Abstract
Soil salinity continuously threatens the sustainability of several economically strategic crop production systems in Tunisia, especially in the arid and Saharan areas. In addition, it also affects microbial populations associated with the roots of crop plants, which are known to contribute efficiently to crop’s productivity and adaptation to environmental stresses. In this respect, the effect of soil salinity on arbuscular mycorrhizal fungi (AMF) associated with date palm (Phoenix dactylifera L.), the flagship crop of Tunisian oases, is still rarely studied. The present work is the first investigation of the colonization of date palm roots by AMF and the production of easily-extractable glomalin related soil protein (EE-GRSP) in different date palm plantations where soils present high salinity rates up to 7.6 dS m−1. The results revealed a negative correlation between soil salinity and the intensity of mycorrhization on one hand but a positive correlation between soil salinity and EE-GRSP and spore density on the other hand. This suggests that the production of EE-GRSP might be involved in the tolerance of AMF to elevated salinity in the soil. In addition, four AMF species, identified based on spore morphology and molecular phylogenetic analyses, have been recovered in single spore derived cultures, namely Albahypha drummondii, Dominikia disticha, Funneliformis coronatus and Rhizoglomus irregulare. The investigation of the current mycorrhizal status of date palm roots and rhizosphere soil EE-GRSP concentrations along a salinity gradient on one side and isolation and identification of AMF strains native to Tunisian oases ecosystems one the other represent first steps towards the development of sustainable agricultural practices in this region where salinity is the main production-limiting factor.
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References
Ahmadi GS, Tavasoli A (2014) Effects of NaCl salinity levels on the glomalin produced by Glomerales in symbiosis with corn plant. J Water Soil Agricul Sci Technol 28:92–100
Ait-El-Mokhtar M, Laouane RB, Anli M, Boutasknit A, Wahbi S, Meddich A (2019) Use of mycorrhizal fungi in improving tolerance of the date palm (Phoenix dactylifera L.) seedlings to salt stress. Sci Hortic 253:429–438. https://doi.org/10.1016/j.scienta.2019.04.066
Aliasgharzadeh N, Saleh Rastin N, Towfighi H, Alizadeh A (2001) Occurrence of arbuscular mycorrhizal fungi in saline soils of the Tabriz plain of Iran in relation to some physical and chemical properties of soil. Mycorrhiza 11:119–122
Al-Yahya'ei MN, Oehl F, Vallino M et al (2011) Unique arbuscular mycorrhizal fungal communities uncovered in date palm plantations and surrounding desert habitats of southern Arabia. Mycorrhiza 21:195–209. https://doi.org/10.1007/s00572-010-0323-5
Antunes PM, Koch AM, Morton JB, Rillig MC, Klironomos JN (2010) Evidence for functional divergence in arbuscular mycorrhizal fungi from contrasting climatic origins. New Phytol 189:507–514. https://doi.org/10.1111/j.1469-8137.2010.03480.x
Askri B, Bouhlila R (2010) Évolution de la salinité dans une oasis moderne de la Tunisie. Etude et Gestion des Sols 17:197–212
Ben Hassine H, Ben Slimane A, Mlawah M et al (2013) Effects of underground water on soil salinity and dates production in oases area (Tunisia): the case of El Bahaier oasis. J Environ Sci, Toxicol Food Technol 4:51–58. https://doi.org/10.9790/2402-0445158
Bencherif K, Boutekrabt A, Fontaine J, Laruelle F, Dalpè Y, Lounès-Hadj Sahraoui A (2015) Impact of soil salinity on arbuscular mycorrhizal fungi biodiversity and microflora biomass associated with Tamarix articulata Vahll rhizosphere in arid and semi-arid Algerian areas. Sci Total Environ 533:488–494. https://doi.org/10.1016/j.scitotenv.2015.07.007
