Role of arbuscular mycorrhizal symbiosis in phosphorus-uptake efficiency and aluminium tolerance in barley growing in acid soils

Crop and Pasture Science

Volumn 66, Issue 7, 2015, Pages 696-705

  Seguel, Alex ^a   Barea, José Miguel ^b   Cornejo, Pablo ^a   Borie, Fernando ^a  

^a UNIVERSIDAD DE LA FRONTERA   (Chile)

^b CSIC   (Spain)

Author keywords

Al tolerant barley cultivars; Arbuscular mycorrhizae; Glomalin related soil protein; Liming; P uptake efficiency

Indexed keywords

ACID SOIL; ARBUSCULAR MYCORRHIZA; BARLEY; COLONIZATION; CULTIVAR; GROWTH RESPONSE; LIMING; PHOSPHORUS CYCLE; PHYTOTOXICITY; POLLUTION TOLERANCE; SOIL QUALITY; SYMBIOSIS;

FUNGI; HORDEUM; HORDEUM VULGARE; HORDEUM VULGARE SUBSP. VULGARE;

EID: 84933041080     PISSN: 18360947     EISSN: 18365795     Source Type: Journal    
DOI: 10.1071/CP14305     Document Type: Article

References (57)

1. Aguilera P, Borie F, Seguel A, Cornejo P (2011) Fluorescence detection of aluminum in arbuscular mycorrhizal fungal structures and glomalin using confocal laser scanning microscopy. Soil Biology & Biochemistry 43, 2427-2431. doi:10.1016/j.soilbio.2011.09.001
2. Aguilera P, Cornejo P, Borie F, Barea JM, von Baer E, Oehl F (2014) Diversity of arbuscular mycorrhizal fungi associated with Triticum aestivum L. plants growing in an Andosol with high aluminum level. Agriculture, Ecosystems and Environment Journal 186, 178-184. doi:10.1016/j.agee.2014.01.029
3. Ashen J, Goff L (2000) Molecular and ecological evidence for species specificity and coevolution in a group of marine algal-bacterial symbiosis. Applied and Environmental Microbiology 66, 3024-3030. doi:10.1128/AEM.66.7.3024-3030.2000
4. Avio L, Cristani C, Giovannetti SP (2009) Genetic and phenotypic diversity of geographically different isolates of Glomus mosseae. Canadian Journal of Microbiology 55, 242-253. doi:10.1139/W08-129
5. Barriga P, Fuentealba J, Manquian N (1998) Capacidad de absorción y utilización del fósforo en genotipos de trigo. Agro sur 26, 1-10. doi:10.4206/agrosur.1998.v26n1-01
6. Bedini S, Avio L, Argese E, Giovannetti M (2007) Effects of long-term land use on arbuscular mycorrhizal fungi and glomalin-related soil protein. Agriculture, Ecosystems and Environment Journal 120, 463-466. doi:10.1016/j.agee.2006.09.010
7. Bever JD, Schultz P, Pringle A, Morton J (2001) Arbuscular mycorrhizal fungi: more diverse than meets the eye, and the ecological tale of why. Bioscience 51, 923-931. doi:10.1641/0006-3568(2001)051[0923:AMFMDT]2.0.CO;2
8. Bona L, Wright RJ, Baligar BC (1991) A rapid method for screening cereals for acid soil tolerance. Cereal Research Communications 19, 465-468.
9. Borie F, Rubio R (1999) Effects of arbuscular mycorrhizae and liming on growth and mineral acquisition of Al-tolerant barley cultivars. Journal of Plant Nutrition 22, 121-137. doi:10.1080/01904169909365612
10. Chen RF, Zhang FL, Zhang KM, Sun QB, Dong XY, Shen RF (2012) Aluminium-phosphorus interactions in plant growing on acid soils: does phosphorus always alleviate aluminium toxicity. Journal of the Science of Food and Agriculture 92, 995-1000. doi:10.1002/jsfa.4566
11. CIREN (2002) 'Descripciones de suelos. Materiales y símbolos.' Estudio agrologico IX region. Publicacion CIREN No. 122. p. 360. (Centro de Información de Recursos Naturales (CIREN): Santiago, Chile)
12. Cornejo P, Meier S, Borie G, Rillig M, Borie F (2008) Glomalin-related soil protein in a Mediterranean ecosystem affected by a copper smelter and its contribution to Cu and Zn sequestration. The Science of the Total Environment 406, 154-160. doi:10.1016/j.scitotenv.2008.07.045
13. Dai H, Zhao J, Ahmed IM, Cao F, Chen ZN, Zhang G, Li C, Wu F (2014) Differences in physiological features associated with aluminum tolerance in Tibetan wild and cultivated barleys. Plant Physiology and Biochemistry 75, 36-44. doi:10.1016/j.plaphy.2013.11.025
14. Darkó E, Ambrus H, Stefanovits Banyai E, Fodor J, Bakos F, Barnabas B (2004) Aluminium toxicity, Al tolerance and oxidative stress in an Al-sensitive wheat genotype and in Al-tolerant lines developed by in vitro microspore selection.Plant Science166, 583-591. doi:10.1016/j.plantsci. 2003.10.023
