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AcPIP2, a plasma membrane intrinsic protein from halophyte Atriplex canescens, enhances plant growth rate and abiotic stress tolerance when overexpressed in Arabidopsis thaliana

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Abstract

Key message

An aquaporin protein AcPIP2 from Atriplex canescens was involved in plant growth rate, abiotic stress tolerance in Arabidopsis. Under limited water condition, AcPIP2 leaded to the sensitivity to drought stress.

Abstract

An aquaporin protein (AcPIP2) was obtained from the saltbush Atriplex canescens, which was in PIP2 subgroup belonging to the PIP subfamily, MIP superfamily. The subcellular localization of AcPIP2 showed the fusion protein AcPIP2-eGFP located at the plasma membrane in Nicotiana benthamiana. Overexpression of AcPIP2 in Arabidopsis fully proved that AcPIP2 was involved in plant growth rate, transpiration rate and abiotic stress tolerance (NaCl, drought and NaHCO3) in Arabidopsis, which is mostly in correspondence to gene expression pattern characterized by qRT-PCR performed in A. canescens. And under limited water condition, AcPIP2 overexpression leaded to the sensitivity to drought stress. In the view of the resistant effect in transgenic Arabidopsis overexpressing AcPIP2, the AcPIP2 may throw some light into understanding how the A. canescens plants cope with abiotic stress, and could be used in the genetic engineering to improve plant growth or selective tolerance to the abiotic stress.

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Abbreviations

AQPs:

Proteins called aquaporins

MIPs:

Major intrinsic proteins

TIPs:

Tonoplast intrinsic proteins

PIPs:

Plasma membrane intrinsic proteins

NIPs:

Noduline 26-like intrinsic membrane proteins

SIPs:

Small basic intrinsic proteins

PCR:

Polymerase chain reaction

eGFP:

Enhance green fluorescent protein

cDNA:

Complementary DNA

MS:

Murashige and Skoog

Hyg:

Hygromycin

OE:

Overexpresser

WT:

Wild-type

VC:

Vector

EF1α:

Elongation factor 1-alpha

FW:

Fresh weight

DW:

Dry weight

WC:

Water contents

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

NBT:

Nitroblue tetrazolium

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 Central  PubMed  Google Scholar 

  • Aroca R, Amodeo G, Fernandez-Illescas S, Herman EM, Chaumont F, Chrispeels MJ (2005) The role of aquaporins and membrane damage in chilling and hydrogen peroxide induced changes in the hydraulic conductance of Maize roots. Plant Physiol 137:341–353

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ayarpadikannan S, Chung E, Cho CW, So HA, Kim SO, Jeon JM, Kwak MH, Lee SW, Lee JH (2011) Exploration for the salt stress tolerance genes from a salt-treated halophyte, Suaeda asparagoides. Plant Cell Rep 31:35–48

    Article  PubMed  Google Scholar 

  • Benga G (2009) Water channel proteins (later called aquaporins) and relatives: past, present, and future. IUBMB Life 61:112–133

    Article  CAS  PubMed  Google Scholar 

  • Benzarti M, Ben Rejeb K, Debez A, Abdelly C (2013) Environmental and economical opportunities for the valorisation of the genus Atriplex: new insights. In: Hakeem KR, Ahmad P, Ozturk M (eds) Crop improvement. Springer, New York, pp 441–457

    Chapter  Google Scholar 

  • Chowdhury SR, Choudhuri MA (1985) Hydrogen peroxide metabolism as an index of water stress tolerance in jute. Physiol Plant 65:476–480

    Article  CAS  Google Scholar 

  • Forrest KL, Bhave M (2007) Major intrinsic proteins (MIPs) in plants: a complex gene family with major impacts on plant phenotype. Funct Integr Genomics 7:263–289

    Article  CAS  PubMed  Google Scholar 

  • Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442

    Article  PubMed  Google Scholar 

  • Guo L, Wang ZY, Lin H, Cui WE, Chen J, Liu M, Chen ZL, Qu LJ, Gu H (2006) Expression and functional analysis of the rice plasma-membrane intrinsic protein gene family. Cell Res 16:277–286

    Article  CAS  PubMed  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  CAS  PubMed  Google Scholar 

