Targeting Aquaporins for Conferring Salinity Tolerance in Crops

  • Kundan Kumar
  • Ankush Ashok Saddhe


Salinity is one of the well-known abiotic stresses which affects crop productivity through imposing ion imbalance and disrupting the metabolic pathways. Soil salinity is dramatically increasing throughout the world because of climate change, rise in sea levels, excessive irrigation, and natural leaching process. To overcome this problem, many approaches were reported including selection of natural salt-tolerant variety, breeding program, and genetic-engineered plants. Membrane intrinsic proteins (MIPs; also called aquaporins) are membrane channel proteins initially discovered as water channels, but their roles in the transport of small neutral solutes, metal ions, and gasses are now well established. Based on homology and subcellular localization, plant MIPs are divided into four major subfamilies: plasma membrane intrinsic proteins (PIPs), tonoplast intrinsic proteins (TIPs), NOD26-like intrinsic proteins (NIPs), and small basic intrinsic proteins (SIPs). Besides these four subfamilies, some unique subfamilies were reported such as GlpF-like intrinsic proteins (GIPs), hybrid intrinsic proteins (HIPs), and the uncategorized X intrinsic proteins (XIPs). In plants, MIPs are involved in diverse physiological roles such as seed germination; fruit ripening; leaf, petal, and stomata movement; phloem loading and unloading; reproduction; and stress response. However, a large number of studies have suggested the involvement of MIPs in various abiotic stresses, including drought, salt, and cold stress. PIPs and TIPs have shown differential regulation pattern in roots and shoots of Arabidopsis, barley, and maize in salinity stress. Moreover, overexpression studies of various PIPs and TIPs in plant suggest their possible role in salt tolerance. Transcriptome analyses of citrus under salt stress showed that in addition to PIPs and TIPs, most of the NIPs, XIPs, and SIPs were differentially regulated in root tissues. In the present chapter, we discussed roles of plant aquaporins in salinity stress and exploitating the same for genetic engineering approach.


Abiotic stress Salinity Aquaporins MIPs PIPs TIPs NIPs SIPs XIPs HIPs GIPs 



GlpF-like intrinsic proteins


Hybrid intrinsic proteins

McMipA and McMipC

Mesembryanthemum crystallinum MIP-related genes


Membrane intrinsic proteins


NOD26-like intrinsic proteins


Plasma membrane intrinsic proteins


Small basic intrinsic proteins


Tonoplast intrinsic proteins


Uncategorized X intrinsic proteins



The work in KK lab was supported by financial assistance from Board of Research in Nuclear Sciences (37(1)/14/28/2016-BRNS/37248), India. AAS acknowledges the Senior Research Fellowship provided by University Grants Commission, India.


