Skip to main content
Log in

Differential tissue-specific expression of NtAQP1 in Arabidopsis thaliana reveals a role for this protein in stomatal and mesophyll conductance of CO2 under standard and salt-stress conditions

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

The regulation of plant hydraulic conductance and gas conductance involves a number of different morphological, physiological and molecular mechanisms working in harmony. At the molecular level, aquaporins play a key role in the transport of water, as well as CO2, through cell membranes. Yet, their tissue-related function, which controls whole-plant gas exchange and water relations, is less understood. In this study, we examined the tissue-specific effects of the stress-induced tobacco Aquaporin1 (NtAQP1), which functions as both a water and CO2 channel, on whole-plant behavior. In tobacco and tomato plants, constitutive overexpression of NtAQP1 increased net photosynthesis (A N), mesophyll CO2 conductance (g m) and stomatal conductance (g s) and, under stress, increased root hydraulic conductivity (L pr) as well. Our results revealed that NtAQP1 that is specifically expressed in the mesophyll tissue plays an important role in increasing both A N and g m. Moreover, targeting NtAQP1 expression to the cells of the vascular envelope significantly improved the plants’ stress response. Surprisingly, NtAQP1 expression in the guard cells did not have a significant effect under any of the tested conditions. The tissue-specific involvement of NtAQP1 in hydraulic and gas conductance via the interaction between the vasculature and the stomata is discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

A N :

Net photosynthesis

AQP:

Aquaporin

AXS:

Artificial xylem sap

Ci :

Substomatal CO2 concentration

FBPase:

Fructose 1,6-bisphosphatase

gm :

Leaf mesophyll conductance for CO2

gs :

Stomatal conductance

Kleaf :

Leaf hydraulic conductivity

Lpr :

Root hydraulic conductivity

SCR:

SCARCROW

GC:

Guard cell

GFP:

Green fluorescent protein

qPCR:

Quantitative PCR

References

  • Ache P, Bauer H, Kollist H, Al-Rasheid KAS, Lautner S, Hartung W, Hedrich R (2010) Stomatal action directly feeds back on leaf turgor: new insights into the regulation of the plant water status from non-invasive pressure probe measurements. Plant J 62:1072–1082

    CAS  PubMed  Google Scholar 

  • Alexandersson E, Fraysse L, Sjovall-Larsen S, Gustavsson S, Fellert M, Karlsson M, Johanson U, Kjellbom P (2005) Whole gene family expression drought stress regulation of aquaporins. Plant Mol Biol 59:469–484

    Article  CAS  PubMed  Google Scholar 

  • Bernacchi CJ, Portis AR, Nakano H, von Caemmerer S, Long SP (2002) Temperature response of mesophyll conductance implications for the determination of Rubisco enzyme kinetics for limitations to photosynthesis in vivo. Plant Physiol 130:1992–1998

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Besford RT, Ludwig LJ, Withers AC (1990) The greenhouse-effect—acclimation of tomato plants growing in high CO2, photosynthesis ribulose-1,5-bisphosphate carboxylase protein. J Exp Bot 41:925–931

    Article  CAS  Google Scholar 

  • Brown NJ, Palmer B, Stanley S, Hajaj H, Janacek S, Quick WP, Trenkam S, Fernie A, Maurino V, Hibberd JM (2010) C4 acid decarboxylases required for C4 photosynthesis are active in the mid-veins of the C3 species Arabidopsis thaliana and are important in sugar and amino acid metabolism. Plant J 61:122–133

    Article  CAS  PubMed  Google Scholar 

  • Chueca A, Sahrawy M, Pagano EA, Gorge JL (2002) Chloroplast fructose-1,6-bisphosphatase: structure and function. Photosynth Res 74:235–249

    Article  CAS  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Eshed Y, Baum SF, Perea JV, Bowman JL (2001) Establishment of polarity in lateral organs of plants. Curr Biol 11:1251–1260

    Article  CAS  PubMed  Google Scholar 

  • Ethier GJ, Livingston NJ (2004) On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar-von Caemmerer-Berry leaf photosynthesis model. Plant, Cell Environ 27:137–153

