Preview

Vavilov Journal of Genetics and Breeding

Advanced search

Aquaporins and their role in plant-microbial systems

https://doi.org/10.18699/vjgb-25-27

Abstract

Global losses of agricultural products from water scarcity could be greater than from all other causes combined. Water deficiency in plants can result from insufficient precipitation, elevated air temperatures, and other factors that reduce the water available in the soil. Most terrestrial plants are able to form symbiosis with arbuscular mycorrhizal fungi. Arbuscular mycorrhiza plays a key role in the mineral nutrition of many terrestrial plant species. Water transport in plants is regulated primarily by aquaporins, transmembrane proteins. Aquaporins help plants save water, which is an important component of the plant’s adaptation strategy to water scarcity. Some studies suggest that arbuscular mycorrhizal fungi can decrease the expression of aquaporin genes in plants under drought conditions, which reduces water transport within host plant tissues and conserves available water. On the other hand, there is little scientific evidence of the interaction mechanisms between plants and arbuscular mycorrhizal fungi during aquaporin regulation. In addition, the information in different sources on the aquaporin functions in different plant species may be contradictory. Plant aquaporins are represented by several subfamilies; their number varies for different species. A more comprehensive study of these transporters can enhance our understanding of water transport in plants and assess how arbuscular mycorrhizal fungi can influence it. This review contains data on the history of studies of the structure, localization, phylogeny, and functions of aquaporins. Advancing the study of the symbiotic system functioning may contribute to the development of biofertilizers based on soil microorganisms for agricultural uses in the Russian Federation.

About the Authors

T. R. Kudriashova
All-Russia Research Institute for Agricultural Microbiology
Russian Federation

Pushkin, St. Petersburg



A. A. Kryukov
All-Russia Research Institute for Agricultural Microbiology
Russian Federation

Pushkin, St. Petersburg



A. I. Gorenkova
All-Russia Research Institute for Agricultural Microbiology
Russian Federation

Pushkin, St. Petersburg



A. P. Yurkov
All-Russia Research Institute for Agricultural Microbiology
Russian Federation

Pushkin, St. Petersburg



References

1. Abascal F., Irisarri I., Zardoya R. Diversity and evolution of membrane intrinsic proteins. Biochim Biophys Acta. 2014;1840(5):1468-1481. doi 10.1016/j.bbagen.2013.12.001

2. Agre P., Preston G.M., Smith B.L., Jung J.S., Raina S., Moon C., Guggino W.B., Nielsen S. Aquaporin CHIP: the archetypal molecular water channel. Am J Physiol. 1993;265(4):F463-F476. doi 10.1152/ajprenal.1993.265.4.F463

3. Afzal Z., Howton T., Sun Y., Mukhtar M. The roles of aquaporins in plant stress responses. J Dev Biol. 2016;4(1):9. doi 10.3390/jdb4010009

4. Ahanger M.A., Agarwal R.M. Salinity stress induced alterations in antioxidant metabolism and nitrogen assimilation in wheat (Triticum aestivum L.) as influenced by potassium supplementation. Plant Physiol Biochem. 2017;115:449-460. doi 10.1016/j.plaphy.2017.04.017

5. Aroca R., Bago A., Sutka M., Paz J.A., Cano C., Amodeo G., RuizLozano J.M. Expression analysis of the first arbuscular mycorrhizal fungi aquaporin described reveals concerted gene expression between salt-stressed and nonstressed mycelium. Mol Plant Microbe Interact. 2009;22(9):1169-1178. doi 10.1094/MPMI-22-9-1169

6. Asadollahi M., Iranbakhsh A., Ahmadvand R., Ebadi M., Mehregan I. Synergetic effect of water deficit and arbuscular mycorrhizal symbiosis on the expression of aquaporins in wheat (Triticum aestivum L.) roots: insights from NGS RNA-sequencing. Physiol Mol Biol Plants. 2023;29(2):195-208. doi 10.1007/s12298-023-01285-w

7. Byrt C.S., Zhao M., Kourghi M., Bose J., Henderson S.W., Qiu J., Gilliham M., Schultz C., Schwarz M., Ramesh S.A., Yool A., Tyerman S. Non‐selective cation channel activity of aquaporin AtPIP2;1 regulated by Ca2+ and pH. Plant Cell Environ. 2017;40(6):802-815. doi 10.1111/pce.12832