  1. Abdelkader AF, El-khawas S, El-Din El-Sherif NA, Hassanein RA, Emam MA, Hassan RE (2012) Expression of aquaporin gene (OsPIP1-3) in salt-stressed rice (Oryza sativa L.) plants pre-treated with the neurotransmitter (dopamine). Plant Omics 5(6):532Google Scholar
  2. Afzal Z, Howton TC, Sun Y, Mukhtar MS (2016) The roles of aquaporins in plant stress responses. J Dev Biol 4(1):9PubMedCentralCrossRefGoogle Scholar
  3. 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(2):439–447PubMedPubMedCentralCrossRefGoogle Scholar
  4. Alexandersson E, Fraysse L, Sjövall-Larsen S, Gustavsson S, Fellert M, Karlsson M et al (2005) Whole gene family expression and drought stress regulation of aquaporins. Plant Mol Biol 59(3):469–484PubMedCrossRefGoogle Scholar
  5. Ampah-Korsah H, Anderberg HI, Engfors A, Kirscht A, Norden K, Kjellstrom S, Kjellbom P, Johanson U (2016) The aquaporin splice variant NbXIP1; 1α is permeable to boric acid and is phosphorylated in the N-terminal domain. Front Plant Sci 7Google Scholar
  6. Ampah-Korsah H, Sonntag Y, Engfors A, Kirscht A, Kjellbom P, Johanson U (2017) Single amino acid substitutions in the selectivity filter render NbXIP1;1α aquaporin water permeable. BMC Plant Biol 17(1):61PubMedPubMedCentralCrossRefGoogle Scholar
  7. Atkinson NJ, Lilley CJ, Urwin PE (2013) Identification of genes involved in the response of Arabidopsis to simultaneous biotic and abiotic stresses. Plant Physiol 162(4):2028–2041PubMedPubMedCentralCrossRefGoogle Scholar
  8. Bienert GP, Bienert MD, Jahn TP, Boutry M, Chaumont F (2011) Solanaceae XIPs are plasma membrane aquaporins that facilitate the transport of many uncharged substrates. Plant J 66(2):306–317PubMedCrossRefGoogle Scholar
  9. Boursiac Y, Chen S, Luu DT, Sorieul M, van den Dries N, Maurel C (2005) Early effects of salinity on water transport in Arabidopsis roots, molecular and cellular features of aquaporin expression. Plant Physiol 139(2):790–805PubMedPubMedCentralCrossRefGoogle Scholar
  10. Byrt CS, Zhao M, Kourghi M, Bose J, Henderson SW, Qiu J, Gilliham M, Schultz C, Schwarz M, Ramesh SA, Yool A (2017) Non-selective cation channel activity of aquaporin AtPIP2;1 regulated by Ca2+ and pH. Plant Cell Environ 40:802–815PubMedCrossRefGoogle Scholar
  11. Calamita G, Bishai WR, Preston GM, Guggino WB, Agre P (1995) Molecular cloning and characterization of AqpZ, a Water Channel from Escherichia coli. J Biol Chem 270(49):29063–29066PubMedCrossRefGoogle Scholar
  12. Carbrey JM, Bonhivers M, Boeke JD, Agre P (2001) Aquaporins in Saccharomyces: characterization of a second functional water channel protein. PNAS 98(3):1000–1005Google Scholar
  13. Cavanagh C, Morell M, Mackay I, Powell W (2008) From mutations to MAGIC: resources for gene discovery, validation and delivery in crop plants. Curr Opin Plant Biol 11(2):215–221PubMedCrossRefGoogle Scholar
  14. Chang W, Liu X, Zhu J, Fan W, Zhang Z (2016) An aquaporin gene from halophyte Sesuvium portulacastrum, SpAQP1, increases salt tolerance in transgenic tobacco. Plant Cell Rep 35(2):385–395PubMedCrossRefGoogle Scholar
  15. 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(4):1025–1034PubMedPubMedCentralCrossRefGoogle Scholar
  16. Chaumont F, Barrieu F, Wojcik E, Chrispeels MJ, Jung R (2001) Aquaporins constitute a large and highly divergent protein family in maize. Plant Physiol 125(3):1206–1215PubMedPubMedCentralCrossRefGoogle Scholar
  17. Chinnusamy V, Zhu JK (2009) Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol 12(2):133–139PubMedPubMedCentralCrossRefGoogle Scholar
  18. Cohen D, Bogeat-Triboulot MB, Vialet-Chabrand S, Merret R, Courty PE, Moretti S, Bizet F, Guilliot A, Hummel I (2013) Developmental and environmental regulation of Aquaporin gene expression across Populus species: divergence or redundancy? PLoS One 8(2):e55506PubMedPubMedCentralCrossRefGoogle Scholar
