Multifaceted roles of aquaporins as molecular conduits in plant responses to abiotic stresses

Critical Reviews in Biotechnology

Volumn 36, Issue 3, 2016, Pages 389-398

  Srivastava, Ashish Kumar ^a   Penna, Suprasanna ^a   Nguyen, Dong Van ^b   Tran, Lam Son Phan ^c  

^a BHABHA ATOMIC RESEARCH CENTRE   (India)

^b Vietnamese Academy of Agricultural Science   (Viet Nam)

^c Elements Chemistry Laboratory   (Japan)

Author keywords

Abiotic stress; aquaporins; plant; regulations; stress tolerance; transport

Indexed keywords

CARBON DIOXIDE; CELL MEMBRANES; CLIMATE CHANGE; CROPS; FOOD SUPPLY; NUTRIENTS; PHYSIOLOGY; PLANTS (BOTANY); PROTEINS; UREA;

ABIOTIC STRESS; AQUAPORINS; PLANT; REGULATIONS; STRESS TOLERANCE; TRANSPORT;

GLYCOPROTEINS;

AQUAPORIN; CALCIUM; HEAVY METAL; REACTIVE OXYGEN METABOLITE; PLANT PROTEIN;

ABIOTIC STRESS; GAS EXCHANGE; GERMINATION; NONHUMAN; NUTRIENT; PLANT RESPONSE; PLANT SEED; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; WATER TRANSPORT; PHYSIOLOGICAL STRESS; TRANSGENIC PLANT;

AQUAPORINS; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; STRESS, PHYSIOLOGICAL;

EID: 84962619164     PISSN: 07388551     EISSN: 15497801     Source Type: Journal    
DOI: 10.3109/07388551.2014.973367     Document Type: Review

References (98)

