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How Does the Use of Non-Host Plants Affect Arbuscular Mycorrhizal Communities and Levels and Nature of Glomalin in Crop Rotation Systems Established in Acid Andisols?

  • Paula AguileraEmail author
  • Fernando Borie
  • Alex Seguel
  • Pablo Cornejo
Chapter
Part of the Fungal Biology book series (FUNGBIO)

Abstract

Acidity and P deficiency are the two most serious limitations of agricultural soil productivity worldwide especially in developing countries where food production is crucial. The main negative effect is assigned to free Al where water and nutrient acquisition are severely restricted. In Chile, the acid soils, like Andisols and Ultisols, account for approximately 43% of agricultural land being cereals the main crops produced in rotation with legumes, rapeseed and lupine. These soils have high P-adsorption capacity and high Al saturation. Arbuscular mycorrhiza (AM) is a widespread symbiosis that helps plants to acquire nutrients being the most important the increase in P absorption. In addition, it has been recently suggested that AM fungi may promote Al resistance to their plant hosts through: a) the increase of root exudation of short chain organic anions with chelant capacity for Al, excluding Al at cell level; b) the increase on P root absorption and consequently increasing P/Al ratio; and c) the release of glomalin. Therefore, AM appear to confer higher Al tolerance and higher P efficiency to host plants. Nevertheless, some species belonging to these families are used by farmers in rotation systems and scarce information have been reported related to the negative effects on AM fungi.

Keywords

Al-phytotoxicity Al-tolerance AMF propagules 

Notes

Acknowledgements

Financial support of FONDECYT 11170641 (P. Aguilera), FONDECYT 1170264 (P. Cornejo), FONDECYT 11160385 (A. Seguel) and FONDECYT 1191551 (F. Borie) Grants from Comisión Nacional Científica y Tecnológica de Chile.

