Arbuscular mycorrhizal symbiosis and osmotic adjustment in response to NaCl stress: A meta-analysis

Frontiers in Plant Science

Volumn 5, Issue OCT, 2014, Pages

  Augé, Robert M ^a   Toler, Heather D ^a   Saxton, Arnold M ^a  

^a UNIVERSITY OF TENNESSEE   (United States)

Author keywords

Arbuscular mycorrhiza; Compatible solutes; K+ Na+ ratio; Meta analysis; NaCl stress; Osmotic adjustment; Salinity; Salt stress

Indexed keywords

EID: 84907965625     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00562     Document Type: Article

References (87)

1. Aboul-Nasr, A. (1999). Alleviation of salt stress by Glomus intraradices on linseed (Linum usitatissimum L.) in hydroponic culture. Alex. J. Agric. Res. 44, 115–127.
2. Adams, D. C., Gurevitch, J., and Rosenberg, M. S. (1997). Resampling tests for meta-analysis of ecological data. Ecology 75,1277-1283. doi: 10.1890/0012-9658(1997)078[1277:RTFMAO]2.0.CO;2
3. Aggarwal, A., Kadian, N., Neetu, K., Tanwar, A., and Gupta, K. K. (2012). Arbuscular mycorrhizal symbiosis and alleviation of salinity stress. J. Appl. Nat. Sci. 4, 144–155.
4. Al-Karaki, G. N., Hammad, R., and Rusan, M. (2001). Response of two tomato cultivars differing in salt tolerance to inoculation with mycorrhizal fungi under salt stress. Mycorrhiza 11, 43–47. doi: 10.1007/s005720100098
5. Aroca, R., Porcel, R., and Ruiz-Lozano, J. M. (2012). Regulation of root water uptake under abiotic stress conditions. J. Exp. Bot. 63, 43–57. doi: 10.1093/jxb/err266
6. Ashraf, M., and Harris, P. J. C. (2004). Potential biochemical indicators of salinity tolerance in plants. Plant Sci. 166, 3–16. doi: 10.1016/j.plantsci.2003.10.024
7. Augé, R. M. (2001). Water relations, drought and VA mycorrhizal symbiosis. Mycorrhiza 11, 3-42. doi: 10.1007/s005720100097
8. Augé, R. M., Saxton, A. M., and Toler, H. D. (2014). Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis. Mycorrhiza. doi: 10.1007/s00572-014-0585-4. [Epub ahead of print].
9. Begg, C. B., and Mazumdar, M. (1994). Operating characteristics of a rank correlation test for publication bias. Biometrics 50,1088-1101. doi: 10.2307/2533446
10. Blaha, G., Stelzl, U., Spahn, C. M. T., Agrawal, R. K., Frank, J., and Nierhaus, K. H. (2000). Preparation of functional ribosomal complexes and effect of buffer conditions on tRNA positions observed by cryoelectron microscopy. Meth. Enzymol. 317, 292–309. doi: 10.1016/S0076-6879(00)17021-1
11. Borde, M., Dudhane, M., and Jite, P. K. (2010). AM fungi influences the photo-synthetic activity, growth and antioxidant enzymes in Allium sativum L. under salinity condition. Notulae Sci. Biol. 2, 64–71.
12. Borenstein, M., Hedges, L., Higgins, J., and Rothstein, J. (2009). Introduction to Meta-Analysis. Wiley: West Sussex.