  19. Cramer GR, Ergül A, Grimplet J, Tillett RL, Tattersall EA, Bohlman MC, Vincent D, Sonderegger J, Evans J, Osborne C, Quilici D (2007) Water and salinity stress in grapevines: early and late changes in transcript and metabolite profiles. Funct integr Genomic 7(2):111–134CrossRefGoogle Scholar
  20. Danielson JÅ, Johanson U (2008) Unexpected complexity of the aquaporin gene family in the moss Physcomitrella patens. BMC Plant Biol 8(1):45PubMedPubMedCentralCrossRefGoogle Scholar
  21. Deshmukh RK, Nguyen HT, Belanger RR (2017) Aquaporins: dynamic role and regulation. Frontiers in Plant Sci 8:1420CrossRefGoogle Scholar
  22. Deshmukh RK, Sonah H, Bélanger RR (2016) Plant Aquaporins: genome-wide identification, transcriptomics, proteomics, and advanced analytical tools. Front Plant Sci 7Google Scholar
  23. Deshmukh RK, Vivancos J, Ramakrishnan G, Guérin V, Carpentier G, Sonah H, Labbé C, Isenring P, Belzile FJ, Bélanger RR (2015) A precise spacing between the NPA domains of aquaporins is essential for silicon permeability in plants. Plant J 83(3):489–500PubMedCrossRefGoogle Scholar
  24. Ermawati N, Liang YS, Cha JY, Shin D, Jung MH, Lee JJ, Lee BH, Han CD, Lee KH, Son D (2009) A new TIP homolog, ShTIP, from Salicornia shows a different involvement in salt stress compared to that of TIP from Arabidopsis. Biol plantarum 53(2):271–277CrossRefGoogle Scholar
  25. Forrest KL, Bhave M (2007) Major intrinsic proteins (MIPs) in plants: a complex gene family with major impacts on plant phenotype. Funct integr genomic 7(4):263CrossRefGoogle Scholar
  26. Fortin MG, Morrison NA, Verma DP (1987) Nodulin-26, a peribacteroid membrane nodulin is expressed independently of the development of the peribacteroid compartment. Nucleic Acids Res 15(2):813–824PubMedPubMedCentralCrossRefGoogle Scholar
  27. Gao Z, He X, Zhao B, Zhou C, Liang Y, Ge R, Shen Y, Huang Z (2010) Overexpressing a putative aquaporin gene from wheat, TaNIP, enhances salt tolerance in transgenic Arabidopsis. Plant Cell Physiol 51(5):767–775PubMedCrossRefGoogle Scholar
  28. Gattolin S, Sorieul M, Hunter PR, Khonsari RH, Frigerio L (2009) In vivo imaging of the tonoplast intrinsic protein family in Arabidopsis roots. BMC Plant Biol 9(1):133PubMedPubMedCentralCrossRefGoogle Scholar
  29. Gillespie J, Rogers SW, Deery M, Dupree P, Rogers JC (2005) A unique family of proteins associated with internalized membranes in protein storage vacuoles of the Brassicaceae. Plant J 41(3):429–441PubMedCrossRefGoogle Scholar
  30. Groszmann M, Osborn HL, Evans JR (2017) Carbon dioxide and water transport through plant aquaporins. Plant Cell Environ 40(6):938–961PubMedCrossRefGoogle Scholar
  31. 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(1):134PubMedPubMedCentralCrossRefGoogle Scholar
  32. 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(3):277–286PubMedCrossRefGoogle Scholar
  33. Horie T, Kaneko T, Sugimoto G, Sasano S, Panda SK, Shibasaka M, Katsuhara M (2011) Mechanisms of water transport mediated by PIP aquaporins and their regulation via phosphorylation events under salinity stress in barley roots. Plant Cell Physiol 52(4):663–675PubMedCrossRefGoogle Scholar
  34. Hove RM, Ziemann M, Bhave M (2015) Identification and expression analysis of the barley (Hordeum vulgare L.) aquaporin gene family. PLoS One 10(6):e0128025PubMedPubMedCentralCrossRefGoogle Scholar
  35. Hu W, Hou X, Huang C, Yan Y, Tie W, Ding Z, Wei Y, Liu J, Miao H, Lu Z, Li M (2015) Genome-wide identification and expression analyses of aquaporin gene family during development and abiotic stress in banana. Int J Mol Sci 16(8):19728–19751PubMedPubMedCentralCrossRefGoogle Scholar
