélanger
Si permeability of a deficient Lsi1 aquaporin in tobacco can be enhanced through a conserved residue substitution
Plant Direct
aquaporin
influx
Lsi1
molecular determinants
NIP2‐1
silicon (Si)
author_facet Devrim Coskun
Rupesh Deshmukh
Humira Sonah
Sheelavanta Matha Shivaraj
Rachelle Frenette‐Cotton
Laurence Tremblay
Paul Isenring
Richard R. Bélanger
author_sort Devrim Coskun
title Si permeability of a deficient Lsi1 aquaporin in tobacco can be enhanced through a conserved residue substitution
title_short Si permeability of a deficient Lsi1 aquaporin in tobacco can be enhanced through a conserved residue substitution
title_full Si permeability of a deficient Lsi1 aquaporin in tobacco can be enhanced through a conserved residue substitution
title_fullStr Si permeability of a deficient Lsi1 aquaporin in tobacco can be enhanced through a conserved residue substitution
title_full_unstemmed Si permeability of a deficient Lsi1 aquaporin in tobacco can be enhanced through a conserved residue substitution
title_sort si permeability of a deficient lsi1 aquaporin in tobacco can be enhanced through a conserved residue substitution
publisher Wiley
series Plant Direct
issn 2475-4455
publishDate 2019-08-01
description Abstract Silicon (Si) is a beneficial substrate for many plants, conferring heightened resilience to environmental stress. A plant's ability to absorb Si is primarily dependent on the presence of a Si‐permeable Lsi1 (NIP2‐1) aquaporin in its roots. Structure‐function analyses of Lsi1 channels from higher plants have thus far revealed two key molecular determinants of Si permeability: (a) the amino acid motif GSGR in the aromatic/arginine selectivity filter and (b) 108 amino acids between two highly conserved NPA domains. Curiously, tobacco (Nicotiana sylvestris) stands as a rare exception as it possesses an Lsi1 (NsLsi1) with these molecular signatures but is reported as a low Si accumulator. The aim of this study was therefore to identify whether additional determinants influence Si permeability via Lsi1 channels, focusing on the role of residues that differ uniquely in NsLsi1 relative to functional Lsi1 homologs. We observed tobacco indeed absorbed Si poorly (0.1% dw), despite NsLsi1 being expressed constitutively in planta. Si influx measured in NsLsi1‐expressing Xenopus oocytes was very low (<13% that of OsLsi1 from rice (Oryza sativa) over a 3‐hr time course), which likely explains why tobacco is a low Si accumulator. Interestingly, NsLsi1P125F displayed a significant gain of function (threefold increase in Si influx relative to NsLsi1WT), which coincided with a threefold increase in plasma membrane localization in planta, as measured by transient expression of GFP constructs in Nicotiana benthamiana leaves. These findings thus reveal a novel molecular determinant of Si transport in plants and inform breeding, biotechnological, and agricultural practices to effectively utilize Si in the context of plant resilience to environmental stress.
topic aquaporin
influx
Lsi1
molecular determinants
NIP2‐1
silicon (Si)
url https://doi.org/10.1002/pld3.163
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