1. Ahamed A, Murai-Hatano M, Ishikawa-Sakurai J, et al. (2012). Cold stress-induced acclimation in rice is mediated by root-specific aquaporins. Plant Cell Physiol, 53, 1445-56.
2. Bárzana G, Aroca R, Bienert GP, et al. (2014). New insights into the regulation of aquaporins by the arbuscular mycorrhizal symbiosis in maize plants under drought stress and possible implications for plant performance. Mol Plant Microbe Interact, 27, 349-63.
3. Besse M, Knipfer T, Miller AJ, et al. (2011). Developmental pattern of aquaporin expression in barley (Hordeum vulgare L.) leaves. J Exp Bot, 62, 4127-42.
4. Bienert GP, Chaumont F. (2014). Aquaporin-facilitated transmembrane diffusion of hydrogen peroxide. Biochim Biophys Acta, 1840, 1596-604.
5. Bienert GP, Heinen RB, Berny MC, et al. (2014). Maize plasma membrane aquaporin ZmPIP2;5, but not ZmPIP1;2, facilitates transmembrane diffusion of hydrogen peroxide. Biochim Biophys Acta, 1838, 216-22.
6. Bienert GP, Moller ALB, Kristiansen KA, et al. (2007). Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J Biol Chem, 282, 1183-92.
7. Bienert GP, Thorsen M, Schussler MD, et al. (2008). A subgroup of plant aquaporins facilitate the bi-directional diffusion of As(OH)3 and Sb(OH)3 across membranes. BMC Biol, 6, 26.
8. Branco MR, Marinho HS, Cyrne L, et al. (2004). Decrease of H2O2 plasma membrane permeability during adaptation to H2O2 in Saccharomyces cerevisiae. J Biol Chem, 279, 6501-6.
9. Calvo-Polanco M, Molina S, Zamarren?o AM, et al. (2014a). The symbiosis with the arbuscular mycorrhizal fungus Rhizophagus irregularis drives root water transport in flooded tomato plants. Plant Cell Physiol, 55, 1017-29.
10. Calvo-Polanco M, Sánchez-Romera B, Aroca R. (2014b). Mild salt stress conditions induce different responses in root hydraulic conductivity of Phaseolus vulgaris over-time. PLoS One, 9, e90631.
11. Chaumont F, Barrieu F, Wojcik E, et al. (2001). Aquaporins constitute a large and highly divergent protein family in maize. Plant Physiol, 125, 1206-15.
12. Chaumont F, Tyerman SD. (2014). Aquaporins: Highly regulated channels controlling plant water relations. Plant Physiol, 164, 1600-18.
13. Chevalier AS, Bienert GP, Chaumont F. (2014). A new LxxxA motif in the transmembrane helix 3 of maize PIP2 aquaporins is required for their trafficking to the plasma membrane. Plant Physiol, 166, 125-38.
14. Chiba Y, Mitani N, Yamaji N, et al. (2009). HvLsi1 is a silicon influx transporter in barley. Plant J, 57, 810-18.
15. De Silva ND, Cholewa E, Ryser P. (2012). Effects of combined drought and heavy metal stresses on xylem structure and hydraulic conductivity in red maple (Acer rubrum L.). J Exp Bot, 63, 5957-66.
16. di Pietro M, Vialaret J, Li GW, et al. (2013). Coordinated posttranslational responses of aquaporins to abiotic and nutritional stimuli in Arabidopsis roots. Mol Cell Proteomics, 12, 3886-97.
17. Dietz KJ. (2014). Redox regulation of transcription factors in plant stress acclimation and development. Antioxid Redox Signal, 21, 1356-72.
18. Gambetta GA, Fei J, Rost TL, et al. (2013). Water uptake along the length of grapevine fine roots: Developmental anatomy, tissue-specific aquaporin expression, and pathways of water transport. Plant Physiol, 163, 1254-65.
19. Gao Z, He X, Zhao B, et al. (2010). Overexpressing a putative aquaporin gene from wheat, TaNIP, enhances salt tolerance in transgenic Arabidopsis. Plant Cell Physiol, 51, 767-75.
20. Gilliham M, Dayod M, Hocking BJ, et al. (2011). Calcium delivery and storage in plant leaves: Exploring the link with water flow. J Exp Bot, 62, 2233-50.
21. Gu R, Chen X, Zhou Y, et al. (2012). Isolation and characterization of three maize aquaporin genes, ZmNIP2;1, ZmNIP2;4 and ZmTIP4;4 involved in urea transport. BMB Rep, 45, 96-101.
22. Gupta AB, Sankararamakrishnan R. (2009). Genome-wide analysis of major intrinsic proteins in the tree plant Populus trichocarpa: Characterization of XIP sub-family of aquaporins from evolutionary perspective. BMC Plant Biol, 9, 134.
23. Ha S, Tran LS. (2014). Understanding plant responses to phosphorus starvation for improvement of plant tolerance to phosphorus deficiency by biotechnological approaches. Crit Rev Biotechnol, 34, 16-30.
