The role of water-transporting aquaporins of the PIP and TIP subfamilies in plant development and adaptation to stress factors

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

The comparative analyses of current knowledge of the diversity of aquaporins in angiosperms are presented in the review. Their structure, coding, and diversity of regulatory pathways are considered. Special attention is paid to aquaporins responsible for water transport. Data on the participation of various aquaporins in plant adaptation to abiotic factors causing hydration and dehydration are presented. The participation of aquaporins in the processes of plant growth and development from germination to seed formation are considered in sufficient detail. The data presented in the review indicate the main directions of further research important for elucidation of the mechanisms involved in regulation of aquaporins, mainly responsive for transmembrane water transport. The special significance of the studies at the omics level — transcriptomic and proteomic is noted. They will allow identifying the specificity of aquaporin isoforms involved in the development of the adaptive response or at different stages of plant development.

About the authors

Georgy V. Danelia

Saint Petersburg State University

Email: georgdanelia@gmail.com
ORCID iD: 0009-0005-9330-4840
Russian Federation, Saint Petersburg

Vladislav V. Emelyanov

Saint Petersburg State University

Email: bootika@mail.ru
ORCID iD: 0000-0003-2323-5235
SPIN-code: 9460-1278

Cand. Sci. (Biology), Associate Professor

Russian Federation, Saint Petersburg

Maria F. Shishova

Saint Petersburg State University

Author for correspondence.
Email: mshishova@mail.ru
ORCID iD: 0000-0003-3657-2986
SPIN-code: 7842-7611