8. Chaumont F., Tyerman S.D. Aquaporins: highly regulated channels controlling plant water relations. Plant Physiol. 2014;164(4):1600- 1618. doi 10.1104/pp.113.233791

9. Chiu C.H., Paszkowski U. Mechanisms and impact of symbiotic phosphate acquisition. Cold Spring Harb Perspect Biol. 2019;11(6): a034603. doi 10.1101/cshperspect.a034603

10. Chrispeels M.J., Agre P. Aquaporins: water channel proteins of plant and animal cells. Trends Biochem Sci. 1994;19(10):421-425. doi 10.1016/0968-0004(94)90091-4

11. Danielson J.Å., Johanson U. Unexpected complexity of the aquaporin gene family in the moss Physcomitrella patens. BMC Plant Biol. 2008;8(1):45. doi 10.1186/1471-2229-8-45

12. Ding M., Li J., Fan X., He F., Yu X., Chen L., Zou S., Liang Y., Yu J. Aquaporin1 regulates development, secondary metabolism and stress responses in Fusarium graminearum. Curr Genet. 2018; 64(5):1057-1069. doi 10.1007/s00294-018-0818-8

13. Evelin H., Devi T.S., Gupta S., Kapoor R. Mitigation of salinity stress in plants by arbuscular mycorrhizal symbiosis: current understanding and new challenges. Front Plant Sci. 2019;10:470. doi 10.3389/fpls.2019.00470

14. Exposito-Rodriguez M., Laissue P.P., Yvon-Durocher G., Smirnoff N., Mullineaux P.M. Photosynthesis-dependent H2O2 transfer from chloroplasts to nuclei provides a high-light signalling mechanism. Nat Commun. 2017;29;8(1):49. doi 10.1038/s41467-017-00074-w

15. Fortin M.G., Morrison N.A., Verma D.P.S. 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

16. Gong M., Bai N., Wang P., Su J., Chang Q., Zhang Q. Co-inoculation with arbuscular mycorrhizal fungi and dark septate endophytes under drought stress: synergistic or competitive effects on maize growth, photosynthesis, root hydraulic properties and aquaporins? Plants. 2023;12(14):2596. doi 10.3390/plants12142596

17. Gupta A., 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(1):134. doi 10.1186/1471-2229-9-134

18. Hiruma K., Gerlach N., Sacristán S., Nakano R.T., Hacquard S., Kracher B., Neumann U., Ramírez D., Bucher M., O’Connell R.J., Schulze-Lefert P. Root endophyte Colletotrichum tofieldiae confers plant fitness benefits that are phosphate status dependent. Cell. 2016;165(2):464-474. doi 10.1016/j.cell.2016.02.028

19. Huey C.J., Gopinath S.C.B., Uda M.N.A., Zulhaimi H.I., Jaafar M.N., Kasim F.H., Yaakub A.R.W. Mycorrhiza: a natural resource assists plant growth under varied soil conditions. 3 Biotech. 2020;10(5): 204. doi 10.1007/s13205-020-02188-3

20. Hussain A., Tanveer R., Mustafa G., Farooq M., Amin I., Mansoor S. 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

21. Irisarri I., Lorente-Martínez H., Strassert J.F.H., Agorreta A., Zardoya R., San Mauro D., De Vries J. Early diversification of membrane intrinsic proteins (MIPs) in eukaryotes. Genome Biol Evol. 2024;16(8):evae164. doi 10.1093/gbe/evae164

22. Ishikawa F., Suga S., Uemura T., Sato M.H., Maeshima M. 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

23. Jia Y., Liu X. Polyploidization and pseudogenization in allotetraploid frog Xenopus laevis promote the evolution of aquaporin family in higher vertebrates. BMC Genomics. 2020;21(1):525. doi 10.1186/s12864-020-06942-y

24. Johnson K.D., Höfte H., Chrispeels M.J. An intrinsic tonoplast protein of protein storage vacuoles in seeds is structurally related to a bacterial solute transporter (GIpF). Plant Cell. 1990;2(6):525-532. doi 10.1105/tpc.2.6.525

25. Kakouridis A., Hagen J.A., Kan M.P., Mambelli S., Feldman L.J., Herman D.J., Weber P.K., Pett‐Ridge J., Firestone M.K. Routes to roots: direct evidence of water transport by arbuscular mycorrhizal fungi to host plants. New Phytol. 2022;236(1):210-221. doi 10.1111/nph.18281

