Constitutive overexpression of soybean plasma membrane intrinsic protein GmPIP1;6 confers salt tolerance

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• 作者：Lian Zhou (34) (35)
  Chuang Wang (34)
  Ruifang Liu (34)
  Qiang Han (34)
  Rebecca K Vandeleur (36)
  Juan Du (34)
  Steven Tyerman (36)
  Huixia Shou (34)
  
  34. State Key Laboratory of Plant Physiology and Biochemistry ; College of Life Sciences ; Zhejiang University ; Hangzhou ; 310058 ; P. R. China
  35. College of Agriculture and Biotechnology ; Southwest University ; 400715 ; Chongqing ; P. R. China
  36. Australian Research Council Centre of Excellence in Plant Energy Biology ; School of Agriculture ; Food and Wine ; Waite Research Institute ; University of Adelaide ; PMB1 ; Glen Osmond ; SA ; 5064 ; Australia
  
• 关键词：Soybean ; Aquaporins ; Salt tolerance ; Ovexpression ; Transformation ; GmPIP1 ; 6
• 刊名：BMC Plant Biology
• 出版年：2014
• 出版时间：December 2014
• 年：2014
• 卷：14
• 期：1
• 全文大小：1,865 KB
• 参考文献：1. Munns, R, Tester, M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59: pp. 651-681 CrossRef
  2. Munns, R (2005) Genes and salt tolerance: bringing them together. New Phytol 167: pp. 645-663 CrossRef
  3. Colmer, TD, Munns, R, Flowers, TJ (2005) Improving salt tolerance of wheat and barley: future prospects. Aust J Exp Agri 45: pp. 1425-1443 CrossRef
  4. Tyerman, SD, Skerrett, IM (1999) Root ion channels and salinity. Sci Hortic 78: pp. 175-235 CrossRef
  5. Teakle, NL, Tyerman, SD (2010) Mechanisms of Cl(-) transport contributing to salt tolerance. Plant Cell Environ 33: pp. 566-589 CrossRef
  6. Horie, T, Schroeder, JI (2004) Sodium transporters in plants. Diverse genes and physiological functions. Plant Physiol 136: pp. 2457-2462 CrossRef
  7. Tester, M, Davenport, R (2003) Na鈥?鈥塼olerance and Na鈥?鈥塼ransport in higher plants. Ann Bot 91: pp. 503-527 CrossRef
  8. Chaumont, F, Tyerman, SD (2014) Aquaporins: highly regulated channels controlling plant water relations. Plant Physiol 164: pp. 1600-1618 CrossRef
  9. Steudle, E (2000) Water uptake by plant roots: an integration of views. Plant Soil 226: pp. 45-56 CrossRef
  10. Krishnamurthy, P, Ranathunge, K, Franke, R, Prakash, HS, Schreiber, L, Mathew, MK (2009) The role of root apoplastic transport barriers in salt tolerance of rice (Oryza sativa L.). Planta 230: pp. 119-134 CrossRef
  11. Hose, E, Clarkson, DT, Steudle, E, Schreiber, L, Hartung, W (2001) The exodermis: a variable apoplastic barrier. J Exp Bot 52: pp. 2245-2264 CrossRef
  12. Steudle, E (2000) Water uptake by roots: effects of water deficit. J Exp Bot 51: pp. 1531-1542 CrossRef
  13. Knepper, MA (1994) The aquaporin family of molecular water channels. Proc Natl Acad Sci U S A 91: pp. 6255-6258 CrossRef
  14. Tyerman, SD, Niemieta, CM, Bramley, H (2002) Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant Cell Environ 25: pp. 173-194 CrossRef
  15. Maurel, C (2007) Plant aquaporins: novel functions and regulation properties. FEBS Lett 581: pp. 2227-2236 CrossRef
  16. Kaldenhoff, R, Ribas-Carbo, M, Sans, JF, Lovisolo, C, Heckwolf, M, Uehlein, N (2008) Aquaporins and plant water balance. Plant Cell Environ 31: pp. 658-666 CrossRef
  17. Sade, N, Gebretsadik, M, Seligmann, R, Schwartz, A, Wallach, R, Moshelion, M (2010) The role of tobacco Aquaporin1 in improving water use efficiency, hydraulic conductivity, and yield production under salt stress. Plant Physiol 152: pp. 245-254 CrossRef
  18. Maurel, C, Verdoucq, L, Luu, DT, Santoni, V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59: pp. 595-624 CrossRef
  19. Hachez, C, Besserer, A, Chevalier, AS, Chaumont, F (2013) Insights into plant plasma membrane aquaporin trafficking. Trends Plant Sci 18: pp. 344-352 CrossRef