Dr. Sci. (Biology), Professor

Russian Federation, Saint Petersburg

References

  1. Krylov AV, Pohl P, Zeidel ML, Hill WG. Water permeability of asymmetric planar lipid bilayers: leaflets of different composition offer independent and additive resistances to permeation. J Gen Physiol. 2001;118(4):333–340. doi: 10.1085/jgp.118.4.333
  2. Mathai JC, Tristram-Nagle S, Nagle JF, Zeidel ML. Structural determinants of water permeability through the lipid membrane. J Gen Physiol. 2008;131(1):69–76. doi: 10.1085/jgp.200709848
  3. Shinoda W. Permeability across lipid membranes. Biochim Biophys Acta Biomembr. 2016;1858(10):2254–2265. doi: 10.1016/j.bbamem.2016.03.032
  4. Kapilan R, Vaziri M, Zwiazek JJ. Regulation of aquaporins in plants under stress. Biol Res. 2018;51(1):4. doi: 10.1186/s40659-018-0152-0
  5. Inden T, Hoshino A, Otagaki S, et al. Genome-wide analysis of aquaporins in Japanese Morning Glory (Ipomoea nil). Plants. 2023;12(7):1511. doi: 10.3390/plants12071511
  6. Afzal Z, Howton TC, Sun Y, Mukhtar MS. The roles of aquaporins in plant stress responses. J Dev Biol. 2016;4(1):9. doi: 10.3390/jdb4010009
  7. Singh S, Bhatt V, Kumar V, et al. Evolutionary understanding of aquaporin transport system in the basal eudicot model species Aquilegia coerulea. Plants. 2020;9(6):799. doi: 10.3390/plants9060799
  8. Wood TE, Takebayashi N, Barker MS, et al. The frequency of polyploid speciation in vascular plants. PNAS USA. 2009;106(33): 13875–13879. doi: 10.1073/pnas.0811575106
  9. Stuessy T, Weiss-Schneeweiss H. What drives polyploidization in plants? New Phytol. 2019;223(4):1690–1692. doi: 10.1111/nph.15929
  10. Groszmann M, Osborn HL, Evans JR. Carbon dioxide and water transport through plant aquaporins. Plant Cell Environ. 2017;40(6):938–961. doi: 10.1111/pce.12844
  11. Sonah H, Deshmukh RK, Labbé C, Bélanger RR. Analysis of aquaporins in Brassicaceae species reveals high-level of conservation and dynamic role against biotic and abiotic stress in canola. Sci Rep. 2017;7(1):2771. doi: 10.1038/s41598-017-02877-9
  12. Su Y, Liu Z, Sun J, et al. Genome-wide identification of maize aquaporin and functional analysis during seed germination and seedling establishment. Front Plant Sci. 2022;13:831916. doi: 10.3389/fpls.2022.831916
  13. Obroucheva NV, Sin’kevich IA. Aquaporins and cell growth. Russ J Plant Physiol. 2010;57(2):153–165. doi: 10.1134/S1021443710020019
  14. Maurel C, Boursiac Y, Luu D-T, et al. Aquaporins in plants. Physiol Rev. 2015;95(4):1321–1358. doi: 10.1152/physrev.00008.2015
  15. Chaumont F, Tyerman SD, editors. Plant aquaporins: From transport to signaling. New York: Springer; 2017. 353 p. doi: 10.1007/978-3-319-49395-4
  16. Wang Y, Zhao Z, Liu F, et al. Versatile roles of aquaporins in plant growth and development. Int J Mol Sci. 2020;21(24):9485. doi: 10.3390/ijms21249485
  17. Koefoed-Johnsen V, Ussing HH. The contributions of diffusion and flow to the passage of D2O through living membranes: Effect of neurohypophyseal hormone on isolated anuran skin. Acta Physiol Scand. 1953;28(1):60–76. doi: 10.1111/j.1748-1716.1953.tb00959.x
  18. Macey RL, Farmer REL. Inhibition of water and solute permeability in human red cells. Biochim Biophys Acta Biomembr. 1970;211(1):104–106. doi: 10.1016/0005-2736(70)90130-6
  19. Denker BM, Smith BL, Kuhajda FP, Agre P. Identification, purification, and partial characterization of a novel Mr 28,000 integral membrane protein from erythrocytes and renal tubules. J Biol Chem. 1988;263(30):15634–15642. doi: 10.1016/s0021-9258(19)37635-5
  20. Preston GM, Carroll TP, Guggino WB, Agre P. Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science. 1992;256(5055):385–387. doi: 10.1126/science.256.5055.385
  21. Fushimi K, Uchida S, Harat Y, et al. Cloning and expression of apical membrane water channel of rat kidney collecting tubule. Nature. 1993;361(6412):549–552. doi: 10.1038/361549a0
  22. Fortin MG, Morrison NA, Verma DPS. Nodulin-26, a peribacteroid membrane nodulin is expressed independently of the development of the peribacteroid compartment. Nucleic Acids Res. 1987;15(2): 813–824. doi: 10.1093/nar/15.2.813
