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Arbuscular Mycorrhizal Symbiosis in Salt-Tolerance Species and Halophytes Growing in Salt-Affected Soils of South America

  • Alejandra G. BecerraEmail author
  • M. Noelia Cofré
  • Ileana García
Chapter
Part of the Fungal Biology book series (FUNGBIO)

Abstract

Arbuscular mycorrhizal fungi (AMF) are ubiquitous soil microorganisms that establish a direct physical link between soil and plant roots constituting an integral component of the natural ecosystems being present in saline environment. These fungi are associated with the roots of over 80% terrestrial plant species including halophytes. Compared with other parts of the world, published information on halophytes vegetation adapted to saline environments in South America, and even more so on their utilization, is quite scarce. This work showed the mycorrhizal status of halophytes and salt-tolerance species capable of growing in salty soils, used as a forage resource for livestock. Specially we made a focus in two saline soils of Argentinean Pampas and Salinas Grandes dominated by Lotus tenuis and members of Chenopodiaceae family respectively. This data is of relevance because they often constitute the only forage resource for the possible way to utilize these plants to remediate salt-affected soils.

Keywords

Argentina pampas Halophytes and feedstuff Mycorrhizal fungi Salinity Salinas Grandes 

Notes

Acknowledgments

This work was financially supported by Secretaría de Ciencia y Técnica - Universidad Nacional de Córdoba, Agencia de Promoción Científica y Tecnológica (PICT 438-2006) and CONICET (PIP0950). All authors are researchers from CONICET.

References

  1. Abril A, Aiazzi M, Torres P, Argüello J (2000) Nutritional value of Atriplex cordobensis grown in dry Chaco of Argentina. Rev Arg Prod An 20(3–4):179–185Google Scholar
  2. Aiazzi M, Abril A, Torres P, Di Rienzo J, Argüello J (1999) Seasonal variations in chemical composition of leaves and stems of Atriplex cordobensis (Gandoger et Stuckert), female and male plants. Phyton 65:173–178Google Scholar
  3. Al-Karaki GN (2000) Growth of mycorrhizal tomato and mineral acquisition under salt stress. Mycorrhiza 10:51–54CrossRefGoogle Scholar
  4. Al-Karaki GN (2006) Nursery inoculation of tomato with arbuscular mycorrhizal fungi and subsequent performance under irrigation with saline water. Sci Hort 109:1–7CrossRefGoogle Scholar
  5. Al-Karaki GN, Hammad R, Rusan M (2001) Response of two tomato cultivars differing in salt tolerance to inoculation with mycorrhizal fungi under salt stress. Mycorrhiza 11:43–47CrossRefGoogle Scholar
  6. Allen MF (1983) Formation of vesicular-arbuscular mycorrhizae in Atriplex gardneri (Chenopodiaceae): seasonal response in a cold desert. Mycologia 75:773–776CrossRefGoogle Scholar
  7. Allen MF, Allen EB (1990). Carbon source of VA mycorrhizal fungi associated with Chenopodiaceae from a semiarid shrub steppe. Ecology 71:2019–2021CrossRefGoogle Scholar
  8. AQUASTAT (1997) Tablas resumen para America Latina y el Caribe. FAO. http://www.fao.org/GEO-2-199
  9. Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42CrossRefGoogle Scholar
  10. Bandera R (2013) Rehabilitación de suelos salino-sódicos: evaluación de enmiendas y de especies forrajeras. Tesis presentada para optar al título de Magíster de la Universidad de Buenos Aires, Área Recursos Naturales, p 66Google Scholar