  36. Ishikawa F, Suga S, Uemura T, Sato MH, Maeshima M (2005) Novel type aquaporin SIPs are mainly localized to the ER membrane and show cell-specific expression in Arabidopsis thaliana. FEBS Lett 579(25):5814–5820PubMedCrossRefGoogle Scholar
  37. Iyer NJ, Tang Y, Mahalingam R (2013) Physiological., biochemical and molecular responses to a combination of drought and ozone in Medicago truncatula. Plant Cell Environ 36(3):706–720PubMedCrossRefGoogle Scholar
  38. 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(5):713–725PubMedCrossRefGoogle Scholar
  39. Jauh GY, Fischer AM, Grimes HD, Ryan CA, Rogers JC (1998) δ-Tonoplast intrinsic protein defines unique plant vacuole functions. PNAS 95(22):12995–12999PubMedPubMedCentralCrossRefGoogle Scholar
  40. Jauh GY, Phillips TE, Rogers JC (1999) Tonoplast intrinsic protein isoforms as markers for vacuolar functions. Plant Cell 11(10):1867–1882PubMedPubMedCentralCrossRefGoogle Scholar
  41. Johanson U, Gustavsson S (2002) A new subfamily of major intrinsic proteins in plants. Mol Biol Evol 19(4):456–461PubMedCrossRefGoogle Scholar
  42. Johanson U, Karlsson M, Johansson I, Gustavsson S, Sjövall S, Fraysse L, Weig AR, Kjellbom P (2001) The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiol 126(4):1358–1369PubMedPubMedCentralCrossRefGoogle Scholar
  43. Kayum MA, Park JI, Nath UK, Biswas MK, Kim HT, Nou IS (2017) Genome-wide expression profiling of aquaporin genes confer responses to abiotic and biotic stresses in Brassica Rapa. BMC Plant Biol 17(1):23PubMedPubMedCentralCrossRefGoogle Scholar
  44. Kirch HH, Vera-Estrella R, Golldack D, Quigley F, Michalowski CB, Barkla BJ, Bohnert HJ (2000) Expression of water channel proteins in Mesembryanthemum crystallinum. Plant Physiol 123(1):111–124PubMedPubMedCentralCrossRefGoogle Scholar
  45. Kozono D, Ding X, Iwasaki I, Meng X, Kamagata Y, Agre P, Kitagawa Y (2003) Functional expression and characterization of an archaeal aquaporin AqpM from Methanothermobacter marburgensis. J Biol Chem 278(12):10649–10656PubMedCrossRefGoogle Scholar
  46. Kumar K, Kumar M, Kim SR, Ryu H, Cho YG (2013) Insights into genomics of salt stress response in rice. Rice 6(1):27PubMedPubMedCentralCrossRefGoogle Scholar
  47. Li DD, Wu YJ, Ruan XM, Li B, Zhu L, Wang H, Li XB (2009) Expressions of three cotton genes encoding the PIP proteins are regulated in root development and in response to stresses. Plant Cell Rep 28(2):291–300PubMedCrossRefGoogle Scholar
  48. Li GW, Peng YH, Yu X, Zhang MH, Cai WM, Sun WN, Su WA (2008) Transport functions and expression analysis of vacuolar membrane aquaporins in response to various stresses in rice. J Plant Physiol 165(18):1879–1888PubMedCrossRefGoogle Scholar
  49. Li J, Cai W (2015) A ginseng PgTIP1 gene whose protein biological activity related to ser 128 residue confers faster growth and enhanced salt stress tolerance in Arabidopsis. Plant Sci 234:74–85PubMedCrossRefGoogle Scholar
  50. Li J, Yu G, Sun X, Liu Y, Liu J, Zhang X, Jia C, Pan H (2015) 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(8):1401–1415PubMedCrossRefGoogle Scholar
  51. Ligaba A, Katsuhara M, Shibasaka M, Djira G (2011) Abiotic stresses modulate expression of major intrinsic proteins in barley (Hordeum vulgare). C R Biol 334(2):127–139PubMedCrossRefGoogle Scholar
  52. Liu Q, Umeda M, Uchimiya H (1994) Isolation and expression analysis of two rice genes encoding the major intrinsic protein. Plant Mol Biol 26(6):2003–2007PubMedCrossRefGoogle Scholar
  53. Lopez D, Bronner G, Brunel N, Auguin D, Bourgerie S, Brignolas F, Carpin S, Tournaire-Roux C, Maurel C, Fumanal B, Martin F, Sakr S, Label P, Julien JL, Gousset-Dupont A, Venisse JS (2012) Insights into Populus XIP aquaporins: evolutionary expansion, protein functionality, and environmental regulation. J Exp Bot 63(5):2217–2230PubMedCrossRefGoogle Scholar