13. Boyer, J. S. (1982). Plant productivity and environment. Science 218, 443-448. doi: 10.1126/science.218.4571.443
14. Bristow, S. M., Bolland, M. J., MacLennan, G. S., Avenell, A., Grey, A., Gamble, G. D., et al. (2013). Calcium supplements and cancer risk: a meta-analysis of randomized controlled trials. Br. J. Nutr. 110, 1384–1393. doi: 10.1017/S0007114513001050
15. Campanelli, A., Ruta, C., DeMastro, G., and Morone-Fortunato, I. (2013). The role of arbuscular mycorrhizal fungi in alleviating salt stress in Medicago sativa L. Car. Icon. Symbiosis 59, 65–76. doi: 10.1007/s13199-012-0191-1
16. Chen, C., and Dickman, M. B. (2005). Proline suppresses apoptosis in the fungal pathogen Colletotrichum trifolii. Proc. Natl. Acad. Sci. U.S.A. 102, 3459–3464. doi: 10.1073/pnas.0407960102
17. Dakessian, S., Brown, M. S., and Bethlenfalvay, G. J. (1986). Relationship of mycor-rhizal growth enhancement and plant growth with soil water and texture. Plant Soil 94, 439-443. doi: 10.1007/BF02374337
18. Diouf, D., Duponnois, R., Ba, A. T., Neyra, M., and Lesueur, D. (2005). Symbiosis of Acacia auriculiformis and Acacia mangium with mycorrhizal fungi and Bradyrhizobium spp. improves salt tolerance in greenhouse conditions. Funct. Plant Biol. 32, 1143–1152. doi: 10.1071/FP04069
19. El-Mesbahi, M. N., Azcon, R., Ruíz-Lozano, J. M., and Aroca, R. (2012). Plant potassium content modifies the effects of arbuscular mycorrhizal symbiosis on root hydraulic properties in maize plants. Mycorrhiza 22, 555-564. doi: 10.1007/s00572-012-0433-3
20. Estrada, B., Aroca, R., Barea, J. M., and Ruíz-Lozano, J. M. (2013). Native arbuscular mycorrhizal fungi isolated from a saline habitat improved maize antioxidant systems and plant tolerance to salinity. Plant Sci. 201, 42-51. doi: 10.1016/j.plantsci.2012.11.009
21. Evelin, H., Giri, B., and Kapoor, R. (2012). Contribution of Glomus intraradices inoculation to nutrient acquisition and mitigation of ionic imbalance in NaCl-stressed Trigonella foenum-graecum. Mycorrhiza 22, 203–217. doi: 10.1007/s00572-011-0392-0
22. Evelin, H., Giri, B., and Kapoor, R. (2013). Ultrastructural evidence for AMF mediated salt stress mitigation in Trigonella foenum-graecum. Mycorrhiza 23, 71–86. doi: 10.1007/s00572-012-0449-8
23. Evelin, H., Kapoor, R., and Giri, B. (2009). Arbuscular mycorrhizal fungi in alleviation of salt stress: A review. Ann. Bot. 104, 1263–1280. doi: 10.1093/aob/mcp251
24. Fitter, A. H., and Merryweather, R. W. (1992). “Why are some plants more myc-orrhizal than others? an ecological inquiry,” in Mycorrhizas in Ecosystems, eds D. J. Read, D. H. Lewis, A. H. Fitter, and I. Alexander (Wallingord: CAB International), 26-36.
25. Forgy, D. (2012). Arbuscular mycorrhizal fungi can benefit heavy metal tolerance and phytoremediation. J. Nat. Res. Life Sci. Ed. 41, 23–26. doi: 10.4195/jnrlse.2012.0001se
26. Garcia, K., and Zimmermann, S. D. (2014). The role of mycorrhizal associations in plant potassium nutrition. Front. Plant Sci. 5:337. doi: 10.3389/fpls.2014.00337
27. Giri, B., Kapoor, R., and Mukerji, K. G. (2007). Improved tolerance of Acacia nilotica to salt stress by arbuscular mycorrhiza, Glomus fasciculatum may be partly related to elevated K/Na ratios in root and shoot tissues. Microb. Ecol. 54, 753-760. doi: 10.1007/s00248-007-9239-9
28. Graham, J. H., and Syvertsen, J. P. (1989). Vesicular-arbuscular mycorrhizas increase chloride concentration in citrus seedlings. New Phytol. 113, 29–36. doi: 10.1111/j.1469-8137.1989.tb02392.x
29. Groppa, M. D., and Benavides, M. P. (2008). Polyamines and abiotic stress: recent advances. Amino Acids 34, 35–45. doi: 10.1007/s00726-007-0501-8
30. Gurevitch, J., and Hedges, L. V. (1999). Statistical issues in ecological meta-analyses. Ecology 80, 1142–1149. doi: 10.1890/0012-9658(1999)080[1142:SIIEMA]2.0.CO;2
31. Hajiboland, R. (2013). “Role of Arbuscular mycorrhiza in amelioration of salinity,” in Salt Stress in Plants: Signalling, Omics and Adaptations, eds P. Ahmad, M. A. Azooz, and M. N. V. Prasad (New York, NY: Springer Science+Business Media), 301–354.