  11. Becerra A, Bartoloni J, Cofré N, Soteras F, Cabello M (2014) Arbuscular mycorrhizal fungi in saline soils: vertical distribution at different soil depths. Braz J Microbiol 45:585–594PubMedPubMedCentralCrossRefGoogle Scholar
  12. Becerra A, Bartolini N, Cofré N, Soteras F, Cabello M (2016) Hongos micorrícico-arbusculares asociados a ambientes salinos de Córdoba. Bol Soc Arg Bot 51(1):5–13CrossRefGoogle Scholar
  13. Bothe H (2012) Arbuscular mycorrhiza and salt tolerance of plants. Symbiosis 58:1–3CrossRefGoogle Scholar
  14. Brevedan RE, Fernández OA, Villamil CB (1994) Halophytes as a resource for livestock husbandry in South America. In: Squires VR, Ayoub AT (eds) Halophytes as a Resource for Livestock and for Rehabilitation of Degraded Lands. Kluwer Acad Publ, Dordrecht, p 175–199CrossRefGoogle Scholar
  15. Brevedan RE, Fernández OA, Fioretti M, Baioni S, Busso CA, Laborde H (2016) Halophytes and Salt Tolerant Crops as a Forage Source for Livestock in South America. In: El Shaer HM, Squires VR (eds) Halophytic and Salt-Tolerant Feedstuffs Impacts on Nutrition, Physiology and Reproduction of Livestock. CRC Press. Taylor & Francis Group, Boca Ratón, p 60–78Google Scholar
  16. Cabido M, Zak M (1999). Vegetación del Norte de Córdoba, Secretaría de Agricultura, Ganadería y Recursos Renovables de Córdoba, Córdoba, ArgentinaGoogle Scholar
  17. Cantrell IC, Linderman RG (2001) Preinoculation of lettuce and onion with VA mycorrhizal fungi reduces deleterious effects of soil salinity. Plant Soil 233:269–281CrossRefGoogle Scholar
  18. Carvalho LM, Cacados I, Martiris-Loucao MA (2001) Temporal and spatial variation of arbuscular mycorrhizas in salt marsh plants of Tagus estuary (Portugal). Mycorrhiza 11:303–309PubMedCrossRefGoogle Scholar
  19. Cavagnaro RA, Oyarzabal M, Oesterheld M, Grimoldi AA (2014) Dinámica de crecimiento de gramíneas C3 y C4 en respuesta a las micorrizas y a la disponibilidad de fósforo. Lilloa 51 (Supl): 164Google Scholar
  20. Cofré MN, Becerra AG, Domínguez LS (2007) Micorrizas en Atriplex argentina, una especie nativa forrajera de las Salinas Grandes de Córdoba. In: III Jornadas Nacionales de Flora Nativa y IV Encuentro de Cactáceas. Córdoba, Argentina. ISBN 978-987.510-079-4, p 209–217Google Scholar
  21. Cofré N, Becerra A, Nouhra E, Soteras F (2012) Arbuscular mycorrhizae and dark-septate endophytes on Atriplex cordobensis in saline sites from Argentina. J Agric Tech 87(7):2201–2214Google Scholar
  22. da Silva Sousa C, Rômulo Simões CM, Valadares de Sá Barreto Sampaio E, de Sousa Lima F, Fritz O, Costa Maia L (2013) Arbuscular mycorrhizal fungi within agroforestry and traditional land use systems in semi-arid Northeast Brazil. Acta Scientiarum 35(3):307–314Google Scholar
  23. Daleo P, Alberti J, Canepuccia A, Escapa M, Fanjul E, Silliman BR, Bertness MD, Iribarne O (2008) Mycorrhizal fungi determine salt-marsh plant zonation depending on nutrient supply. J Ecol 96:431–437CrossRefGoogle Scholar
  24. Di Bárbaro G, Espeche E, Manenti L, Rizo M, Andrada H, Viale S, Batallán Morales S (2018) Asociaciones micorrícicas entre hongos nativos y plantas forrajeras cultivadas en el valle central de Catamarca. 1° Jornadas de divulgación científica y técnica Facultad de Ciencias Agrarias Universidad Nacional de Catamarca, ISBN 978-987-661-299-9, p 19–20Google Scholar