  54. Luu D-T, Martinière A, Sorieul M, Runions J, Maurel C (2012) Fluorescence recovery after photobleaching reveals high cycling dynamics of plasma membrane aquaporins in Arabidopsis roots under salt stress. Plant J 69(5):894–905PubMedCrossRefGoogle Scholar
  55. Maeshima M, Ishikawa F (2008) ER membrane aquaporins in plants. Pflügers Arch-EJP 456(4):709–716CrossRefGoogle Scholar
  56. Martins CD, Pedrosa AM, Du D, Gonçalves LP, Yu Q, GmitterJr FG, Costa MG (2015) Genome-wide characterization and expression analysis of major intrinsic proteins during abiotic and biotic stresses in sweet orange (Citrus sinensis L. Osb.) PLoS One 10(9):e0138786CrossRefGoogle Scholar
  57. Martins CP, Neves DM, Cidade LC, Mendes AF, Silva DC, Almeida AA, Coelho-Filho MA, Gesteira AS, Soares-Filho WS, Costa MG (2017) Expression of the citrus CsTIP2;1 gene improves tobacco plant growth, antioxidant capacity and physiological adaptation under stress conditions. Planta 245(5):951–963PubMedCrossRefGoogle Scholar
  58. Maurel C, Boursiac Y, Luu DT, Santoni V, Shahzad Z, Verdoucq L (2015) Aquaporins in plants. Physiol Rev 95(4):1321–1358PubMedCrossRefGoogle Scholar
  59. Maurel C, Verdoucq L, Luu DT, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624PubMedCrossRefGoogle Scholar
  60. Menon TG, Soniya EV (2014) Isolation and characterization of salt-induced genes from Rhizophora apiculata Blume, a true mangrove by suppression subtractive hybridization. Curr Sci 107(4):650–655Google Scholar
  61. Mitra BN, Yoshino R, Morio T, Yokoyama M, Maeda M, Urushihara H, Tanaka Y (2000) Loss of a member of the aquaporin gene family, aqpA affects spore dormancy in Dictyostelium. Gene 251(2):131–139PubMedCrossRefGoogle Scholar
  62. Mittler R, Blumwald E (2010) Genetic engineering for modern agriculture: challenges and perspectives. Annu Rev Plant Biol 61:443–462PubMedCrossRefGoogle Scholar
  63. Mohammadkhani N, Heidari R, Abbaspour N, Rahmani F (2012) Growth responses and aquaporin expression in grape genotypes under salinity. Iran J Plant Physiol 2:497–507Google Scholar
  64. Mosa KA, Kumar K, Chhikara S, Musante C, White JC, Dhankher OP (2016) Enhanced boron tolerance in plants mediated by bidirectional transport through plasma membrane intrinsic proteins. Sci Rep 6(1)Google Scholar
  65. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681PubMedCrossRefGoogle Scholar
  66. Pang Y, Li L, Ren F, Lu P, Wei P, Cai J, Xin L, Zhang J, Chen J, Wang X (2010) Overexpression of the tonoplast aquaporin AtTIP5;1 conferred tolerance to boron toxicity in Arabidopsis. J Genet Genomics 37(6):389–397PubMedCrossRefGoogle Scholar
  67. Paris N, Stanley CM, Jones RL, Rogers JC (1996) Plant cells contain two functionally distinct vacuolar compartments. Cell 85(4):563–572PubMedCrossRefGoogle Scholar
  68. Park W, Scheffler BE, Bauer PJ, Campbell BT (2010) Identification of the family of aquaporin genes and their expression in upland cotton (Gossypium hirsutum L.) BMC Plant Biol 10(1):142PubMedPubMedCentralCrossRefGoogle Scholar
  69. Pawłowicz I, Rapacz M, Perlikowski D, Gondek K, Kosmala A (2017) Abiotic stresses influence the transcript abundance of PIP and TIP aquaporins in Festuca species. J Appl Genet 4:1–5Google Scholar
  70. Peng Y, Lin W, Cai W, Arora R (2007) Overexpression of a Panax ginseng tonoplast aquaporin alters salt tolerance, drought tolerance and cold acclimation ability in transgenic Arabidopsis plants. Planta 226(3):729–740PubMedCrossRefGoogle Scholar
