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Ukr. Bot. J. 2021, 78(3): 221–234
https://doi.org/10.15407/ukrbotj78.03.221
Cell Biology and Molecular Biology

Aquaporins in regulation of plant protective responses to drought

Ovrutska I.I.
Abstract

Plasmolemma permeability is an integral indicator of the functional state of plant cells under stress. Aquaporins (AQPs), specialized transmembrane proteins that form water channels and play an important role in the adaptation of plants to adverse conditions and, in particular, to lack or excess of water, are involved in the formation of the response to drought. The main function of AQPs is to facilitate the movement of water across cell membranes and maintain aqueous cell homeostasis. Under stressful conditions, there is both an increase and decrease in the expression of individual aquaporin genes. Analysis of the data revealed differences in the expression of AQPs genes in stable and sensitive plant genotypes. It turned out that aquaporins in different stress-resistant varieties of the same species also respond differently to drought. The review provides brief information on the history of the discovery of aquaporins, the structure and function of these proteins, summarizes the latest information on the role of aquaporins in the regulation of metabolism and the response of plants to stressors, with particular emphasis on aquaporins in drought protection. The discovery and study of AQPs expands the possibilities of using genetic engineering methods for the selection of new plant species, in particular, more resistant to drought and salinization of the soil, as well as to increase their productivity. The use of aquaporins in biotechnology to improve drought resistance of various species has many prospects.

Keywords: aquaporins, gene expression, tolerant and sensitive plant genotypes, water stress

Full text: PDF (Ukr) 1.12M

References
  1. Agre P. 2006. The aquaporin water channels. Proceedings of the American Thoracic Society, 3(1): 5–13. https://doi.org/10.1513/pats.200510-109JH
  2. Afzal Z., Howton T.C., Sun Y., Mukhtar M.S. 2016. The roles of aquaporins in plant stress responses. Journal of Developmental Biology, 4(1): 9. https://doi.org/10.3390/jdb4010009
  3. Alexandersson E., Fraysse L., Sjovall-Larsen S., Gustavsson S., Fellert M., Karlsson M., Johanson U., Kjellbom P. 2005. Whole gene family expression and drought stress regulation of aquaporins. Plant Molecular Biology, 59(3): 469–484. https://doi.org/10.1007/s11103-005-0352-1
  4. Alexandersson E., Danielson J.A., Rade J., Moparthi V.K., Fontes M., Kjellbom P., Johanson U. 2008. Transcriptional regulation of aquaporins in accessions of Arabidopsis in response to drought stress. Plant Journal, 61(4): 650–660. https://doi.org/10.1111/j.1365-313X.2009.04087.x
  5. Almeida-Rodriguez A.M., Cooke J.E., Yeh F. Zwiazek J.J. 2010. Functional characterization of drought responsive aquaporins in Populus balsamifera and Populus simonii×balsamifera clones with different drought resistance strategies. Physiologia Plantarum, 140(4): 321–333. https://doi.org/10.1111/j.1399-3054.2010.01405.x
  6. Anderberg H.I., Danielson J.Á.H., Johanson U. 2011. Algal MIPs, high diversity and conserved motifs. BMC Evolutionary Biology, 11(1): 110. https://doi.org/10.1186/1471-2148-11-110
  7. Anderberg H.I., Per K., Urban J. 2012. Annotation of Selaginella moellendorffii major intrinsic proteins and the evolution of the protein family in terrestrial plants. Frontiers in Plant Science, 3: 33. https://doi.org/10.3389/fpls.2012.00033