  • Jang J, Lee S, Rhee J, Chung G, Ahn S, Kang H (2007) Transgenic Arabidopsis and tobacco plants overexpressing an aquaporin respond differently to various abiotic stresses. Plant Mol Biol 64:621–632

    Article  CAS  PubMed  Google Scholar 

  • Kammerloher W, Fischer U, Piechottka GP, Schiiffner AR (1994) Water channels in the plant plasma membrane cloned by immunoselection from a mammalian expression system. Plant J 6:187–199

    Article  CAS  PubMed  Google Scholar 

  • Katsuhara M, Akiyama Y, Koshio K, Shibasaka M, Kasamo K (2002) Functional analysis of water channels in barley roots. Plant Cell Physiology 43:885–893

    Article  CAS  PubMed  Google Scholar 

  • Katsuhara M, Koshio K, Shibasaka M, Hayashi Y, Hayakawa T, Kasamo K (2003) Overexpression of a barley aquaporin increased the shoot-root ratio and raised salt sensitivity in transgenic rice plants. Plant Cell Physiology 44:1378–1383

    Article  CAS  PubMed  Google Scholar 

  • Kourie JI (1998) Interaction of reactive oxygen species with ion transport mechanisms. Am J Physiol Cell Physiol 275:C1–C24

    CAS  Google Scholar 

  • Li L, Li S, Tao Y, Kitagawa Y (2000) Molecular cloning of a novel water channel from rice its products expression in Xenopus oocytes and involvement in chilling tolerance. Plant Sci 154:43–51

    Article  CAS  PubMed  Google Scholar 

  • Li DD, Tai FJ, Zhang ZT, Li Y, Zheng Y, Wu YF, Li XB (2009) A cotton gene encodes a tonoplast aquaporin that is involved in cell tolerance to cold stress. Gene 438:26–32

    Article  CAS  PubMed  Google Scholar 

  • Li J, Sun X, Yu G, Jia C, Liu J, Pan H (2014a) Generation and analysis of expressed sequence tags (ESTs) from halophyte Atriplex canescens to explore salt-responsive related genes. Int J Mol Sci 15:11172–11189

    Article  PubMed Central  PubMed  Google Scholar 

  • Li JT, Yu G, Sun XH, Jia CG, Du Q, Li QY, Pan HY (2014b) Modification of vectors for functional genomic analysis in plants. Genet Mol Res 13:7815–7825

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Wang L, Xing X, Sun L, Pan J, Kong X, Zhang M, Li D (2013) ZmLEA3, a multifunctional group 3 LEA protein from Maize (Zea mays L.), is involved in biotic and abiotic stresses. Plant Cell Physiol 54:944–959

    Article  CAS  PubMed  Google Scholar 

  • Mao X, Zhang H, Qian X, Li A, Zhao G, Jing R (2012) TaNAC2, a NAC-type wheat transcription factor conferring enhanced multiple abiotic stress tolerances in Arabidopsis. J Exp Bot 63:2933–2946

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Martinez-Ballesta MC, Carvajal M (2014) New challenges in plant aquaporin biotechnology. Plant Sci 217–218:71–77

    Article  Google Scholar 

  • Matus J, Ferrier T, Riechmann J (2014) Identification of Arabidopsis knockout lines for genes of interest. In: Development Flower (ed) Riechmann JL, Wellmer F. Springer New, York, pp 347–362

    Google Scholar 

  • Nogueira FTS, Rosa VED, Menossi M, Ulian EC, Arruda P (2003) RNA expression profiles and data mining of sugarcane response to low temperature. Plant Physiol 132:1811–1824

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pandey P, Senthil-Kumar M, Mysore K (2015) Advances in plant gene silencing methods. In: Mysore KS, Senthil-Kumar M (eds) Plant gene silencing. Springer, New York, pp 3–23

    Google 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(9):1568–1577

    Article  CAS  PubMed  Google Scholar 

  • Sales AD, Lobo CH, Carvalho AA, Moura AA, Rodrigues APR (2013) Structure, function, and localization of aquaporins: their possible implications on gamete cryopreservation. Genet Mol Res 12:6718–6732

    Article  CAS  PubMed  Google Scholar 

  • Shanker AK, Maheswari M, Yadav SK, Desai S, Bhanu D, Attal NB, Venkateswarlu B (2014) Drought stress responses in crops. Funct Integr Genomics 14:11–22