26. Kaldenhoff R., Fischer M. Functional aquaporin diversity in plants. Biochim Biophys Acta. 2006;1758(8):1134-1141. doi 10.1016/j.bbamem.2006.03.012

27. Kapilan R., Vaziri M., Zwiazek J.J. Regulation of aquaporins in plants under stress. Biol Res. 2018;51(1):4. doi 10.1186/s40659-018-0152-0

28. Keller-Pearson M., Bortolazzo A., Willems L., Smith B., Peterson A., Ané J.-M., Silva E.M. A dual transcriptomic approach reveals contrasting patterns of differential gene expression during drought in arbuscular mycorrhizal fungus and carrot. Mol Plant Microbe Interact. 2023;36(12):821-832. doi 10.1094/MPMI-04-23-0038-R

29. Knepper M.A., Nielsen S. Peter Agre, 2003 Nobel Prize winner in chemistry. J Am Soc Nephrol. 2004;15(4):1093-1095. doi 10.1097/01.ASN.0000118814.47663.7D

30. Krajinski F., Biela A., Schubert D., Gianinazzi-Pearson V., Kaldenhoff R., Franken P. Arbuscular mycorrhiza development regulates the mRNA abundance of Mtaqp1 encoding a mercury-insensitive aquaporin of Medicago truncatula. Planta. 2000;211(1):85-90. doi 10.1007/s004250000263

31. Kruse E., Uehlein N., Kaldenhoff R. The aquaporins. Genome Biol. 2006;7(2):206. doi 10.1186/gb-2006-7-2-206

32. Kuila D., Ghosh S. Aspects, problems and utilization of Arbuscular Mycorrhizal (AM) application as bio-fertilizer in sustainable agriculture. Curr Res Microb Sci. 2022;3:100107. doi 10.1016/j.crmicr.2022.100107

33. Lagrée V., Froger A., Deschamps S., Hubert J.-F., Delamarche C., Bonnec G., Thomas D., Gouranton J., Pellerin I. Switch from an aquaporin to a glycerol channel by two amino acids substitution. J Biol Chem. 1999;274(11):6817-6819. doi 10.1074/jbc.274.11.6817

34. Li G., Chen T., Zhang Z., Li B., Tian S. Roles of aquaporins in plantpathogen interaction. Plants. 2020;9(9):1134. doi 10.3390/plants9091134

35. Lopez D., Amira M.B., Brown D., Muries B., Brunel-Michac N., Bourgerie S., Porcheron B., Lemoine R., Chrestin H., Mollison E., Di Cola A., Frigerio L., Julien J.-L., Gousset-Dupont A., Fumanal B., Label P., Pujade-Renaud V., Auguin D., Venisse J.-S. The Hevea brasiliensis XIP aquaporin subfamily: genomic, structural and functional characterizations with relevance to intensive latex harvesting. Plant Mol Biol. 2016;91(4-5):375-396. doi 10.1007/s11103-016-0462-y

36. 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

37. Loque D., Ludewig U., Yuan L., von Wirén N. Tonoplast intrinsic proteins AtTIP2;1 and AtTIP2;3 facilitate NH3 transport into the vacuole. Plant Physiol. 2005;137(2):671-680. doi 10.1104/pp.104.051268

38. Lu L., Dong C., Liu R., Zhou B., Wang C., Shou H. Roles of soybean plasma membrane intrinsic protein GmPIP2;9 in drought tolerance and seed development. Front Plant Sci. 2018;9:530. doi 10.3389/fpls.2018.00530

39. Luo Y., Ma L., Du W., Yan S., Wang Z., Pang Y. Identification and characterization of salt- and drought-responsive AQP family genes in Medicago sativa L. Int J Mol Sci. 2022;23(6):3342. doi 10.3390/ijms23063342

40. Ma J.F., Tamai K., Yamaji N., Mitani N., Konishi S., Katsuhara M., Ishiguro M., Murata Y., Yano M. A silicon transporter in rice. Nature. 2006;440(7084):688-691. doi 10.1038/nature04590

41. Maloy S., Hughes K. (Eds) Brenner’s Encyclopedia of Genetics. London: Elsevier, 2013 Martynenko E., Arkhipova T., Akhiyarova G., Sharipova G., Galin I., Seldimirova O., Ivanov R., Nuzhnaya T., Finkina E., Ovchinnikova T., Kudoyarova G. Effects of a Pseudomonas strain on the lipid transfer proteins, appoplast barriers and activity of aquaporins associated with hydraulic conductance of pea plants. Membranes. 2023; 13(2):208. doi 10.3390/membranes13020208