  20. Fetter, K, Van Wilder, V, Moshelion, M, Chaumont, F (2004) Interactions between plasma membrane aquaporins modulate their water channel activity. Plant Cell 16: pp. 215-228 CrossRef
  21. Zelazny, E, Borst, JW, Muylaert, M, Batoko, H, Hemminga, MA, Chaumont, F (2007) FRET imaging in living maize cells reveals that plasma membrane aquaporins interact to regulate their subcellular localization. Proc Natl Acad Sci U S A 104: pp. 12359-12364 CrossRef
  22. Temmei, Y, Uchida, S, Hoshino, D, Kanzawa, N, Kuwahara, M, Sasaki, S, Tsuchiya, T (2005) Water channel activities of Mimosa pudica plasma membrane intrinsic proteins are regulated by direct interaction and phosphorylation. FEBS Lett 579: pp. 4417-4422 CrossRef
  23. Vandeleur, RK, Mayo, G, Shelden, MC, Gilliham, M, Kaiser, BN, Tyerman, SD (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 Physiol 149: pp. 445-460 CrossRef
  24. Alleva, K, Marquez, M, Villarreal, N, Mut, P, Bustamante, C, Bellati, J, Martinez, G, Civello, M, Amodeo, G (2010) Cloning, functional characterization, and co-expression studies of a novel aquaporin (FaPIP2;1) of strawberry fruit. J Exp Bot 61: pp. 3935-3945 CrossRef
  25. Bellati, J, Alleva, K, Soto, G, Vitali, V, Jozefkowicz, C, Amodeo, G (2010) Intracellular pH sensing is altered by plasma membrane PIP aquaporin co-expression. Plant Mol Biol 74: pp. 105-118 CrossRef
  26. Chen, W, Yin, X, Wang, L, Tian, J, Yang, R, Liu, D, Yu, Z, Ma, N, Gao, J (2013) Involvement of rose aquaporin RhPIP1;1 in ethylene-regulated petal expansion through interaction with RhPIP2;1. Plant Mol Biol 83: pp. 219-233 CrossRef
  27. Yaneff, A, Sigaut, L, Marquez, M, Alleva, K, Pietrasanta, LI, Amodeo, G (2014) Heteromerization of PIP aquaporins affects their intrinsic permeability. Proc Natl Acad Sci U S A 111: pp. 231-236 CrossRef
  28. Johanson, U, Karlsson, M, Johansson, I, Gustavsson, S, Sjovall, S, Fraysse, L, Weig, AR, Kjellbom, P (2001) The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiol 126: pp. 1358-1369 CrossRef
  29. Sakurai, J, Ishikawa, F, Yamaguchi, T, Uemura, M, Maeshima, M (2005) Identification of 33 rice aquaporin genes and analysis of their expression and function. Plant Cell Physiol 46: pp. 1568-1577 CrossRef
  30. Zhang, DY, Ali, Z, Wang, CB, Xu, L, Yi, JX, Xu, ZL, Liu, XQ, He, XL, Huang, YH, Khan, IA, Trethowan, RM, Ma, HX (2013) Genome-wide sequence characterization and expression analysis of major intrinsic proteins in soybean (Glycine max L.). PLoS One 8: pp. e56312 CrossRef
  31. Maurel, C, Javot, H, Lauvergeat, V, Gerbeau, P, Tournaire, C, Santoni, V, Heyes, J (2002) Molecular physiology of aquaporins in plants. Int Rev Cytol 215: pp. 105-148 CrossRef
  32. Fricke, W, Chaumont, F Solute and Water Relations of Growing Plant Cells. In: Verbelen, JP, Vissenberg, K eds. (2007) The Expanding Cell, Volume 6. Springer, Berlin Heidelberg, pp. 7-31 CrossRef
  33. Liu, D, Tu, L, Wang, L, Li, Y, Zhu, L, Zhang, X (2008) Characterization and expression of plasma and tonoplast membrane aquaporins in elongating cotton fibers. Plant Cell Rep 27: pp. 1385-1394 CrossRef
  34. Ma, N, Xue, J, Li, Y, Liu, X, Dai, F, Jia, W, Luo, Y, Gao, J (2008) Rh-PIP2;1, a rose aquaporin gene, is involved in ethylene-regulated petal expansion. Plant Physiol 148: pp. 894-907 CrossRef
  35. Peret, B, Li, G, Zhao, J, Band, LR, Voss, U, Postaire, O, Luu, DT, Da Ines, O, Casimiro, I, Lucas, M, Wells, DM, Lazzerini, L, Nacry, P, King, JR, Jensen, OE, Schaffner, AR, Maurel, C, Bennett, MJ (2012) Auxin regulates aquaporin function to facilitate lateral root emergence. Nat Cell Biol 14: pp. 991-998 CrossRef