32. Hammer, E. C., Nasr, H., Pallon, J., Olsson, P. A., and Wallander, H. (2011). Elemental composition of arbuscular mycorrhizal fungi at high salinity. Mycorrhiza 21, 117–129. doi: 10.1007/s00572-010-0316-4
33. Hartmond, U., Schaesberg, N. V., Graham, J. H., and Syvertsen, J. P. (1987). Salinity and flooding stress effects on mycorrhizal and non-mycorrhizal citrus rootstock seedlings. Plant Soil 104, 37–43. doi: 10.1007/BF02370622
34. Hayat, S., Hayat, Q., Alyemeni, M. N., Wani, A. S., Pichtel, J., and Ahmad, A. (2012). Role of proline under changing environments. A review. Plant Signal. Behav. 7, 1–11. doi: 10.4161/psb.21949
35. He, Z. Q., Tang, H. R., Li, H. X., He, C. X., Zhang, Z. B., and Wang, H. S. (2010). Arbuscular mycorrhizal alleviated ion toxicity, oxidative damage and enhanced osmotic adjustment in tomato subjected to NaCl stress. Am. Eur. J. Agric. Environ. Sci. 7, 676–683.
36. Higgins, J. P. T., and Green, S. (2011). Cochrane Handbook for Systematic Reviews of Interventions 5.1.0. The Cochrane Collaboration. Available online at: www.cochrane-handbook.org.
37. Higgins, J. P. T., and Thompson, S. G. (2002). Quantifying heterogeneity in a meta-analysis. Stat. Med. 21,1539–1558. doi: 10.1002/sim.1186
38. Hoeksema, J. D., Chaudhary, V. B., Gehring, C. A., Johnson, N. C., Karst, J., Koide, R. T., et al. (2010). A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol. Lett. 13, 394-407. doi: 10.1111/j.1461-0248.2009.01430.x
39. Holmgren, M., Gómez-Aparicio, L., Quero, J. L., and Valladares, F. (2012). Nonlinear effects of drought under shade -reconciling physiological and ecological models in plant communities. Oecologia 169, 293-305. doi: 10.1007/s00442-011-2196-5
40. 2 index? Psychol. Methods 11, 193-206. doi: 10.1037/1082-989X.11.2.193
41. Iacovelli, R., Alesini, D., Antonella Palazzo, A., Trenta, P., Santoni, M., De Marchis, L., et al. (2014). Targeted therapies and complete responses in first line treatment of metastatic renal cell carcinoma. A meta-analysis of published trials. Cancer Treat. Rev. 40, 271–275. doi: 10.1016/j.ctrv.2013. 09.003
42. IntHout, J., Ioannidis, J. P. A., and Borm, G. F. (2014). The Hartung-Knapp-Sidik-Jonkman method for random effects meta-analysis is straightforward and considerably outperforms the standard DerSimonian-Laird method. BMC Med. Res. Methodol. 14:25. doi: 10.1186/1471-2288-14-25
43. Jagendorf, A. T., and Takabe, T. (2001). Inducers of glycine betaine synthesis in barley. Plant Physiol. 127, 1827–1835. doi: 10.1104/pp.010392
44. James, D. W., Tindall, T. A., Hurst, C. J., and Hussein, N. (1995). Alfalfa cultivar responses to phosphorous and potassium deficiency: Biomass. J. Plant Nutr. 18, 2413–2445.