42. Mashini A.G., Oakley C.A., Grossman A.R., Weis V.M., Davy S.K. Immunolocalization of metabolite transporter proteins in a model cnidarian-dinoflagellate symbiosis. Appl Environ Microbiol. 2022; 88(12):e00412-22. doi 10.1128/aem.00412-22

43. Maurel C., Reizer J., Schroeder J.I., Chrispeels M.J. The vacuolar membrane protein gamma-TIP creates water specific channels in Xenopus oocytes. EMBO J. 1993;12(6):2241-2247. doi 10.1002/j.1460-2075.1993.tb05877.x

44. Maurel C., Boursiac Y., Luu D.-T., Santoni V., Shahzad Z., Verdoucq L. Aquaporins in plants. Physiol Rev. 2015;95(4):1321-1358. doi 10.1152/physrev.00008.2015

45. Min X., Wu H., Zhang Z., Wei X., Jin X., Ndayambaza B., Wang Y., Liu W. Genome-wide identification and characterization of the aquaporin gene family in Medicago truncatula. J Plant Biochem Biotechnol. 2019;28(3):320-335. doi 10.1007/s13562-018-0484-4

46. Mizutani M., Watanabe S., Nakagawa T., Maeshima M. Aquaporin NIP2;1 is mainly localized to the ER membrane and shows rootspecific accumulation in Arabidopsis thaliana. Plant Cell Physiol. 2006;47(10):1420-1426. doi 10.1093/pcp/pcl004

47. Mosse B., Stribley D.P., LeTacon F. Ecology of mycorrhizae and mycorrhizal fungi. In: Alexander M. (Ed.) Advances in Microbial Ecology, vol. 5. Boston, MA: Springer US, 1981;5137-5210. doi 10.1007/978-1-4615-8306-6_4

48. Ni Y., Bao H., Zou R., Wang Y., Xie K., Cheng B., Li X. Aquaporin ZmPIP2;4 promotes tolerance to drought during arbuscular mycorrhizal fungi symbiosis. Plant Soil. 2024. doi 10.1007/s11104-024-06778-5

49. Nielsen S., Frøkiær J., Marples D., Kwon T.-H., Agre P., Knepper M.A. Aquaporins in the kidney: from molecules to medicine. Physiol Rev. 2002;82(1):205-244. doi 10.1152/physrev.00024.2001

50. Noronha H., Araújo D., Conde C., Martins A.P., Soveral G., Chaumont F., Delrot S., Gerós H. The grapevine uncharacterized intrinsic protein 1 (VvXIP1) is regulated by drought stress and transports glycerol, hydrogen peroxide, heavy metals but not water. PLoS One. 2016;11(8):e0160976. doi 10.1371/journal.pone.0160976

51. Park W., Scheffler B.E., Bauer P.J., Campbell B.T. Identification of the family of aquaporin genes and their expression in upland cotton (Gossypium hirsutum L.). BMC Plant Biol.10;142(2010). doi 10.1186/1471-2229-10-142

52. Pommerrenig B., Diehn T.A., Bienert G.P. Metalloido-porins: essentiality of Nodulin 26-like intrinsic proteins in metalloid transport. Plant Sci. 2015;238:212-227. doi 10.1016/j.plantsci.2015.06.002

53. Preston G.M., Carroll T.P., Guggino W.B., 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

54. Quiroga G., Erice G., Aroca R., Chaumont F., Ruiz-Lozano J.M. Enhanced drought stress tolerance by the arbuscular mycorrhizal symbiosis in a drought-sensitive maize cultivar is related to a broader and differential regulation of host plant aquaporins than in a drought-tolerant cultivar. Front Plant Sci. 2017;8:1056. doi 10.3389/fpls.2017.01056

55. Savary S., Willocquet L., Pethybridge S.J., Esker P., McRoberts N., Nelson A. The global burden of pathogens and pests on major food crops. Nat Ecol Evol. 2019;3(3):430-439. doi 10.1038/s41559-018-0793-y

56. Schachtman D.P., Reid R.J., Ayling S.M. Phosphorus uptake by plants: from soil to cell. Plant Physiol. 1998;116(2):447-453. doi 10.1104pp.116.2.447