  8. de-Andrade L.M, Nobile P.M., Ribeiro R.V., de-Oliveira J.F.N.C., Figueira A.V.O., Frigel L.T.M., Nunes D., Perecin D., Brito M.S., Pires R.C.M., Landell M.G.A., Creste S. 2016. Characterization of PIP2 aquaporins in Saccharum hybrids. Plant Gene, 5: 31–37. https://doi.org/10.1016/j.plgene.2015.11.004
  9. Aroca R., Porcel R., Ruiz-Lozano J.M. 2007. How does arbuscular mycorrhizal symbiosis regulate root hydraulic properties and plasma membrane aquaporins in Phaseolus vulgaris under drought, cold or salinity stresses? New Phytologist, 173(4): 808–816. https://doi.org/10.1111/j.1469-8137.2006.01961.x
  10. Aroca R., Vernieri P., Ruiz-Lozano J.M. 2008. Mycorrhizal and non-mycorrhizal Lactuca sativa plants exhibit contrasting responses to exogenous ABA during drought stress and recovery. Journal of Experimental Botany, 59(8): 2029–2041. https://doi.org/10.1093/jxb/ern057
  11. Aroca R., Porcel R., Ruiz-Lozano J.M. 2012. Regulation of root water uptake under abiotic stress conditions. Journal of Experimental Botany, 63 (1): 43–57. https://doi.org/10.1093/jxb/err266
  12. 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 Physiology and Biochemistry, 49(9): 1029–1039. https://doi.org/10.1016/j.plaphy.2011.06.002
  13. Ayadi M., Brini F., Masmoudi K. 2019. Overexpression of a wheat aquaporin gene, TdPIP 2; 1, enhances salt and drought tolerance in transgenic durum wheat cv. Maali. International Journal of Molecular Sciences, 20(10): 2389. https://doi.org/10.3390/ijms20102389
  14. Azad A.K., Yoshikawa N., Ishikawa T., Sawa Y., Shibata H. 2012. Substitution of a single amino acid residue in the aromatic/arginine selectivity filter alters the transport profiles of tonoplast aquaporin homologs. Biochimica et Biophysica Acta, 818(1): 1–11. https://doi.org/10.1016/j.bbamem.2011.09.014
  15. 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 × P. tremula var. glandulosa). Gene, 483(1-2): 43–48. https://doi.org/10.1016/j.gene.2011.05.015
  16. Banerjee A., Roychoudhury A. 2020. The role of aquaporins during plant abiotic stress responses. In: Tripathi D.K., Chauhan D.K. et al. (Eds.), Plant Life under Changing Environment. Responses and Management. London, etc.: Academic Press / Elsevier, pp. 643–661. https://doi.org/10.1016/B978-0-12-818204-8.00028-X
  17. Bárzana G., Aroca R., Bienert G.P., Chaumont F., Ruiz-Lozano J.M. 2014. New insights into the regulation ofaquaporins by the arbuscular mycorrhizal symbiosis in maize plants under drought stress and possible implications for plant performance. Molecular Plant Microbe Interactions, 27(4): 349–363. https://doi.org/10.1094/MPMI-09-13-0268-R
  18. Bárzana G., Carvajal M. 2020. Genetic regulation of water and nutrient transport in water stress tolerance in roots. Journal of Biotechnology, 324: 134–142. https://doi.org/10.1016/j.jbiotec.2020.10.003
  19. Beaudette P.C., Chlup M., Yee J., Emery R. 2007. Relationships of root conductivity and aquaporin gene expression in Pisum sativum: diurnal patterns and the response to HgCl2 and ABA. Journal of Experimental Botany, 58(6): 1291–1300. https://doi.org/10.1093/jxb/erl289
  20. Beitz E., Wu B., Holm L.M., Schultz J.E., Zeuthen T. 2006. Point mutations in the aromatic/arginine region in aquaporin 1 allow passage of urea, glycerol, ammonia, and protons. Proceedings of the National Academy of Sciences of the USA, 103(2): 269–274. https://doi.org/10.1073/pnas.0507225103
  21. Benga G. 2009. Water channel proteins (later called aquaporins) and relatives: past, resent, and future. IUBMB Life, 61(2): 112–133. https://doi.org/10.1002/iub.156
  22. Bliuma D. 2010. Scientific Issue Ternopil Volodymyr Hnatiuk National Pedagogical University Series: Biology, 45(4): 3–8.