45. Jayne, B., and Quigley, M. (2014). Influence of arbuscular mycorrhiza on growth and reproductive response of plants under water deficit: a meta-analysis. Mycorrhiza 24, 109–119. doi: 10.1007/s00572-013-0515-x
46. Jindal, V., Atwal, A., Sekhon, B. S., and Singh, R. (1993). Effect of vesicular-arbuscular mycorrhizae on metabolism of moong plants under NaCl salinity. Plant Physiol. Biochem. 31, 475–481.
47. Jones, R. G. W., and Gorham, J. (1983). Osmoregulation. Physiol. Plant Ecol. 12, 33–58.
48. Jung, S. C., Martinez-Medina, A., Lopez-Raez, J. A., and Pozo, M. J. (2012). Mycorrhiza-induced resistance and priming of plant defenses. J. Chem. Ecol. 38, 651–664. doi: 10.1007/s10886-012-0134-6
49. Kafkafi, U., Gilat, R., Yoles, D., and Noy, Y. (1977). Studies on fertilization of field-grown irrigated alfalfa I. Effect of potassium source and time of application. Plant Soil 46, 165–173. doi: 10.1007/BF00693123
50. Lajeunesse, M. J., and Forbes, M. R. (2003). Variable reporting and quantitative reviews: a comparison of three meta-analytical techniques. Ecol. Lett. 6, 448-454. doi: 10.1046/j.1461-0248.2003.00448.x
51. Lehmann, A., Barto, E. K., Powell, J. R., and Rillig, M. C. (2012). Mycorrhizal responsiveness trends in annual crop plants and their wild relatives-a meta-analysis on studies from 1981 to 2010. Plant Soil 355, 231-250. doi: 10.1007/s11104-011-1095-1
52. Leyva, A., Quintana, A., Sánchez, M., Rodríguez, E. N., Cremata, J., and Sánchez, J. C. (2008). Rapid and sensitive anthrone–sulfuric acid assay in microplate format to quantify carbohydrate in biopharmaceutical products: Method development and validation. Biologicals 36, 134–141. doi: 10.1016/j.biologicals.2007.09.001
53. Maya, M. A., and Matsubara, Y. (2013). Influence of arbuscular mycorrhiza on the growth and antioxidative activity in cyclamen under heat stress. Mycorrhiza 23, 381–390. doi: 10.1007/s00572-013-0477-z
54. Mayerhofer, M. S., Kernaghan, G., and Harper, K. A. (2013). The effects of fungal root endophytes on plant growth. Mycorrhiza 23, 199-128. doi: 10.1007/s00572-012-0456-9
55. McGrath, J. M., and Lobell, D. B. (2013). Reduction of transpiration and altered nutrient allocation contribute to nutrient decline of crops grown in elevated CO2 concentrations. Plant Cell Environ. 36, 697-705. doi: 10.1111/pce.12007
56. Miransari, M. (2013). Corn (Zea mays L.) growth as affected by soil compaction and arbuscular mycorrhizal fungi. J. Plant Nutr. 36, 1853–1867. doi: 10.1080/01904167.2013.816729
57. Moftah, A. E., and Michel, B. E. (1987). The effect of sodium chloride on solute potential and proline accumulation in soybean leaves. Plant Physiol. 83, 238–240. doi: 10.1104/pp.83.2.238
58. Morgan, J. M. (1984). Osmoregulation and water stress in higher plants. Ann. Rev. Plant Physiol. 35, 299-319. doi: 10.1146/annurev.pp.35.060184.001503
59. Munns, R., James, R. A., and Läuchli, A. (2006). Approaches to increasing the salt tolerance of wheat and other cereals. J. Exp. Bot. 57, 1025–1043. doi: 10.1093/jxb/erj100
60. Nadeem, S. M., Ahmad, M., Zahir, A., Javaid, A., and Ashraf, M. (2014). The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnology Adv. 32, 429–448. doi: 10.1016/j.biotechadv.2013.12.005
61. Pitman, M. G., and Läuchli, A. (2002). “Global impact of salinity and agricultural ecosystems,” in Salinity: Environment – Plants – Molecules, ed A. Läuchli (Kluwer: Dordrecht), 3–20.