References

  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 Biol Biochem 43: 2427–2431CrossRefGoogle Scholar
  2. Aguilera P, Larsen J, Borie F et al (2018) New evidences on the contribution of arbuscular mycorrhizal fungi inducing Al tolerance in wheat. Rhizosphere 5: 43–50CrossRefGoogle Scholar
  3. Aguilera P, Marín C, Oehl F, Godoy R, Borie F, Cornejo P (2017) Selection of aluminum tolerant cereal genotypes strongly influences the arbuscular mycorrhizal fungal communities in an acidic Andosol. Agric Ecosyst Environm 246: 86–93CrossRefGoogle Scholar
  4. Aguilera P (2014) Diversity of arbuscular mycorrhizal fungi and their incidence in aluminum tolerance of Triticum aestivum L. growing in acidic soils with phytotoxic aluminum levels Doctoral Thesis, Universidad de La Frontera, 150 pGoogle Scholar
  5. 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. Agr Ecosyst Environ 186: 178–184CrossRefGoogle Scholar
  6. Araújo PJ, Quiquampoix H, Matumoto-Pintro PT, Staunton S (2015) Glomalin-related soil protein in French temperate forest soils: interference in the Bradford assay caused by co-extracted humic substances. Eur J Soil Sci 66: 311–319CrossRefGoogle Scholar
  7. Arihara J, Karasawa T (2000) Effect of previous crops in arbuscular mycorrhizal formation on growth of succeeding maize. Soil Sci Plant Nut 46: 43–51CrossRefGoogle Scholar
  8. Azcón-Aguilar C, Barea JM (1996) Arbuscular mycorrhizas and biological control of soil-borne plant pathogens. An overview. Mycorrhiza 6: 457–464CrossRefGoogle Scholar
  9. Borie F, Rubio R, Morales A (2008) Arbuscular mycorrhizal fungi and soil aggregation. J Soil Sci Plant Nut 8: 9–18Google Scholar
  10. Borie F, Rubio R, Curaqueo G, Cornejo P (2010) Arbuscular mycorrhizae in agricultural and forests ecosystems in Chile. J Soil Sci Plant Nut 10: 185–206Google Scholar
  11. Bullock D (1992) Crop rotation. Crit Rev Plant Sci 11: 309–326CrossRefGoogle Scholar
  12. Brundrett M (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320: 37–77CrossRefGoogle Scholar
  13. Castillo C, Borie F, Oehl F, Sieverding E (2016) Arbuscular mycorrhizal fungal biodiversity: prospecting in Southern- Central Zone of Chile. A review. J Soil Sci Plant Nut 16: 400–422Google Scholar
  14. Castillo C, Rubio R, Borie F, Sieverding E (2010) Diversity of arbuscular fungi in horticultural production systems in Souhtern Chile. J Soil Sci Plant Nut 10:407–413CrossRefGoogle Scholar
  15. 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. Sci Total Environ 406: 154–160CrossRefGoogle Scholar
  16. Cornejo P, Pérez-Tienda J, Meier S, Valderas A, Borie F, Azcón-Aguilar C, Ferrol N (2013) Copper compartmentalization in spores as survival strategy of arbuscular mycorrhizal fungi in copper-polluted environments. Soil Biol Biochem 57: 925–928CrossRefGoogle Scholar
  17. Cumming J, Ning J (2003) Arbuscular mycorrhizal fungi enhance aluminum resistance of broomsedge (Andropogon virginicus L). J Exp Bot 54: 1447–1459CrossRefGoogle Scholar
  18. Driver J, Holben W, Rillig M (2005) Characterization of glomalin as a hyphal wall component of arbuscular mycorrhizal fungi. Soil Biol Biochem 37: 101–106CrossRefGoogle Scholar
  19. Ferrufino A, Smyth T, Israel D, Carter E (2000) Root elongation of soybean genotypes in response to acidity by constraints in a subsurface solution compartment. Crop Sci 40:413–421CrossRefGoogle Scholar
  20. Fokom R, Adamou S, Teugwa MC, Begoude Boyoguenob AD, Nanaa WL, Ngonkeu MEL, Tchameni NS, Nwaga D, Tsala Ndzomo G, Amvam Zollo PH (2012). Glomalin-related soil protein, carbon, nitrogen, and soil aggregate stability as affected by land use variation in the humid forest zone of South Cameroon. Soil Till Res126: 69–75CrossRefGoogle Scholar
  21. Guillespie A, Farrel L, Walley F, Ross A, Leinweber P, Eckhardt K, Regier T, Blyth R (2011) Glomalin-related soil protein contains non-mycorrhizal related heat stable proteins, lipids and humic materials. Soil Biol Biochem 43: 766–777CrossRefGoogle Scholar
