Skip to main content
SpringerLink
Log in

The expression patterns of plasma membrane aquaporins in leaves of sugar beet and its halophyte relative, Beta vulgaris ssp. maritima, in response to salt stress

  • Published:
Biologia Aims and scope Submit manuscript

Abstract

Salt tolerance is largely dependent on a plant’ ability to maintain optimal water status in leaves. The adjustment of water relations under salinity involves changes in the transcriptional activity of genes encoding plasma membrane aquaporins (PIPs). Here, we report the effects of long-term or short-term treatments with moderate or strong salt stress on the expression of BvPIP1;1, BvPIP2;1 and BvPIP2;2 in the leaves of sugar beet, Beta vulgaris cv. Huzar, and its halophyte relative, Beta vulgaris ssp. maritima. Plants subjected to long-term treatment were watered with salt-supplemented media during a 32 day long culture period. Short-term salt treatments were executed either by immersing the petioles of excised leaves into salt solutions for 48h, or incubating excised leaf blades in salt-supplemented media for 20h. B. vulgaris ssp. maritima reacted to long-term salt treatment with a decrease in BvPIP1;1, BvPIP2;l and BvPIP2;2 expression. Contrastingly, only BvPIP2;2 transcript was down-regulated by salinity in leaves of B. vulgaris cv. Huzar, whereas BvPIP1;1 and BvPIP2;1 did not vary in response to salt-treatments. On the other hand, the expression of BvPIP1;1, BvPIP2;1 and BvPIP2;2 was enhanced by salinity if salt solutions was supplied through leaf petioles, irrespective of genotype. PIP expression in excised leaf blades revealed a complex pattern of changes. BvPIP1;1 and BvPIP2;1 expression underwent a period of transient increase in both the control and salt-treated leaves. Furthermore, BvPIP1;1 expression was enhanced by strong salinity. BvPIP2;2 expression was up-regulated by strong salinity or up- or down-regulated by moderate salinity during the treatment period.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aroca R. Porcel R. & Ruiz-Lozano J.M. 2011. Regulation of root water uptake under abiotic stress conditions. J. Exp. Bot. 63: 43–57.

    Article  PubMed  CAS  Google Scholar 

  • Ayadi M., Cavez D., Miled N., Chaumont F. & Masmoudi K. 2011. Identification and characterization of two plasma membrane aquaporins in durum wheat (Triticum turgidum L. subsp. durum) and their role in abiotic stress tolerance. Plant Physiol. Biochem. 49: 1029–1039.

    Article  CAS  PubMed  Google Scholar 

  • Bae E.K., Lee H., Lee J.S. & Noh E.W. 2011. Drought, salt and wounding stress induce the expression of the plasma membrane intrinsic protein 1 gene in poplar (Populus alba X P. tremula var. glandulosa). Gene 483: 43–48.

    Article  CAS  PubMed  Google Scholar 

  • Bagatta M., Pacifico D. & Mandolino G. 2008. Evaluation of the osmotic adjustment response within the genus Beta. J. Sugar Beet Res. 45: 119–133.

    Article  Google Scholar 

  • Bellati J., Alleva K., Soto G., Vitali V., Jozefkowicz C. & Amodeo G. 2010. Intracellular pH sensing is altered by plasma membrane PIP aquaporin co-expression. Plant Mol. Biol. 74: 105–118.

    Article  CAS  PubMed  Google Scholar 

  • Boursiac Y., Chen S., Luu D.T., Sorieul M., Dries N. & Maurel C. 2005. Early effects of salinity on water transport in Ara-bidopsis roots. Molecular and cellular features of aquaporin expression. Plant Physiol. 139: 790–805.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campos P.S., Quartin V., Ramalho J.C. & Nunes M.A. 2003. Electrolyte leakage and lipid degradation account for cold sensitivity in leaves of Coffea sp. plants. J. Plant Physiol. 160: 283–292.