  23. Boursiac Y., Chen S., Luu D.T., 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 Physiology, 139(2): 790–805. https://doi.org/10.1104/pp.105.065029
  24. Carbrey J. M., P. Agre, 2009. Discovery of the Aquaporins and Development of the Field. In: Beitz E. (Ed.). Aquaporins (Series Handbook of Experimental Pharmacology, vol. 190). Berlin; Heidelberg: Springer, pp. 3–28. https://doi.org/10.1007/978-3-540-79885-9_1
  25. Chaumont F., Barrieu F., Jung R., Chrispeels M.J. 2000. Plasma membrane intrinsic proteins from maize cluster in two sequence subgroups with differential aquaporin activity. Plant Physiology, 122(4): 1025–1034. https://doi.org/10.1104/pp.122.4.1025
  26. Chaumont F., Tyerman S.D. 2014. Aquaporins: highly regulated channels controlling plant water relations. Plant Physiology, 164(4): 1600–1618. https://doi.org/10.1104/pp.113.233791
  27. Cui X.H., Hao F.S., Chen H., Chen J., Wang X.C. 2008. Expression of the Vicia faba VfPIP1 gene in Arabidopsis thaliana plants improves their drought resistance. Journal of Plant Research, 121(2): 207–214. https://doi.org/10.1007/s10265-007-0130-z
  28. Cuneo I.F., Barrios-Masias F., Knipfer T., Uretsky J., Reyes C., Lenain P., Brodersen C.R., Walker M.A., McElrone A.J. 2020. Differences in grapevine rootstock sensitivity and recovery from drought are linked to fine root cortical lacunae and root tip function. New Phytologist, 229(1): 272–283. https://doi.org/10.1111/nph.16542
  29. Danielson J.A., Johanson U. 2008. Unexpected complexity of the aquaporin gene family in the moss Physcomitrella patens. BMC Plant Biology, 8(1): 45. https://doi.org/10.1186/1471-2229-8-45
  30. Danielson J.A., Johanson U. 2010. Phylogeny of major intrinsic proteins. Advances in Experimental Medicine and Biology, 679: 19–31. https://doi.org/10.1007/978-1-4419-6315-4_2
  31. Demirevska K., Zasheva D., Dimitrov R., Simova-Stoilova L., Stamenova M., Feller U. 2009. Drought stress effects on Rubisco in wheat: changes in the Rubisco large subunit. Acta Physiologiae Plantarum, 31(6): 11–29. https://doi.org/10.1007/s11738-009-0331-2
  32. Deshmukh R.K., Sonah H., Bélanger R.R., 2016. Plant Aquaporins: genome-wide identification, transcriptomics, proteomics, and advanced analytical tools. Frontiers in Plant Science, 7: 18–96. https://doi.org/10.3389/fpls.2016.01896
  33. Ding L., Lu Z., Gao L., Guo S., Shen Q. 2018. Is nitrogen a key determinant of water transport and photosynthesis in higher plants upon drought stress? Frontiers in Plant Science, 9: 1143 https://doi.org/10.3389/fpls.2018.01143
  34. Ehlert C., Maurel C., Tardieu F., Simonneau T. 2009. Aquaporin-mediated reduction in maize root hydraulic conductivity impacts cell turgor and leaf elongation even without changing transpiration. Plant Physiology, 150(2): 1093–1104. https://doi.org/10.1104/pp.108.131458
  35. Fetter K., Van Wilder V., Moshelion M., Chaumont F. 2004. Interactions between plasma membrane aquaporins modulate their water channel activity. Plant Cell, 16(1): 215–228. https://doi.org/10.1105/tpc.017194
  36. Flexas J., Ribas-CarbÓ M., Hanson D.T., Bota J., Otto B., Cifre J., McDowell N., Medrano H., Kaldenhoff R. 2006. Tobacco aquaporin NtAQP1 is involved in mesophyll conductance to CO2 in vivo. Plant Journal, 48(3): 427–439. https://doi.org/10.1111/j.1365-313X.2006.02879.x
  37. Forrest K. L., Bhave M. 2008. The TIP and PIP aquaporins in wheat form a large and diverse family with unique gene structures and functionally important features. Functional and Integrative Genomics, 8(2): 115–133. https://doi.org/10.1007/s10142-007-0065-4
  38. Galmés J., Pou A., Alsina M.M., Tomas M., Medrano H., Flexas J. 2007. Aquaporin expression in response to different water stress intensities and recovery in Richter-110 (Vitis sp.): relationship with ecophysiological status. Planta, 226(3): 671–681. https://doi.org/10.1007/s00425-007-0515-1