  25. Di Bella CE, Rodríguez AM, Jacobo E, Golluscio RA, Taboada MA (2015) Impact of cattle grazing on temperate coastal salt marsh soils. Soil Use Manag 31:299–307CrossRefGoogle Scholar
  26. Druille M, Cabello MN, García Parisi PA, Golluscio RA, Omacini M (2015) Glyphosate vulnerability explains changes in root-symbionts propagules viability in pampean grasslands. Agric Ecos Env 202:48–55CrossRefGoogle Scholar
  27. Dudal R, Purnell MF (1986) Land Resources: salt affected soils. Reclamation and Revegetation Res 5:1–9Google Scholar
  28. El Shaer H (2010) Halophytes and salt-tolerant plants as potential forage for ruminants in the Near East region. Small Rum Res 91:3–12CrossRefGoogle Scholar
  29. Escudero VG, Mendoza RE (2005) Seasonal variation of arbuscular mycorrhizal fungi in temperate grasslands along a wide hydrologic gradient. Mycorrhiza 15:291–299CrossRefGoogle Scholar
  30. Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280PubMedPubMedCentralCrossRefGoogle Scholar
  31. Evelin H, Giri B, Kapoor R (2013) Ultrastructural evidence for AMF mediated salt stress mitigation in Trigonella foenum-graecum. Mycorrhiza 23:71–86PubMedCrossRefGoogle Scholar
  32. FAO (2015) Status of the World’s report resources. Main Report, p 364–398Google Scholar
  33. FAO-UNESCO (1974) Soil Map f the World. 1: 5 000 000. Volume I. Legend. United Nations Educational, Scientific and Cultural Organization, Paris, pp 59Google Scholar
  34. FAO-UNESCO (1971) Soil Map f the World. 1: 5 000 000. Volume IV South America. United Nations Educational, Scientific and Cultural Organization, Paris, pp 193Google Scholar
  35. Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963CrossRefGoogle Scholar
  36. Fontenla S, Puntieri J, Ocampo JA (2001a) Mycorrhizal associations in the Patagonian steppe, Argentina. Plant Soil 233:13–29CrossRefGoogle Scholar
  37. Fontenla S, Chaia E, Bustos C, Pelliza A (2001b) Microorganismos simbióticos en Atriplex. XXVIII Jornadas Argentinas de Botánica, La Pampa, Argentina. Bol Soc Arg Bot 36:114Google Scholar
  38. Fracchia S, Aranda A, Gopar A, Silvani V, Fernandez L, Godeas A (2009) Mycorrhizal status of plant species in the Chaco Serrano Woodland from central Argentina. Mycorrhiza 19:205–214CrossRefGoogle Scholar
  39. García I, Mendoza RE (2007) Arbuscular mycorrhizal fungi and plant symbiosis in a saline-sodic soil. Mycorrhiza 17:167–174PubMedCrossRefGoogle Scholar
  40. García I, Mendoza RE (2008) Relationships among soil properties, plant nutrition and arbuscular mycorrhizal fungi-plant symbioses in a temperate grassland along hydrologic, saline and sodic gradients. FEMS Microbiol Ecol 63:359–71PubMedCrossRefGoogle Scholar
  41. García I, Cabello M, Fernández-López C, Chippano T, Mendoza R (2017) Hongos micorrícicos arbusculares en asociación con Lotus tenuis en ambientes halomórficos de la Cuenca del río Salado. CONEBIOS V Ecología y Biología de Suelos. ISBN 978-987-3941-39-9. Buenos Aires. ArgentinaGoogle Scholar
  42. Gerdemann JW (1968) Vesicular arbuscular mycorrhiza and plant growth. Ann Rev Phytopatol 6:397–418CrossRefGoogle Scholar
  43. Giri B, Kapoor R, Mukerji KG (2003) Influence of arbuscular mycorrhizal fungi and salinity on growth, biomass, and mineral nutrition of Acacia auriculiformis. Biol Fertil Soils 38:170–175CrossRefGoogle Scholar