24. Hachez C, Besserer A, Chevalier AS, et al. (2013). Insights into plant plasma membrane aquaporin trafficking. Trends Plant Sci, 18, 344-52.
25. Hanaoka H, Uraguchi S, Takano J, et al. (2014). OsNIP3;1, a rice boric acid channel, regulates boron distribution and is essential for growth under boron-deficient conditions. Plant J, 78, 890-902.
26. Heckwolf M, Pater D, Hanson DT, et al. (2011). The Arabidopsis thaliana aquaporin AtPIP1;2 is a physiologically relevant CO transport facilitator. Plant J, 67, 795-804.
27. Henzler T, Steudle E. (2000). Transport and metabolic degradation of hydrogen peroxide in Chara corallina: Model calculations and measurements with the pressure probe suggest transport of H2O2 across water channels. J Exp Bot, 51, 2053-66.
28. Hooijmaijers C, Rhee JY, Kwak KJ, et al. (2012). Hydrogen peroxide permeability of plasma membrane aquaporins of Arabidopsis thaliana. J Plant Res, 125, 147-53.
29. Hu W, Yuan Q, Wang Y, et al. (2012). Overexpression of a wheat aquaporin gene, TaAQP8, enhances salt stress tolerance in transgenic tobacco. Plant Cell Physiol, 53, 2127-41.
30. Ishibashi K, Kondo S, Hara S, et al. (2011). The evolutionary aspects of aquaporin family. Am J Physiol Regul Integr Comp Physiol, 300, 566-76.
31. Jogaiah S, Govind SR, Tran LS. (2013). Systems biology-based approaches toward understanding drought tolerance in food crops. Crit Rev Biotechnol, 33, 23-39.
32. Johanson U, Karlsson M, Johansson I, et al. (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, 1358-69.
33. Kaldenhoff R, Kai L, Uehlein N. (2014). Aquaporins and membrane diffusion of CO2 in living organisms. Biochim Biophys Acta, 1840, 1592-5.
34. Kelly G, Sade N, Attia Z, et al. (2014). Relationship between hexokinase and the aquaporin PIP1 in the regulation of photosynthesis and plant growth. PLoS One, 9, e87888.
35. Khabudaev KV, Petrova DP, Grachev MA, et al. (2014). A new subfamily LIP of the major intrinsic proteins. BMC Genomics, 15, 173.
36. Kumar K, Mosa K, Chhikara S, et al. (2014). Two rice plasma membrane intrinsic proteins, OsPIP2;4 and OsPIP2;7, are involved in transport and providing tolerance to boron toxicity. Planta, 239, 187-98.
37. Laur J, Hacke UG. (2013). Transpirational demand affects aquaporin expression in poplar roots. J Exp Bot, 64, 2283-29.
38. Leitao L, Prista C, Moura TF, et al. (2012). Grapevine aquaporins: Gating of a tonoplast intrinsic protein (TIP2;1) by cytosolic pH. PLoS One, 7, e33219.
39. Li G, Santoni V, Maurel C. (2014). Plant aquaporins: Roles in plant physiology. Biochim Biophys Acta, 1840, 1574-82.
40. Liu C, Fukumoto T, Matsumoto T, et al. (2013). Aquaporin OsPIP1;1 promotes rice salt resistance and seed germination. Plant Physiol Biochem, 63, 151-8.
41. Liu P, Yin L, Deng X, et al. (2014). Aquaporin-mediated increase in root hydraulic conductance is involved in silicon-induced improved root water uptake under osmotic stress in Sorghum bicolor L. J Exp Bot, 65, 4747-56.
42. Luu DT, Martinière A, Sorieul M, et al. (2012). Fluorescence recovery after photobleaching reveals high cycling dynamics of plasma membrane aquaporins in Arabidopsis roots under salt stress. Plant J, 69, 894-905.
43. Ma JF, Yamaji N, Mitani N, et al. (2008). Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc Natl Acad Sci USA, 105, 9931-5.
44. Makino N, Sasaki K, Hashida K, et al. (2004). A metabolic model describing the H2O2 elimination by mammalian cells including H2O2 permeation through cytoplasmic and peroxisomal membranes: Comparison with experimental data. Biochim Biophys Acta, 1673, 149-59.
45. Matoh T. (1997). Boron in plant cell walls. Plant Soil, 193, 59-70.
46. Maurel C, Verdoucq L, Luu D-T, et al. (2008). Plant aquaporins: Membrane channels with multiple integrated functions. Annu Rev Plant Biol, 59, 595-624.
47. Mitani-Ueno N, Yamaji N, Zhao FJ, et al. (2011). The aromatic/arginine selectivity filter of NIP aquaporins plays a critical role in substrate selectivity for silicon, boron, and arsenic. J Exp Bot, 62, 4391-8.
48. Mori IC, Rhee J, Shibasaka M, et al. (2014). CO2 transport by PIP2 aquaporins of barley. Plant Cell Physiol, 55, 251-7.
49. Nable RO, Ban?uelos GS, Paull JG. (1997). Boron toxicity. Plant Soil, 193, 181-98.
50. Negishi T, Oshima K, Hattori M, et al. (2012). Tonoplast- and plasma membrane-localized aquaporin-family transporters in blue hydrangea sepals of aluminum hyperaccumulating plant. PLoS One, 7, e43189.
