Cargando…

Overexpression of X Intrinsic Protein 1;1 in Nicotiana tabacum and Arabidopsis reduces boron allocation to shoot sink tissues

Major Intrinsic Proteins (MIP) are a family of channels facilitating the diffusion of water and/or small solutes across cellular membranes. X Intrinsic Proteins (XIP) form the least characterized MIP subfamily in vascular plants. XIPs are mostly impermeable to water but facilitate the diffusion of h...

Descripción completa

Detalles Bibliográficos
Autores principales: Bienert, Manuela Desiree, Muries, Beatriz, Crappe, Delphine, Chaumont, François, Bienert, Gerd Patrick
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6549384/
https://www.ncbi.nlm.nih.gov/pubmed/31245781
http://dx.doi.org/10.1002/pld3.143
_version_ 1783423996262350848
author Bienert, Manuela Desiree
Muries, Beatriz
Crappe, Delphine
Chaumont, François
Bienert, Gerd Patrick
author_facet Bienert, Manuela Desiree
Muries, Beatriz
Crappe, Delphine
Chaumont, François
Bienert, Gerd Patrick
author_sort Bienert, Manuela Desiree
collection PubMed
description Major Intrinsic Proteins (MIP) are a family of channels facilitating the diffusion of water and/or small solutes across cellular membranes. X Intrinsic Proteins (XIP) form the least characterized MIP subfamily in vascular plants. XIPs are mostly impermeable to water but facilitate the diffusion of hydrogen peroxide, urea and boric acid when expressed in heterologous expression systems. However, their transport capabilities in planta and their impact on plant physiology are still unknown. Here, we demonstrated that overexpression of NtXIP1;1 in Nicotiana tabacum by the En2pPMA4 or the 35S CaMV promoter and in Arabidopsis, which does not contain any XIP gene, by the 35S CaMV promoter, resulted in boron (B)‐deficiency symptoms such as death of the shoot apical meristem, infertile flowers, and puckered leaves. Leaf B concentrations in symptomatic tissues and B xylem sap concentrations were lower in the overexpressors than in control plants. Importantly, expression of NtXIP1;1 under the control of the AtNIP5;1 promoter complemented the B deficiency phenotype of the Atnip5;1 knockout mutant, defining its ability to act as a boric acid channel in planta. Protein quantification analysis revealed that NtXIP1;1 was predominantly expressed in young B‐demanding tissues and induced under B‐deficient conditions. Our results strongly suggest that NtXIP1;1 plays a role in B homeostasis and its tissue‐specific expression critically contributes to the distribution of B within tobacco.
format Online
Article
Text
id pubmed-6549384
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher John Wiley and Sons Inc.
record_format MEDLINE/PubMed
spelling pubmed-65493842019-06-26 Overexpression of X Intrinsic Protein 1;1 in Nicotiana tabacum and Arabidopsis reduces boron allocation to shoot sink tissues Bienert, Manuela Desiree Muries, Beatriz Crappe, Delphine Chaumont, François Bienert, Gerd Patrick Plant Direct Original Research Major Intrinsic Proteins (MIP) are a family of channels facilitating the diffusion of water and/or small solutes across cellular membranes. X Intrinsic Proteins (XIP) form the least characterized MIP subfamily in vascular plants. XIPs are mostly impermeable to water but facilitate the diffusion of hydrogen peroxide, urea and boric acid when expressed in heterologous expression systems. However, their transport capabilities in planta and their impact on plant physiology are still unknown. Here, we demonstrated that overexpression of NtXIP1;1 in Nicotiana tabacum by the En2pPMA4 or the 35S CaMV promoter and in Arabidopsis, which does not contain any XIP gene, by the 35S CaMV promoter, resulted in boron (B)‐deficiency symptoms such as death of the shoot apical meristem, infertile flowers, and puckered leaves. Leaf B concentrations in symptomatic tissues and B xylem sap concentrations were lower in the overexpressors than in control plants. Importantly, expression of NtXIP1;1 under the control of the AtNIP5;1 promoter complemented the B deficiency phenotype of the Atnip5;1 knockout mutant, defining its ability to act as a boric acid channel in planta. Protein quantification analysis revealed that NtXIP1;1 was predominantly expressed in young B‐demanding tissues and induced under B‐deficient conditions. Our results strongly suggest that NtXIP1;1 plays a role in B homeostasis and its tissue‐specific expression critically contributes to the distribution of B within tobacco. John Wiley and Sons Inc. 2019-06-05 /pmc/articles/PMC6549384/ /pubmed/31245781 http://dx.doi.org/10.1002/pld3.143 Text en © 2019 The Authors. Plant Direct published by American Society of Plant Biologists, Society for Experimental Biology and John Wiley & Sons Ltd. This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Research
Bienert, Manuela Desiree
Muries, Beatriz
Crappe, Delphine
Chaumont, François
Bienert, Gerd Patrick
Overexpression of X Intrinsic Protein 1;1 in Nicotiana tabacum and Arabidopsis reduces boron allocation to shoot sink tissues
title Overexpression of X Intrinsic Protein 1;1 in Nicotiana tabacum and Arabidopsis reduces boron allocation to shoot sink tissues
title_full Overexpression of X Intrinsic Protein 1;1 in Nicotiana tabacum and Arabidopsis reduces boron allocation to shoot sink tissues
title_fullStr Overexpression of X Intrinsic Protein 1;1 in Nicotiana tabacum and Arabidopsis reduces boron allocation to shoot sink tissues
title_full_unstemmed Overexpression of X Intrinsic Protein 1;1 in Nicotiana tabacum and Arabidopsis reduces boron allocation to shoot sink tissues
title_short Overexpression of X Intrinsic Protein 1;1 in Nicotiana tabacum and Arabidopsis reduces boron allocation to shoot sink tissues
title_sort overexpression of x intrinsic protein 1;1 in nicotiana tabacum and arabidopsis reduces boron allocation to shoot sink tissues
topic Original Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6549384/
https://www.ncbi.nlm.nih.gov/pubmed/31245781
http://dx.doi.org/10.1002/pld3.143
work_keys_str_mv AT bienertmanueladesiree overexpressionofxintrinsicprotein11innicotianatabacumandarabidopsisreducesboronallocationtoshootsinktissues
AT muriesbeatriz overexpressionofxintrinsicprotein11innicotianatabacumandarabidopsisreducesboronallocationtoshootsinktissues
AT crappedelphine overexpressionofxintrinsicprotein11innicotianatabacumandarabidopsisreducesboronallocationtoshootsinktissues
AT chaumontfrancois overexpressionofxintrinsicprotein11innicotianatabacumandarabidopsisreducesboronallocationtoshootsinktissues
AT bienertgerdpatrick overexpressionofxintrinsicprotein11innicotianatabacumandarabidopsisreducesboronallocationtoshootsinktissues