title: A precise spacing between the NPA domains of aquaporins is essential for silicon permeability in plants.
abstract: The controversy surrounding silicon (Si) benefits and essentiality in plants is exacerbated by the differential ability of species to absorb this element. This property is seemingly enhanced in species carrying specific nodulin 26-like intrinsic proteins (NIPs), a subclass of aquaporins. In this work, our aim was to characterize plant aquaporins to define the features that confer Si permeability. Through comparative analysis of 985 aquaporins in 25 species with differing abilities to absorb Si, we were able to predict 30 Si transporters and discovered that Si absorption is exclusively confined to species that possess NIP-III aquaporins with a GSGR selectivity filter and a precise distance of 108 amino acids (AA) between the asparagine-proline-alanine (NPA) domains. The latter feature is of particular significance since it had never been reported to be essential for Si selectivity. Functionality assessed in the Xenopus oocyte expression system showed that NIPs with 108 AA spacing exhibited Si permeability, while proteins differing in that distance did not. In subsequent functional studies, a Si transporter from poplar mutated into variants with 109- or 107-AA spacing failed to import, and a tomato NIP gene mutated from 109 to 108 AA exhibited a rare gain of function. These results provide a precise molecular basis to classify higher plants into Si accumulators or excluders.
authors.affiliation: Département de Phytologie, Faculté des Sciences de l'Agriculture et de l'Alimentation, Centre de Recherche en Horticulture, Université Laval, Québec, QC, Canada.
authors.forename: Rupesh Kailasrao
authors.identifier: http://orcid.org/0000-0003-4167-6552
authors.initials: RK
authors.lastname: Deshmukh
authors.affiliation: Département de Phytologie, Faculté des Sciences de l'Agriculture et de l'Alimentation, Centre de Recherche en Horticulture, Université Laval, Québec, QC, Canada.
authors.forename: Julien
authors.initials: J
authors.lastname: Vivancos
authors.affiliation: Département de Phytologie, Faculté des Sciences de l'Agriculture et de l'Alimentation, Centre de Recherche en Horticulture, Université Laval, Québec, QC, Canada.
authors.forename: Gowsica
authors.initials: G
authors.lastname: Ramakrishnan
authors.affiliation: Département de Phytologie, Faculté des Sciences de l'Agriculture et de l'Alimentation, Centre de Recherche en Horticulture, Université Laval, Québec, QC, Canada.
authors.forename: Valérie
authors.initials: V
authors.lastname: Guérin
authors.affiliation: Nephrology Group, L'Hôtel-Dieu de Québec Institution, Department of Medicine, Faculty of Medicine, Université Laval, Québec, QC, G1R 2J6, Canada.
authors.forename: Gabriel
authors.initials: G
authors.lastname: Carpentier
authors.affiliation: Département de Phytologie, Faculté des Sciences de l'Agriculture et de l'Alimentation, Centre de Recherche en Horticulture, Université Laval, Québec, QC, Canada.
authors.forename: Humira
authors.initials: H
authors.lastname: Sonah
authors.affiliation: Département de Phytologie, Faculté des Sciences de l'Agriculture et de l'Alimentation, Centre de Recherche en Horticulture, Université Laval, Québec, QC, Canada.
authors.forename: Caroline
authors.initials: C
authors.lastname: Labbé
authors.affiliation: Nephrology Group, L'Hôtel-Dieu de Québec Institution, Department of Medicine, Faculty of Medicine, Université Laval, Québec, QC, G1R 2J6, Canada.
authors.forename: Paul
authors.initials: P
authors.lastname: Isenring
authors.affiliation: Département de Phytologie, Faculté des Sciences de l'Agriculture et de l'Alimentation, Centre de Recherche en Horticulture, Université Laval, Québec, QC, Canada.
authors.forename: Francois J
authors.initials: FJ
authors.lastname: Belzile
authors.affiliation: Département de Phytologie, Faculté des Sciences de l'Agriculture et de l'Alimentation, Centre de Recherche en Horticulture, Université Laval, Québec, QC, Canada.
authors.forename: Richard R
authors.initials: RR
authors.lastname: Bélanger
mesh_terms: D000818:Animals; D020346:Aquaporins / Q000235:genetics*; D023281:Genomics; D009842:Oligopeptides / Q000235:genetics*; D012825:Silicon / Q000378:metabolism*; D014982:Xenopus laevis
chemical_list: D020346:Aquaporins; D009842:Oligopeptides; C550288:asparagine-proline-alanine; D012825:Silicon
keywords: NPA domains; aquaporins; comparative genomics; plant species; silicon role in plants; silicon transporter