  44. Grigera G, Oesterheld M (2004) Mycorrhizal colonization patterns under contrasting grazing and topographic conditions in flooding Pampa (Argentina). Rang Ecol Manag 57:601–605Google Scholar
  45. Hack CM, Porta M, Tomei CE, Grimoldi AA (2009) Inoculación con hongos micorrícicos arbusculares y fertilización fosfatada en Melilotus alba. Comunicaciones Científicas y Tecnológicas. Universidad Nacional del Nordeste. CA-009Google Scholar
  46. Harley JL, Harley EL (1987) A check-list of mycorrhiza in the British flora. New Phytol 105:1–102CrossRefGoogle Scholar
  47. Hasanuzzaman M, Nahar K, Alam MM, Bhowmik PC, Hossain MA, Rahman MM, Prasad MNV, Ozturk M, Fujita M (2014) Potential use of halophytes to remediate saline soils. BioMed Res Internat, Article ID 589341, 12 pagesGoogle Scholar
  48. Hensen I (1994) Estudios ecológicos y fenológicos sobre Polylepis besseri Hieron en la Cordillera Oriental Boliviana. Ecología Bolivia 23:21–32Google Scholar
  49. Hildebrandt U, Janetta K, Fouad O, Renne B, Nawrath K, Bothe H (2001) Arbuscular mycorrhizal colonization of halophytes in Central European salt marshes. Mycorrhiza 10:175–183CrossRefGoogle Scholar
  50. Hirrel MC (1981) The effect of sodium and chloride salts on the germination of Gigaspora margarita. Mycology 43:610–617CrossRefGoogle Scholar
  51. Hirrel MC, Mehravaran H, Gerdemann JW (1978) Vesicular arbuscular mycorrhizae in the Chenopodiaceae and Cruciferae: do they occur? Can J Bot 56:2813–2817CrossRefGoogle Scholar
  52. INTA (1977) La Pampa Deprimida. Condiciones de drenaje de sus suelos. INTA. Departamento de Suelos. Publicación No. 154, Serie suelos, p 162, Buenos AiresGoogle Scholar
  53. INTA-CIRN (1990) Atlas de suelos de la República Argentina. Escala 1:500.000, 1: 1.000.000. Secretaría de Agricultura, Ganadería y Pesca. Proyecto PNUD ARG 85/109, Buenos AiresGoogle Scholar
  54. INTA (2003) Recursos Naturales de La Provincia de Córdoba: Los Suelos. Nivel de Reconocimiento 1:500.000. Secretaria de Ambiente de Córdoba, Argentina, CórdobaGoogle Scholar
  55. Jahromi F, Aroca R, Porcel R, Ruiz-Lozano JM (2008) Influence of salinity on the in vitro development of Glomus intraradices and on the in vivo physiological and molecular responses of mycorrhizal lettuce plants. Microbial Ecol 55:45–53CrossRefGoogle Scholar
  56. Juniper S, Abbott L (1993) Vesicular–arbuscular mycorrhizas and soil salinity. Mycorrhiza4:45–57CrossRefGoogle Scholar
  57. Juniper S, Abbott L (2006) Soil salinity delays germination and limits growth of hyphae from propagules of arbuscular mycorrhizal fungi. Mycorrhiza16:371–379PubMedCrossRefGoogle Scholar
  58. Kalaji HM, Jajoo A, Oukarroum A, Brestic, M, Zivcak, M, Samborska A, Cetner MD, Łukasik I, Goltsev V, Ladle RJ (2016) Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiol Plant 38:102CrossRefGoogle Scholar
  59. Kim C-K, Weber DJ (1985) Distribution of VA mycorrhiza on halophytes on inland salt playas. Plant Soil 83:207–214CrossRefGoogle Scholar
  60. Landwehr M, Hildebrandt U, Wilde P, Nawrath K, Toth T, Biro B, Bothe H (2002) The arbuscular mycorrhizal fungus Glomus geosporum in European saline, sodic and gypsum soils. Mycorrhiza 12:199–211PubMedCrossRefPubMedCentralGoogle Scholar
  61. Lavado RS, Taboada MA (1988) Water, salt and sodium dynamics in a natraquoll in Argentina. Catena 15:577–594CrossRefGoogle Scholar