57. Schuurmans J.A.M.J., Van Dongen J.T., Rutjens B.P.W., Boonman A., Pieterse C.M.J., Borstlap A.C. 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

58. Seka A.M., Zhang J., Prodhan F.A., Ayele G.T., Finsa M.M., Sharma T.P.P., Melesse A.M. Hydrological drought impacts on water storage variations: a focus on the role of vegetation changes in the East Africa region. A systematic review. Environ Sci Pollut Res. 2022;29(53):80237-80256. doi 10.1007/s11356-022-23313-0

59. Singh R.K., Deshmukh R., Muthamilarasan M., Rani R., Prasad M. Versatile roles of aquaporin in physiological processes and stress tolerance in plants. Plant Physiol Biochem. 2020;149:178-189. doi 10.1016/j.plaphy.2020.02.009

60. Spatafora J.W., Chang Y., Benny G.L., Lazarus K., Smith M.E., Berbee M.L., Bonito G., Corradi N., Grigoriev I., Gryganskyi A., James T.Y., O’Donnell K., Roberson R.W., Taylor T.N., Uehling J., Vilgalys R., White M.M., Stajich J.E. A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia. 2016;108(5):1028-1046. doi 10.3852/16-042

61. Tian S., Wang X., Li P., Wang H., Ji H., Xie J., Qiu Q., Shen D., Dong H. Plant aquaporin AtPIP1;4 links apoplastic H2O2 induction to disease immunity pathways. Plant Physiol. 2016;171(3):1635- 1650. doi 10.1104/pp.15.01237

62. Wang C., Hu H., Qin X., Zeise B., Xu D., Rappel W.-J., Boron W.F., Schroeder J.I. Reconstitution of CO2 regulation of SLAC1 anion channel and function of CO2 – permeable PIP2;1 aquaporin as CARBONIC ANHYDRASE4 interactor. Plant Cell. 2016;28(2): 568-582. doi 10.1105/tpc.15.00637

63. Wang D., Ni Y., Xie K., Li Y., Wu W., Shan H., Cheng B., Li X. Aquaporin ZmTIP2;3 promotes drought resistance of maize through symbiosis with arbuscular mycorrhizal fungi. Int J Mol Sci. 2024;25(8): 4205. doi 10.3390/ijms25084205

64. Wang Y., Zhao Z., Liu F., Sun L., Hao F. Versatile roles of aquaporins in plant growth and development. Int J Mol Sci. 2020;21(24):9485. doi 10.3390/ijms21249485

65. Wayne R., Tazawa M. Nature of the water channels in the internodal cells of Nitellopsis. J Membrain Biol. 1990;116(1):31-39. doi 10.1007/BF01871669

66. Yaneff A., Sigaut L., Marquez M., Alleva K., Pietrasanta L.I., Amodeo G. Heteromerization of PIP aquaporins affects their intrinsic permeability. Proc Natl Acad Sci USA. 2014;111(1):231-236. doi 10.1073/pnas.1316537111

67. Yatsenko-Stepanova T.N., Nemtseva N.V., Ignatenko M.E. The diversity of simbioses and their part in the evolution of the organic world. Vestnik Orenburgskogo Gosudarstvennogo Universiteta = Vestnik of the Orenburg State University. 2014;13(174):142-147 (in Russian)

68. Zhang X., Han C., Gao H., Cao Y. Comparative transcriptome analysis of the garden asparagus (Asparagus officinalis L.) reveals the molecular mechanism for growth with arbuscular mycorrhizal fungi under salinity stress. Plant Physiol Biochem. 2019;141:20-29. doi 10.1016/j.plaphy.2019.05.013

69. Zhang X., Zhuang L., Liu Y., Yang Z., Huang B. Protein phosphorylation associated with drought priming-enhanced heat tolerance in a temperate grass species. Hortic Res. 2020;7(1):207. doi 10.1038/s41438-020-00440-8

70. Zhou X., Yi D., Ma L., Wang X. Genome-wide analysis and expression of the aquaporin gene family in Avena sativa L. Front Plant Sci. 2024;14:1305299. doi 10.3389/fpls.2023.1305299

71. Zhou Y., MacKinnon R. The occupancy of ions in the K+ selectivity filter: charge balance and coupling of ion binding to a protein conformational change underlie high conduction rates. J Mol Biol. 2003;333(5):965-975. doi 10.1016/j.jmb.2003.09.022


Review

Views: 178


Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.


ISSN 2500-3259 (Online)