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Over-expression of PIP2;5 aquaporin alleviates gas exchange and growth inhibition in poplars exposed to mild osmotic stress with polyethylene glycol

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Abstract

The effects of mild osmotic stress conditions on aquaporin-mediated water transport are not well understood. In the present study, mild osmotic stress treatments with 20 and 50 g L−1 polyethylene glycol 6000 (PEG) in Hoagland’s mineral solution were applied for 3 weeks under controlled environmental conditions to transgenic Populus tremula × Populus alba plants constitutively over-expressing a Populus PIP2;5 aquaporin and compared with the wild-type plants. The PEG treatments resulted in growth reductions and triggered changes in net photosynthesis, transpiration, stomatal conductance and root hydraulic conductivity in the wild-type plants. However, height growth, leaf area, gas exchange, and root hydraulic conductivity were less affected by the PEG treatments in PIP2;5-over-expressing poplar lines. These results suggest that water transport across the PIP2;5 aquaporin is an important process contributing to tolerance of mild osmotic stress in poplar. Greater membrane abundance of PIP2;5 was most likely the factor that was responsible for higher root hydraulic conductivity leading to improved plant water flux and, consequently, greater gas exchange and growth rates under mild osmotic stress conditions. The results also provide evidence for the functional significance of PIP2;5 aquaporin in water transport and its strong link to growth processes in poplar.

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References

  • Aharon R, Shahak Y, Wininger S, Bendov R, Kapulnik Y, Galili G (2003) Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress. Plant Cell 15:439–447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allakhverdiev SI, Sakamoto A, Nishiyama Y, Inaba M, Murata N (2000) Ionic and osmotic effects of NaCl-induced inactivation of photosystems I and II in Synechococcus sp. Plant Physiol 123:1047–1056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Almeida-Rodriguez AM, Cooke JEK, Yeh F, Zwiazek JJ (2010) Functional characterization of drought- responsive aquaporins in Populus balsamifera and Populus simonii × balsamifera clones with different drought resistance strategies. Physiol Plant 140:321–333

    Article  CAS  PubMed  Google Scholar 

  • Apostol KG, Zwiazek JJ, MacKinnon MD (2004) Naphthenic acids affect water conductance but do not alter shoot sodium and chloride concentrations in jack pine (Pinus banksiana) seedlings. Plant Soil 263:183–190

    Article  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 

  • Baiges I, Schaffner AR, Affenzeller MJ, Mas A (2002) Plant aquaporins. Physiol Plant 115:175–182

    Article  CAS  PubMed  Google Scholar 

  • Barbieri G, Vallone S, Orsini F, Paradiso R, De Pascale S, Negre-Zakharov F, Maggio A (2012) Stomatal density and metabolic determinants mediate salt stress adaptation and water use efficiency in basil (Ocimum basilicum L.). J Plant Physiol 169(17):1737–1746

    Article  CAS  PubMed  Google Scholar 

  • Bidabadi SS, Meon S, Wahab Z, Subramaniam S, Mahmood M (2012) In vitro selection and characterization of water stress tolerant lines among methanesulphonate (EMS) induced variants of banana (Musa spp., with AAA genome). Aust J Crop Sci 6:567–575

    CAS  Google Scholar 

  • Biswas J, Chowdhury B, Bhattacharya A (2002) In vitro screening for increased drought tolerance in rice. In Vitro Cell Dev Biol Plant 38:525–530

    Article  Google Scholar 

  • Bogeat-Triboulot MB, Brosche M, Renaut J, Jouve L, Le Thiec D, Fayyaz P, Vinocur B, Witters E, Laukens K, Teichmann T, Altman A, Hausman JF, 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 143:876–892

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caruso A, Chefdor F, Carpin S, Depierreux C, Delmotte FM, Kahlem G, Morabito D (2008) Physiological characterization and identification of genes differentially expressed in response to drought induced by PEG 6000 in Populus canadensis leaves. J Plant Physiol 165:932–941

    Article  CAS  PubMed  Google Scholar 

  • Chaumont F, Barrieu F, Jung R, Chrispeels MJ (2000) Plasma membrane intrinsic proteins from maize cluster in two sequence subgroups with differential aquaporin activity. Plant Physiol 122:1025–1034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Claeys H, Inzé D (2013) The agony of choice: how plants balance growth and survival under water-limiting conditions. Plant Physiol 162:1768–1779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cui X, Hao F, Chen H, Cai J, Chen J, Wang XC (2005) Isolation and expression of an aquaporin-like gene VfPIP1 in Vicia faba. Prog Nat Sci 15:496–501