  36. Aroca, R, Porcel, R, Ruiz-Lozano, JM (2012) Regulation of root water uptake under abiotic stress conditions. J Exp Bot 63: pp. 43-57 CrossRef
  37. Hu, W, Yuan, Q, Wang, Y, Cai, R, Deng, X, Wang, J, Zhou, S, Chen, M, Chen, L, Huang, C, Ma, Z, Yang, G, He, G (2012) Overexpression of a wheat aquaporin gene, TaAQP8, enhances salt stress tolerance in transgenic tobacco. Plant Cell Physiol 53: pp. 2127-2141 CrossRef
  38. Zhou, S, Hu, W, Deng, X, Ma, Z, Chen, L, Huang, C, Wang, C, Wang, J, He, Y, Yang, G, He, G (2012) Overexpression of the wheat aquaporin gene, TaAQP7, enhances drought tolerance in transgenic tobacco. PLoS One 7: pp. e52439 CrossRef
  39. Gao, Z, He, X, Zhao, B, Zhou, C, Liang, Y, Ge, R, Shen, Y, Huang, Z (2010) Overexpressing a putative aquaporin gene from wheat, TaNIP, enhances salt tolerance in transgenic Arabidopsis. Plant Cell Physiol 51: pp. 767-775 CrossRef
  40. Sreedharan, S, Shekhawat, UK, Ganapathi, TR (2013) Transgenic banana plants overexpressing a native plasma membrane aquaporin MusaPIP1;2 display high tolerance levels to different abiotic stresses. Plant Biotechnol J 11: pp. 942-952 CrossRef
  41. Delgado, MJ, Ligero, F, Lluch, C (1994) Effects of salt stress on growth and nitrogen fixation by pea, faba-bean, common bean and soybean plants. Soil Biol Biochem 26: pp. 371-376 CrossRef
  42. Vandeleur, RK, Sullivan, W, Athman, A, Jordans, C, Gilliham, M, Kaiser, BN, Tyerman, SD (2014) Rapid shoot-to-root signalling regulates root hydraulic conductance via aquaporins. Plant Cell Environ 37: pp. 520-538 CrossRef
  43. Tournaire-Roux, C, Sutka, M, Javot, H, Gout, E, Gerbeau, P, Luu, DT, Bligny, R, Maurel, C (2003) Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. Nature 425: pp. 393-397 CrossRef
  44. Siefritz, F, Tyree, MT, Lovisolo, C, Schubert, A, Kaldenhoff, R (2002) PIP1 plasma membrane aquaporins in tobacco: from cellular effects to function in plants. Plant Cell 14: pp. 869-876 CrossRef
  45. Martinez-Ballesta, MC, Aparicio, F, Pallas, V, Martinez, V, Carvajal, M (2003) Influence of saline stress on root hydraulic conductance and PIP expression in Arabidopsis. J Plant Physiol 160: pp. 689-697 CrossRef
  46. Boursiac, Y, Chen, S, Luu, DT, Sorieul, M, van den Dries, N, Maurel, C (2005) Early effects of salinity on water transport in Arabidopsis roots. Molecular and cellular features of aquaporin expression. Plant Physiol 139: pp. 790-805 CrossRef
  47. Marulanda, A, Azcon, R, Chaumont, F, Ruiz-Lozano, JM, Aroca, R (2010) Regulation of plasma membrane aquaporins by inoculation with a Bacillus megaterium strain in maize (Zea mays L.) plants under unstressed and salt-stressed conditions. Planta 232: pp. 533-543 CrossRef
  48. Muries, B, Faize, M, Carvajal, M, Martinez-Ballesta Mdel, C (2011) Identification and differential induction of the expression of aquaporins by salinity in broccoli plants. Mol Biosyst 7: pp. 1322-1335 CrossRef
  49. Calvo-Polanco, M, Sanchez-Romera, B, Aroca, R (2014) Mild salt stress conditions induce different responses in root hydraulic conductivity of phaseolus vulgaris over-time. PLoS One 9: pp. e90631 CrossRef
  50. Liu, C, Fukumoto, T, Matsumoto, T, Gena, P, Frascaria, D, Kaneko, T, Katsuhara, M, Zhong, S, Sun, X, Zhu, Y, Iwasaki, I, Ding, X, Calamita, G, Kitagawa, Y (2012) Aquaporin OsPIP1;1 promotes rice salt resistance and seed germination. Plant Physiol Biochem 63C: pp. 151-158
  51. Durand, M, Lacan, D (1994) Sodium partitioning within the shoot of soybean. Physiol Plant 91: pp. 65-71 CrossRef
  52. Lauchli, A Salt exclusion: An adaptation of legumes for crops and pastures under saline conditions. In: Staples, RC, Toenniessen, GH eds. (1984) Salinity Tolerance in Piants, Strategies for Crop Improvement. John Wiley & Sons, New York, pp. 171-187
