Role of arbuscular mycorrhizal fungi in alleviating the adverse effects of acidity and aluminium toxicity in zucchini squash

Scientia Horticulturae

Volumn 188, Issue , 2015, Pages 97-105

  Rouphael, Youssef ^a   Cardarelli, Mariateresa ^b   Colla, Giuseppe ^c  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b ISTITUTO NAZIONALE DELLA NUTRIZIONE   (Italy)

^c UNIVERSITY OF TUSCIA   (Italy)

Author keywords

Acid soil; Aluminium; Arbuscular mycorrhizal; Cucurbita pepo L.; Nutritional status; PH level

Indexed keywords

ACIDITY; ALUMINUM; BIOMASS; BIOREMEDIATION; CONCENTRATION (COMPOSITION); FUNGUS; NUTRIENT CYCLING; PLANT COMMUNITY; ROOT COLONIZATION;

CUCURBITA PEPO; CUCURBITA PEPO VAR. MELOPEPO; FUNGI;

EID: 84926484312     PISSN: 03044238     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.scienta.2015.03.031     Document Type: Article

References (65)

1. Andrade S.A.L., Mazzafera P., Schiavinato M.A., Silveira A.P.D. Arbuscular mycorrhizal association in coffee. J. Agric. Sci. 2009, 147:105-115.
2. Borie F., Rubio R. Effects of arbuscular mycorrhiza and liming on growth and mineral acquisition of Al-tolerant barley cultivars. J. Plant Nutr. 1999, 22:121-137.
3. Borer C.H., Schaberg P.G., DeHayes D.H. Acidic mist reduces foliar membrane-associated calcium and impairs stomatal responsiveness in red spruce. Tree Physiol. 2005, 24:929-939.
4. Bremner J.M. Total nitrogen. Methods of Soil Analysis 1965, 1149-1178. American Society of Agronomy, Madison, WI, Agronomy Monograph 9 (Part 2). C.A. Black, D.D. Evans, I.L. White, L.E. Ensminger, F.E. Clark (Eds.).
5. Cardarelli M., Rouphael Y., Rea E., Colla G. Mitigation of alkaline stress by arbuscular mycorrhiza in zucchini plants grown under mineral and organic fertilization. J. Plant Nutr. Soil Sci. 2010, 173:778-787.
6. Cartmill A.D., Valdez-Aguilar L.A., Bryan D.L., Alarcón A. Arbuscular mycorrhizal fungi enhance tolerance of vinca to high alkalinity in irrigation water. Sci. Hortic. 2008, 115:275-284.
7. Chen B.D., Shen H., Li X.L., Feng G., Christie P. Effects of EDTA application and arbuscular mycorrhizal colonization on growth and zinc uptake by maize (Zea mays L.) in soil experimentally contaminated with zinc. Plant Soil 2004, 261:219-229.
8. Clark R. Arbuscular mycorrhizal adaptation, spore germination, root colonization, and host plant growth and mineral acquisition at low pH. Plant Soil 1997, 192:15-22.
9. Clark R.B., Zeto S.K. Mineral acquisition by arbuscular mycorrhizal plants. J. Plant Nutr. 2000, 23:867-902.
10. Colla G., Rouphael Y., Cardarelli M., Tullio M., Rivera C.M., Rea E. Alleviation of salt stress by arbuscular mycorrhizal in zucchini plants grown at low and high phosphorus concentration. Biol. Fertil. Soils 2008, 44:501-509.
11. Colla G., Rouphael Y., Cardarelli M., Salerno A., Rea E. The effectiveness of grafting to improve alkalinity tolerance in watermelon. Environ. Exp. Bot. 2010, 68:283-291.
12. Cumming J.R., Ning J. Arbuscular mycorrhizal fungi enhance aluminium resistance of broomsedge (Andropogon virginicus L.). J. Exp. Bot. 2003, 54:1447-1459.
13. Danielson R.M. Mycorrhizae and reclamation of stressed terrestrial environments. Soil Reclamation Processes: Microbiological Analysis and Applications 1985, 173-201. Marcel Dekker, New York, NY. R.L. Tate, D.A. Klein (Eds.).
14. Dudhane M., Borde M., Jite P.R. Effect of aluminium toxicity on growth responses and antioxidant activities in Gmelina arborea roxb. inoculated with AM fungi. Int. J. Phytoremediation 2012, 14:643-655.
15. Foy C.D. The physiology of plant adaptation to mineral stress. Iowa State J. Res. 1983, 57:355-391.
16. Foy C.D., Chaney R.L., White M.C. The physiology of metal Al toxicity in plants. Annu. Rev. Plant Physiol. 1978, 29:511-566.
17. Giovannetti M., Mosse B. An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol. 1980, 84:489-500.
18. Isaac R.A., Johnson W.C. Elemental determination by inductively coupled plasma atomic emission spectrophotometry. Handbook of Reference Methods for Plant Analysis 1998, 165-170. CRC Press Inc, Boca Raton, FL. Y.P. Kalra (Ed.).