  39. Gambetta G.A., Knipfer T., Fricke W., McElrone A.J. 2017.
  40. Aquaporins and root water uptake. In: Chaumont F., Tyerman S. (Eds.), Plant Aquaporins, From Transport to Signaling. Cham: Springer, pp. 133–154. https://doi.org/10.1007/978-3-319-49395-4
  41. 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 Physiology, 51(5): 767–775. https://doi.org/10.1093/pcp/pcq036
  42. Grondin A., Mauleon R., Vadez V., Henry A. 2016. Root aquaporins contribute to whole plant water fluxes under drought stress in rice (Oryza sativa L.). Plant, Cell & Environment, 39(2): 347–365. https://doi.org/10.1111/pce.12616
  43. Hachez C., Zelazny E., Chaumont F. 2006. Modulating the expression of aquaporin genes in planta: a key to understand their physiological functions? Biochimica et Biophysica Acta (BBA) – Biomembranes, 1758(8): 1142–1156. https://doi.org/10.1016/j.bbamem.2006.02.017
  44. 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 Molecular Biology, 68(4–5): 337–353. https://doi.org/10.1007/s11103-008-9373-x
  45. Heinen R.B., Ye Q., Chaumont F. 2009. Role of aquaporins in leaf physiology. Journal of Experimental Botany, 60(11): 2971–2985. https://doi.org/10.1093/jxb/erp171
  46. Horie T., Kaneko T., Sugimoto G., Sasano S., Panda S.K., 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 Physiology, 52(4): 663–675. https://doi.org/10.1093/pcp/pcr027
  47. Hub J.S., Grubmüller H., de Groot B.L. 2009. Dynamics and energetics of permeation through aquaporins. What do we learn from molecular dynamics simulations? In: Beitz E. (Ed.). Aquaporins (Series Handbook of Experimental Pharmacology, vol. 190). Berlin; Heidelberg: Springer, pp. 57–76. https://doi.org/10.1007/978-3-540-79885-9
  48. Ishibashi K. 2006. Aquaporin superfamily with unusual npa boxes: S-aquaporins (superfamily, sip-like and subcellularaquaporins). Cellular and Molecular Biology (Noisy-le-Grand, France), 52(7): 20–27. PMID: 17543217
  49. 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 stresses in Arabidopsis thaliana. Plant Molecular Biology, 54(5): 713–725. https://doi.org/10.1023/B:PLAN.0000040900.61345.a6
  50. Jang J.Y., Lee S.H., Rhee J.Y., Chung G.C., Ahn S.J., Kang H. 2007. Transgenic Arabidopsis and tobacco plants overexpressing an aquaporin respond differently to various abiotic stresses. Plant Molecular Biology, 64: 621–632. https://doi.org/10.1007/s11103-007-9181-8
  51. Jarzyniak K.M., Jasiński M. 2014. Membrane transporters and drought resistance – a complex issue. Frontiers in Plant Science, 5: 1–15. https://doi.org/10.3389/fpls.2014.00687
  52. Johanson U., Karlsson M., Johansson I., Gustavsson S., Sjövall S., Fraysse L., Weig A.R., 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 Physiology, 126(4): 1358–1369. https://doi.org/10.1104/pp.126.4.1358
  53. Khan K., Agarwal P., Shanware A., Sane V.A. 2015. Heterologous expression of two Jatropha aquaporins imparts drought and salt tolerance and improves seed viability in transgenic Arabidopsis thaliana. PLoS ONE, 10(6): e0128866. https://doi.org/10.1371/journal.pone.0128866
  54. Kirscht A., Kaptan S.S., Bienert G.P., Chaumont F., Nissen P., de Groot B.L., Kjellbom P., Gourdon P., Johanson U. 2016. Crystal structure of an ammonia-permeable aquaporin. PLoS Biology, 14(3): e1002411. https://doi.org/10.1371/journal.pbio.1002411
  55. Knipfer T., Besse M., Verdeil J.L., Fricke W. 2011. Aquaporin-facilitated water uptake in barley (Hordeum vulgare L.) roots. Journal of Experimental Botany, 62(12): 4115–4126. https://doi.org/10.1093/jxb/err075