    Article  CAS  Google Scholar 

  • Dhanda SS, Sethi GS, Behl RK (2004) Indices of drought tolerance in wheat genotypes at early stages of plant growth. J Agron Crop Sci 190:6–12

    Article  Google Scholar 

  • Fetter K, Van Wilder V, Moshelion M, Chaumont F (2004) Interactions between plasma membrane aquaporins modulate their water channel activity. Plant Cell 16:215–228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Greenway H, Munns R (1980) Mechanisms of salt tolerance in non-halophytes. Annu Rev Plant Physiol 31:149–190

    Article  CAS  Google Scholar 

  • Gupta AB, Sankararamakrishnan R (2009) Genome-wide analysis of major intrinsic proteins in the tree plant Populus trichocarpa: characterization of XIP subfamily of aquaporins from evolutionary perspective. BMC Plant Biol 9:134

    Article  PubMed  PubMed Central  Google Scholar 

  • Hanba YT, Shibasaka M, Hayashi Y, Hayakawa T, Kasamo K, Terashima I, Katsuhara M (2004) Over expression of the barley aquaporin HvPIP2;1 increases internal CO 2 conductance and CO2 assimilation in the leaves of transgenic rice plants. Plant Cell Physiol 45:521–529

    Article  CAS  PubMed  Google Scholar 

  • Heinen RB, Ye Q, Chaumont F (2009) Role of aquaporins in leaf physiology. J Exp Bot 60:2971–2985

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann WA, Poorter H (2002) Avoiding bias in calculations of relative growth rate. Ann Bot (Lond) 90:37–42

    Article  Google Scholar 

  • Jang JY, Kim DG, Kim YO, Kim JS, Kang H (2004) An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana. Plant Mol Biol 54:713–725

    Article  CAS  PubMed  Google Scholar 

  • Kamaluddin M, Zwiazek JJ (2003) Fluoride inhibits root water flow and affects leaf expansion and gas exchange in aspen (Populus tremuloides) seedlings. Physiol Plant 117:368–375

    Article  CAS  PubMed  Google Scholar 

  • Kawase M, Hanba YT, Katsuhara M (2013) The photosynthetic response of tobacco plants over-expressing ice plant aquaporin McMIPB to a soil water deficit and high vapor pressure deficit. J Plant Res 126:517–527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laur J, Hacke UG (2013) Transpirational demand affects aquaporin expression in poplar roots. J Exp Bot 64:2283–2293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lawlor DW (1970) Absorption of polyethylene glycols by plants and their effects on plant growth. New Phytol 69:501–513

    Article  CAS  Google Scholar 

  • Lee SH, Chung GC, Jang JY, Ahn SJ, Hong SW, Zwiazek JJ (2012) Over-expression of PIP2;5 aquaporin alleviates effects of low root temperature on cell hydraulic conductivity and growth in Arabidopsis. Plant Physiol 159:479–488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lian HL, Yu X, Ye Q, Ding XS, Kitagawa Y, Kwa KSS, Su WA, Tang ZC (2004) The role of aquaporin RWC3 in drought avoidance in rice. Plant Cell Physiol 45:481–489

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Equiza MA, Navarro-Rodenas A, Lee SH, Zwiazek JJ (2014) Hydraulic adjustments in aspen (Populus tremuloides) seedlings following defoliation involve root and leaf aquaporins. Planta 240:553–564

    Article  CAS  PubMed  Google Scholar 

  • Lu Y, Equiza MA, Deng X, Tyree MT (2010) Recovery of Populus tremuloides seedlings following severe drought causing total leaf mortality and extreme stem embolism. Physiol Plant 1:246–257

    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 

  • Maurel C, Boursiac Y, Luu DT, Santoni V, Shahzad Z, Verdoucq L (2015) Aquaporins in plants. Physiol Rev 95:1321–1358

    Article  CAS  PubMed  Google Scholar 

  • Michel BE, Kaufmann MR (1973) The osmotic potential of polyethylene glycol 6000. Plant Physiol 51:914–916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mujtaba SM, Khanzada B, Ali M, Naqvi MH, Mughal S, Alam SM, Shirazi MU, Khan MA, Mumtaz S (2005) The effect of polyethylene glycol on seed germination of wheat (Triticum aestivum L.) genotypes/lines. Wheat Inform Serv 99:58–60