  53. Lohaus, G, Hussmann, M, Pennewiss, K, Schneider, H, Zhu, JJ, Sattelmacher, B (2000) Solute balance of a maize (Zea mays L.) source leaf as affected by salt treatment with special emphasis on phloem retranslocation and ion leaching. J Exp Bot 51: pp. 1721-1732 CrossRef
  54. Li, WY, Wong, FL, Tsai, SN, Phang, TH, Shao, G, Lam, HM (2006) Tonoplast-located GmCLC1 and GmNHX1 from soybean enhance NaCl tolerance in transgenic bright yellow (BY)-2 cells. Plant Cell Environ 29: pp. 1122-1137 CrossRef
  55. Uehlein, N, Lovisolo, C, Siefritz, F, Kaldenhoff, R (2003) The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature 425: pp. 734-737 CrossRef
  56. Flexas, J, Ribas-Carbo, M, Hanson, DT, 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 J 48: pp. 427-439 CrossRef
  57. Heckwolf, M, Pater, D, Hanson, DT, Kaldenhoff, R (2011) The Arabidopsis thaliana aquaporin AtPIP1;2 is a physiologically relevant CO(2) transport facilitator. Plant J 67: pp. 795-804 CrossRef
  58. Uehlein, N, Sperling, H, Heckwolf, M, Kaldenhoff, R (2012) The Arabidopsis aquaporin PIP1;2 rules cellular CO(2) uptake. Plant Cell Environ 35: pp. 1077-1083 CrossRef
  59. Evans, JR, Kaldenhoff, R, Genty, B, Terashima, I (2009) Resistances along the CO2 diffusion pathway inside leaves. J Exp Bot 60: pp. 2235-2248 CrossRef
  60. Patrick, JW, Zhang, W, Tyerman, SD, Offler, CE, Walker, NA (2001) Role of membrane transport in phloem translocation of assimilates and water. Func Plant Biol 28: pp. 697-709 CrossRef
  61. Song, ZY, Tian, JL, Fu, WZ, Li, L, Lu, LH, Zhou, L, Shan, ZH, Tang, GX, Shou, HX (2013) Screening Chinese soybean genotypes for Agrobacterium-mediated genetic transformation suitability. J Zhejiang Univ Sci B 14: pp. 289-298 CrossRef
  
• 刊物主题：Plant Sciences; Agriculture; Tree Biology;
• 出版者：BioMed Central
• ISSN：1471-2229

文摘

Background Under saline conditions, plant growth is depressed via osmotic stress and salt can accumulate in leaves leading to further depression of growth due to reduced photosynthesis and gas exchange. Aquaporins are proposed to have a major role in growth of plants via their impact on root water uptake and leaf gas exchange. In this study, soybean plasma membrane intrinsic protein 1;6 (GmPIP1;6) was constitutively overexpressed to evaluate the function of GmPIP1;6 in growth regulation and salt tolerance in soybean. Results GmPIP1;6 is highly expressed in roots as well as reproductive tissues and the protein targeted to the plasma membrane in onion epidermis. Treatment with 100 mM NaCl resulted in reduced expression initially, then after 3 days the expression was increased in root and leaves. The effects of constitutive overexpression of GmPIP1;6 in soybean was examined under normal and salt stress conditions. Overexpression in 2 independent lines resulted in enhanced leaf gas exchange, but not growth under normal conditions compared to wild type (WT). With 100 mM NaCl, net assimilation was much higher in the GmPIP1;6-Oe and growth was enhanced relative to WT. GmPIP1;6-Oe plants did not have higher root hydraulic conductance (L o) under normal conditions, but were able to maintain L o under saline conditions compared to WT which decreased L o. GmPIP1;6-Oe lines grown in the field had increased yield resulting mainly from increased seed size. Conclusions The general impact of overexpression of GmPIP1;6 suggests that it may be a multifunctional aquaporin involved in root water transport, photosynthesis and seed loading. GmPIP1;6 is a valuable gene for genetic engineering to improve soybean yield and salt tolerance.