19. Ishikawa S., Wagatsuma T., Ikarashi T. Rapid changes in levels of mineral nutrients in root-tip cells following short-term exposure to aluminum. Plant Soil 2003, 225:245-251.
20. Jeffries P., Gianianazzi S., Perotto S., Turnau K., Barea J.M. The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol. Fertil. Soils 2003, 37:1-16.
21. Jones D.L., Kochian L.V., Gilroy S. Aluminum induces a decrease in cytosolic calcium concentration in BY-2 tobacco cell culture. Plant Physiol. 1998, 116:81-89.
22. Kelly C.N., Morton J.B., Cumming J.R. Variation in aluminum resistance among arbuscular mycorrhizal fungi. Mycorrhiza 2005, 15:193-201.
23. Kiehl P.A., Lieth J.H., Burger D.W. Growth response of chrysanthemum to various container medium moisture tension levels. J. Am. Soc. Hortic. Sci. 1992, 114:387-392.
24. Lindberg S., Strid H. Aluminium induces rapid changes in cytosolic pH and free calcium and potassium concentrations in root protoplasts of wheat. Physiol. Planta. 1997, 99:405-414.
25. Lutts S., Kinet J.M., Bouharmont J. Changes in plant response to NaCl during development of rice varieties differing in salinity resistance. J. Exp. Bot. 1995, 46:1843-1852.
26. Lux H.B., Cumming J.R. Effect of aluminium on the growth and nutrition of tulip-poplar seedlings. Can. J. For. Res. 1999, 29:2003-2007.
27. Lux H., Cumming J. Mycorrhizae confer aluminum resistance to tulip-poplar seedlings. Can. J. For. Res. 2001, 31:694-702.
28. Ma J.F., Ryan P.R., Delhaize E. Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci. 2001, 6:273-278.
29. Macklon A.E.S., Lumsdon D.G., Sim A. Phosphate uptake and transport in Agrostis capillaris L.: effects of non-toxic levels of aluminium and the significance of P and Al speciation. J. Exp. Bot. 1994, 45:887-894.
30. Marschner H. Mineral Nutrition of Higher Plants 1995, Academic Press Limited, London, (889 p). second ed.
31. Martens D. Nitrogen cycling under different soil management systems. Adv. Agron. 2001, 70:143-189.
32. Mendoza J., Borie F. Effect of Glomus etunicatum inoculation on aluminium, phosphorus, calcium, and magnesium uptake of two barley genotypes with different aluminium tolerance. Commun. Soil Sci. Plant Anal. 1998, 29:681-695.
33. Miller R.M., Jastrow J.D. Mycorrhizal fungi influence soil structure. Arbuscular Mycorrhizas: Physiology and Function 2000, 3-18. Kluwer Academic Publication, Dordrecht, The Netherlands. Y. Kapulnik, D.D. Douds (Eds.).
34. Miransari M. Contribution of arbuscular mycorrhizal symbiosis to plant growth under different types of soil stress. Plant Biol. 2010, 12:563-569.
35. Miyasaka S.C., Habte M. Plant mechanisms and mycorrhizal symbioses to increase phosphorus uptake efficiency. Commun. Soil Sci. Plant Anal. 2001, 32:1101-1147.
36. Nawrot M., Szarejko I., Maluszynski M. Barley mutants with increased tolerance to aluminium toxicity. Euphytica 2002, 120:345-356.
37. Nichol B.E., Oliveira L.A., Class A.D.M., Siddiqi M.Y. The effects of aluminum on the influx of calcium, potassium, ammonium, nitrate, and phosphate in an aluminum sensitive cultivar of barley (Hordeum vulgare L.). Plant Physiol. 1993, 101:1263-1266.
38. Panda S.K., Baluska F., Matsumoto H. Aluminum stress signaling in plants. Plant Signal. Behav. 2009, 4:592-597.
39. Pereira L.C., de A., Mazzanti C.M., Goncalves J.F., Cargnelutti D., Tabaldi L.A., Becker A.G., Calgarto N.S., Farias J.G., Battisti V., Bohrer D., Nicoloso F.T., Morsch V.M., Schetinger M.R.C. Aluminium-induced oxidative stress in cucumber. Plant Physiol. Biochem. 2010, 48:683-689.
40. Phillips J., Hayman D. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Br. Mycol. Soc. 1970, 55:158-161.
41. Reid R.J., Tester M.A., Smith F.A. Calcium/aluminum interactions in the cell wall and plasma membrane of Chara. Planta 1995, 195:362-368.
42. Rengel Z. Disturbance of cell Ca2+ homeostasis as a primary trigger of Al toxicity syndrome. Plant Cell. Environ. 1992, 15:931-938.
43. Rengel Z., Elliott D.C. Mechanism of aluminum inhibition of net Ca2+ uptake by Amaranthus protoplasts. Plant Physiol. 1992, 98:632-638.