15. Dawood M, Cao F, Jahangir MM, Zhang G, Wu F (2012) Alleviation of aluminum toxicity by hydrogen sulfide is related to elevated ATPase, and suppressed aluminum uptake and oxidative stress in barley. Journal of Hazardous Materials 209-210, 121-128. doi:10.1016/j.jhazmat. 2011.12.076
16. Delhaize E, Gruber BD, Ryan PR (2007) The roles of organic anion permeases in aluminium resistance and mineral nutrition. FEBS Letters 581, 2255-2262. doi:10.1016/j.febslet.2007.03.057
17. Dudhane M, Borde M, Kaur P (2012) Effect of aluminium toxicity on growth responses and antioxidant activities in Gmelina arborea Roxb. inoculated with AM fungi. International Journal of Phytoremediation 14, 643-655. doi:10.1080/15226514.2011.619230
18. Gardner FP, Pearce RB, Mitchell RL (1985) 'Physiology of crop plants.' pp. 187-208. (Iowa State University Press: Ames, IA, USA)
19. Garg N, Chandel S (2010) Arbuscular mycorrhizal networks: process and functions. A review. Agronomy for Sustainable Development 30, 581-599. doi:10.1051/agro/2009054
20. Gil-Cardeza ML, Ferri A, Cornejo P, Gomez E (2014) Distribution of chromium species in a Cr-polluted soil: presence of Cr(III) in glomalin related protein fraction. The Science of the Total Environment 493, 828-833. doi:10.1016/j.scitotenv.2014.06.080
21. Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytologist 84, 489-500. doi:10.1111/j.1469-8137.1980.tb04556.x
22. Gómez-Paccard C, Mariscal-Sancho I, León P, Benito M, González P, Ordóñez R, Espejo R, Hontoria C (2013) Ca-amendment and tillage: Medium term synergies for improving key soil properties of acid soils. Soil & Tillage Research 134, 195-206. doi:10.1016/j.still.2013.08.009
23. Gruber BD, Ryan PR, Richardson AE, Tyerman SD, Ramesh S, Hebb DM, Howitt SM, Delhaize E (2010) HvALMT1 from barley is involved in the transport of organic anions. Journal of Experimental Botany 61, 1455-1467. doi:10.1093/jxb/erq023
24. Guo TR, Zhang GP, Zhou MX, Wu FB, Chen JX (2004) Effect of aluminium and cadmium toxicity on growth and antioxidant enzyme activities of two barley genotypes with different Al resistance. Plant and Soil 258, 241-248.
25. Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Annals of Microbiology 60, 579-598. doi:10.1007/s13213-010-0117-1
26. Jones GPD, Jessop RS, Beair GJ (1992) Alternative methods for the selection of phosphorus efficiency in wheat. Field Crops Research 30, 29-40. doi:10.1016/0378-4290(92)90054-D
27. Jones DL, Blancaflor EB, Kochian LV, Gilroy S (2006) Spatial coordination of aluminum uptake, production of reactive oxygen species, callosa production and wall rigidification in maize roots. Plant, Cell & Environment 29, 1309-1318. doi:10.1111/j.1365-3040.2006.01509.x
28. Klugh KR, Cumming JR (2007) Variations in organic acid exudation and aluminum resistance among arbuscular mycorrhizal species colonizing Liriodendron tulipifera. Tree Physiology 27, 1103-1112. doi:10.1093/ treephys/27.8.1103
29. Klugh-Stewart K, Cumming JR (2009) Organic acid exudation by mycorrhizal Andropogon virginicus L. (broomsedge) roots in response to aluminum. Soil Biology & Biochemistry 41, 367-373. doi:10.1016/ j.soilbio.2008.11.013
30. Kochian LV, Hoekenga OA, Piñeros MA (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annual Review of Plant Biology 55, 459-493. doi:10.1146/ annurev.arplant.55.031903.141655
31. Liang C, Piñeros MA, Tian J, Yao Z, Sun L, Liu J, Shaff J, Coluccio A, Kochian LV, Liao H (2013) Low pH, aluminum, and phosphorus coordinately regulate malate exudation through GmALMT1 to improve soybean adaptation to acid soils. Plant Physiology 161, 1347-1361. doi:10.1104/pp.112.208934
32. Liao H, Wan H, Shaff J, Wang X, Yan X, Kochian LV (2006) Phosphorus and aluminum interactions in soybean in relation to aluminum tolerance: exudation of specific organic acids from different regions of the intact root system. Plant Physiology 141, 674-684. doi:10.1104/ pp.105.076497
33. Lux HB, Cumming JR (2001) Mycorrhizae confer aluminum resistance to tulip-poplar seedlings. Canadian Journal of Forest Research 31, 694-702. doi:10.1139/cjfr-31-4-694
34. Marschner H (1995) 'Mineral nutrition of higher plants.' 2nd edn (Academic Press, Inc.: San Diego, CA, USA)