62. Porcel, R., Aroca, R., and Ruiz-Lozano, J. M. (2012). Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron. Sust. Devel. 32, 181–200. doi: 10.1007/s13593-011-0029-x
63. Porcel, R., and Ruíz-Lozano, J. M. (2004). Arbuscular mycorrhizal influence on leaf water potential, solute accumulation, and oxidative stress in soybean plants subjected to drought stress. J. Exp. Bot. 55, 1743–1750. doi: 10.1093/jxb/erh188
64. 18O by native and nonnative arbuscular mycorrhizal fungi in a semiarid environment. New Phytol. 169, 379–387. doi: 10.1111/j.1469-8137.2005.01599.x
65. Rai, A. K., and Takabe, T. (2006). Abiotic Stress Tolerance in Plants: Toward the Improvement of Global Environment and Food. New York, NY: Springer.
66. Rogatgi, A. (2011). WebPlotDigitizer. Available online at: http://arohatgi.info/ WebPlotDigitizer/app/. (Accessed March-June 2014).
67. Rosenberg, M. S., Adams, D. C., and Gurevitch, J. (2000). MetaWin: Statistical Software for Meta-Analysis, Version 2. Sunderland: Sinauer Associates.
68. Rosendahl, C. N., and Rosendahl, S. (1991). Influence of vesicular-arbuscular myc-orrhizal fungi (Glomus spp.) on the response of cucumber (Cucumis sativus L.) to salt stress. Environ. Exp. Bot. 31, 313–318. doi: 10.1016/0098-8472(91)90055-S
69. Ruíz-Lozano, J. M., and Aroca, R. (2010a). “Modulation of aquaporin genes by the arbuscular mycorrhizal symbiosis in relation to osmotic stress tolerance;” in Symbioses and Stress, Vol. 17, Cellular Origin, Life in Extreme Habitats and Astrobiology, eds J. Seckbach and M. Grube (Berlin: Springer), 357–374.
70. Ruiz-Lozano, J. M., and Azcón, R. (2000). Symbiotic efficiency and infectivity of an autochthonous arbuscular mycorrhizal Glomus sp. from saline soils and Glomus deserticola under salinity. Mycorrhiza 10, 137–143. doi: 10.1007/s0057200 00075
71. Ruíz-Lozano, J. M., Azcón, R., and Gómez, M. (1996). Alleviation of salt stress by arbuscular-mycorrhizal Glomus species in Lactuca sativa plants. Physiol. Plant 98, 767–772. doi: 10.1111/j.1399-3054.1996.tb06683.x
72. Ruiz-Lozano, J. M., Gómez, M., and Azcón, R. (1995). Influence of different Glomus species on the time-course of physiological plant responses of lettuce to progressive drought stress periods. Plant Sci. 110, 37-44. doi: 10.1016/0168-9452(95)04184-V
73. Ruíz-Lozano, J. M., Perálvarez, M. C., Aroca, R., and Azcón, R. (2011). The application of a treated sugar beet waste residue to soil modifies the responses of mycorrhizal and non mycorrhizal lettuce plants to drought stress. Plant Soil. 346, 153–166. doi: 10.1007/s11104-011-0805-z
74. Ruíz-Lozano, R. M., and Aroca, R. (2010b). “Host Response to osmotic stresses – stomatal behaviour and water use efficiency of arbuscular mycorrhizal plants,” in Arbuscular Mycorrhizas: Physiology and Function, eds H. Koltai and Y. Kapulnik Y (Netherlands: Springer), 239–256.