  23. Hussain A, Tanveer R, Mustafa G, et al. Comparative phylogenetic analysis of aquaporins provides insight into the gene family expansion and evolution in plants and their role in drought tolerant and susceptible chickpea cultivars. Genomics. 2020;112(1):263–275. doi: 10.1016/j.ygeno.2019.02.005
  24. Rabeh K, Sallami A, Gaboun F, et al. Genome-wide analysis of aquaporin and their responses to abiotic stresses in plants: A systematic review and meta-analysis. Plant Stress. 2024;11:100362. doi: 10.1016/j.stress.2024.100362
  25. Lopez-Zaplana A, Nicolas-Espinosa J, Carvajal M, Bárzana G. Genome-wide analysis of the aquaporin genes in melon (Cucumis melo L.) Sci Rep. 2020;10(1):22240. doi: 10.1038/s41598-020-79250-w
  26. Møller IM, Rao RSP, Jiang Y, et al. Proteomic and bioinformatic profiling of transporters in higher plant mitochondria. Biomolecules. 2020;10(8):1190. doi: 10.3390/biom10081190
  27. Kudoyarova G, Veselov D, Yemelyanov V, Shishova M. The role of aquaporins in plant growth under conditions of oxygen deficiency. Int J Mol Sci. 2022;23(17):10159. doi: 10.3390/ijms231710159
  28. Lopez-Zaplana A, Bárzana G, Ding L, et al. Aquaporins involvement in the regulation of melon (Cucumis melo L.) fruit cracking under different nutrient (Ca, B and Zn) treatments. Environ Exp Bot. 2022;201:104981. doi: 10.1016/j.envexpbot.2022.104981
  29. Ishikawa F, Suga S, Uemura T, et al. Novel type aquaporin SIPs are mainly localized to the ER membrane and show cell-specific expression in Arabidopsis thaliana. FEBS Lett. 2005;579(25): 5814–5820. doi: 10.1016/j.febslet.2005.09.076
  30. Lopez D, Bronner G, Brunel N, et al. Insights into Populus XIP aquaporins: evolutionary expansion, protein functionality, and environmental regulation. J Exp Bot. 2012;63(5):2217–2230. doi: 10.1093/jxb/err404
  31. Luang S, Hrmova M. Structural basis of the permeation function of plant aquaporins. In: Chaumont F, Tyerman SD, editors. Plant aquaporins: From transport to signaling. New York: Springer; 2017. P. 1–28. doi: 10.1007/978-3-319-49395-4_1
  32. Noronha H, Agasse A, Martins AP, et al. The grape aquaporin VvSIP1 transports water across the ER membrane. J Exp Bot. 2014;65(4):981–993. doi: 10.1093/jxb/ert448
  33. Shivaraj SM, Deshmukh R, Sonah H, Bélanger RR. Identification and characterization of aquaporin genes in Arachis duranensis and Arachis ipaensis genomes, the diploid progenitors of peanut. BMC Genom. 2019;20:222. doi: 10.1186/s12864-019-5606-4
  34. Quigley F, Rosenberg JM, Shachar-Hill Y, Bohnert HJ. From genome to function: the Arabidopsis aquaporins. Genome Biol. 2001;3(1):research0001.1. doi: 10.1186/gb-2001-3-1-research0001
  35. Nicolas-Espinosa J, Carvajal M. Genome-wide identification and biological relevance of broccoli aquaporins. Plant Genome. 2022;15(4):e20262. doi: 10.1002/tpg2.20262
  36. Park W, Scheffler BE, Bauer PJ, Campbell BT. Identification of the family of aquaporin genes and their expression in upland cotton (Gossypium hirsutum L.). BMC Plant Biol. 2010;10:142. doi: 10.1186/1471-2229-10-142
  37. Gupta AB, Sankararamakrishnan R. 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. 2009;9:134. doi: 10.1186/1471-2229-9-134
  38. Zhang DY, Ali Z, Wang CB, et al. Genome-wide sequence characterization and expression analysis of major intrinsic proteins in soybean (Glycine max L.). PLoS One. 2013;8(2):e56312. doi: 10.1371/journal.pone.0056312
  39. Rajora N, Thakral V, Geetika, et al. Understanding aquaporins regulation and silicon uptake in carrot (Daucus carota). J Plant Biochem Biotechnol. 2023;32(1):51–62. doi: 10.1007/s13562-022-00780-7
  40. Sakurai J, Ishikawa F, Yamaguchi T, et al. Identification of 33 rice aquaporin genes and analysis of their expression and function. Plant Cell Physiol. 2005;46(9):1568–1577. doi: 10.1093/pcp/pci172
  41. Hove RM, Ziemann M, Bhave M. Identification and expression analysis of the barley (Hordeum vulgare L.) aquaporin gene family. PLoS One. 2015;10(6): e0128025. doi: 10.1371/journal.pone.0128025
  42. Reddy PS, Bhadra Rao TSR, Sharma KK, Vadez V. Genome-wide identification and characterization of the aquaporin gene family in Sorghum bicolor (L.). Plant Gene. 2015;1:18–28. doi: 10.1016/j.plgene.2014.12.002