35. Miranda D, Fischer G, Ulrichs C (2011) The influence of arbuscular mycorrhizal colonization on the growth parameters of cape gooseberry (Physalis peruviana l.) plants grown in a saline soil. Journal of Soil Science and Plant Nutrition 11, 18-30. doi:10.4067/S0718-9516201100 0200003
36. Miransari M (2010) Contribution of arbuscular mycorrhizal symbiosis to plant growth under different types of soil stress. Plant Biology 12, 563-569.
37. Moore JD, Camire C, Ouimet R (2000) Effects of liming on the nutrition, vigor, and growth of sugar maple at the Lake Clair Watershed, Quebec, Canada.Canadian Journal of Forest Research30, 725-732. doi:10.1139/ x00-009
38. Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society 55, 158-161. doi:10.1016/S0007-1536(70)80110-3
39. Pigna M, Caporale AG, Cartes P, Cozzolino V, Mora ML, Sommella A, Violante A (2014) Effects of arbuscular mycorrhizal inoculation and phosphorus fertilization on the growth of escarole (Cichorium endivia L.) in an arsenic polluted soil. Journal of Soil Science and Plant Nutrition 14, 199-209.
40. Richardson A, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability. Plant Physiology 156, 989-996. doi:10.1104/ pp.111.175448
41. Richardson A, Barea JM, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant and Soil 321, 305-339. doi:10.1007/s11104-009-9895-2
42. Rillig MC (2004) Arbuscular mycorrhizae, glomalin and soil quality. Canadian Journal of Soil Science 84, 355-363. doi:10.4141/S04-003
43. Rillig M, Mummey D (2006) Mycorrhizas and soil structure.New Phytologist 171, 41-53. doi:10.1111/j.1469-8137.2006.01750.x
44. Rubio R, Borie F, Schalchli C, Castillo C, Azcón R (2003) Occurrence and effect of arbuscular mycorrhizal propagules in wheat as affected by the source and amount of phosphorus fertilizer and fungal inoculation. Applied Soil Ecology 23, 245-255. doi:10.1016/S0929-1393(03) 00045-3
45. Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annual Review of Plant Physiology and Plant Molecular Biology 52, 527-560. doi:10.1146/annurev. arplant.52.1.527
46. Seguel A, Medina J, Rubio R, Cornejo P, Borie F (2012) Effects of soil aluminum on early arbuscular mycorrhizal colonization of aluminum tolerant wheat and barley cultivars. Chilean Journal of Agricultural Research 72, 449-455. doi:10.4067/S0718-58392012000300022
47. Seguel A, Cumming J, Klugh-Stewart K, Cornejo P, 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
48. Sieverding E (1991) Vesicular-arbuscular mycorrhiza management in tropical agrosystems. Report No. 224. Deustche Gesellschaft für Technische Zusammenarbeit (GTZ), Eschborn, Germany.
49. Sumner ME, Noble AD (2003) Soil acidification: The world story. In 'Handbook of soil acidity'. (Ed. Z Rengel) pp. 1-28. (Marcel Dekker: New York)
50. Tang C, Rengel Z (2003) Role of plant cation/anion uptake ratio in soil acidification. In 'Handbook of soil acidity'. (Ed. Z Rengel) pp. 57-81. (Marcel Dekker: New York)
51. Tanwar A, Aggarwal A, Kadian N, Gupta A (2013) Arbuscular mycorrhizal inoculation and super phosphate application influence plant growth and yield of Capsicum annuum. Journal of Soil Science and Plant Nutrition 13, 55-66.
52. Tennant D (1975) A test of a modified line intersect method of estimating root length. Journal of Ecology 63, 995-1001. doi:10.2307/2258617
53. Wang J, Raman H, Zhou M, Ryan PR, Delhaize E, Hebb DM, Coombes N, Mendham N (2007) High-resolution mapping of the Alp locus and identification of a candidate gene HvMATE controlling aluminium tolerance in barley (Hordeum vulgare L.). Theoretical and Applied Genetics 115, 265-276. doi:10.1007/s00122-007-0562-9
54. Wright SF, Upadhyaya A (1998) A survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi. Plant and Soil 198, 97-107. doi:10.1023/A:1004347701584
55. Zagal E, Sadzawka A (2007) 'Protocolo de métodos de análisis para suelos y lodos.' (Universidad de Concepción, Servicio Agrícola y Ganadero: Santiago, Chile)
56. Zhao ZQ, Ma JF, Sato K, Takeda K (2003) Differential Al resistance and citrate secretion in barley (Hordeum vulgare L.). Planta 217, 794-800. doi:10.1007/s00425-003-1043-2
57. Zhou G, Pereira J, Delhaize E, Zhou M, Magalhaes J, Ryan P (2014) Enhancing the aluminium tolerance of barley by expressing the citrate transporter genes SbMATE and FRD3. Journal of Experimental Botany 65, 2381-2390. doi:10.1093/jxb/eru121