  62. Le Houérou HN (1993) Salt-tolerant plants for the arid regions of the Mediterranean isoclimatic zone. In: Lieth H, Al Masoon AA (eds) Towards the rational use of high salinity tolerant plants, Vol. 1. Kluwer Academic Publisher, Dordrecht, The Netherlands, p 403–422CrossRefGoogle Scholar
  63. Lugo MA, Anton AM, Cabello MN (2005). Arbuscular mycorrhizas in the Larrea divaricata scrubland of the arid “Chaco”, Central Argentina. Journal Agric Tech 1:163–178Google Scholar
  64. Lugo MA, Reinhart KO, Menoyo E, Crespo EM, Urcelay C (2015) Plant functional traits and phylogenetic relatedness explain variation in associations with root fungal endophytes in an extreme arid environment. Mycorrhiza 25:85–95CrossRefGoogle Scholar
  65. Mazzanti A, Montes L, Minon D, Sarlangue H, Chepi C (1988) Utilización de Lotus tenuis en la Pampa Deprimida: resultado de una encuesta. Rev Agric Prod Anim 8:301–305Google Scholar
  66. McMillen BG, Juniper S, Abbott LK (1998) Inhibition of hyphal growth of a vesicular–arbuscular mycorrhizal fungus in soil containing sodium chloride limits the spread of infection from spores. Soil Biol Biochem 30:1639–1646CrossRefGoogle Scholar
  67. Mendoza R, Pagani E (1997) Influence of phosphorus nutrition on mycorrhizal growth response and morphology of mycorrhizae in Lotus tenuis. J Plant Nutr 20:625–639CrossRefGoogle Scholar
  68. Mendoza R, Pagani E, Pomar MC (2000) Variabilidad poblacional de Lotus glaber en relación con la absorción de fósforo en suelo. Ecol Austral 10:3–14Google Scholar
  69. Mijaluk A, Brandán de Weht C, García Paulucci D (2011) Micorrizas arbusculares en arbóreas nativas y en gramíneas en un sistema silvopastoril del chaco húmedo, Argentina. II Jornada sobre Ciencias del Suelo del NOA para estudiantes y jóvenes profesionales. Universidad Nacional de Tucumán, p 24Google Scholar
  70. Miransari M (2010) Contribution of arbuscular mycorrhizal symbiosis to plant growth under different types of soil stress. Plant Biol 12:563–569PubMedGoogle Scholar
  71. Mohankumar V, Mahadevan A (1987) Vesicular-arbuscular mycorrhizal association in plants of Kalakad reserve forest, India. Angew Bot 61:255–274Google Scholar
  72. Morras H, Candioti L (1982) Relación entre permeabilidad, ciertos caracteres analíticos y situación topográfica de algunos suelos de los bajos submeridionales (Santa Fé). Rev Invest Agro 26:23–32Google Scholar
  73. Munns R (1993) Physiological processes limiting plant growth in saline soils: some dogmas and hypotheses. Plant Cell Environ 16:15–24CrossRefGoogle Scholar
  74. Nieva AS, Bailleres MA, Llames ME, Taboada MA, Ruiz OA, Menendez A (2018) Promotion of Lotus tenuis in the Flooding Pampa (Argentina) increases the soil fungal diversity. Fungal Ecol 33:80–91CrossRefGoogle Scholar
  75. O’Leary JO (1988) Saline environments and halophytic crops. In: Arid land, today and tomorrow. West view Press, Boulder, Colorado, p 773–790Google Scholar
  76. Pagano MC, Lugo MA, Araújo FS, Ferrero MA, Menoyo E, Steinaker D (2011) Native species for restoration and conservation of biodiversity in South America. In: Marín L, Kovač D (eds) Native Species: Identification, Conservation and Restoration. Nova Science Publishers, New York, p 1–55Google Scholar
  77. Paoli HP, Volante JN, Noe YE, Vale LM, Castrillo S, Osinaga R, Chafatinos T, Nadir A (2009) Adecuación a un sistema de información geográfica del estudio “Los Suelos del NOA (Salta y Jujuy), Nadir A, Chafatinos T, 1990”. Convenio INTA-UNSa. Salta: Ediciones INTA. ISBN 978-987-25050-8-0Google Scholar