    Article  CAS  Google Scholar 

  • Evans JR, von Caemmerer S (1996) Carbon dioxide diffusion inside leaves. Plant Physiol 110:339–346

    CAS  PubMed Central  PubMed  Google Scholar 

  • Farquhar GD, Caemmerer SV, Berry JA (1980) A biochemical-model of photosynthetic CO2 assimilation in leaves of C-3 species. Planta 149:78–90

    Article  CAS  PubMed  Google Scholar 

  • Flexas J, Ribas-Carbo M, Hanson DT, Bota J, Otto B, Cifre J, McDowell N, Medrano H, Kaldenhoff R (2006) Tobacco aquaporin NtAQP1 is involved in mesophyll conductance to CO2 in vivo. Plant J 48:427–439

    Article  CAS  PubMed  Google Scholar 

  • Flexas J, Diaz-Espejo A, Galmes J, Kaldenhoff R, Medrano H, Ribas-Carbo M (2007) Rapid variations of mesophyll conductance in response to changes in CO2 concentration around leaves. Plant Cell Environ 30:1284–1298

    Article  CAS  PubMed  Google Scholar 

  • Flexas J, Ribas-Carbo M, Diaz-Espejo A, Galmes J, Medrano H (2008) Mesophyll conductance to CO2: current knowledge future prospects. Plant Cell Environ 31:602–621

    Article  CAS  PubMed  Google Scholar 

  • Flexas J, Barbour MM, Brendel O, Cabrera HM, Carriqui M, Diaz-Espejo A, Douthe C, Dreyer E, Ferrio JP, Gago J, Galle A, Galmes J, Kodama N, Medrano H, Niinemets U, Peguero-Pina JJ, Pou A, Ribas-Carbo M, Tomas M, Tosens T, Warren CR (2012) Mesophyll diffusion conductance to CO2: an unappreciated central player in photosynthesis. Plant Sci 193:70–84

    Article  PubMed  Google Scholar 

  • Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron-transport quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    Article  CAS  Google Scholar 

  • Harley PC, Loreto F, Dimarco G, Sharkey TD (1992) Theoretical considerations when estimating the mesophyll conductance to CO2 flux by analysis of the response of photosynthesis to CO2. Plant Physiol 98:1429–1436

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Heckwolf M, Pater D, Hanson DT, Kaldenhoff R (2011) The Arabidopsis thaliana aquaporin AtPIP1;2 is a physiologically relevant CO2 transport facilitator. Plant J 67:795–804

    Article  CAS  PubMed  Google Scholar 

  • Hibberd JM, Quick WP (2002) Characteristics of C4 photosynthesis in stems and petioles of C3 flowering plants. Nature 415:451–454

    Article  CAS  PubMed  Google Scholar 

  • Janacek SH, Trenkamp S, Palmer B, Brown NJ, Parsley K, Stanley S, Astley HM, Rolfe SA, Paul Quick W, Fernie AR, Hibberd JM (2007) Photosynthesis in cells around veins of the C3 plant Arabidopsis thaliana is important for both the shikimate pathway and leaf senescence as well as contributing to plant fitness. Plant J 59:469–484

    Google Scholar 

  • Kaldenhoff R, Bertl A, Otto B, Moshelion M, Uehlein N (2007) Characterization of plant aquaporins. Methods Enzymol 428:505–531

    Article  PubMed  Google Scholar 

  • Karimi M, Inzé D, Depicker A (2002) Gateway vectors for agrobacterium-mediated plant transformation. Trends Plant Sci 7:193–195

    Article  CAS  PubMed  Google Scholar 

  • Kelly G, David-Schwartz R, Sade N, Moshelion M, Levi A, Alchanatis V, Granot D (2012) The pitfalls of transgenic selection and new roles of AtHXK1: a high level of AtHXK1 expression uncouples hexokinase1-dependent sugar signaling from exogenous sugar. Plant Physiol 159:47–51

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kelly G, Moshelion M, David-Schwartz R, Halperin O, Wallach R, Attia Z, Belausov E, Granot D (2013) Hexokinase mediates stomatal closure. Plant J 75:977–988