51. Novikova GV, Tournaire-Roux C, Sinkevich IA, et al. (2014). Vacuolar biogenesis and aquaporin expression at early germination of broad bean seeds. Plant Physiol Biochem, 82, 123-32.
52. Osakabe Y, Osakabe K, Shinozaki K, et al. (2014). Response of plants to water stress. Front Plant Sci, 5, 86.
53. Otto B, Uehlein N, Sdorra S, et al. (2010). Aquaporin tetramer composition modifies the function of tobacco aquaporins. J Biol Chem, 285, 31253-60.
54. Pandey B, Sharma P, Pandey DM, et al. (2013). Identification of new aquaporin genes and single nucleotide polymorphism in bread wheat. Evol Bioinform Online, 9, 437-52.
55. Pang Y, Li L, Ren F, et al. (2010). Overexpression of the tonoplast aquaporin AtTIP5;1 conferred tolerance to boron toxicity in Arabidopsis. J Genet Genomics, 37, 389-97.
56. Park W, Scheffler BE, Bauer PJ, et al. (2010). Identification of the family of aquaporin genes and their expression in upland cotton (Gossypium hirsutum L.). BMC Plant Biol, 10, 142.
57. Péret B, Li G, Zhao J, et al. (2012). Auxin regulates aquaporin function to facilitate lateral root emergence. Nature Cell Biol, 14, 991-8.
58. Petrov VD, Breusegem FV. (2012). Hydrogen peroxide- a central hub for information in plant cells. AoB Plants, 2012, pls014.
59. Prado K, Boursiac Y, Tournaire-Roux C, et al. (2013). Regulation of Arabidopsis leaf hydraulics involves light-dependent phosphorylation of aquaporins in veins. Plant Cell, 25, 1029-39.
60. Przedpelska-Wasowicz EM, Wierzbicka M. (2011). Gating of aquaporins by heavy metals in Allium cepa L. epidermal cells. Protoplasma, 248, 663-71.
61. Qian ZJ, Song JJ, Chaumont F, et al. (2014). Differential responses of plasma membrane aquaporins in mediating water transport of cucumber seedlings under osmotic and salt stresses. Plant Cell Environ. doi: 10.1111/pce.12319.
62. Reuscher S, Akiyama M, Mori C, et al. (2013). Genome-wide identification and expression analysis of aquaporins in tomato. PLoS One, 8, e79052.
63. Sade N, Galle A, Flexas J, et al. (2014). Differential tissue-specific expression of NtAQP1 in Arabidopsis thaliana reveals a role for this protein in stomatal and mesophyll conductance of CO2 under standard and salt-stress conditions. Planta, 239, 357-66.
64. Sakurai J, Ishikawa F, Yamaguchi T, et al. (2005). Identification of 33 rice aquaporin genes and analysis of their expression and function. Plant Cell Physiol, 46, 1568-77.
65. Schnurbusch T, Hayes J, Hrmova M, et al. (2010). Boron toxicity tolerance in barley through reduced expression of the multifunctional aquaporin HvNIP2;1. Plant Physiol, 153, 1706-15.
66. Seaver LC, Imlay JA. (2001). Hydrogen peroxide fluxes and compartmentalization inside growing Escherichia coli. J Bacteriol, 183, 7182-9.
67. Secchi F, Zwieniecki MA. (2013). The physiological response of Populus tremula x alba leaves to the down-regulation of PIP1 aquaporin gene expression under no water stress. Front Plant Sci, 4, 507.
68. Secchi F, Zwieniecki MA. (2014). Down-regulation of plasma intrinsic protein1 aquaporin in poplar trees is detrimental to recovery from embolism. Plant Physiol, 164, 1789-99.
69. Sewelam N, Jaspert N, Van Der Kelen K, et al. (2014). Spatial H2O2 signaling specificity: H2O2 from chloroplasts and peroxisomes modulates the plant transcriptome differentially. Mol Plant, 7, 1191-210.
70. Soto G, Alleva K, Mazzella MA, et al. (2008). AtTIP1;3 and AtTIP5;1, the only highly expressed Arabidopsis pollen-specific aquaporins, transport water and urea. FEBS Lett, 582, 4077-82.
71. Soto G, Fox R, Ayub N, et al. (2010). TIP5;1 is an aquaporin specifically targeted to pollen mitochondria and is probably involved in nitrogen remobilization in Arabidopsis thaliana. Plant J, 64, 1038-47.
72. Sreedharan S, Shekhawat UKS, Ganapathi TR. (2013). Transgenic banana plants overexpressing a native plasma membrane aquaporin MusaPIP1;2 display high tolerance levels to different abiotic stresses. Plant Biotechnol J, 11, 942-52.
73. Srivastava AK, Suprasanna P, Srivastava S, et al. (2010). Thiourea mediated regulation in the expression profile of aquaporins and its impact on water homeostasis under salinity stress in Brassica juncea roots. Plant Sci, 178, 517-22.