Bird SB, Herrick JE, Wander MM, Wright SF (2002) Spatial heterogeneity of aggregate stability and soil carbon in semi-arid rangeland. Environ Pollut 116:445–455. https://doi.org/10.1016/s0269-7491(01)00222-6
Błaszkowski J (2012) Glomeromycota. W. Szafer Institute of Botany, Polish Academy of Sciences. https://doi.org/10.5586/am.2013.015, Błaszkowski J. 2012. Glomeromycota. Book review
Błaszkowski J, Chwat G, Góralska A, Ryszka P, Kovács GM (2015) Two new genera, Dominikia and Kamienskia, and D disticha sp nov in Glomeromycota. Nova Hedwigia 100:225–238. https://doi.org/10.1127/nova_hedwigia/2014/0216
Bouamri R, Dalpé Y, Serrhini MN et al (2006) Arbuscular mycorrhiza fungi species associated with rhizosphere of Phoenix dactylifera in Morocco. Afr J Biotechnol 5:510–516
Bouamri R, Dalpe Y, Serrhini M (2014) Effect of seasonal variation on arbuscular mycorrhizal fungi associated with date palm. Emirates J Food Agricul 26:977–986. https://doi.org/10.9755/ejfa.v26i11.18985
Brundrett M, Melville L. Peterson L (1994) Practical Methods in Mycorrhizal Research Mycologue Publications Ltd, Waterloo
Carter MR, Gregorich EG (2007) Soil sampling and methods of analysis, 2nd edn. CRC Press, Boca Raton
Carter KA, Smith JF, White MM, Serpe MD (2013) Assessing the diversity of arbuscular mycorrhizal fungi in semiarid shrublands dominated by Artemisia tridentata ssp Wyomingensis. Mycorrhiza 24:301–314. https://doi.org/10.1007/s00572-013-0537-4
Castillo CG, Borie F, Oehl F, Sieverding E (2016) Arbuscular mycorrhizal fungi biodiversity: prospecting in southern central zone of Chile. J Soil Sci Plant Nutr 16:11–24. https://doi.org/10.4067/S0718-95162016005000036
Channabasava A, Lakshman H, Jorquera M (2015) Effect of fungicides on association of arbuscular mycorrhiza fungus Rhizophagus fasciculatus and growth of Proso millet (Panicum miliaceum L. journal of soil science and plant nutrition, (ahead) https://doi.org/10.4067/s0718-95162015005000004
Chao CT, Krueger RR (2007) The date palm (Phoenix dactylifera L): overview of biology, uses, and cultivation. Hortic Sci 42, 1077:–1082. https://doi.org/10.21273/HORTSCI.42.5.1077
Chi GG, Srivastava AK, Wu QS (2018) Exogenous easily extractable glomalin-related soil protein improves drought tolerance of trifoliate orange. Arch Agron Soil Sci 64:1341–1350. https://doi.org/10.1080/03650340.2018.1432854
Daniels BA, Skipper HD (1982) Methods for the recovery and quantitative estimation of propagules from soil in: Schneck NC (eds) methods and principles of mycorrhizal research, American Phytopathological Society, St Paul. pp 29–35
Dashtebani F, Hajiboland R, Aliasgharzad N (2014) Characterization of salt-tolerance mechanisms in mycorrhizal (Claroideoglomus etunicatum) halophytic grass, Puccinellia distans. Acta Physiol Plant 36:1713–1726. https://doi.org/10.1007/s11738-014-1546-4
Diatta ILD, Kane A, Agbangba CE et al (2014) Inoculation with arbuscular mycorrhizal fungi improves seedlings growth of two sahelian date palm cultivars (Phoenix dactylifera L, cv Nakhla hamra and cv Tijib) under salinity stresses. Adv Biosci Biotechnol 5:64–72. https://doi.org/10.4236/abb.2014.51010
Dreyer B, Morte A, López JÁ, Honrubia M (2009) Comparative study of mycorrhizal susceptibility and anatomy of four palm species. Mycorrhiza 20:103–115. https://doi.org/10.1007/s00572-009-0266-x
Druva-Lusite I, Ievinsh G (2010) Diversity of arbuscular mycorrhizal symbiosis in plants from coastal habitats. Environ Exp Biol 8:17–34
El Kinany S, Achbani E, Faggroud M, Ouahmane L, El Hilali R, Haggoud A, Bouamri R (2019) Effect of organic fertilizer and commercial arbuscular mycorrhizal fungi on the growth of micro propagated date palm cv. Feggouss. J Saudi Soc Agric Sci. https://doi.org/10.1016/j.jssas.2018.01.004