    Article  CAS  PubMed  Google Scholar 

  • Kimball BA, Idso SB (1983) Increasing atmospheric CO2—effects on crop yield, water-use and climate. Agric Water Manage 7:55–72

    Article  Google Scholar 

  • Li J, Zhou JM, Duan ZQ (2007) Effects of elevated CO2 concentration on growth and water usage of tomato seedlings under different ammonium/nitrate ratios. J Environ Sci China 19:1100–1107

    Article  CAS  PubMed  Google Scholar 

  • Lloyd JC, Raines CA, John UP, Dyer TA (1991) The chloroplast fbpase gene of wheat—structure and expression of the promoter in photosynthetic meristematic cells of transgenic tobacco plants. Mol Gen Genet 225:209–216

    Article  CAS  PubMed  Google Scholar 

  • Loreto F, Harley PC, Dimarco G, Sharkey TD (1992) Estimation of mesophyll conductance to CO2 flux by 3 different methods. Plant Physiol 98:1437–1443

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mahdieh M, Mostajeran A, Horie T, Katsuhara M (2008) Drought stress alters water relations and expression of PIP-type aquaporin genes in Nicotiana tabacum plants. Plant Cell Physiol 49:801–812

    Article  CAS  PubMed  Google Scholar 

  • Martre P, Morillon R, Barrieu F, North GB, Nobel PS, Chrispeels MJ (2002) Plasma membrane aquaporins play a significant role during recovery from water deficit. Plant Physiol 130:2101–2110

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Maurel C, Verdoucq L, Luu DT, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624

    Article  CAS  PubMed  Google Scholar 

  • Mott KA (2009) Opinion: stomatal responses to light and CO2 depend on the mesophyll. Plant Cell Environ 32:1479–1486

    Article  CAS  PubMed  Google Scholar 

  • Mott KA, Sibbernsen ED, Shope JC (2008) The role of the mesophyll in stomatal responses to light and CO2. Plant Cell Environ 31:1299–1306

    Article  CAS  PubMed  Google Scholar 

  • Otto B, Kaldenhoff R (2000) Cell-specific expression of the mercury-insensitive plasma-membrane aquaporin NtAQP1 from Nicotiana tabacum. Planta 211:167–172

    Article  CAS  PubMed  Google Scholar 

  • Otto B, Uehlein N, Sdorra S, Fischer M, Ayaz M, Belastegui-Macadam X, Heckwolf M, Lachnit M, Pede N, Priem N, Reinhard A, Siegfart S, Urban M, Kaldenhoff R (2010) Aquaporin tetramer composition modifies the function of tobacco aquaporins. J Biol Chem 285:31253–31260

    Article  CAS  PubMed  Google Scholar 

  • Pantin F, Monnet F, Jannaud D, Costa JM, Renaud J, Muller B, Simonneau T, Genty B (2013) The dual effect of abscisic acid on stomata. New Phytol 197:65–72

    Article  CAS  PubMed  Google Scholar 

  • Plesch G, Ehrhardt T, Mueller-Roeber B (2001) Involvement of TAAAG elements suggests a role for Dof transcription factors in guard cell-specific gene expression. Plant J 28:455–464

    Article  CAS  PubMed  Google Scholar 

  • Postaire O, Tournaire-Roux C, Grondin A, Boursiac Y, Morillon R, Schaffner AR, Maurel C (2010) A PIP1 aquaporin contributes to hydrostatic pressure-induced water transport in both the root and rosette of Arabidopsis. Plant Physiol 152:1418–1430

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Prado K, Boursiac Y, Tournaire-Roux C, Monneuse JM, Postaire O, Da Ines O, Schaffner AR, Hem S, Santoni V, Maurel C (2013) Regulation of Arabidopsis leaf hydraulics involves light-dependent phosphorylation of aquaporins in veins. Plant Cell 25:1029–1039

    Article  CAS  PubMed  Google Scholar 

  • Sade N, Gebretsadik M, Seligmann R, Schwartz A, Wallach R, Moshelion M (2010) The role of tobacco Aquaporin1 in improving water use efficiency, hydraulic conductivity and yield production under salt stress. Plant Physiol 152:245–254

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL (2007) Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant Cell Environ 30:1035–1040