    Google Scholar 

  • R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing Vienna Austria. http://www.R-project.org/

  • Ranganathan K, El Kayal W, Cooke JEK, Zwiazek JJ (2016) Responses of hybrid aspen over-expressing PIP2;5 aquaporin to low root temperature. J Plant Physiol 192:98–104

    Article  CAS  PubMed  Google Scholar 

  • Siemens JA, Zwiazek JJ (2004) Changes in root water flow properties of solution culture-grown trembling aspen (Populus tremuloides) seedlings under different intensities of water-deficit stress. Physiol Plant 121:44–49

    Article  CAS  PubMed  Google Scholar 

  • Sreedharan S, Shekhawat UKS, Ganapathi TR (2013) Transgenic banana plants over-expressing a native plasma membrane aquaporin MusaPIP1;2 display high tolerance levels to different abiotic stresses. Plant Biotechnol J 11(8):942–952

    Article  CAS  PubMed  Google Scholar 

  • Steudle E, Peterson CA (1988) How does water get through roots? J Exp Bot 49:775–788

    Google Scholar 

  • Tsuchihira A, Hanba YT, Kato N, Doi T, Kawazu T, Maeshima M (2010) Effect of over-expression of radish plasma membrane aquaporins on water-use efficiency, photosynthesis and growth of Eucalyptus trees. Tree Physiol 30:417–430

    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 

  • Vandeleur RK, Mayo G, Shelden MC, Gilliham M, Kaiser BN, Tyerman SD (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 149:445–460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Voicu MC, Zwiazek JJ (2004) Cycloheximide inhibits root water flow and stomatal conductance in aspen (Populus tremuloides) seedlings. Plant Cell Environ 27:199–208

    Article  CAS  Google Scholar 

  • Voicu MC, Zwiazek JJ, Tyree MT (2008) Light response of hydraulic conductance in bur oak (Quercus macrocarpa) leaves. Tree Physiol 28:1007–1015

    Article  CAS  PubMed  Google Scholar 

  • Wan X, Zwiazek JJ (2001) Root water flow and stomatal conductance in aspen (Populus tremuloides) seedlings treated with abscisic acid. Planta 213:741–747

    Article  CAS  PubMed  Google Scholar 

  • Zhang W, Calvo-Polanco M, Chen ZC, Zwiazek JJ (2013) Growth and physiological responses of trembling aspen (Populus tremuloides), white spruce (Picea glauca) and tamarack (Larix laricina) seedlings to root zone pH. Plant Soil 373:775–786

    Article  CAS  Google Scholar 

  • Zwiazek JJ, Tan X, Xu H, Navarro-Ródenas A, Morte A (2016) Functional significance of oxygen transport through aquaporins. Sci Rep 17:40411

    Google Scholar 

  • Zhou S, Hu W, Deng X, Ma Z, Chen L, Huang C, Wang C, Wang J, He Y, Yang G, He G (2012) Overexpression of the wheat aquaporin gene, TaAQP7, enhances drought tolerance in transgenic tobacco. PLoS ONE 7(12):e52439. doi:10.1371/journal.pone.0052439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This study was funded by Discovery Grants from the Natural Sciences and Engineering Research Council of Canada to J. J. Zwiazek and J. E. K. Cooke.

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Authors and Affiliations

  1. Department of Renewable Resources, University of Alberta, Edmonton, AB, T6G 2E3, Canada

    Kapilan Ranganathan, Maria A. Equiza, Maryamsadat Vaziriyeganeh & Janusz J. Zwiazek

  2. Department of Biological Sciences, University of Alberta, Edmonton, AB, Canada

    Janice E. K. Cooke & Walid El Kayal

  3. Department of Forestry and Wood Technology, Faculty of Agriculture, Alexandria University, EL-Shatby, Alexandria, Egypt

    Walid El Kayal

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  1. Kapilan Ranganathan
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  2. Janice E. K. Cooke
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  4. Maria A. Equiza
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  5. Maryamsadat Vaziriyeganeh
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Correspondence to Janusz J. Zwiazek.

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Communicated by MG dos Santos.

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Ranganathan, K., Cooke, J.E.K., El Kayal, W. et al. Over-expression of PIP2;5 aquaporin alleviates gas exchange and growth inhibition in poplars exposed to mild osmotic stress with polyethylene glycol. Acta Physiol Plant 39, 187 (2017). https://doi.org/10.1007/s11738-017-2486-6

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  • DOI: https://doi.org/10.1007/s11738-017-2486-6

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