75. Ruíz-Lozano, J. M., Porcel, R., Azcón, C., and Aroca, R. (2012). Regulation by arbuscular mycorrhizae of the integrated physiological response to salinity in plants: new challenges in physiological and molecular studies. J. Exp. Bot. 63, 695–709. doi: 10.1093/jxb/ers126
76. Sannazzaro, A. I., Echeverria, M., Alberto, E. O., Ruiz, O. A., and Menendez, A. B. (2007). Modulation of polyamine balance in Lotus glaber by salin ity and arbuscular mycorrhiza. Plant Physiol. Biochem. 45, 39–46. doi: 10.1016/j.plaphy.2006.12.008
77. Scheloske, S., Maetz, M., Schneider, T., Hildebrandt, U., Bothe, H., and Povh, B. (2004). Element distribution in mycorrhizal and nonmycorrhizal roots of the halophyte Aster tripolium determined by proton induced X-ray emission. Protoplasma 223, 183–189. doi: 10.1007/s00709-003-0027-1
78. Seguel, A., Cumming, J. R., Klugh-Stewart, K., Cornejo, P., and Borie, F. (2013). The role of arbuscular mycorrhizas in decreasing aluminium phytotoxicity in acidic soils: a review. Mycorrhiza 23, 167–183. doi: 10.1007/s00572-013-0479-x
79. Serraj, R., and Sinclair, T. R. (2002). Osmolyte accumulation: can it really help increase crop yield under drought conditions? Plant Cell Environ. 25, 333–341. doi: 10.1046/j.1365-3040.2002.00754.x
80. Sharifi, M., Ghorbanli, M., and Ebrahimzadeh, H. (2007). Improved growth of salinity-stressed soybean after inoculation with salt pre-treated mycor-rhizal fungi. J. Plant Physiol. 164, 1144–1151. doi: 10.1016/j.jplph.2006.06.016
81. Valdés-Santiago, L., and Ruiz-Herrera, J. (2014). Stress and polyamine metabolism in fungi. Front. Chem. 1:42. doi: 10.3389/fchem.2013.00042
82. Veresoglou, S. D., Menexes, G., and Rillig, M. C. (2012). Do arbuscular mycor-rhizal fungi affect the allometric partition of host plant biomass to shoots and roots? A meta-analysis of studies from 1990 to 2010. Mycorrhiza 22, 227-235. doi: 10.1007/s00572-011-0398-7
83. Yancey, P. H. (1994). “Compatible and counteracting solutes,” in Cellular and Molecular Physiology of Cell Volume Regulation, ed K. Strange (Boca Raton, FL: CRC Press), 81–109.
84. Yokoi, S., Bressan, R. A., and Hasegawa, P. M. (2002). Salt Stress Tolerance of Plants. JIRCAS Working Report no. 23, 25-33. Available Online at: http://www.plantstress.com/articles/salinity_m/salinity_m_files/jircas.pdf. [7/9/2014]
85. Zeng, G. P., Zhang, X., Liu, H. L., Tan, Y., and Zhu, L. J. (2011). Effect of AM fungi on salt tolerance of Carthamus tinctorius under salt stress. Plant Physiol. Comm. 47, 1064–1068.
86. Zhu, J. (2003). Regulation of ion homeostasis under salt stress. Curr. Opin. Plant Biol. 6, 441–445. doi: 10.1016/S1369-5266(03)00085-2
87. Zhu, X. C., Song, F. B., and Xu, H. W. (2010). Influence of arbuscular mycor-rhiza on lipid peroxidation and antioxidant enzyme activity of maize plants under temperature stress. Mycorrhiza 20, 325–332. doi: 10.1007/s00572-009-0285-7.