  56. Kong W., Shaozong Y., Yulu W., Mohammed B., Xiaopeng F. 2017. Genome-wide identification and characterization of aquaporin gene family in Beta vulgaris. PeerJ, 5(333): e3747. https://doi.org/10.7717/peerj.3747
  57. Kumar D. 2021. Transcriptional insights into sugarcane aquaporin genes under water deficit conditions. Plant Cell Report: 1–12. https://doi.org/10.21203/rs.3.rs-185344/v1
  58. Li G., Santoni V., Maurel C. 2014. Plant aquaporins: roles in plant physiology. Biochimica et Biophysica Acta, 1840(5): 1574–1582. https://doi.org/10.1016/j.bbagen.2013.11.004
  59. Li D., Wu, Y., Ruan X., Li B., Zhu L., Wang H., Li X. 2009. Expressions of three cotton genes encoding the PIP proteins are regulated in root development and in response to stresses. Plant Cell Reports, 28(2): 291–300. https://doi.org/10.1007/s00299-008-0626-6
  60. Li J., Cai W. 2015. A ginseng PgTIP1 gene whose protein biological activity related to Ser128 residue confers faster growth and enhanced salt stress tolerance in Arabidopsis. Plant Science: an International Journal of Experimental Plant Biology, 234: 74–85. https://doi.org/10.1016/j.plantsci.2015.02.001
  61. Lian H.-L., Yu X., Ye Q., Ding X.-S., Kitagawa Y., Kwak S.-S., Su W.-A., Tang Z.-C. 2004. The role of aquaporin RWC3 in drought avoidance in rice. Plant Cell Physiology, 45(4): 481–489. https://doi.org/10.1093/pcp/pch058
  62. Liu L.H., Ludewig U., Gassert B., Frommer W.B., von Wire´n N. 2003. Urea transport by nitrogen-regulated tonoplast intrinsic proteins in Arabidopsis. Plant Physiology, 133(3): 1220–1228. https://doi.org/10.1104/pp.103.027409
  63. Liu Q., Wang H., Zhang Z., Wu J., Feng Y., Zhu Z. 2009. Divergence in function and expression of the NOD26-like intrinsic proteins in plants. BMC Genomics, 10(1): 313. https://doi.org/10.1186/1471-2164-10-313
  64. Liu Z., Xin M., Qin J., Peng H., Ni Z., Yao Y., Sun Q. 2015. Temporal transcriptome profiling reveals expression partitioning of homeologous genes contributing to heat and drought acclimation in wheat (Triticum aestivum L.). BMC Plant Biology, 15(1): 152. https://doi.org/10.1186/s12870-015-0511-8
  65. Ma J.F., Yamaji N. 2008. Functions and transport of silicon in plants. Cellular and Molecular Life Sciences, 65(19): 3049–3057. https://doi.org/10.1007/s00018-008-7580-x
  66. Maeshima M. 2001. Tonoplast transporters: organization and function. Annual Review of Plant Physiology and Plant Molecular Biology, 52(1): 469–497. https://doi.org/10.1146/annurev.arplant.52.1.469
  67. Mahdieh M., Mostajeran A., Horie T., Katsuhara M. 2008. Drought stress alters water relations and expression of PIPtype aquaporin genes in Nicotiana tabacum plants. Plant Cell Physiology, 49(5): 801–813. https://doi.org/10.1093/pcp/pcn054
  68. Martinez-Ballesta M., Carvajal M. 2014. New challenges in plant aquaporin biotechnology. Plant Science: an International Journal of Experimental Plant Biology, 217–218: 71–77. https://doi.org/10.1016/j.plantsci.2013.12.006
  69. Martins C.D.P.S., Pedrosa A.M., Du D., Gonçalves L.P., Yu Q., Gmitter F.G., Costa M.G.C. 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): e0138786. https://doi.org/10.1371/journal.pone.0138786
  70. Martre P., Morillon R., Barrieu F., North G.B., Nobel P.S., Chrispeels M.J. 2002. Plasma membrane aquaporins play a significant role during recovery from water deficit. Plant Physiology, 130: 2101–2110. https://doi.org/10.1104/pp.009019
