Salinity-mediated transcriptional and post-translational regulation of the Arabidopsis aquaporin PIP2;7
- 1.2k Downloads
Salt stress triggers a simultaneous transcriptional repression and aquaporin internalization to modify root cell water conductivity.
Plasma membrane intrinsic proteins (PIPs) are involved in the adjustment of plant water balance in response to changing environmental conditions. In this study, Arabidopsis wild-type (Col-0) and transgenic lines overexpressing PIP2;7 were used to investigate and compare their response to salt stress. Hydraulic conductivity measurements using a high-pressure flowmeter (HPFM) revealed that overexpression of PIP2;7 induced a sixfold increase in root hydraulic conductivity of four week-old Arabidopsis thaliana plants compared to WT. Exposure to a high salt stress (150 mM NaCl) triggered a rapid repression of overall aquaporin activity in both genotypes. Response to salt stress was also investigated in 8 day-old seedlings. Exposure to salt led to a repression of PIP2;7 promoter activity and a significant decrease in PIP2;7 mRNA abundance within 2 h. Concomitantly, a rapid internalization of fluorescently-tagged PIP2;7 proteins was observed but removal from the cell membrane was not accompanied by further degradation of the protein within 4 h of exposure to salinity stress. These data suggest that PIP transcriptional repression and channel internalization act in concert during salt stress conditions to modulate aquaporin activity, thereby significantly altering the plant hydraulic parameters in the short term.
KeywordsAquaporin Plasma membrane Root hydraulic conductivity Salt stress Water relation
We thank Ewelina Grzeskiewicz for her help in this work and Frank Van Breusegem (PSB, VIB, Ghent) for lending the Licor infrared gas-exchange system. Confocal microscopy was carried out at the UCL imaging platform IMABIOL. This work was supported by grants from the Belgian National Fund for Scientific Research (FNRS), the Interuniversity Attraction Poles Programme-Belgian Science Policy (IAP7/29), the Belgian French community ARC11/16–036 project and the Bauchau Award. A. P. was supported by an UCL Incoming post-doctoral Fellowship co-funded by the Marie Curie Actions of the European Commission. C.H. was a FNRS postdoctoral researcher. T.M. was a research fellow at the Fonds de Formation à la Recherche dans l’Industrie et l’Agriculture.
Alicia Pou: Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting and revising the article. Linda Jeanguenin: Acquisition of data, Analysis and interpretation of data, Drafting and revising the article. Thomas Milhiet: Acquisition of data, Analysis and interpretation of data. Henri Batoko: Drafting and revising the article. François Chaumont: Conception and design, Analysis and interpretation of data, Drafting and revising the article. Charles Hachez: Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting and revising the article.
Forty seven min time-lapse analysis of the Venus-PIP2;7 fluorescence in root PM. Arabidopsis root cells expressing the PIP2;7:Venus-PIP2;7 construct were monitored by confocal microscopy and images were taken every 6 min during an interval of 48 min. Recording started at the onset of the stress. Note 1/the decrease in fluorescence of Venus-PIP2;7 in the PM 2/ the concomitant cell plasmolysis and 3/ the presence of PM invaginations in cortical root cells in response to this salt treatment (AVI 1064 KB)
- Alexandersson E, Fraysse L, Sjövall-Larsen S, Gustavsson S, Fellert M, Karlsson M, Johanson U, Kjellbom P (2005) Whole gene family expression and drought stress regulation of aquaporins. Plant Mol Biol 59:469–484Google Scholar
- Bogeat-Triboulot M-B, Brosche M, Renaut J, Jouve L, Le Thiec D, Fayyaz P, Vinocur B, Witters E, Laukens K, Teichmann T, Altman A, Hausman J-F, Polle A, Kangasjarvi J, Dreyer E (2007) Gradual soil water depletion results in reversible changes of gene expression, protein profiles, ecophysiology, and growth performance in Populus euphratica, a poplar growing in arid regions. Plant Physiol 143:876–892CrossRefPubMedPubMedCentralGoogle Scholar
- Brugnoli E, Lauteri M (1991) Effects of salinity on stomatal conductance, photosynthetic capacity, and carbon ısotope discrimination of salt-resistant (Gossypium hirsutum L.) and saltsensitive (Phaseolus vulgaris L.) C3 non-halophytes. Plant Physiol 95:628–635CrossRefPubMedPubMedCentralGoogle Scholar
- Caldeira CF, Jeanguenin L, Chaumont F, Tardieu F (2014b) Circadian rhythms of hydraulic conductance and growth are enhanced by drought and improve plant performance. Nat Commun 5:5365Google Scholar
- Conn SJ, Hocking B, Dayod M, Xu B, Athman A, Henderson S, Aukett L, Conn V, Shearer MK, Fuentes S, Tyerman SD, Gilliham M (2013) Protocol: optimising hydroponic growth systems for nutritional and physiological analysis of Arabidopsis thaliana and other plants. Plant Methods 9:4CrossRefPubMedPubMedCentralGoogle Scholar
- Hachez C, Laloux T, Reinhardt H, Cavez D, Degand H, Grefen C, De Rycke R, Inze D, Blatt MR, Russinova E, Chaumont F (2014a) Arabidopsis SNAREs SYP61 and SYP121 coordinate the trafficking of plasma membrane aquaporin PIP2;7 to modulate the cell membrane water permeability. Plant Cell 26:3132–3147CrossRefPubMedPubMedCentralGoogle Scholar
- Hachez C, Veljanovski V, Reinhardt H, Guillaumot D, Vanhee C, Chaumont F, Batoko H (2014b) The Arabidopsis abiotic stress-induced TSPO-related protein reduces cell-surface expression of the aquaporin PIP2;7 through protein–protein interactions and autophagic degradation. Plant Cell 26:4974–4990CrossRefPubMedPubMedCentralGoogle Scholar
- Johanson U, Karlsson M, Johansson I, Gustavsson S, Sjovall S, Fraysse L, Weig AR, Kjellbom P (2001) The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiol 126:1358–1369CrossRefPubMedPubMedCentralGoogle Scholar
- Kilian J, Whitehead D, Horak J, Wanke D, Weinl S, Batistic O, D’Angelo C, Bornberg-Bauer E, Kudla J, Harter K (2007) The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J 50:347–363CrossRefPubMedGoogle Scholar
- Prak S, Hem S, Boudet J, Viennois G, Sommerer N, Rossignol M, Maurel C, Santoni V (2008) Multiple phosphorylations in the C-terminal tail of plant plasma membrane aquaporins: role in subcellular trafficking of AtPIP2;1 in response to salt stress. MolCell Prot 7:1019–1030Google Scholar
- Sakurai J, Ishikawa F, Yamaguchi T, Uemura M, Maeshima M (2005) Identification of 33 rice aquaporin genes and analysis of their expression and function. Plant Cell Physiol 46:1568–1577Google Scholar
- Vandeleur RK, Mayo G, Shelden MC, Gilliham M, Kaise BN, Tyerman S (2009) The role of plasma membrane intrinsic protein aquaporins in water transport through roots: diurnal and drought stress responses reveal different strategies between isohydric and anisohydric cultivars of grapevine. Plant Physiol 149:445–460CrossRefPubMedPubMedCentralGoogle Scholar
- Zhu C, Schraut D, Hartung W, Schäffner AR (2005) Differential responses of maize MIP genes to salt stress and ABA. J Exp Bot 56(2):971–2981Google Scholar