    Article  CAS  PubMed  Google Scholar 

  • Chaouachi M., Alaya A., Ali I.B.H., Hafsa A.B., Nabi N., Bérard A., Romaniuk M., Skhiri F. & Said K. 2013. Development of real-time PCR method for the detection and the quantification of new endogenous references gene in sugar beet “Beta vulgaris L.”: GMO application Plant Cell. Rep. 32: 117–128.

    Article  CAS  PubMed  Google Scholar 

  • Dadkhah A. & Moghtader S.H. 2008. Growth and gas exchange response of sugar beet (Beta vulgaris L.) cultivars grown under salt stress, pp. 1431–1434. In: Allen J.F., Gantt E., Golbeck J.H. & Osmond B. (eds), Photosynthesis. Energy from the Sun. Springer, Netherlands.

    Chapter  Google Scholar 

  • Daoud S., Harrouni C., Huchezermeyer B. & Koyro H.W. 2008. Comparison of salinity tolerance of two related subspecies of Beta vulgaris: the sea beet (Beta vulgaris ssp. maritima) and the sugar beet (Beta vulgaris ssp. vulgaris), pp. 115–129. In: Abdelly C., Öztürk M., Ashraf M. & Grignon C. (eds), Biosaline Agriculture and High Salinity Tolerance, Birkhäuser Verlag/Switzerland.

    Chapter  Google Scholar 

  • Dunajska-Ordak K., Skorupa-Kiaput M., Kurnik K., Tretyn A. & Tyburski J. 2014. Cloning and expression analysis of a gene encoding for ascorbate peroxidase and responsive to salt stress in beet (Beta vulgaris). Plant Mol. Biol. Rep. 32: 162–175.

    Article  CAS  Google Scholar 

  • Farkhondeh R., Nabizadeh E. & Jalilnezhad N. 2012. Effect of salinity stress on proline content, membrane stability and water relations in two sugar beet cultivars. Int. J. AgriSci. 2: 385–392.

    CAS  Google Scholar 

  • Ghoulam C. & Fares K. 2001. Effect of salinity on seed germination and early seedling growth of sugar beet (Beta vulgaris L.). Seed Sci. Technol. 29: 357–364.

    Google Scholar 

  • Ghoulam C., Foursy A. & Fares K. 2002. Effects of salt stress on growth, inorganic ions and proline accumulation in relation to osmotic adjustment in five sugar beet cultivars. Env. Exp. Bot. 47: 39–50.

    Article  CAS  Google Scholar 

  • Hachez C., Heinen R.B., Draye X. & Chaumont F. 2008. The expression pattern of plasma membrane aquaporins in maize leaf highlights their role in hydraulic regulation. Plant Mol. Biol. 68: 337–353.

    Article  CAS  PubMed  Google Scholar 

  • Hachez C., Zelazny E. & Chaumont F. 2006. Modulating the expression of aquaporin genes in planta: A key to understand their physiological functions? Biochim. Biophys. Acta 1758: 1142–1156.

    Article  CAS  PubMed  Google Scholar 

  • Hasanuzzaman M., Nahar K. & Fujita M. 2013. Plant response to salt stress and role of exogenous protectants to mitigate salt-induced damages, pp. 25–87. In: Ahmad P. et al. (eds), Ecophysiology and Responses of Plants under Salt Stress, Springer, New York.

    Chapter  Google Scholar 

  • Heinen R.B., Ye Q. & Chaumont F. 2009. Role of aquaporins in leaf physiology. J. Exp. Bot. 11: 2971–2985.

    Article  CAS  Google Scholar 

  • Hoffmann C.M. 2010. Sucrose accumulation in sugar beet under drought stress. J. Agronomy Crop Sci. 196: 243–252.

    CAS  Google Scholar 

  • Horie T., Kaneko T., Sugimoto G., Sasano S., Panda S.K., Shibasaka M. & Katsuhara M. 2011. Mechanism of water transport mediated by PIP aquaporins and their regulation via phosphorylation events under salinity stress in Barley roots. Plant Cell Physiol. 52: 663–675.

    Article  CAS  PubMed  Google Scholar 

  • Jang J.Y., Kim D.G., Kim Y.O., Kim J.S. & Kang H. 2004. An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stress in Arabidopsis thaliana. Plant Mol. Biol. 54: 713–725.

