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Constitutive and stress-inducible overexpression of a native aquaporin gene (MusaPIP2;6) in transgenic banana plants signals its pivotal role in salt tolerance

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Abstract

High soil salinity constitutes a major abiotic stress and an important limiting factor in cultivation of crop plants worldwide. Here, we report the identification and characterization of a aquaporin gene, MusaPIP2;6 which is involved in salt stress signaling in banana. MusaPIP2;6 was firstly identified based on comparative analysis of stressed and non-stressed banana tissue derived EST data sets and later overexpression in transgenic banana plants was performed to study its tangible functions in banana plants. The overexpression of MusaPIP2;6 in transgenic banana plants using constitutive or inducible promoter led to higher salt tolerance as compared to equivalent untransformed control plants. Cellular localization assay performed using transiently transformed onion peel cells indicated that MusaPIP2;6 protein tagged with green fluorescent protein was translocated to the plasma membrane. MusaPIP2;6-overexpressing banana plants displayed better photosynthetic efficiency and lower membrane damage under salt stress conditions. Our results suggest that MusaPIP2;6 is involved in salt stress signaling and tolerance in banana.

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References

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

    Article  CAS  PubMed  Google Scholar 

  • Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. Plant Cell 7:1099–1111

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Boyer JS (1982) Plant productivity and environment. Science 218:443–448

    Article  CAS  PubMed  Google Scholar 

  • Cabot C, Sibole JV, Barcelo J, Poschenrieder C (2014) Lessons from crop plants struggling with salinity. Plant Sci 226:2–13

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Zhong HY, Kuang JF, Li JG, Lu WJ, Chen JY (2011) Validation of reference genes for RT-qPCR studies of gene expression in banana fruit under different experimental conditions. Planta 234:377–390

    Article  CAS  PubMed  Google Scholar 

  • Dai JR, LiuB Feng DR, Liu HY, He YM, Qi KB, Wang HB, Wang JF (2011) MpAsr encodes an intrinsically unstructured protein and enhances osmotic tolerance in transgenic Arabidopsis. Plant Cell Rep 30:1219–1230

    Article  CAS  PubMed  Google Scholar 

  • D’Hont A, Denoeud F, Aury JM, Baurens FC, Carreel F et al (2012) The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488:213–217

    Article  PubMed  Google Scholar 

  • Feng DR, Liu B, Li WY, He YM, Qi KB, Wang HB, Wang JF (2009) Over-expression of a cold-induced plasma membrane protein gene (MpRCI) from plantain enhances low temperature resistance in transgenic tobacco. Environ Exp Bot 65:395–402

    Article  CAS  Google Scholar 

  • Ganapathi TR, Higgs NS, Balint-Kurti PJ, Arntzen CJ, May GD, Van Eck JM (2001) Agrobacterium-mediated transformation of embryogenic cell suspensions of the banana cultivar Rasthali (AAB). Plant Cell Rep 20:157–162

    Article  CAS  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 

  • Hu W, Yuan Q, Wang Y, Cai R, Deng X et al (2012) Overexpression of a wheat aquaporin gene, TaAQP8, enhances salt stress tolerance in transgenic tobacco. Plant Cell Physiol 53:2127–2141

    Article  CAS  PubMed  Google Scholar 

  • Huang G-T, Ma S-L, Bai L-P, Zhang L, Ma H, Jia P et al (2012) Signal transduction during cold, salt, and drought stresses in plants. Mol Biol Rep 39:969–987

    Article  PubMed  Google Scholar 

  • Liu HY, Dai JR, Feng DR, Liu B, Wang HB, Wang JF (2010) Characterization of a novel plantain Asr gene, MpAsr, that is regulated in response to infection of Fusarium oxysporum f. sp. cubense and abiotic stresses. J Integr Plant Biol 52:315–323

    Article  CAS  PubMed  Google Scholar 

  • Liu C, Fukumoto T, Matsumoto T, Gena P, Frascaria D et al (2012) Aquaporin OsPIP1;1 promotes rice salt resistance and seed germination. Plant Physiol Biochem 63:151–158