  71. Pou A, Jeanguenin L, Milhiet T, Batoko H, Chaumont F, Hachez C (2016) Salinity-mediated transcriptional and post-translational regulation of the Arabidopsis aquaporin PIP2;7. Plant Mol Biol 92(6):731–744PubMedCrossRefGoogle Scholar
  72. Poxleitner M, Rogers SW, Lacey Samuels A, Browse J, Rogers JC (2006) A role for caleosin in degradation of oil-body storage lipid during seed germination. Plant J 47(6):917–933PubMedCrossRefGoogle Scholar
  73. Prasch CM, Sonnewald U (2013) Simultaneous application of heat, drought, and virus to Arabidopsis plants reveals significant shifts in signaling networks. Plant Physiol 162(4):1849–1866PubMedPubMedCentralCrossRefGoogle Scholar
  74. Qian Z-J, Song J-J, Chaumont F, Ye Q (2015) Differential responses of plasma membrane aquaporins in mediating water transport of cucumber seedlings under osmotic and salt stresses. Plant Cell Environ 38(3):461–473PubMedCrossRefGoogle Scholar
  75. Rasmussen S, Barah P, Suarez-Rodriguez MC, Bressendorff S, Friis P, Costantino P, Bones AM, Nielsen HB, Mundy J (2013) Transcriptome responses to combinations of stresses in Arabidopsis. Plant Physiol 161(4):1783–1794PubMedPubMedCentralCrossRefGoogle Scholar
  76. Reddy PS, Rao TS, Sharma KK, Vadez V (2015) Genome-wide identification and characterization of the aquaporin gene family in Sorghum bicolor (L.) Plant Gene 1:18–28CrossRefGoogle Scholar
  77. Rougé P, Barre A (2008) A molecular modeling approach defines a new group of Nodulin 26-like aquaporins in plants. Biochem Biophys Res Commun 367(1):60–66PubMedCrossRefGoogle Scholar
  78. 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):1568–1577PubMedCrossRefGoogle Scholar
  79. Secchi F, Pagliarani C, Zwieniecki MA (2017) The functional role of xylem parenchyma cells and aquaporins during recovery from severe water stress. Plant Cell Environ 40(6):858–871PubMedCrossRefGoogle Scholar
  80. Shelden MC, Howitt SM, Kaiser BN, Tyerman SD (2009) Identification and functional characterisation of aquaporins in the grapevine, Vitis vinifera. Funct Plant Biol 36(12):1065–1078CrossRefGoogle Scholar
  81. Sreedharan S, Shekhawat UK, Ganapathi TR (2015) 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(1–2):41–52PubMedCrossRefGoogle Scholar
  82. Sreedharan S, Shekhawat UK, 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(8):942–952PubMedCrossRefGoogle Scholar
  83. Srivastava AK, Penna S, Nguyen DV, Tran LS (2016) Multifaceted roles of aquaporins as molecular conduits in plant responses to abiotic stresses. Crit Rev Biotechnol 36(3):389–398PubMedGoogle Scholar
  84. Suga S, Komatsu S, Maeshima M (2002) Aquaporin isoforms responsive to salt and water stresses and phytohormones in radish seedlings. Plant Cell Physiol 43(10):1229–1237PubMedCrossRefGoogle Scholar
  85. Sun H, Li L, Lou Y, Zhao H, Yang Y, Wang S, Gao Z (2017) The bamboo aquaporin gene PeTIP4;1–1 confers drought and salinity tolerance in transgenic Arabidopsis. Plant Cell Rep 36(4):597–609PubMedCrossRefGoogle Scholar
  86. Tao P, Zhong X, Li B, Wang W, Yue Z, Lei J, Guo W, Huang X (2014) Genome-wide identification and characterization of aquaporin genes (AQPs) in Chinese cabbage (Brassica rapa ssp. pekinensis). Mol Gen Genomics 289(6):1131–1145CrossRefGoogle Scholar
  87. Ueda M, Tsutsumi N, Fujimoto M (2016) Salt stress induces internalization of plasma membrane aquaporin into the vacuole in Arabidopsis thaliana. Biochem Biophys Res Commun 474(4):742–746PubMedCrossRefGoogle Scholar
  88. Venkatesh J, Yu JW, Park SW (2013) Genome-wide analysis and expression profiling of the Solanum tuberosum aquaporins. Plant Physiol Biochem 73:392–404PubMedCrossRefGoogle Scholar
  89. Vera-Estrella R (2004) Novel regulation of Aquaporins during osmotic stress. Plant Physiol 135(4):2318–2329PubMedPubMedCentralCrossRefGoogle Scholar