    Article  CAS  PubMed  Google Scholar 

  • Jozefkowicz C., Rosi P., Sigaut L., Soto G., Pietrasanta L.I., Amodeo G. & Alleva K. 2013. Loop A is critical for the functional interaction of two Beta vulgaris PIP aquaporins. PLOS 8: 1–13.

    Google Scholar 

  • Katerij N., Hoorn J.W., Hamdy A., Mas-Trorilli M. & Karzel E.M. 1997. Osmotic adjustment of sugar beets in response to salinity and its influence on stomatal conductance, growth and yield. Agr. Water Manage. 34: 57–69.

    Article  Google Scholar 

  • Kerstiens G., Tych W., Robinson M.F. & Mansfield T.A. 2002. Sodium-related partial stomatal closure and salt tolerance of Aster tripolium. New Phytol. 153: 509–515.

    Article  CAS  PubMed  Google Scholar 

  • Koyro H.W., Daoud S., Harrouni C. & Huchzermeyer B. 2006. Strategies of a potential cash crop halophyte (Beta vulgaris ssp. maritima) to avoid salt injury. Tropical Ecol. 47: 191–200.

    CAS  Google Scholar 

  • Martinez-Ballesta M.C., Silva C., López-Berenguer C., Cabanero F.J., Cabañero F.J. & Carvajal M. 2006. Plant Aquaporins: New perspectives on water and nutrient uptake in saline environment. Plant Biol. 8: 535–546.

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • McCrea K.J. & Richardson S.G. 1987. Stomatal closure vs. osmotic adjustment: A comparison of stress responses. Crop Sci. 27: 539–543.

    Google Scholar 

  • Mostafavi K. 2012. Effect of salt stress on germination and early seedling growth stage of sugar beet cultivars. Amer.-Eurasian J. Sust. Agricult. 6: 120–125.

    Google Scholar 

  • Munns R. 2002. Comparative physiology of salt and water stress. Plant Cell Env. 25: 239–250.

    Article  CAS  Google Scholar 

  • Munns R., James R.A. & Lauchli A. 2006. Approaches to increasing the salt tolerance of wheat and other cereals. J. Exp. Bot. 57: 1025–1043.

    Article  CAS  PubMed  Google Scholar 

  • Munns R. & Tester M. 2008. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59: 651–681.

    Article  CAS  PubMed  Google Scholar 

  • Muries B., Carvajal M. & Martinez-Ballesta M.C. 2013. Response of three broccoli cultivars to salt stress, in relation to water status and expression of two leafaquaporins. Planta 235: 1298–1310.

    Google Scholar 

  • Muries B., Mohamed F., Carvajal M. & Martinez-Ballesta M.C. 2011. Differential aquaporin expression induced by salinity in broccoli plants. Mol. Biol. Syst. 7: 1322–1335.

    CAS  Google Scholar 

  • Liu C., Li C., Liang D., Wei Z., Zhou S., Wang R. & Ma F. 2012. Differential expression of ion transporters and aqua porins in leaves may contribute to different salt tolerance in Malus species. Plant Physiol. Bioch. 58: 159–165.

    Article  CAS  Google Scholar 

  • Ouziad F., Wilde P., Schmelzer E., Hildebrandt U. & Bothe H. 2006. Analysis of expression of aquaporins and Na+ /H+ transporters in tomato colonized by arbuscular mycorrhizal fungi and affected by salt stress. Environ. Bot. 57: 177–186.

    Article  CAS  Google Scholar 

  • Pfaffl M.W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29: 2002–2007.

    Article  Google Scholar 

  • Pfaffl M.W., Tichopad A., Prgomet C. & Neuvians T.P. 2004. Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper-Exel-based tool using pair-wise correlations. Biotechnol. Lett. 26: 509–515.

    Article  CAS  PubMed  Google Scholar 

  • Pakniyat H. & Armion M. 2007. Sodium and proline accumulation as osmoregulators in tolerance of sugar beet genotypes to salinity. Pak. J. Biol. Sci. 22: 4081–4086.