    Article  PubMed  Google Scholar 

  • Matsumoto T, Lian HL, Su WA, Tanaka D, Liu CW, Iwasaki I, Kitagawa Y (2009) Role of the aquaporin PIP1 subfamily in the chilling tolerance of rice. Plant Cell Physiol 50:216–229

    Article  CAS  PubMed  Google Scholar 

  • Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36

    Article  PubMed Central  PubMed  Google Scholar 

  • Podevin N, Krauss A, Henry I, Swennen R, Remy S (2012) Selection and validation of reference genes for quantitative RT-PCR expression studies of the non-model crop Musa. Mol Breed 30:1237–1252

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shekhawat UKS, Ganapathi TR (2013) MusaWRKY71 overexpression in banana plants leads to altered abiotic and biotic stress responses. PLoS One 8:e75506

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shekhawat UKS, Ganapathi TR (2014) Transgenic banana plants overexpressing MusabZIP53 display severe growth retardation with enhanced sucrose and polyphenol oxidase activity. Plant Cell Tissue Organ Cult 116:387–402

    Article  CAS  Google Scholar 

  • Shekhawat UKS, Srinivas L, Ganapathi TR (2011a) MusaDHN-1, a novel multiple stress-inducible SK(3)-type dehydrin gene, contributes affirmatively to drought- and salt-stress tolerance in banana. Planta 234:915–932

    Article  CAS  PubMed  Google Scholar 

  • Shekhawat UKS, Ganapathi TR, Srinivas L (2011b) Cloning and characterization of a novel stress-responsive WRKY transcription factor gene (MusaWRKY71) from Musa spp. cv. Karibale Monthan (ABB group) using transformed banana cells. Mol Biol Rep 38:4023–4035

    Article  CAS  PubMed  Google Scholar 

  • Sreedharan S, Shekhawat UKS, Ganapathi TR (2012) MusaSAP1, a A20/AN1 zinc finger gene from banana functions as a positive regulator in different stress responses. Plant Mol Biol 80:503–517

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Turner DW (2005) Factors affecting the physiology of the banana root system. Methodologies for root system assessment in bananas and plantains (Musa spp.). In: Turner DW, Rosales FE (eds) Banana root system: towards a better understanding for its productive management. Proceedings of an international symposium (INIBAP, Montpellier) pp 107–113

  • Xu Y, Wei H, Juhua L, Jianbin Z, Caihong J, Hongxia M, Biyu X, Zhiqiang J (2014) A banana aquaporin gene, MaPIP1;1, is involved in tolerance to drought and salt stresses. BMC Plant Biol 14:59

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhou S, Hu W, Deng X, Ma Z, Chen L et al (2012) Overexpression of the wheat aquaporin gene, TaAQP7, enhances drought tolerance in transgenic tobacco. PLoS One 7:e52439

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

Authors thank Dr. S P Kale, Head, Nuclear Agriculture and Biotechnology Division, BARC for his continuous support and encouragement.

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    Authors and Affiliations

    1. Plant Cell Culture Technology Section, Nuclear Agriculture and Biotechnology Division, Bhabha Atomic Research Centre, Trombay, Mumbai, 400 085, India

      Shareena Sreedharan, Upendra K. Singh Shekhawat & Thumballi R. Ganapathi

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    1. Shareena Sreedharan
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    2. Upendra K. Singh Shekhawat
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    3. Thumballi R. Ganapathi
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    Correspondence to Thumballi R. Ganapathi.

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    Shareena Sreedharan and Upendra K Singh Shekhawat have contributed equally to this work.

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    Sreedharan, S., Shekhawat, U.K.S. & Ganapathi, T.R. Constitutive and stress-inducible overexpression of a native aquaporin gene (MusaPIP2;6) in transgenic banana plants signals its pivotal role in salt tolerance. Plant Mol Biol 88, 41–52 (2015). https://doi.org/10.1007/s11103-015-0305-2

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    • DOI: https://doi.org/10.1007/s11103-015-0305-2

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