    Article  CAS  PubMed  Google Scholar 

  • Shao Y, Guan Y, Wang L, Qiu Z, Liu M, Chen Y, Wu L, Li Y, Ma X, Liu M, Li D (2014) CRISPR/Cas-mediated genome editing in the rat via direct injection of one-cell embryos. Nat Protoc 9:2493–2512

    Article  CAS  PubMed  Google Scholar 

  • Shi J, Fu XZ, Peng T, Huang XS, Fan QJ, Liu JH (2010) Spermine pretreatment confers dehydration tolerance of citrus in vitro plants via modulation of antioxidative capacity and stomatal response. Tree Physiol 30:914–922

    Article  CAS  PubMed  Google Scholar 

  • Sun XH, Yu G, Li JT, Jia P, Zhang JC, Jia CG, Zhang YH, Pan HY (2014a) A heavy metal-associated protein (AcHMA1) from the halophyte, Atriplex canescens (Pursh) Nutt., confers tolerance to iron and other abiotic stresses when expressed in Saccharomyces cerevisiae. Int J Mol Sci 15:14891–14906

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sun Y, Yan F, Cui X, Liu F (2014b) Plasticity in stomatal size and density of potato leaves under different irrigation and phosphorus regimes. J Plant Physiol 171:1248–1255

    Article  CAS  PubMed  Google Scholar 

  • Thomashow MF (2001) So what’s new in the field of plant cold acclimation? Lots! Plant Physiol 125:89–93

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Törnroth-Horsefield S, Wang Y, Hedfalk K, Johanson U, Karlsson M, Tajkhorshid E, Neutze R, Kjellbom P (2006) Structural mechanism of plant aquaporin gating. Nature 439:688–694

    Article  PubMed  Google Scholar 

  • Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Jing R, Mao X, Chang X, Li A (2010) TaABC1, a member of the activity of bc 1 complex protein kinase family from common wheat, confers enhanced tolerance to abiotic stresses in Arabidopsis. J Exp Bot 62:1299–1311

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang J, Sun PP, Chen CL, Wang Y, Fu XZ, Liu JH (2011) An arginine decarboxylase gene PtADC from Poncirus trifoliata confers abiotic stress tolerance and promotes primary root growth in Arabidopsis. J Exp Bot 62:2899–2914

    Article  CAS  PubMed  Google Scholar 

  • Yang L, Ji W, Gao P, Li Y, Cai H, Bai X, Chen Q, Zhu Y (2012) GsAPK, an ABA-activated and calcium-independent SnRK2-Type kinase from G. soja, mediates the regulation of plant tolerance to salinity and ABA stress. PLoS One 7(3):e33838

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang X, Henriques R, Lin SS, Niu QW, Chua NH (2006) Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat Protoc 1:641–646

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Li Y, Lai J, Zhang H, Liu Y, Liang L, Xie Q (2011) Ectopic expression of a LEA protein gene TsLEA1 from Thellungiella salsuginea confers salt-tolerance in yeast and Arabidopsis. Mol Biol Rep 39:4627–4633

    Article  PubMed  Google Scholar 

  • Zhu C, Schraut D, Hartung W, Schäffner AR (2005) Differential responses of maize MIP genes to salt stress and ABA. J Exp Bot 56:2971–2981

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grants of the 12th Five-Year Plan Project of Science and Technology Support, China (2012BAD19B04, 2014BAD14B02), and by the Research and Development of Industrial Technology Special at Jilin Provincial Development and Reform Commission (2013C001), and by the Ministry of Agriculture Key Project of GM Cultivation of New Varieties (2013ZX08004004), P. R. China, and by the Project 2014119 Supported by Graduate Innovation Fund of Jilin University.

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The authors declare that they have no conflict of interest.

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Correspondence to Hongyu Pan.

Additional information

Communicated by H. Ebinuma.

J. Li and G. Yu contributed equally to this work.

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Li, J., Yu, G., Sun, X. et al. AcPIP2, a plasma membrane intrinsic protein from halophyte Atriplex canescens, enhances plant growth rate and abiotic stress tolerance when overexpressed in Arabidopsis thaliana . Plant Cell Rep 34, 1401–1415 (2015). https://doi.org/10.1007/s00299-015-1796-7

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  • DOI: https://doi.org/10.1007/s00299-015-1796-7

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