44. Rengel Z., Robinson D.L. Competitive A13+ inhibition of net Mg2+ uptake by intact Lolium multiflorum roots. Plant Physiol. 1989, 91:1407-1413.
45. Rillig M.C., Mummey D.L. Mycorrhizas and soil structure. New Phytol. 2006, 171:41-53.
46. Rohyadi A., Smith F.A., Murray R.S., Smith S.E. Effects of pH on mycorrhizal colonization and nutrient uptake in cowpea under conditions that minimize confounding effects of elevated available aluminium. Plant Soil 2004, 260:283-290.
47. Rouphael Y., Colla G., Battistelli A., Moscatello S., Proietti S., Rea E. Yield, water requirement, nutrient uptake and fruit quality of zucchini squash grown in soil and soilless culture. J. Hortic. Sci. Biotechnol. 2004, 79:423-430.
48. Rouphael Y., Colla G. Radiation and water use efficiencies of greenhouse zucchini squash in relation to different climate parameters. Eur. J. Agron. 2005, 23:183-194.
49. Rouphael Y., Cardarelli M., Rea E., Battistelli A., Colla G. Comparison of the subirrigation and drip-irrigation systems for greenhouse zucchini squash production using saline and non-saline nutrient solutions. Agric. Water Manage. 2006, 82:99-117.
50. Rouphael Y., Cardarelli M., Rea E., Colla G. Grafting of cucumber as a means to minimize copper toxicity. Environ. Exp. Bot. 2008, 63:49-58.
51. Rouphael Y., Cardarelli M., Di Mattia E., Tullio M., Rea E., Colla G. Enhancement of alkalinity tolerance in two cucumber genotypes inoculated with an arbuscular mycorrhizal biofertilizer containing Glomus intraradices. Biol. Fertil. Soils 2010, 46:409-509.
52. Rufyikiri G., DeClerk S., Duffey J.E., Delvaux B. Arbuscular mycorrhizal fungi might alleviate Al toxicity in banana plants. New Phytol. 2000, 148:343-352.
53. Ryan M.H., McCully M.E., Huang C.X. Location and quantification of phosphorus and other elements in fully hydrated, soil grown arbuscular mycorrhizas: a cryo-analytical scanning electron microscopy study. New Phytol. 2003, 160:429-441.
54. Ryan M.H., McCully M.E., Huang C.X. Relative amounts of soluble and insoluble forms of phosphorus and other elements in intraradical hyphae and arbuscules mycorrhizas. Funct. Plant Biol. 2007, 34:457-464.
55. Sanchez Blanco M.J., Ferrández T., Angeles Morales M., Morte A., Alarcón J.J. Variations in water status, gas exchange, and growth in Rosmarinus officinalis infected with Glomus desrticola under drought conditions. J. Plant Physiol. 2004, 161:675-682.
56. Seguel A., Medina J., Rubio R., Cornejo P., Borie F. Effects of soil aluminum on arbuscular mycorrhizal colonization of early aluminum tolerant wheat and barley cultivars. Chil. J. Agric. Res. 2012, 72:449-455.
57. Seguel A., Cumming J.R., Klugh-Stewart K., Cornejo P., Borie F. The role of arbuscular mycorrhizas in decreasing aluminium phototoxicity in acidic soils: a review. Mycorrhiza 2013, 23:167-183.
58. Silva I.R., Smyth T.J., Israel D.W., Raper C.D., Rufty T.W. Magnesium is more efficient than calcium in alleviating aluminum toxicity in soybean and its ameliorative effect is not explained by the Gouy-Chapman-Stern model. Plant Cell Physiol. 2001, 42:538-545.
59. Smith S.E., Read D.W. Mycorrhizal Symbiosis 1997, Academic Press, London. second ed.
60. SPSS SPSS 10 for Windows. Applications Guide 2001, SPSS Inc., Chicago, IL.
61. Tang C., Rengel Z. Role of plant cation/anion uptake ratio in soil acidification. Handbook of Soil Acidity 2003, 57-81. Marcel Dekker, New York, NY. Z. Rengel (Ed.).
62. Watanabe T., Okada K. Interactive effects of Al, Ca and other cations on root elongation on rice cultivars under low pH. Ann. Bot. 2005, 95:379-385.
63. Wright D.P., Scholes J.D., Read D.J. Effects of VA mycorrhizal colonization on photosynthesis and biomass production of Trifolium repens L. Plant Cell Environ. 1998, 21:209-216.
64. Zhang X.H., Zhu Y.G., Chen B.D., Lin A.J., Smith S.E., Smith F.A. Arbuscular mycorrhizal fungi contribute to the resistance of upland rice to combined metal contamination of soil. J. Plant Nutr. 2005, 28:2065-2077.
65. Zhang L., Zhang J., Christie P. Pre-inoculation with arbuscualr mycorrhizal fungi suppresses root knot nematode (Meloidogyne incognita) on cucumber (Cucumis sativus). Biol. Fertil. Soils 2008, 45:205-211.