  43. Pawłowicz I, Rapacz M, Perlikowski D, et al. Abiotic stresses influence the transcript abundance of PIP and TIP aquaporins in Festuca species. J Appl Genet. 2017;58:421–435. doi: 10.1007/s13353-017-0403-8
  44. Lu Y, Jeffers R, Raju A, et al. Does night-time transpiration provide any benefit to wheat (Triticum aestivum L.) plants which are exposed to salt stress? Physiol Plant. 2023;175(1):e13839. doi: 10.1111/ppl.13839
  45. Jang JY, Kim DG, Kim YO, et al. An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana. Plant Mol Biol. 2004;54(5):713–725. doi: 10.1023/b: plan.0000040900.61345.a6
  46. Lopez-Zaplana A, Martinez-Garcia N, Carvajal M, Bárzana G. Relationships between aquaporins gene expression and nutrient concentrations in melon plants (Cucumis melo L.) during typical abiotic stresses. Environ Exp Bot. 2022;195:104759. doi: 10.1016/j.envexpbot.2021.104759
  47. Solouki A, Berna-Sicilia JÁ, Martinez-Alonso A, et al. Onion plants (Allium cepa L.) react differently to salinity levels according to the regulation of aquaporins. Heliyon. 2023;9(3):e13815. doi: 10.1016/j.heliyon.2023.e13815
  48. Quiroga G, Erice G, Ding L, et al. The arbuscular mycorrhizal symbiosis regulates aquaporins activity and improves root cell water permeability in maize plants subjected to water stress. Plant Cell Environ. 2019;42(7):2274–2290. doi: 10.1111/pce.13551
  49. Nicolas-Espinosa J, Yepes-Molina L, Martinez-Bernal F, et al. Deciphering the effect of salinity and boron stress on broccoli plants reveals that membranes phytosterols and PIP aquaporins facilitate stress adaptation. Plant Sci. 2024;338:111923. doi: 10.1016/j.plantsci.2023.111923
  50. Verdoucq L, Rodrigues O, Martinière A, et al. Plant aquaporins on the move: Reversible phosphorylation, lateral motion and cycling. Curr Opin Plant Biol. 2014;22:101–107. doi: 10.1016/j.pbi.2014.09.011
  51. Li C, Wang W. Molecular biology of aquaporins. In: Yang B, editor. Aquaporins. Advances in experimental medicine and biology. Vol. 969. Dordrecht: Springer; 2017. P. 1–34. doi: 10.1007/978-94-024-1057-0_1
  52. Wu XN, Rodriguez CS, Pertl-Obermeyer H, et al. Sucrose-induced receptor kinase SIRK1 regulates a plasma membrane aquaporin in Arabidopsis. Mol Cell Proteom. 2013;12(10):2856–2873. doi: 10.1074/mcp.M113.029579
  53. Bellati J, Champeyroux C, Hem S, et al. Novel aquaporin regulatory mechanisms revealed by interactomics. Mol Cell Proteom. 2016;15(11):3473–3487. doi: 10.1074/mcp.M116.060087
  54. Fushimi K, Sasaki S, Marumo F. Phosphorylation of serine 256 is required for cAMP-dependent regulatory exocytosis of the aquaporin-2 water channel. J Biol Chem. 1997;272(23):14800–14804. doi: 10.1074/jbc.272.23.14800
  55. Javot H, Maurel C. The role of aquaporins in water uptake. Ann Bot. 2002;90(3):301–313. doi: 10.1093/aob/mcf199
  56. Przedpelska-Wasowicz EM, Wierzbicka M. Gating of aquaporins by heavy metals in Allium cepa L. epidermal cells. Protoplasma. 2011;248(4):663–671. doi: 10.1007/s00709-010-0222-9
  57. Henzler T, Ye Q, Steudle E. Oxidative of water channels (aquaporins) in Chara by hydroxyl radicals. Plant Cell Environ. 2004;27(9):1184–1195. doi: 10.1111/j.1365-3040.2004.01226.x
  58. Aroca R. Exogenous catalase and ascorbate modify the effects of abscisic acid (ABA) on root hydraulic properties in Phaseolus vulgaris L. plants. J Plant Growth Regul. 2006;25(1):10–17. doi: 10.1007/s00344-005-0075-1
  59. Luu D-T, Maurel C. Aquaporin trafficking in plant cells: an emerging membrane-protein model. Traffic. 2013;14(6):629–635. doi: 10.1111/tra.12062
  60. Sun Q, Liu X, Kitagawa Y, et al. Plant aquaporins: Their roles beyond water transport. Crop J. 2024;12(3):641–655. doi: 10.1016/j.cj.2024.04.005
  61. Yepes-Molina L, Bárzana G, Carvajal M. Controversial regulation of gene expression and protein transduction of aquaporins under drought and salinity stress. Plants. 2020;9(12):1662. doi: 10.3390/plants9121662
  62. Jackson MB, Davies WJ, Else M. Pressure-flow relationships, xylem solutes and root hydraulic conductance in flooded tomato plants. Ann Bot. 1996;77(1):17–24. doi: 10.1006/anbo.1996.0003