Estrada B, Barea JM, Aroca R, Ruiz-Lozano JM (2012) A native Glomus intraradices strain from a Mediterranean saline area exhibits salt tolerance and enhanced symbiotic efficiency with maize plants under salt stress conditions. Plant Soil 366:333–349. https://doi.org/10.1007/s11104-012-1409-y
Estrada B, Aroca R, Azcón-Aguilar C, Barea JM, Ruiz-Lozano JM (2013a) Importance of native arbuscular mycorrhizal inoculation in the halophyte Asteriscus maritimus for successful establishment and growth under saline conditions. Plant Soil 370:175–185. https://doi.org/10.1007/s11104-013-1635-y
Estrada B, Beltrán-Hermoso M, Palenzuela J, Iwase K, Ruiz-Lozano JM, Barea JM, Oehl F (2013b) Diversity of arbuscular mycorrhizal fungi in the rhizosphere of Asteriscus maritimus (L.) less., a representative plant species in arid and saline Mediterranean ecosystems. J Arid Environ 97:170–175. https://doi.org/10.1016/j.jaridenv.2013.05.019
Freitas RO, Buscardo E, Nagy L et al (2014) Arbuscular mycorrhizal fungal communities along a pedo-hydrological gradient in a central Amazonian terra firme forest. Mycorrhiza 24:21–32. https://doi.org/10.1007/s00572-013-0507-x
Furrazola E, Covacevich F, Torres-Arias Y, Rodríguez-Rodríguez RM, Ley-Rivas JF, Izquierdo K, Fernández-Valle R, Louro Berbara RL (2015) Functionality of arbuscular mycorrhizal fungi in three plant communities in the managed floristic reserve San Ubaldo-Sabanalamar, Cuba. Rev Biol Trop 63:341–356
Ghazouani W, Marlet S, Mekki I, Vidal A (2009) Farmers perceptions and engineering approaching the modernization of a community-managed irrigation scheme. A case study from an oases of the Nefzawa (South of Tunisia). Irrig Drain 58:285–296. https://doi.org/10.1002/ird.528
Habib HM, Ibrahim WH (2011) Nutritional quality of 18 date fruit varieties. Int J Food Sci Nutr 62:544–551. https://doi.org/10.3109/09637486.2011.558073
Hachicha M, Ben Aissa I (2014) Managing salinity in Tunisian oases. Journal of. Life Sci 8:775–782. https://doi.org/10.17265/1934-7391/2014.09.007
Haj-Amor Z, Toth T, Ibrahimi MK et al (2017) Effects of excessive irrigation of date palm on soil salinization, shallow groundwater properties, and water use in a Saharan oasis. Environ Earth Sci 76:590. https://doi.org/10.1007/s12665-017-6935-8
Hamed Y, Hadji R, Redhaounia B et al (2018) Climate impact on surface and groundwater in north Africaa global synthesis of findings and recommendations. Euro-Med J Environ Integ 3:25. https://doi.org/10.1007/s41207-018-0067-8
Hammer EC, Rillig MC (2011) The influence of different stresses on glomalin levels in an arbuscular mycorrhizal fungus salinity increases glomalin content. PLoS One 6:e28426. https://doi.org/10.1371/journal.pone.0028426
Hamza H, Jemni M, Benabderrahim MA, Mrabet A, Touil S, Othmani A, Salah MB 2015 Date palm status and perspective in Tunisia. En: Date palm genetic resources and utilization volume 1: Africa and the Americas, Eds Al-Khayri J.M, Jain SM, Johnson DV. Springer, Dordrecht, Paises Bajos, 193–221. https://doi.org/10.1007/978-94-017-9694-1_6
Hashem A, AbdAllah EF, Alqarawi AA et al (2015) Arbuscular mycorrhizal fungi enhance salinity tolerance of Panicum turgidum Forssk by altering photosynthetic and antioxidant pathways. J Plant Interact 10:230–242. https://doi.org/10.1080/17429145.2015.1052025
Hashem A, AbdAllah EF, Alqarawi AA et al (2016) Comparing symbiotic performance and physiological responses of two soybean cultivars to arbuscular mycorrhizal fungi under salt stress. Saudi J Biol Sci 26:38–48. https://doi.org/10.1016/j.sjbs.2016.11.015
Hashem AA, Alqarawi A, Radhakrishnan R et al (2018) Arbuscular mycorrhizal fungi regulate the oxidative system, hormones and ionic equilibrium to trigger salt stress tolerance in Cucumis sativus L. Saudi J Biol Sci 25:1102–1114. https://doi.org/10.1016/j.sjbs.2018.03.009