74. Srivastava S, Srivastava AK, Suprasanna P, et al. (2013). Quantitative real-time expression profiling of aquaporins-isoforms and growth response of Brassica juncea under arsenite stress. Mol Biol Rep, 40, 2879-86.
75. Steinhorst L, Kudla J. (2013). Calcium and reactive oxygen species rule the waves of signaling. Plant Physiol, 163, 471-85.
76. Surbanovski N, Sargent DJ, Else MA, et al. (2013). Expression of Fragaria vesca PIP aquaporins in response to drought stress: PIP down-regulation correlates with the decline in substrate moisture content. PLoS One, 8, e74945.
77. Tajkhorshid E, Nollert P, Jensen M, et al. (2002). Control of the selectivity of the aquaporin water channel family by global orientation tuning. Science, 296, 525-30.
78. Tao P, Zhong X, Li B, et al. (2014). Genome-wide identification and characterization of aquaporin genes (AQPs) in Chinese cabbage (Brassica rapa ssp. pekinensis). Mol Genet Genomics. doi: 10.1007/s00438-014-0874-9.
79. Terashima I, Ono K. (2002). Effects of HgCl2 on CO2 dependence of leaf photosynthesis: Evidence indicating involvement of aquaporins in CO2 diffusion across the plasma membrane. Plant Cell Physiol, 43, 70-8.
80. Tester M, Langridge P. (2010). Breeding technologies to increase crop production in a changing world. Science, 327, 818-22.
81. Thao NP, Tran LS. (2012). Potentials toward genetic engineering of drought-tolerant soybean. Crit Rev Biotechnol, 32, 349-62.
82. Uehlein N, Lovisolo C, Siefritz F, et al. (2003). The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature, 425, 734-7.
83. Uehlein N, Sperling H, Heckwolf M, et al. (2012). The Arabidopsis aquaporin PIP1;2 rules cellular CO2 uptake. Plant Cell Environ, 35, 1077-83.
84. USDA-NASS (United States Department of Agriculture-National Agricultural Statistics Service). (2013). Field crops statistics. USDA-NASS USA.
85. Vander Willigen C, Postaire O, Tournaire-Roux C, et al. (2006). Expression and inhibition of aquaporins in germinating Arabidopsis seeds. Plant Cell Physiol, 47, 1241-50.
86. Venkatesh J, Yu JW, Park SW. (2013). Genome-wide analysis and expression profiling of the Solanum tuberosum aquaporins. Plant Physiol Biochem, 73, 392-404.
87. Wang LL, Chen AP, Zhong NQ, et al. (2014). The Thellungiella salsuginea tonoplast aquaporin TsTIP1;2 functions in protection against multiple abiotic stresses. Plant Cell Physiol, 55, 148-61.
88. Wang Y, Tajkhorshid E. (2010). Nitric oxide conduction by the brain aquaporin AQP4. Proteins, 78, 661-70.
89. Webb AAR, McAinsh MR, Taylor JE, et al. (1996). Calcium ions as intracellular second messengers in higher plants. Adv Bot Res, 22, 45-96.
90. Wudick MM, Luu DT, Tournaire-Roux C, et al. (2014). Vegetative and sperm cell-specific aquaporins of Arabidopsis highlight the vacuolar equipment of pollen and contribute to plant reproduction. Plant Physiol, 164, 1697-706.
91. Xu C, Wang M, Zhou L, et al. (2013). Heterologous expression of the wheat aquaporin gene TaTIP2;2 compromises the abiotic stress tolerance of Arabidopsis thaliana. PLoS One, 8, e79618.
92. Yamaji N, Ma JF. (2007). Spatial distribution and temporal variation of the rice silicon transporter Lsi1. Plant Physiol, 143, 1306-13.
93. Yaneff A, Sigaut L, Marquez M, et al. (2014). Heteromerization of PIP aquaporins affects their intrinsic permeability. Proc Natl Acad Sci USA, 111, 231-6.
94. Zaghdoud C, Mota-Cadenas C, Carvajal M, et al. (2013). Elevated CO2 alleviates negative effects of salinity on broccoli (Brassica oleracea L. var Italica) plants by modulating water balance through aquaporins abundance. Env Exp Bot, 95, 15-24.
95. Zhang DY, Ali Z, Wang CB, et al. (2013). Genome-wide sequence characterization and expression analysis of major intrinsic proteins in soybean (Glycine max L.). PLoS One, 8, e56312.
96. Zhang Y, Wang Z, Chai T, et al. (2008). Indian mustard aquaporin improves drought and heavy-metal resistance in tobacco. Mol Biotechnol, 40, 280-92.
97. Zhou Y, Setz N, Niemietz C, et al. (2007). Aquaporins and unloading of phloem-imported water in coats of developing bean seeds. Plant Cell Environ, 30, 1566-77.
98. Zhu D, Wu Z, Cao G, et al. (2014). TRANSLUCENT GREEN, an ERF family transcription factor, controls water balance in Arabidopsis by activating the expression of aquaporin genes. Mol Plant, 7, 601-15.