  63. Törnroth-Horsefield S, Wang Y, Hedfalk K, et al. Structural mechanism of plant aquaporin gating. Nature. 2006;439(7077): 688–694. doi: 10.1038/nature04316
  64. Gitto A, Fricke W. Zinc treatment of hydroponically-grown barley (H. vulgare) plants causes a reduction in root and cell hydraulic conductivity and isoform-dependent decrease in aquaporin gene expression. Physiol Plant. 2018;164(2):176–190. doi: 10.1111/ppl.12697
  65. Burke S, Sadaune E, Rognon L, et al. A redundant hydraulic function of root hairs in barley plants grown in hydroponics. Funct Plant Biol. 2020;48(4):448–459. doi: 10.1071/fp20287
  66. Matsuo N, Nanjo Y, Tougou M, et al. Identification of putative aquaporin genes and their expression analysis under hypoxic conditions in soybean [Glycine max (L.) Merr.]. Plant Prod Sci. 2012;15(4):278–283. doi: 10.1626/pps.15.278
  67. Shivaraj SM, Deshmukh R, Bhat JA, et al. Understanding aquaporin transport system in eelgrass (Zostera marina L.), an aquatic plant species. Front Plant Sci. 2017;8:1334. doi: 10.3389/fpls.2017.01334
  68. Yanada K-i, Kondo K, Ino N, et al. Plasma membrane aquaporins function in moisture regulation during seed germination and leaf hydration in eelgrass. Aquat Bot. 2024;192:103760. doi: 10.1016/j.aquabot.2024.103760
  69. Cozza R, Pangaro T. Tissue expression pattern of two aquaporin-encoding genes in different organs of the seagrass Posidonia oceanica. Aquat Bot. 2009;91(2):117–121. doi: 10.1016/j.aquabot.2009.03.007
  70. Serra IA, Nicastro S, Mazzuca S, et al. Response to salt stress in seagrasses: PIP1;1 aquaporin antibody localization in Posidonia oceanica leaves. Aquat Bot. 2013;104:213–219. doi: 10.1016/j.aquabot.2011.05.008
  71. Hoai PTT, Tyerman SD, Schnell N, et al. Deciphering aquaporin regulation and roles in seed biology. J Exp Bot. 2020;71(6): 1763–1773. doi: 10.1093/jxb/erz555
  72. Obroucheva NV, Sinkevich IA, Lityagina SV, Novikova GV. Water relations in germinating seeds. Russ J Plant Physiol. 2017;64(4): 625–633. doi: 10.1134/s102144371703013x
  73. Nonogaki H. Seed germination and dormancy: The classic story, new puzzles, and evolution. J Integr Plant Biol. 2019;61(5):541–563. doi: 10.1111/jipb.12762
  74. Liu H-Y, Yu X, Cui D-Y, et al. The role of water channel proteins and nitric oxide signaling in rice seed germination. Cell Res. 2007;17(7):638–649. doi: 10.1038/cr.2007.34
  75. Footitt S, Clewes R, Feeney M, et al. Aquaporins influence seed dormancy and germination in response to stress. Plant Cell Environ. 2019;42(8):2325–2339. doi: 10.1111/pce.13561
  76. Novikova GV, Tournaire-Roux C, Sin’kevich IA, et al. Vacuolar biogenesis and aquaporin expression at early germination of broad bean seeds. Plant Physiol Biochem. 2014;82:123–132. doi: 10.1016/j.plaphy.2014.05.014
  77. Hachez C, Moshelion M, Zelazny E, et al. Localization and quantification of plasma membrane aquaporin expression in maize primary root: a clue to understanding their role as cellular plumbers. Plant Mol Biol. 2006;62(1–2):305–323. doi: 10.1007/s11103-006-9022-1
  78. Sakurai J, Ahamed A, Murai M, et al. Tissue and cell-specific localization of rice aquaporins and their water transport activities. Plant Cell Physiol. 2008;49(1):30–39. doi: 10.1093/pcp/pcm162
  79. Gambetta GA, Fei J, Rost TL, et al. Water uptake along the length of grapevine fine roots: Developmental anatomy, tissue-specific aquaporin expression, and pathways of water transport. Plant Physiol. 2013;163(3):1254–1265. doi: 10.1104/pp.113.221283
  80. Suga S, Murai M, Kuwagata T, Maeshima M. Differences in aquaporin levels among cell types of radish and measurement of osmotic water permeability of individual protoplasts. Plant Cell Physiol. 2003;44(3):277–286. doi: 10.1093/pcp/pcg032
  81. Knipfer T, Besse M, Verdeil J-L, Fricke W. Aquaporin-facilitated water uptake in barley (Hordeum vulgare L.) roots. J Exp Bot. 2011;62(12):4115–4126. doi: 10.1093/jxb/err075
  82. Javot H, Lauvergeat V, Santoni V, et al. Role of a single aquaporin isoform in root water uptake. Plant Cell. 2003;15(2):509–522. doi: 10.1105/tpc.008888
  83. Hejnowicz Z, Sievers A. Reversible closure of water channels in parenchymatic cells of sunflower hypocotyl depends on turgor status of the cells. J Plant Physiol. 1996;147(5):516–520. doi: 10.1016/s0176-1617(96)80040-x