  71. Maurel C., Verdoucq L., Luu D.-T., Santoni V. 2008. Plant aquaporins: membrane channels with multiple integrated functions. Annual Review of Plant Biology, 59: 595–624. https://doi.org/10.1146/annurev.arplant.59.032607.092734
  72. Maurel C., Boursiac Y., Luu D.T., Santoni V., Shahzad Z., Verdoucq L. 2015. Aquaporins in plants. Physiological Reviews, 95(4): 1321–1358. https://doi.org/10.1152/physrev.00008.2015
  73. Mitani-Ueno N., Yamaji N., Zhao F.J., Ma J.F. 2011. The aromatic/arginine selectivity filter of NIP aquaporins plays a critical role in substrate selectivity for silicon, boron, and arsenic. Journal of Experimental Botany, 62(12): 4391–4398. https://doi.org/10.1093/jxb/err158
  74. Molina C., Rotter B.R., Horres R., Udupa S.M., Besser B., Bellarmino L., Baum M., Matsumura H., Terauchi R., Kahl G., Winter P. 2008. SuperSAGE: the drought stressresponsive transcriptome of chickpea roots. BMC Genomics, 9: 553. https://doi.org/10.1186/1471-2164-9-553
  75. Morgun V.V., Kiriziy D.A., Shadchina T.M. 2010. Physiology and biochemistry of cultivated plants, 42(1): 3–22. Available at: http://dspace.nbuv.gov.ua/handle/123456789/66260
  76. Morillon R., Maarten J., Chrispeels D. 2001.The role of ABA and the transpiration stream in the regulation of the osmotic water permeability of leaf cells. Proceedings of the National Academy of Sciences of the USA, 98(24): 14138–14143. https://doi.org/10.1073/pnas.231471998
  77. Muto Y., Segami S., Hayashi H., Sakurai J., Murai-Hatano M., Hattori Y., Ashikari M., Maeshima M. 2011.Vacuolar proton pumps and aquaporins involved in rapid internode elongation of deep water rice. Bioscience, Biotechnology, and Biochemistry, 75(1): 114–122. https://doi.org/10.1271/bbb.100615
  78. Obroucheva N.V., Sinkevich I.A. 2010. Russian Journal of Plant Physiology, 57(2): 153–165. https://doi.org/10.1134/S1021443710020019
  79. Ovrutska I.I., Kordyum E.L. 2019. PIP 2; 1 aquaporin gene expression in maize hybrids different for drought tolerance to water deficit. Reports of the National Academy of Sciences of Ukraine, 5: 97–101. http://dspace.nbuv.gov.ua/handle/123456789/158112
  80. Park W., Scheffler B.E., Bauer P.J., Campbell B.T. 2010. Identification of the family of aquaporin genes and their expression in upland cotton (Gossypium hirsutum L.). BMC Plant Biology, 10: 142. https://doi.org/10.1186/1471-2229-10-142
  81. 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): 729–740. https://doi.org/10.1007/s00425-007-0520-4
  82. Perrone I., Gambino G., Chitarra W., Vitali M., Pagliarani C., Riccomagno N., Balestrini R., Kaldenhoff R., Uehlein N., Gribaudo I., Schubert A., Lovisolo C. 2012. The grapevine root-specific aquaporin VvPIP 2; 4 N controls root hydraulic conductance and leaf gas exchange under well-watered conditions but not under water stress. Plant Physiology, 160(2): 965–977. https://doi.org/10.1104/pp.112.203455
  83. Preston G.M., Carroll T.P., Guggino W.B., Agre P. 1992. Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science, 256: 385–387. https://doi.org/10.1126/science.256.5055.385
  84. Pou A., Hipolito M., Jaume F., Stephen D.T. 2013. A putative role for TIP and PIP aquaporins in dynamics of leaf hydraulic and stomatal conductances in grapevine under water stress and rewatering. Plant, Cell and Environment, 36(4): 828–843. https://doi.org/10.1111/pce.12019
  85. Prado K., Maurel C. 2013. Regulation of leaf hydraulics: from molecular to whole plant levels. Frontiers in Plant Science, 4: 255. https://doi.org/10.3389/fpls.2013.00255