  22. Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root- induced chemical changes: a review. Plant Soil 237: 173–195CrossRefGoogle Scholar
  23. Jansa J, Mozafar A, Anken T, Ruh R, Sanders I R, Frossard E (2002) Diversity and structure of AMF communities as affected by tillage in a temperate soil. Mycorrhiza 12: 225–234CrossRefGoogle Scholar
  24. Jansa J, Mozafar A, Kuhn G, Anken T, Ruh R, Sanders R, Frossard E (2003) Soil tillage affects the community structure of mycorrhizal fungi in maize roots. Ecol Appl 13(4): 1164–1176CrossRefGoogle Scholar
  25. Javaid A (2007) Allellophatic interactions in mycorrhizal associations. Allellophaty J, 20: 29–42.Google Scholar
  26. Kabir Z (2005) Tillage or no-tillage: impact on mycorrhizae. Can J Plant Sci 85: 23–29CrossRefGoogle Scholar
  27. Kanerva S, Smolander A, Kitunen V, Ketola RA, Kotiaho T (2013) Comparison of extractants and applicability of MALDI-TOF- MS in the analysis of soil proteinaceous materials from different types of soil. Organic Geochem 56: 1–9CrossRefGoogle Scholar
  28. Karasawa T, Kasahara Y, Takebe M (2001) Variable response of growth and arbuscular mycorrhizal causing by fluctuation in the populations of indigenous arbuscular mycorrizal fungi. Soil Biol and Biochem 34: 851–857CrossRefGoogle Scholar
  29. Karasawa T, Kasahara Y, Takebe M (2002) Differences in growth responses of maize to preceding cropping caused by fluctuation in the population of indigenous arbuscular mycorrhizal fungi. Soil Biol Biochem 34(6): 851–857CrossRefGoogle Scholar
  30. Kochian L, Piñeros M, Hoekenga O (2005) How do crop plants tolerate acid soils?. Mechanisms of aluminum tolerance and phosphorus efficiency. Ann Rev Plant Biol 55: 459–493CrossRefGoogle Scholar
  31. Klironomos J, Kendrick W (1996) Palability of microfungi to soil arthropods in relation to the functioning of arbuscular mycorrhizae. Biol Fert Soils 21: 43–52CrossRefGoogle Scholar
  32. Koide R, Peoples M (2013) Behavior of Bradford-reactive substances is consistent with predictions for glomalin. Appl Soil Ecol 63: 8–14CrossRefGoogle Scholar
  33. Lambers H, Shane W, Cramer M, Pearse S, Veneklaas E (2006) Root structure and functioning for efficient acquisition of phosphorus: Matching morphological and physiological traits. Ann Bot 98: 693–213CrossRefGoogle Scholar
  34. Lambers H, Teste F (2013) Interactions between arbuscular mycorrhizal and non-mycorrhizal plants: do mycorrhizal species at both extremes of plant availability play the same play. Plant Cell Environ 36: 1911–1919PubMedGoogle Scholar
  35. Lavaud C, Voutquenne L, Bal P, Pouny I (2000) Saponins from Chenopodium album. Fitoterapia 71: 338–340CrossRefGoogle Scholar
  36. Leake J, Jhonson D, Donnelly D, Muckle G, Boddy L, Read D (2004) Netwoks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agrosystem functioning. Can J Bot 82: 1016–1045CrossRefGoogle Scholar
  37. Lenoir I, Fontaine J, Sahraoui A (2016) Arbuscular mycorrhizal fungal responses to abiotic stresses: a review. Phytochemistry 123: 4–15CrossRefGoogle Scholar
  38. Lovelock C, Right S, Clark D, Ruess R (2004) Soil stocks of glomalin produced by arbuscular mycorrhizal fungi across a tropical rain forest landscape. J Ecol 92: 278–287CrossRefGoogle Scholar
  39. Lupwayi N, Rice W, Clayton G (1998) Soil microbial diversity and community structure under wheat as influenced by tillage and crop rotation. Soil Biol Biochem 30: 1733–1741CrossRefGoogle Scholar
  40. Meier S, Borie F, Curaqueo G, Bolan N, Cornejo P (2012) Effects of arbuscular mycorrhizal inoculation on methallophyte and agricultural plants growing at increasing copper levels. Appl Soil Ecol 61: 280–287CrossRefGoogle Scholar
  41. Miransari M (2011) Hiperaccumulators, arbuscular mycorrhizal fungal and stress of heavy metals. Biothec Adv 29: 645–653CrossRefGoogle Scholar
  42. Navarro-Noya YE, Gómez-Acata S, Montoya-Ciriaco N, Rojas-Valdez A, Suárez-Arriaga MC, Valenzuela-Encinas C, Jiménez-Bueno N, Verhulst N, Govaerts B, Dendooven L (2013) Relative impacts of tillage, residue management and crop-rotation on soil bacterial communities in a semi-arid agroecosystem. Soil Biol Biochem 65:86–95CrossRefGoogle Scholar