  84. Suga S, Imagawa S, Maeshima M. Specificity of the accumulation of mRNAs and proteins of the plasma membrane and tonoplast aquaporins in radish organs. Planta. 2001;212(2):294–304. doi: 10.1007/s004250000396
  85. Suga S, Komatsu S, Maeshima M. Aquaporin isoforms responsive to salt and water stresses and phytohormones in radish seedlings. Plant Cell Physiol. 2002;43(10):1229–1237. doi: 10.1093/pcp/pcf148
  86. Ludevid D, Höfte H, Himelblau E, Chrispeels MJ. The expression pattern of the tonoplast intrinsic protein γ-TIP in Arabidopsis thaliana is correlated with cell enlargement. Plant Physiol. 1992;100(4):1633–1639. doi: 10.1104/pp.100.4.1633
  87. Daniels MJ, Chaumont F, Mirkov TE, Chrispeels MJ. Characterization of a new vacuolar membrane aquaporin sensitive to mercury at a unique site. Plant Cell. 1996;8(4):587–599. doi: 10.2307/3870337
  88. Eisenbarth DA, Weig AR. Dynamics of aquaporins and water relations during hypocotyl elongation in Ricinus communis L. seedlings. J Exp Bot. 2005;56(417):1831–1842. doi: 10.1093/jxb/eri173
  89. Schuurmans JAMJ, van Dongen JT, Rutjens BPW, et al. Members of the aquaporin family in the developing pea seed coat include representatives of the PIP, TIP, and NIP subfamilies. Plant Mol Biol. 2003;53(5):655–667. doi: 10.1023/b: plan.0000019070.60954.77
  90. McGaughey SA, Osborn HL, Chen L, et al. Roles of aquaporins in Setaria viridis stem development and sugar storage. Front Plant Sci. 2016;7:1815. doi: 10.3389/fpls.2016.01815
  91. Muto Y, Segami S, Hayashi H, et al. Vacuolar proton pumps and aquaporins involved in rapid internode elongation of deepwater rice. Biosci Biotechnol Biochem. 2011;75(1):114–122. doi: 10.1271/bbb.100615
  92. Shivaraj SM, Deshmukh RK, Rai R, et al. Genome-wide identification, characterization, and expression profile of aquaporin gene family in flax (Linum usitatissimum). Sci Rep. 2017;7(1):46137. doi: 10.1038/srep46137
  93. Besse M, Knipfer T, Miller AJ, et al. Developmental pattern of aquaporin expression in barley (Hordeum vulgare L.) leaves. J Exp Bot. 2011;62(12):4127–4142. doi: 10.1093/jxb/err175
  94. Fricke W, Knipfer T. Plant aquaporins and cell elongation. In: Chaumont F, Tyerman SD, editors. Plant aquaporins: From transport to signaling. New York: Springer; 2017. P. 107–131. doi: 10.1007/978-3-319-49395-4_5
  95. Schünmann PHD, Ougham HJ. Identification of three cDNA clones expressed in the leaf extension zone and with altered patterns of expression in the slender mutant of barley: A tonoplast intrinsic protein, a putative structural protein and protochlorophyllide oxidoreductase. Plant Mol Biol. 1996;31(3):529–537. doi: 10.1007/bf00042226
  96. Wei W, Alexandersson E, Golldack D, et al. HvPIP1;6, a barley (Hordeum vulgare L.) plasma membrane water channel particularly expressed in growing compared with non-growing leaf tissues. Plant Cell Physiol. 2007;48(8):1132–1147. doi: 10.1093/pcp/pcm083
  97. Barrieu F, Chaumont F, Chrispeels MJ. High expression of the tonoplast aquaporin ZmTIP1 in epidermal and conducting tissues of maize. Plant Physiol. 1998;117(4):1153–1163. doi: 10.1104/pp.117.4.1153
  98. Frangne N, Maeshima M, Schäffner AR, et al. Expression and distribution of a vacuolar aquaporin in young and mature leaf tissues of Brassica napus in relation to water fluxes. Planta. 2001;212(2):270–278. doi: 10.1007/s004250000390
  99. Yooyongwech S, Horigane AK, Yoshida M, et al. Changes in aquaporin gene expression and magnetic resonance imaging of water status in peach tree flower buds during dormancy. Physiol Plant. 2008;134(3):522–533. doi: 10.1111/j.1399-3054.2008.01143.x
  100. Azad AK, Sawa Y, Ishikawa T, Shibata H. Characterization of protein phosphatase 2A acting on phosphorylated plasma membrane aquaporin of tulip petals. Biosci Biotechnol Biochem. 2004;68(5):1170–1174. doi: 10.1271/bbb.68.1170
  101. Nemoto K, Niinae T, Goto F, et al. Calcium-dependent protein kinase 16 phosphorylates and activates the aquaporin PIP2;2 to regulate reversible flower opening in Gentiana scabra. Plant Cell. 2022;34(7):2652–2670. doi: 10.1093/plcell/koac120