  86. Reddy K.S., Sekhar K.M., Reddy A.R. 2017. Genotypic variation in tolerance to drought stress is highly coordinated with hydraulic conductivity–photosynthesis interplay and aquaporin expression in field-grown mulberry (Morus spp.). Tree Physiology, 37(7): 926–937. https://doi.org/10.1093/treephys/tpx051
  87. Regon P., Panda P., Kshetrimayum E., Panda S.K. 2014. Genome-wide comparative analysis of tonoplast intrinsic protein (TIP) genes in plants. Functional & Integrative Genomics, 14(4): 617–629. https://doi.org/10.1007/s10142-014-0389-9
  88. Rizhsky L., Liang H., Shuman J., Shulaev V., Davletova S., Mittler R. 2004. When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiology,134(4): 1683–1696. https://doi.org/10.1104/pp.103.033431
  89. Rodrigues M.I., Bravo J.P., Sassaki F.T., Severino F.E., Maia I.G. 2013. The tonoplast intrinsic aquaporin (TIP) subfamily of Eucalyptus grandis: characterization of EgTIP2, a root-specific and osmotic stress-responsive gene. Plant Science, 213: 106–113. https://doi.org/10.1016/j.plantsci.2013.09.005
  90. Ruiz-Lozano J.M., del Mar Alguacil M., B´árzana G., Vernieri P., Aroca R. 2009. Exogenous ABA accentuates the differences in root hydraulic properties between mycorrhizal and non mycorrhizal maize plants through regulation of PIP aquaporins. Plant Molecular Biology, 70(5): 565–579. https://doi.org/10.1007/s11103-009-9492-z
  91. Sade N., Vinocur B.J., Diber A., Shatil A., Ronen G., Nissan H., Wallach R., Karchi H., Moshelion M. 2009. Improving plant stress tolerance and yield production: is the tonoplast aquaporin SlTIP2; 2 a key to isohydric to anisohydric conversion? The New Phytologist, 181(3): 651–661. https://doi.org/10.1111/j.1469-8137.2008.02689.x
  92. Sahitya U. L., Krishna M. S. R., Suneetha P. 2019. Integrated approaches to study the drought tolerance mechanism in hot pepper (Capsicum annuum L.). Physiology and Molecular Biology of Plants, 25(3): 637–647. https://doi.org/10.1007/s12298-019-00655-7
  93. Santos A.B., Mazzafera P. 2013. Aquaporins and the control of the water status in coffee plants. Theoretical and Experimental Plant Physiology, 25(2): 79–93. https://doi.org/10.1590/S2197-00252013000200001
  94. Secchi F., Pagliarani C., Zwieniecki M.A. 2017. The functional role of xylem parenchyma cells and aquaporins during recovery from severe water stress. Plant, Cell and Environment, 40(6): 858–871. https://doi.org/10.1111/pce.12831
  95. Shekoofa A., Sinclair T.R. 2018. Aquaporin activity to improve crop drought tolerance. Cells, 7(9): 123. https://doi.org/10.3390/cells7090123
  96. Siefritz F., Biela A., Eckert M., Otto B., Uehlein N., Kaldenhoff R. 2001. The tobacco plasma membrane aquaporin NtAQP1. Journal of Experimental Botany, 52(363): 1953–1957. https://doi.org/10.1093/jexbot/52.363.1953
  97. Siefritz F., Tyree M.T., Lovisolo C., Schubert A., Kaldenhoff R. 2002. PIP1 plasma membrane aquaporins in tobacco: from cellular effects to function in plants. Plant Cell, 14(4): 869–876. https://doi.org/10.1105/tpc.000901
  98. Siemens J., Zwiazek J. 2004. Changes in root water flow properties of solution culture grown trembling aspen (Populus tremuloides) seedlings under different intensities of water-deficit stress. Physiologia Plantarum, 121(1): 44–49. https://doi.org/10.1111/j.0031-9317.2004.00291.x
  99. Silva M.D., Silva R.L.O., Ferreira-Neto J.R.C., Guimarães A.C.R., Veiga D.T., Chabregas S.M., Burnquist W.L., Kahl G., Benko-Iseppon A.M., Kido E.A. 2013. Expression analysis of sugarcane aquaporin genes under water deficit. Journal of Nucleic Acids, 2013: 1–14. https://doi.org/10.1155/2013/763945