  43. Oehl F, Laczko E, Bogenrieder A, Stahr K, Bösch R, van der Heijden M, Sieverding E (2010) Soil type and land use intensity determine the composition of arbuscular mycorrhizal fungal communities. Soil Biol Biochem 42: 724–738CrossRefGoogle Scholar
  44. Öpik M, Moora M, Liira J, Zobel M (2006) Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. J Ecol 94: 778–790CrossRefGoogle Scholar
  45. Potsma-Blaauw M, de Goede R, Bloem J, Faber J, Brussaard L (2010) Soil biota community structure and abundance under agricultural intensification and extensification. Ecology 91: 460–463CrossRefGoogle Scholar
  46. Purin S, Rillig M (2007) The arbuscular mycorrhizal fungal protein glomalin: limitations, progress, and a new hypothesis for its function. Pedobiologia 51: 123–130CrossRefGoogle Scholar
  47. Qiang-Sheng W, Ming-Qin C, Ying-Ning Z, Xin Hua H (2014) Direct and indirect effects of glomalin, mycorrhizal hyphae, and roots on aggregate stability in rhizosphere of trifoliate orange. Nature DOI: https://doi.org/10.1038/srep05823.
  48. Richardson A, Lynch E, Jonathan P, Delhaize E, Smith F, Smith S, Harvey P, Ryan M, Veneklaas E, Lambers H, Oberson A, Culbernor R, Simpon R (2011) Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant Soil 349: 121–156CrossRefGoogle Scholar
  49. Rillig M, Mummey D (2006) Mycorrhizas and soil structure. New Phytol 171: 41–53CrossRefGoogle Scholar
  50. Rillig M (2004) Arbuscular mycorrhizae, glomalin and soil aggregation. Can J Soil Sci 84: 355–363CrossRefGoogle Scholar
  51. Rillig M, Ramsey P, Morris S, Paul E (2003). Glomalin, an arbuscular mycorrhizal fungal soil protein, responds to land-use change. Plant Soil 253: 293–299CrossRefGoogle Scholar
  52. Rosier C, Hoye A, Rillig M (2006) Glomalin-related soil protein: assessment of current detection and quantification tools. Soil Biol Biochem 38: 2205–2211CrossRefGoogle Scholar
  53. Ryan P, Delhaize E, Jones L (2001) Function and mechanisms of organic anion exudation from plant roots. Annual Review of Plant Physiology Plant Molecular Biology 52: 527–560CrossRefGoogle Scholar
  54. Schindler F, Mercer E, Rice J (2007) Chemical characteristics of glomalin-related soil protein (GRSP) extracted from soils of varying organic matter content. Soil Biol Biochem 39: 320–329CrossRefGoogle Scholar
  55. Schreiner R, Koide R (1993) Antifungal compounds from the root of mycothrophic and non-mycothrophic plant species. New Phytol 123: 99–105CrossRefGoogle Scholar
  56. Seguel A, Rubio R, Carrillo R, Borie F (2008) Levels of glomalin and their relation with soil chemical and soil and biological soil characteristics in a relict of native forest of Southern Chile. Bosque 29: 11–22CrossRefGoogle Scholar
  57. Seguel A, Cumming J, Klug-Stewart K, Cornejo P, Borie F (2013) The role of arbuscular mycorrhizas in decreasing aluminium phytotoxicity in acidic soils: a review. Mycorrhiza 23: 167–183CrossRefGoogle Scholar
  58. Seguel A, Cumming J, Cornejo P, Borie F (2016) Aluminum tolerance of wheat cultivars in a non-limed and limed Andisol. Appl Soil Ecol 108: 228–237CrossRefGoogle Scholar
  59. Seguel A, Cornejo, Ramos A, von Baer E, Cumming J, Borie F (2017) Phosphorus acquisition by three wheat cultivars contrasting in aluminum tolerance growing in an aluminum-rich Andisol. Crop Pasture Sci 68: 315–316CrossRefGoogle Scholar
  60. Smith S, Read D (2008) Mycorrhizal symbiosis. Cambridge, UK: Academic Press.Google Scholar
  61. Smith S, Smith F (2013) How useful is the mutualism-parasitism continuum of arbuscular mycorrhizas functioning?. Plant Soil 349: 121–156Google Scholar
  62. Smith R, Gross K, Robertson G (2008) Effects on crop diversity on agroecosystem function. Ecosystems 11: 355–366CrossRefGoogle Scholar
  63. Tiemann L, Grandy A, Atkinson, Marin E, McDaniel M (2015) Crop rotational diversity enhances belowground communities and function in an agroecosystem. Ecol Lett 18: 761–771CrossRefGoogle Scholar