    Article  CAS  PubMed  Google Scholar 

  • Shatil-Cohen A, Attia Z, Moshelion M (2011) Bundle-sheath cell regulation of xylem-mesophyll water transport via aquaporins under drought stress: a target of xylem-borne ABA? Plant J 67:72–80

    Article  CAS  PubMed  Google Scholar 

  • Siefritz F, Biela A, Eckert M, Otto B, Uehlein N, Kaldenhoff R (2001) The tobacco plasma membrane aquaporin NtAQP1. J Exp Bot 52:1953–1957

    Article  CAS  PubMed  Google Scholar 

  • Siefritz F, Tyree MT, Lovisolo C, Schubert A, Kaldenhoff R (2002) PIP1 plasma membrane aquaporins in tobacco: from cellular effects to function in plants. Plant Cell 14:869

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Terashima I, Ono K (2002) Effects of HgCl2 on CO2 dependence of leaf photosynthesis: evidence indicating involvement of aquaporins in CO2 diffusion across the plasma membrane. Plant Cell Physiol 43:70–78

    Article  CAS  PubMed  Google Scholar 

  • Tyerman SD, Niemietz CM, Bramley H (2002) Plant aquaporins: multifunctional water solute channels with expanding roles. Plant Cell Environ 25:173–194

    Article  CAS  PubMed  Google Scholar 

  • Uehlein N, Lovisolo C, Siefritz F, Kaldenhoff R (2003) The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature 425:734–737

    Article  CAS  PubMed  Google Scholar 

  • Uehlein N, Otto B, Hanson DT, Fischer M, McDowell N, Kaldenhoff R (2008) Function of Nicotiana tabacum aquaporins as chloroplast gas pores challenges the concept of membrane CO2 permeability. Plant Cell 20:648–657

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Uehlein N, Sperling H, Heckwolf M, Kaldenhoff R (2012) The Arabidopsis aquaporin PIP1;2 rules cellular CO2 uptake. Plant Cell Environ 35:1077–1083

    Article  CAS  PubMed  Google Scholar 

  • Villar R, Held AA, Merino J (1995) Dark leaf respiration in light and darkness of an evergreen and a deciduous plant species. Plant Physiol 107:421–427

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wilkinson S, Corlett JE, Oger L, Davies WJ (1998) Effects of xylem pH on transpiration from wild-type flacca tomato leaves: a vital role for abscisic acid in preventing excessive water loss even from well-watered plants. Plant Physiol 117:703–709

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wysocka-Diller JW, Helariutta Y, Fukaki H, Malamy JE, Benfey PN (2000) Molecular analysis of SCARECROW function reveals a radial patterning mechanism common to root and shoot. Development 127:595–603

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by a grant from the Rehovot-Hohenheim partnership program and the Israel Science Foundation, Jerusalem (ISF; Grant # 1311/12) to MM. JF acknowledges the support of Plan Nacional (Spain) project grant MECOME (BFU2011-23294). We thank Dr. Orit Edelbaum and Professor Shmuel Wolf (Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture, Hebrew University of Jerusalem, Rehovot, Israel), Dr. Einat Sadot and Dr. Mohamad Abu-Abied (Institute of Plant Sciences, Agricultural Research Organization, The Volcani Center, Bet Dagan, Israel), Professor Yuval Eshed (Department of Plant Sciences, Weizmann Institute of Science, Rehovot, Israel) and Professor Ralf Kaldenhoff (Department of Biology, Applied Plant Sciences, Technische Universität Darmstadt, Darmstadt, Germany) for supplying the different constructs and plant materials. Eduard Belausov (Institute of Plant Sciences, Agricultural Research Organization, The Volcani Center, Bet Dagan, Israel) helped with microscopy imaging.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Menachem Moshelion.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PPTX 70 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sade, N., Gallé, A., Flexas, J. et al. Differential tissue-specific expression of NtAQP1 in Arabidopsis thaliana reveals a role for this protein in stomatal and mesophyll conductance of CO2 under standard and salt-stress conditions. Planta 239, 357–366 (2014). https://doi.org/10.1007/s00425-013-1988-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-013-1988-8

Keywords

Navigation