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Life with and without AtTIP1;1, an Arabidopsis aquaporin preferentially localized in the apposing tonoplasts of adjacent vacuoles

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Abstract

The Arabidopsis thaliana Tonoplast Intrinsic Protein 1;1 (AtTIP1;1) is a member of the tonoplast aquaporin family. The tissue-specific expression pattern and intracellular localization of AtTIP1;1 were characterized using GUS and GFP fusion genes. Results indicate that AtTIP1;1 is expressed in almost all cell types with the notable exception of meristematic cells. The highest level of AtTIP1;1 expression was detected in vessel-flanking cells in vascular bundles. AtTIP1;1-GFP fusion protein labelled the tonoplast of the central vacuole and other smaller peripheral vacuoles. The fusion protein was not found evenly distributed along the tonoplast continuum but concentrated in contact zones of tonoplasts from adjacent vacuoles and in invaginations of the central vacuole. Such invaginations may result from partially engulfed small vacuoles. A knockout mutant was isolated and characterized to gain insight into AtTIP1;1 function. No phenotypic alteration was found under optimal growth conditions indicating that AtTIP1;1 function is not essential to the plant and that some members of the TIP family may act redundantly to facilitate water flow across the tonoplast. However, a conditional root phenotype was observed when mutant plants were grown on a glycerol-containing medium.

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Abbreviations

AQP:

Aquaporin

GFP:

Green fluorescent protein

GUS:

β-Glucuronidase

MIP:

Membrane intrinsic protein

NIP:

Nodulin-like intrinsic protein

PIP:

Plasma membrane intrinsic protein

TIP:

Tonoplast intrinsic protein

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Acknowledgments

Azeez Beebo gratefully acknowledges the support of a doctoral fellowship from the French Ministère des Affaires Etrangères et Européennes and the Institut Kurde de Paris. This work was also supported by grants from the French Ministère de l’Enseignement Supérieur et de la Recherche, INRA and CNRS. The authors thank the Arabidopsis Knockout Facility of the University of Wisconsin Biotech Center for providing the pools of T-DNA mutants. We are grateful to Dr. Jeannine Lherminier for her help with electron microscopy. We also wish to thank Dr. Vivienne Gianinazzi-Pearson for her helpful comments on the manuscript.

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Correspondence to Karim Bouhidel.

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Azeez Beebo and Dominique Thomas have contributed equally to this work.

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The Arabidopsis Genome Initiative locus identifier for the AtTIP1;1 (γ-TIP) gene is At2g36830.

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Table S1. Primers used for qRT-PCR analysis (DOC 23 kb)

Movie 1

Motion of highly fluorescent vacuolar membranes in leaf epidermal cells (MPG 2741 kb)

Movie 2

Cytochalasin D-induced immobilization of highly fluorescent vacuolar membranes in leaf epidermal cells (MPG 1326 kb)

Movie 3

Constrained motion of nested vacuolar membranes in cortical parenchyma cells of stamen filament (MPG 425 kb)

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Beebo, A., Thomas, D., Der, C. et al. Life with and without AtTIP1;1, an Arabidopsis aquaporin preferentially localized in the apposing tonoplasts of adjacent vacuoles. Plant Mol Biol 70, 193–209 (2009). https://doi.org/10.1007/s11103-009-9465-2

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