  78. Passera CB, Borsetto O (1989) Aspectos ecológicos de Atriplex lampa. Invest Agrar Prod Prot Veg 4:179–198Google Scholar
  79. Peterson RL, Ashford AE, Allaway WG (1985) Vesicular-arbuscular mycorrhizal association of vascular plants on Heron Island, a great barrier reef coral ray. Aust J Bot 33:669–676CrossRefGoogle Scholar
  80. Pfeiffer CM, Bloss HE (1988) Growth and nutrition of guayule (Parthenium argentatum) in a saline soil as influenced by vesicular–arbuscular mycorrhiza and phosphorus fertilization. New Phytol 108:315–321CrossRefGoogle Scholar
  81. Plenchette C, Duponnois R (2005) Growth response of the saltbush Atriplex nummularia L. to inoculation with the arbuscular mycorrhizal fungus Glomus intraradices. J Arid Environ 61:535–540CrossRefGoogle Scholar
  82. Porcel P, Aroca R, Ruiz-Lozano JM (2012) Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agron Sustain Dev 32:181–200CrossRefGoogle Scholar
  83. Rozema J, Arp W, van Diggelen J, van Esbroek M, Broekmann R, Punte H (1986) Occurrence and ecological significance of vesicular arbuscular mycorrhiza in the salt marsh environment. Acta Bot Neerlandica 35:457–467CrossRefGoogle Scholar
  84. Ruan C-J, Teixeira da Silva JA, Mopper S, Qin P, Lutts S (2010) Halophyte improvement for a salinized world. Crit Rev Plant Sci 29:329–359CrossRefGoogle Scholar
  85. Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza 13:309–317PubMedGoogle Scholar
  86. Ruiz-Lozano JM, Azcón R (2000) Symbiotic efficiency and infectivity of an autochthonous arbuscular mycorrhizal Glomus sp. from saline soils and G. deserticola under salinity. Mycorrhiza 10:137–143CrossRefGoogle Scholar
  87. Ruiz-Lozano JM, Porcel R, Azcón R, 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 63:4033–4044CrossRefGoogle Scholar
  88. Sala OE (1988) The effect of herbivory on vegetation structure. In: Werger MJA, van der Aart PJM, During HJ, Verboeven JTA (eds) Plant form and vegetation structure. SPB Academic Publishing, The Hague, The Netherlands, p 317–330Google Scholar
  89. Schalamuk S, Druille M, Cabello M (2015) Arbuscular mycorrhizal fungi: Influence of agronomic practices on diversity and dynamics of colonization. In: García de Salomone I, Vázquez S, Penna C, Cassán F (eds) Rizosfera, biodiversidad y agricultura sustentable. Asoc Argent Microbiol, p 47–71Google Scholar
  90. Schwab M, Di Bella CE, Casas C, Clavijo MP, Druille M, Lattanzi FA, Schaufele R, Grimoldi AA (2016) Evaluación de la incorporación de Panicum coloratum como fitorremediadora de suelos sódicos de la Pampa Deprimida. 39° Congreso de la Asociación Argentina de Producción Animal, PP2Google Scholar
  91. Sengupta A, Chaudhuri S (1990) Vesicular arbuscular mycorrhiza (VAM) in pioneer salt marsh plants of the Ganges River delta in West Bengal (India). Plant Soil 122:111–113CrossRefGoogle Scholar
  92. Shabala S (2013) Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops. Ann Bot 112:1209–1221PubMedPubMedCentralCrossRefGoogle Scholar
  93. Sharifi M, Ghorbanli M, Ebrahimzadeh H (2007) Improved growth of salinity-stressed soybean after inoculation with pre-treated mycorrhizal fungi. J Plant Physiol 164:1144–1151PubMedCrossRefGoogle Scholar
  94. Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic Press, San DiegoGoogle Scholar
  95. Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, LondonGoogle Scholar
