Localization and quantification of plasma membrane aquaporin expression in maize primary root: A clue to understanding their role as cellular plumbers

Charles Hachez; Menachem Moshelion; Enric Zelazny; Damien Cavez; François Chaumont

doi:10.1007/s11103-006-9022-1

Localization and quantification of plasma membrane aquaporin expression in maize primary root: A clue to understanding their role as cellular plumbers

Charles Hachez, Menachem Moshelion, Enric Zelazny, Damien Cavez, François Chaumont^*

^*Corresponding author for this work

Institute of Plant Sciences and Genetics in Agriculture

Research output: Contribution to journal › Article › peer-review

200 Scopus citations

Abstract

Water movement across root tissues occurs by parallel apoplastic, symplastic, and transcellular pathways that the plant can control to a certain extent. Because water channels or aquaporins (AQPs) play an important role in regulating water flow, studies on AQP mRNA and protein expression in different root tissues are essential. Here, we quantified and localized the expression of Zea mays plasma membrane AQPs (ZmPIPs) in primary root tip using in situ and quantitative RT-PCR and immunodetection approaches. All ZmPIP genes except ZmPIP2;7 were expressed in primary roots. Expression was found to be dependent on the developmental stage of the root, with, in general, an increase in expression towards the elongation and mature zones. Two genes, ZmPIP1;5 and ZmPIP2;5, showed the greatest increase in expression (up to 11- and 17-fold, respectively) in the mature zone, where they accounted for 50% of the total expressed ZmPIPs. The immunocytochemical localization of ZmPIP2;1 and ZmPIP2;5 in the exodermis and endodermis indicated that they are involved in root radial water movement. In addition, we detected a polar localization of ZmPIP2;5 to the external periclinal side of epidermal cells in root apices, suggesting an important role in water uptake from the root surface. Finally, protoplast swelling assays showed that root cells display a variable, but globally low, osmotic water permeability coefficient (P _f < 10 μm/s). However, the presence of a population of cells with a higher P _f (up to 26 μm/s) in mature zone of the root might be correlated with the increased expression of several ZmPIP genes.

Original language	English
Pages (from-to)	305-323
Number of pages	19
Journal	Plant Molecular Biology
Volume	62
Issue number	1-2
DOIs	https://doi.org/10.1007/s11103-006-9022-1
State	Published - Sep 2006

Bibliographical note

Funding Information:
Acknowledgements This work was supported by grants from the Belgian National Fund for Scientific Research (FNRS), the Interuniversity Attraction Poles Programme—Belgian Science Policy, and the ‘‘Communauté franc¸aise de Belgique—Actions de Recherches Concertées’’. F.C. is a Senior Research Associate and C.H. a Research Fellow at the FNRS; E.Z. is a Research Fellow at the Fonds pour la Formation à la Recherche dans l’Industrie et dans l’Agriculture. We thank R. Jung (Pioneer Hi-Bred International) for providing ZmPIP cDNAs, M. Maeshima (Nagoya University, Japan) and M. Boutry (Uni-versité catholique de Louvain) for supplying the anti-RsPIP1 and anti-PMA antibodies, respectively, and T. Trombik and E. Peeters (Université catholique de Louvain) for supplying pGex-KG’ plasmid. We are very grateful to X. Draye and T. Lavigne for the use of the aeroponics facility and advices, and to M. Boutry and X. Draye for their critical reading of the manuscript.

Keywords

Aquaporin
PIP
Root water movement
mRNA and protein expression

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10.1007/s11103-006-9022-1

Cite this

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title = "Localization and quantification of plasma membrane aquaporin expression in maize primary root: A clue to understanding their role as cellular plumbers",

abstract = "Water movement across root tissues occurs by parallel apoplastic, symplastic, and transcellular pathways that the plant can control to a certain extent. Because water channels or aquaporins (AQPs) play an important role in regulating water flow, studies on AQP mRNA and protein expression in different root tissues are essential. Here, we quantified and localized the expression of Zea mays plasma membrane AQPs (ZmPIPs) in primary root tip using in situ and quantitative RT-PCR and immunodetection approaches. All ZmPIP genes except ZmPIP2;7 were expressed in primary roots. Expression was found to be dependent on the developmental stage of the root, with, in general, an increase in expression towards the elongation and mature zones. Two genes, ZmPIP1;5 and ZmPIP2;5, showed the greatest increase in expression (up to 11- and 17-fold, respectively) in the mature zone, where they accounted for 50% of the total expressed ZmPIPs. The immunocytochemical localization of ZmPIP2;1 and ZmPIP2;5 in the exodermis and endodermis indicated that they are involved in root radial water movement. In addition, we detected a polar localization of ZmPIP2;5 to the external periclinal side of epidermal cells in root apices, suggesting an important role in water uptake from the root surface. Finally, protoplast swelling assays showed that root cells display a variable, but globally low, osmotic water permeability coefficient (P f < 10 μm/s). However, the presence of a population of cells with a higher P f (up to 26 μm/s) in mature zone of the root might be correlated with the increased expression of several ZmPIP genes.",