  102. Bots M, Feron R, Uehlein N, et al. PIP1 and PIP2 aquaporins are differentially expressed during tobacco anther and stigma development. J Exp Bot. 2005;56(409):113–121. doi: 10.1093/jxb/eri009
  103. Soto G, Fox R, Ayub N, et al. TIP5;1 is an aquaporin specifically targeted to pollen mitochondria and is probably involved in nitrogen remobilization in Arabidopsis thaliana. Plant J. 2010;64(6): 1038–1047. doi: 10.1111/j.1365-313x.2010.04395.x
  104. Wudick MM, Luu D-T, Tournaire-Roux C, et al. Vegetative and sperm cell-specific aquaporins of Arabidopsis highlight the vacuolar equipment of pollen and contribute to plant reproduction. Plant Physiol. 2014;164(4):1697–1706. doi: 10.1104/pp.113.228700
  105. Zhou Y, Setz N, Niemietz C, et al. Aquaporins and unloading of phloem-imported water in coats of developing bean seeds. Plant Cell Environ. 2007;30(12):1566–1577. doi: 10.1111/j.1365-3040.2007.01732.x
  106. Ozga JA, van Huizen R, Reinecke DM. Hormone and seed-specific regulation of pea fruit growth. Plant Physiol. 2002;128(4): 1379–1389. doi: 10.1104/pp.010800
  107. Schlosser J, Olsson N, Weis M, et al. Cellular expansion and gene expression in the developing grape (Vitis vinifera L.). Protoplasma. 2008;232(3–4):255–265. doi: 10.1007/s00709-008-0280-9
  108. Fouquet R, Léon C, Ollat N, Barrieu F. Identification of grapevine aquaporins and expression analysis in developing berries. Plant Cell Rep. 2008;27(9):1541–1550. doi: 10.1007/s00299-008-0566-1
  109. Shiota H, Sudoh T, Tanaka I. Expression analysis of genes encoding plasma membrane aquaporins during seed and fruit development in tomato. Plant Sci. 2006;171(2):277–285. doi: 10.1016/j.plantsci.2006.03.021
  110. O’Brien M, Bertrand C, Matton DP. Characterization of a fertilization-induced and developmentally regulated plasma-membrane aquaporin expressed in reproductive tissues, in the wild potato Solanum chacoense Bitt. Planta. 2002;215(3):485–493. doi: 10.1007/s00425-002-0770-0
  111. Smart LB, Vojdani F, Maeshima M, Wilkins TA. Genes involved in osmoregulation during turgor-driven cell expansion of developing cotton fibers are differentially regulated. Plant Physiol. 1998;116(4):1539–1549. doi: 10.1104/pp.116.4.1539
  112. Hu C-G, Hao H-J, Honda C, et al. Putative PIP1 genes isolated from apple: Expression analyses during fruit development and under osmotic stress. J Exp Bot. 2003;54(390):2193–2194. doi: 10.1093/jxb/erg238
  113. Lv J, CaoY, Tai R, et al. Comparative study of expression patterns of aquaporin (AQP) genes in apple fruits with contrasting ripening behavior. Sci Hortic. 2023;318:112133. doi: 10.1016/j.scienta.2023.112133
  114. Zhu Y-X, Yang L, Liu N, et al. Genome-wide identification, structure characterization, and expression pattern profiling of aquaporin gene family in cucumber. BMC Plant Biol. 2019;19:345. doi: 10.1186/s12870-019-1953-1
  115. Chinnasamy GP, Sundareswaran S, Subramanian KS, et al. Aquaporins and their implications on seeds: A brief review. J Appl Nat Sci. 2021;13(3):970–980. doi: 10.31018/jans.v13i3.2830
  116. Maurel C, Kado RT, Guern J, Chrispeels MJ. Phosphorylation regulates the water channel activity of the seed-specific aquaporin α-TIP. EMBO J. 1995;14(13):3028–3035. doi: 10.1002/j.1460-2075.1995.tb07305.x
  117. Hunter PR, Craddock CP, Di Benedetto S, et al. Fluorescent reporter proteins for the tonoplast and the vacuolar lumen identify a single vacuolar compartment in Arabidopsis cells. Plant Physiol. 2007;145(4):1371–1382. doi: 10.1104/pp.107.103945
  118. Gattolin S, Sorieul M, Frigerio L. Mapping of tonoplast intrinsic proteins in maturing and germinating Arabidopsis seeds reveals dual localization of embryonic TIPs to the tonoplast and plasma membrane. Mol Plant. 2011;4(1):180–189. doi: 10.1093/mp/ssq051
  119. Kirpichnikova А, Chen Т, Teplyakova S, Shishova M. Proton pump and plant cell elongation. Biol Commun. 2018;63(1):32–42. doi: 10.21638/spbu03.2018.105
  120. Kirpichnikova AA, Kudoyarova GR, Yemelyanov VV, Shishova MF. The peculiarities of cell elongation growth of cereal coleoptiles under normal and flooding conditions. Ecological genetics. 2023;21(4):401–417. EDN: QWDPWQ doi: 10.17816/ecogen623901