  64. Torrecillas E, Alguacil M, Roldan A (2012) Host preferences of arbuscular mycorrhizal fungi colonizing annual herbaceous plant species in semiarid Mediterranean prairies. Appl Environ Microbiol 78: 6180–6186CrossRefGoogle Scholar
  65. Treseder K, Turner K (2007) Glomalin in ecosystems. Soil Science Society of America Journal 71: 1257–1266CrossRefGoogle Scholar
  66. Valetti L, Iriarte L, Fabra A (2016) Effect of previous cropping of rapeseed (Brassica napus L) on soybean (Glycine max) root mycorrhization, nodulation and plant growth. Eur J Soil Biol 76: 103–106CrossRefGoogle Scholar
  67. van der Heijden M, Bardgett R, van Straalen N (2008) The unseen majority: Soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11: 296–310CrossRefGoogle Scholar
  68. van der Heijden M, Klironomos J, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396: 69–72CrossRefGoogle Scholar
  69. Verbruggen E, Röling W, Gamper H, Kowalchuk G, Verhoef H, van der Heijden M (2010) Positive effects of organic farming on below- groundmutualists: large-scale comparison of mycorrhizal fungal communities in agricultural soils. New Phytol 186: 968–979CrossRefGoogle Scholar
  70. Villagarcia M, Thomas E, Carter J (2001) Genotypic rankings for aluminum tolarnace of soybean roots grown in hydroponics and sand cultura. Crop Sci 41: 1499–1507CrossRefGoogle Scholar
  71. Wang Q, Wu Y, Wang W, Zhong Z, Pei Z, Ren J, Wang H, Zu Y (2014) Spacial variations in concentration, compositions of glomalin related soil protein in poplar plantations in Northeastern China, and possible relations with soil physicochemical properties. The Scientific World Journal Volume 2014, Article ID 160403, 13 pagesGoogle Scholar
  72. Wang Q, Wang W, He X (2015) Role and variation of the amount and composition of glomalin in soil properties in farmland and adjacent plantations with reference to a primary forest in North-Eastern China. PLoS One DOI:  https://doi.org/10.1371/journal.pone.01 39623. October 2, 2015 (19 pages)
  73. Wardle D, Bardgett R, Klironomos J (2004) Ecological linkages between aboveground and belowground biota. Science, 304 (5677): 1629–1633CrossRefGoogle Scholar
  74. Wagg C, Franz Bender S, Widmer F (2014) Soil biodiversity and soil community composition determines ecosystem multifunctionality. Pro. Natl Acad. Si USA 111: 5266–5670.CrossRefGoogle Scholar
  75. Whiffen L, Midley D, Mc Gee P (2007) Polyphenolic compounds interfere with quantification of protein extracts using the Bradford method. Soil Biol Biochem 39: 691–694CrossRefGoogle Scholar
  76. Wright S, Upadhyaya A (1996) Extraction of an abundant and unusual protein from soil and comparison with hyphal protein of arbuscular mycorrhizal fungi. Soil Sci 161: 575–586CrossRefGoogle Scholar
  77. Wright S, Upadhyaya A (1998) A survey of soils fro aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi. Plant Soil 198: 97–107CrossRefGoogle Scholar
  78. Woignier T, Etcheverria P, Borie F (2014) Role of allophanes in the accumulation of glomalin-related soil protein in tropical soils (Martinique, French West Indes) Eur J Soil Sci 65: 531–538CrossRefGoogle Scholar
  79. Yin C, Jones L, Peterson D et al (2011) Members of soil bacterial communities sensitive to tillage and crop rotation. Soil Biol Biochem 42: 2111–2118CrossRefGoogle Scholar
  80. Zhang J, Tang X, Zhong S (2017) Recalcitrant carbon components in glomalin-related soil protein facilitate soil organic carbon preservation in tropical forests. Nature  https://doi.org/10.1038/s41598-017-02486-6

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Paula Aguilera
    • 1
    Email author
  • Fernando Borie
    • 1
    • 2
  • Alex Seguel
    • 1
  • Pablo Cornejo
    • 1
  1. 1.Scientific and Technological Bioresources Nucleus (BIOREN-UFRO), Centro de Investigación en Micorrizas y Sustentabilidad Agroambiental (CIMYSA-UFRO)Universidad la FronteraTemucoChile
  2. 2.Facultad de Recursos NaturalesUniversidad Católica de TemucoTemucoChile

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