  100. Sreedharan S., Shekhawat U.K.S., Ganapathi T.R. 2013. Transgenic banana plants overexpressing a native plasma membrane aquaporin MusaPIP1; 2 display high tolerance levels to different abiotic stresses. Plant Biotechnology Journal, 11(8): 942–952. https://doi.org/10.1111/pbi.12086
  101. Sutka M. R., Manzur M.E., Vitali V.A., Micheletto S., Amodeo G. 2016. Evidence for the involvement of hydraulic root or shoot adjustments as mechanisms underlying water deficit tolerance in two Sorghum bicolor genotypes. Journal of Plant Physiology, 192: 13–20. https://doi.org/10.1016/j.jplph.2016.01.002
  102. Uehlein N., Sperling H., Heckwolf M., Kaldenhoff R. 2012. The Arabidopsis aquaporin PIP1; 2 rules cellular CO2 uptake. Plant Cell Environment, 35(6): 1077–7083. https://doi.org/10.1111/j.1365-3040.2011.02473.x
  103. Vandeleur R.K., Mayo G., Shelden M.C., Gilliham M., Kaiser B.N., Tyerman S.D. 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 Physiology, 149(1): 445–460. https://doi.org/10.1104/pp.108.128645
  104. Venkatesh J., Yu J-W., Park S.W. 2013. Genome-wide analysis and expression profiling of the Solanum tuberosum aquaporins. Plant Physiology and Biochemistry, 73: 392–404. https://doi.org/10.1016/j.plaphy.2013.10.025
  105. Wang L.L., Chen A.P., Zhong N.Q., Liu N., Wu X.M., Wang F., Yang C.L., Romero M.F., Xia G.X. 2013. The Thellungiella salsuginea tonoplast aquaporin TsTIP1; 2 functions in protection against multiple abiotic stresses. Plant and Cell Physiology, 55(1): 148–161. https://doi.org/10.1093/pcp/pct166
  106. Wang C., Hu H., Qin X., Zeise B., Xu D., Rappel W.J., Boron W.F., Schroeder J.I. 2016. Reconstitution of CO2 regulation of SLAC1 anion channel and function of CO2-permeable PIP 2; 1 aquaporin as CARBONIC ANHYDRASE 4 interactor. Plant Cell, 28(2): 568–582. https://doi.org/10.1105/tpc.15.00637
  107. Xu Y., Hu W., Liu J., Zhang J., Jia C., Miao H., Xu B., Jin Z. 2014. A banana aquaporin gene, MaPIP 1; 1, is involved in tolerance to drought and salt stresses. BMC Plant Biology, 14: 59. https://doi.org/10.1186/1471-2229-14-59
  108. Yu Q.J., Hu Y.L., Li J.F., Wu Q., Lin Z.P. 2005. Sense and antisense expression of plasma membrane aquaporin BnPIP1 from Brassica napus in tobacco and its effect on plant drought resistance. Plant Science, 169(4): 647–656. https://doi.org/10.1016/j.plantsci.2005.04.013
  109. Yu G., Li J., Sun X., Zhang X., Liu J., Pan H. 2015. Overexpression of AcNIP 5; 1, a novel nodulin-like intrinsic protein from halophyte Atriplex canescens, enhances sensitivity to salinity and improves drought tolerance in Arabidopsis. Plant Molecular Biology Reporter, 33(6): 1–12. https://doi.org/10.1007/s11105-015-0881-y
  110. Zhu J.K. 2016. Abiotic stress signalling and responses in plants. Cell, 167(2): 313–324. https://doi.org/10.1016/j.cell.2016.08.029
  111. Zhuang L., Liu M., Yuan X., Yang Z., Huang B., Burgess P., Jespersen D., Keough J. 2015. Physiological effects of aquaporin in regulating drought tolerance through overexpressing of Festuca arundinacea aquaporin gene FaPIP2; 1. Journal of the American Society for Horticultural Science, 140(5): 404–412. https://doi.org/10.21273/JASHS.140.5.404
  112. Zwiazek J.J., Xu H., Tan X., Navarro-Rodenas A., Morte A. 2017. Significance of oxygen transport through aquaporins. Scientific Reports, 7: 40411. https://doi.org/10.1038/srep40411