  90. Wallace IS, Choi WG, Roberts DM (2006) The structure, function and regulation of the nodulin 26-like intrinsic protein family of plant aquaglyceroporins. Biochimica et Biophysica Acta (BBA)-Biomembranes 1758(8):1165–1175CrossRefGoogle Scholar
  91. Wang X, Li Y, Ji W, Bai X, Cai H, Zhu D et al (2011) A novel Glycine soja tonoplast intrinsic protein gene responds to abiotic stress and depresses salt and dehydration tolerance in transgenic Arabidopsis thaliana. J Plant Physiol 168(11):1241–1248PubMedCrossRefGoogle Scholar
  92. Wang L-L, Chen A-P, Zhong N-Q, Liu N, Wu X-M, Wang F, Yang C-L, Romero MF, Xia G-X (2014) The Thellungiella salsuginea tonoplast aquaporin TsTIP1;2 functions in protection against multiple abiotic stresses. Plant Cell Physiol 55(1):148–161PubMedCrossRefGoogle Scholar
  93. Wudick MM, Luu DT, Tournaire-Roux C, Sakamoto W, Maurel C (2014) Vegetative and sperm cell-specific aquaporins of Arabidopsis highlight the vacuolar equipment of pollen and contribute to plant reproduction. Plant Physiol 164(4):1697–1706PubMedPubMedCentralCrossRefGoogle Scholar
  94. Xin S, Yu G, Sun L, Qiang X, Xu N, Cheng X (2014) Expression of tomato SlTIP2;2 enhances the tolerance to salt stress in the transgenic Arabidopsis and interacts with target proteins. J Plant Res 127(6):695–708PubMedCrossRefGoogle Scholar
  95. Xu Y, Hu W, Liu J, Zhang J, Jia C, Miao H, Xu B, Jin Z (2014) A banana aquaporin gene, MaPIP1;1, is involved in tolerance to drought and salt stresses. BMC Plant Biol 14(1):59PubMedPubMedCentralCrossRefGoogle Scholar
  96. Yamada S, Katsuhara M, Kelly WB, Michalowski CB, Bohnert HJ (1995) A family of transcripts encoding water channel proteins: tissue-specific expression in the common ice plant. Plant Cell 7(8):1129–1142PubMedPubMedCentralCrossRefGoogle Scholar
  97. Yool AJ, Stamer WD, Regan JW (1996) Forskolin stimulation of water and cation permeability in aquaporin1 water channels. Science 30:1216–1218CrossRefGoogle Scholar
  98. Yu GH, Zhang X, Ma HX (2015) Changes in the physiological parameters of -transformed wheat plants under salt stress. Int J Genomics 2015:1–6CrossRefGoogle Scholar
  99. Zhang DY, Ali Z, Wang CB, Xu L, Yi JX, Xu ZL, Liu XQ, He XL, Huang YH, Khan IA, Trethowan RM (2013) Genome-wide sequence characterization and expression analysis of major intrinsic proteins in soybean (Glycine max L.) PLoS One 8(2):e56312PubMedPubMedCentralCrossRefGoogle Scholar
  100. Zhang DY, Kumar M, Xu L, Wan Q, Huang YH, Xu ZL, He XL, Ma JB, Pandey GK, Shao HB (2017a) Genome-wide identification of major intrinsic proteins in Glycine soja and characterization of GmTIP2;1 function under salt and water stress. Sci Rep 7Google Scholar
  101. Zhang D, Huang Y, Kumar M, Wan Q, Xu Z, Shao H, Pandey GK (2017b) Heterologous expression of GmSIP1;3 from soybean in tobacco showed and growth retardation and tolerance to hydrogen peroxide. Plant Sci 263:210–218PubMedCrossRefGoogle Scholar
  102. Zhao YY, Yan F, Hu LP, Zhou XT, Zou ZR, Cui LR (2015) Effects of exogenous 5-aminolevulinic acid on photosynthesis, stomatal conductance, transpiration rate, and PIP gene expression of tomato seedlings subject to salinity stress. Genet Mol Res 14(2):6401–6412PubMedCrossRefGoogle Scholar
  103. Zhou L, Wang C, Liu R, Han Q, Vandeleur RK, Du J, Tyerman S, Shou H (2014) Constitutive overexpression of soybean plasma membrane intrinsic protein GmPIP1;6 confers salt tolerance. BMC Plant Biol 14(1):181PubMedPubMedCentralCrossRefGoogle Scholar
  104. Zhu C, Schraut D, Hartung W, Schäffner AR (2005) Differential responses of maize MIP genes to salt stress and ABA. J Exp Bot 56(421):2971–2981PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biological SciencesBirla Institute of Technology & Science PilaniGoaIndia

Personalised recommendations