    Google Scholar 

  • Prado K. & Maurel C. 2013. Regulation of leaf hydraulics: from molecular to whole plant levels. Front. Plant Sci. 4: 1–14.

    Article  CAS  Google Scholar 

  • Romero-Aranda R., Soria T. & Cuartero S. 2001. Tomato plant-water uptake and plant-water relationships under saline growth conditions. Plant Sci. 160: 265–272.

    Article  CAS  PubMed  Google Scholar 

  • Russell B.L., Rathinasabapathi B. & Hanson A.D. 1998. Osmotic stress induces expression of choline monooxygenase in sugar beet and amaranth. Plant Physiol. 116: 859–865.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smethurst C.F., Gill W.M. & Shabala S. 2009. Using excised leaves to screen lucerne for salt tolerance. Physiological and cytological evidence. Plant Signal. Behav. 4: 39–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steudle E. 2000. Water uptake by roots: effects of water deficit. J. Exp. Bot. 51: 1531–1542.

    Article  CAS  PubMed  Google Scholar 

  • Suga S., Komatsu S. & Maeshima M. 2002. Aquaporin isoforms responsive to salt and water stresses and phytohormones in radish seedlings. Plant Cell Physiol. 43: 1237–1237.

    Article  Google Scholar 

  • Uno Y., Urao T., Yamaguchi-Shinozaki K., Kanechi M., Inagaki N., Maekawa S. & Shinozaki M. 1998. Early salt-stress effects on expression of genes for aquaporin homologues in the halophyte sea aster. J. Plant Res. 111: 411–419.

    Article  CAS  Google Scholar 

  • Venkatesh J., Yu J.W. & Park S.W. 2013. Genomewide analysis and expression profiling of the Solarium tuberosum aquaporins. Plant Physiol. Biochem. 73: 392–404.

    Article  CAS  PubMed  Google Scholar 

  • Very A.A., Robinson M.F., Mansfield T.A. & Sanders D. 1998. Guard cell cation channels are involved in Na+ -induced stomatal closure in a halophyte. Plant J. 14: 509–521.

    Article  CAS  Google Scholar 

  • Vysotskaya L., Hedley P.E., Sharipova G., Veselov D., Kudoyarova G., Morris J. & Jones H.G. 2010. Effect of salinity on water relations of wild barley plants differing in salt tolerance. AoB PLANTS. doi:10.1093/aobpla/plq006

    Google Scholar 

  • Zhu C., Schraut D., Hartung W. & Schaffner A.R. 2005. Differential responses of maize MIP genes to salt stress and ABA. J. Exp. Bot. 56: 2971–2981.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Chair of Plant Physiology and Biotechnology, Nicolaus Copernicus University, Lwowska 1, PL-87-100, Toruń, Poland

    Monika Skorupa-Kłaput, Joanna Szczepanek, Katarzyna Kurnik, Andrzej Tretyn & Jaroslaw Tyburski

  2. Centre for Modern Interdisciplinary Technologies, Nicolaus Copernicus University, Wileńska 4, PL-87-100, Toruń, Poland

    Joanna Szczepanek, Andrzej Tretyn & Jaroslaw Tyburski

Authors
  1. Monika Skorupa-Kłaput
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joanna Szczepanek
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Katarzyna Kurnik
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Andrzej Tretyn
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jaroslaw Tyburski
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jaroslaw Tyburski.

Supplementary data

11756_2015_7004467_MOESM1_ESM.pdf

The expression patterns of plasma membrane aquaporins in leaves of sugar beet and its halophyte relative, Beta vulgaris ssp. maritima, in response to salt stress

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Skorupa-Kłaput, M., Szczepanek, J., Kurnik, K. et al. The expression patterns of plasma membrane aquaporins in leaves of sugar beet and its halophyte relative, Beta vulgaris ssp. maritima, in response to salt stress. Biologia 70, 467–477 (2015). https://doi.org/10.1515/biolog-2015-0056

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1515/biolog-2015-0056

Key words

Search

Navigation