keywords = "Aquaporin, PIP, Root water movement, mRNA and protein expression",

author = "Charles Hachez and Menachem Moshelion and Enric Zelazny and Damien Cavez and Fran{\c c}ois Chaumont",

note = "Funding Information: Acknowledgements This work was supported by grants from the Belgian National Fund for Scientific Research (FNRS), the Interuniversity Attraction Poles Programme—Belgian Science Policy, and the {\textquoteleft}{\textquoteleft}Communaut{\'e} franc¸aise de Belgique—Actions de Recherches Concert{\'e}es{\textquoteright}{\textquoteright}. F.C. is a Senior Research Associate and C.H. a Research Fellow at the FNRS; E.Z. is a Research Fellow at the Fonds pour la Formation {\`a} la Recherche dans l{\textquoteright}Industrie et dans l{\textquoteright}Agriculture. We thank R. Jung (Pioneer Hi-Bred International) for providing ZmPIP cDNAs, M. Maeshima (Nagoya University, Japan) and M. Boutry (Uni-versit{\'e} catholique de Louvain) for supplying the anti-RsPIP1 and anti-PMA antibodies, respectively, and T. Trombik and E. Peeters (Universit{\'e} catholique de Louvain) for supplying pGex-KG{\textquoteright} plasmid. We are very grateful to X. Draye and T. Lavigne for the use of the aeroponics facility and advices, and to M. Boutry and X. Draye for their critical reading of the manuscript.",

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AU - Cavez, Damien

AU - Chaumont, François

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N2 - Water movement across root tissues occurs by parallel apoplastic, symplastic, and transcellular pathways that the plant can control to a certain extent. Because water channels or aquaporins (AQPs) play an important role in regulating water flow, studies on AQP mRNA and protein expression in different root tissues are essential. Here, we quantified and localized the expression of Zea mays plasma membrane AQPs (ZmPIPs) in primary root tip using in situ and quantitative RT-PCR and immunodetection approaches. All ZmPIP genes except ZmPIP2;7 were expressed in primary roots. Expression was found to be dependent on the developmental stage of the root, with, in general, an increase in expression towards the elongation and mature zones. Two genes, ZmPIP1;5 and ZmPIP2;5, showed the greatest increase in expression (up to 11- and 17-fold, respectively) in the mature zone, where they accounted for 50% of the total expressed ZmPIPs. The immunocytochemical localization of ZmPIP2;1 and ZmPIP2;5 in the exodermis and endodermis indicated that they are involved in root radial water movement. In addition, we detected a polar localization of ZmPIP2;5 to the external periclinal side of epidermal cells in root apices, suggesting an important role in water uptake from the root surface. Finally, protoplast swelling assays showed that root cells display a variable, but globally low, osmotic water permeability coefficient (P f < 10 μm/s). However, the presence of a population of cells with a higher P f (up to 26 μm/s) in mature zone of the root might be correlated with the increased expression of several ZmPIP genes.

AB - Water movement across root tissues occurs by parallel apoplastic, symplastic, and transcellular pathways that the plant can control to a certain extent. Because water channels or aquaporins (AQPs) play an important role in regulating water flow, studies on AQP mRNA and protein expression in different root tissues are essential. Here, we quantified and localized the expression of Zea mays plasma membrane AQPs (ZmPIPs) in primary root tip using in situ and quantitative RT-PCR and immunodetection approaches. All ZmPIP genes except ZmPIP2;7 were expressed in primary roots. Expression was found to be dependent on the developmental stage of the root, with, in general, an increase in expression towards the elongation and mature zones. Two genes, ZmPIP1;5 and ZmPIP2;5, showed the greatest increase in expression (up to 11- and 17-fold, respectively) in the mature zone, where they accounted for 50% of the total expressed ZmPIPs. The immunocytochemical localization of ZmPIP2;1 and ZmPIP2;5 in the exodermis and endodermis indicated that they are involved in root radial water movement. In addition, we detected a polar localization of ZmPIP2;5 to the external periclinal side of epidermal cells in root apices, suggesting an important role in water uptake from the root surface. Finally, protoplast swelling assays showed that root cells display a variable, but globally low, osmotic water permeability coefficient (P f < 10 μm/s). However, the presence of a population of cells with a higher P f (up to 26 μm/s) in mature zone of the root might be correlated with the increased expression of several ZmPIP genes.

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Localization and quantification of plasma membrane aquaporin expression in maize primary root: A clue to understanding their role as cellular plumbers

Abstract

Bibliographical note

Keywords

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