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Fig. 1. Cellular localization of aquaporins. PIP, TIP, NIP, and XIP aquaporins are localized primarily in the plasma membrane and are present on the entire cell surface. SIP aquaporins and some NIP aquaporins were found in the endoplasmic reticulum (ЭПС) membrane. TIP aquaporins are localized in the tonoplast, the vacuole membrane. Some PIP and TIP aquaporins were predicted to be localized in the inner chloroplast membrane and the thylakoid membrane. A number of TIP aquaporins were found in mitochondrial (МТХ) membranes

Download (79KB)
Indexing metadata
3. Fig. 2. The structure of plant aquaporin. Transmembrane domains (1–6), loops (A–E), NPA (Asn-Pro-Ala) motifs are located in loops B and E. Posttranslational modification is possible as a result of changes in phosphorylation, depends on pH, Ca2+ ions, and the presence of reactive oxygen species (ROS). Dark ellipse — aromatic/arginine filter — ar/R filter (from [4], with alterations)

Download (55KB)
Indexing metadata

Copyright (c) 2024 Eco-Vector


 


Согласие на обработку персональных данных с помощью сервиса «Яндекс.Метрика»

1. Я (далее – «Пользователь» или «Субъект персональных данных»), осуществляя использование сайта https://journals.rcsi.science/ (далее – «Сайт»), подтверждая свою полную дееспособность даю согласие на обработку персональных данных с использованием средств автоматизации Оператору - федеральному государственному бюджетному учреждению «Российский центр научной информации» (РЦНИ), далее – «Оператор», расположенному по адресу: 119991, г. Москва, Ленинский просп., д.32А, со следующими условиями.

2. Категории обрабатываемых данных: файлы «cookies» (куки-файлы). Файлы «cookie» – это небольшой текстовый файл, который веб-сервер может хранить в браузере Пользователя. Данные файлы веб-сервер загружает на устройство Пользователя при посещении им Сайта. При каждом следующем посещении Пользователем Сайта «cookie» файлы отправляются на Сайт Оператора. Данные файлы позволяют Сайту распознавать устройство Пользователя. Содержимое такого файла может как относиться, так и не относиться к персональным данным, в зависимости от того, содержит ли такой файл персональные данные или содержит обезличенные технические данные.

3. Цель обработки персональных данных: анализ пользовательской активности с помощью сервиса «Яндекс.Метрика».

4. Категории субъектов персональных данных: все Пользователи Сайта, которые дали согласие на обработку файлов «cookie».

5. Способы обработки: сбор, запись, систематизация, накопление, хранение, уточнение (обновление, изменение), извлечение, использование, передача (доступ, предоставление), блокирование, удаление, уничтожение персональных данных.

6. Срок обработки и хранения: до получения от Субъекта персональных данных требования о прекращении обработки/отзыва согласия.

7. Способ отзыва: заявление об отзыве в письменном виде путём его направления на адрес электронной почты Оператора: info@rcsi.science или путем письменного обращения по юридическому адресу: 119991, г. Москва, Ленинский просп., д.32А

8. Субъект персональных данных вправе запретить своему оборудованию прием этих данных или ограничить прием этих данных. При отказе от получения таких данных или при ограничении приема данных некоторые функции Сайта могут работать некорректно. Субъект персональных данных обязуется сам настроить свое оборудование таким способом, чтобы оно обеспечивало адекватный его желаниям режим работы и уровень защиты данных файлов «cookie», Оператор не предоставляет технологических и правовых консультаций на темы подобного характера.

9. Порядок уничтожения персональных данных при достижении цели их обработки или при наступлении иных законных оснований определяется Оператором в соответствии с законодательством Российской Федерации.

10. Я согласен/согласна квалифицировать в качестве своей простой электронной подписи под настоящим Согласием и под Политикой обработки персональных данных выполнение мною следующего действия на сайте: https://journals.rcsi.science/ нажатие мною на интерфейсе с текстом: «Сайт использует сервис «Яндекс.Метрика» (который использует файлы «cookie») на элемент с текстом «Принять и продолжить».