  96. Soteras F, Becerra A, Cofré N, Nouhra E (2009). Variación estacional de la colonización micorrícica de Atriplex lampa (Moq.) D. Dietr. en dos salinas de Córdoba. XXXII Jornadas Argentinas de Botánica. Bol Soc Argent Bot Córdoba, Argentina, p 130Google Scholar
  97. Soteras F, Becerra A, Cofré N, Bartoloni, Cabello M (2012) Arbuscular mycorrhizal fungal species in saline environments of Central Argentina: seasonal variation and distribution of spores at different soil depth. Sydowia 64:301–311Google Scholar
  98. Soteras F, Cofré N, Bartoloni J, Cabello M, Becerra A (2013) Colonización radical de Atriplex lampa en dos ambientes salinos de Córdoba, Argentina. Bol Soc Arg Bot 48:211–219Google Scholar
  99. Stuart JR, Tester M, Gaxiola RA, Flowers TJ (2012) Plants of saline environments in AccessScience, ©McGraw-Hill Companies, PennsylvaniaGoogle Scholar
  100. Szabolcs I (1979) Review of Research on salt-affected soils. United Nations of Educational, Scientific and Cultural Organizations. Paris, ISBN 92-3-101613-XGoogle Scholar
  101. Taboada MA, Rubio G, Chaneton EJ (2011) Grazing impacts on soil physical, chemical and ecological properties in forage production systems. In: Hatfield JL, Sauer TJ (eds) Soil management: building a stable base for agriculture. American Society of Agronomy & Soil Science Society of America, p 301–320Google Scholar
  102. Tang ZS, An H, Shangguan ZP (2015) The impact of desertification on carbon and nitrogen storage in the desert steppe ecosystem. Ecol Eng 84:92–99CrossRefGoogle Scholar
  103. Ter Braak CJF (1987–1992) CANOCO—a FORTRAN program for canonical community ordination. Microcomputer Power, Ithaca, NYGoogle Scholar
  104. Tian CY, Feng G, Li XL, Zhang FS (2004) Different effects of arbuscular mycorrhizal fungal isolates from saline or non-saline soil on salinity tolerance of plants. App Soil Ecol 26:143–148CrossRefGoogle Scholar
  105. Vignolio O, Fernández O, Maceira N (1996) Respuestas de Lotus tenuis y Lotus corniculatus (Leguminosae) al anegamiento en plantas de distintas edades. Rev Fac Agron La Plata 101:57–66Google Scholar
  106. Vignolio O, Fernández O, Maceira N (1999) Flooding tolerance in five populations of Lotus glaber Mill. (Syn. Lotus tenuis Waldst. Et. Kit.). Aust J Agric Res 50:555–559CrossRefGoogle Scholar
  107. Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363CrossRefGoogle Scholar
  108. Wang FY, Liu RJ, Lin XG, Zhou JM (2004) Arbuscular mycorrhizal status of wild plants in saline-alkaline soils of the Yellow River Delta. Mycorrhiza 14:133–137PubMedCrossRefPubMedCentralGoogle Scholar
  109. Yeo AR, Flowers TJ (1980) Salt tolerance in the halophyte Suaeda maritima (L.) Dum.: evaluation of the effect of salinity upon growth. J Experiment Bot 31:1171–1183CrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Alejandra G. Becerra
    • 1
    Email author
  • M. Noelia Cofré
    • 2
  • Ileana García
    • 3
  1. 1.Laboratorio de Micología, IMBIV, CONICET, and Cátedra de Diversidad Biológica I, Facultad de Ciencias Exactas, Físicas y NaturalesUniversidad Nacional de CórdobaCórdobaArgentina
  2. 2.Laboratorio de Micología, IMBIV, CONICETUniversidad Nacional de CórdobaCórdobaArgentina
  3. 3.Museo Argentino de Ciencias Naturales Bernardino Rivadavia (CONICET)Buenos AiresArgentina

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