He F, Chen H, Tang M (2019) Arbuscular Mycorrhizal fungal communities are influenced by host tree species on the loess plateau, Northwest China. Forests 10:930. https://doi.org/10.3390/f10100930
Hniličková H, Hnilička F, Martinkova J, Kraus K (2017) Effects of salt stress on water status, photosynthesis and chlorophyll fluorescence of rocket. Plant Soil Environ 63:362–367. https://doi.org/10.17221/398/2017-pse
Huang YM, Zou YN, Wu QS (2017) Alleviation of drought stress by mycorrhizas is related to increased root H2O2 efflux in trifoliate orange. Scientific reports 7. https://doi.org/10.1038/srep42335
Institut National de la météorologie (2020) https://www.meteo.tn/fr/donnees-climatiques
INVAM (2017) https://invam.wvu.edu/methods/spores/enumeration-of-spores
Klironomos JN, Hart MM, Gurney JE, Moutoglis P (2001) Interspecific differences in the tolerance of arbuscular mycorrhizal fungi to freezing and drying. Can J Bot 79:1161–1166. https://doi.org/10.1139/b01-099
Koch AM, Antunes PM, Kathryn Barto E, Cipollini D, Mummey DL, Klironomos JN (2010) The effects of arbuscular mycorrhizal (AM) fungal and garlic mustard introductions on native AM fungal diversity. Biol Invasions 13:1627–1639. https://doi.org/10.1007/s10530-010-9920-7
Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA mycorrhizas. Mycol Res 92:486–505
Koske RE, Tessier B (1983) A convenient, permanent slide mounting medium. Mycol Soc Am Newslet 34:59
Krishnamoorthy R, Kim K, Kim C, Sa T (2014) Changes of arbuscular mycorrhizal traits and community structure with respect to soil salinity in a coastal reclamation land. Soil Biol Biochem 72:1–10. https://doi.org/10.1016/j.soilbio.2014.01.017
Krishnamoorthy R, Kim CG, Subramanian P, Kim KY, Selvakumar G, Sa TM (2015) Arbuscular Mycorrhizal Fungi community structure, Abundance and Species Richness Changes in Soil by Different Levels of Heavy Metal and Metalloid Concentration. PLoS One 10:e0128784. https://doi.org/10.1371/journal.pone.0128784
Krüger M, Stockinger H, Krüger C, Schüßler A (2009) DNA-based species level detection of Glomeromycota: one PCR primer set for all arbuscular mycorrhizal fungi. New Phytol 183:212–223. https://doi.org/10.1111/j.1469-8137.2009.02835.x
Lekberg Y, Koide RT, Rohr JR (2007) Role of niche restrictions and dispersal in the composition of arbuscular mycorrhizal fungal communities. J Ecol 95:95–105. https://doi.org/10.1111/j.1365-2745.2006.01193.x
Liu H, Wang Y, Tang M (2017) Arbuscular mycorrhizal fungi diversity associated with two halophytes Lycium barbarum L and Elaeagnus angustifolia L in Ningxia, China. Arch Agron Soil Sci 63:796–806. https://doi.org/10.1080/03650340.2016.1235783
Majewska ML, Błaszkowski J, Nobis M, Rola K, Nobis A, Łakomiec D, Czachura P, Zubek S (2015) Root-inhabiting fungi in alien plant species in relation to invasion status and soil chemical properties. Symbiosis 65:101–115
Manga A, Diop A, Diop TA (2017) Functional diversity of Mycorrhizal Fungi has differential effects on salinity tolerance of Acacia seyal (Del) seedlings. Open J Soil Sci 7:315–332
Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159:89–102
Marulanda A, Porcel R, Barea JM, Azcon R (2007) Drought tolerance and antioxidant activities in lavender plants colonized by native drought-tolerant or drought-sensitive Glomus species. Microb Ecol 54:543–552
Mathieu C, Pieltain F (2003) Analyse chimique des sols méthodes choisies. Editions Tec et Doc/Lavoisier, Paris
Meddich A, Ait El Mokhtar M, Bourzik W et al (2018). Optimizing Growth and Tolerance of Date Palm (Phoenix dactylifera L) to Drought, Salinity, and Vascular Fusarium-Induced Wilt (Fusarium oxysporum) by Application of Arbuscular Mycorrhizal Fungi (AMF). Root Biol 239–258
Mummey DL, Antunes PM, Rillig MC (2009) Arbuscular mycorrhizal fungi pre-inoculant identity determines community composition in roots. Soil Biol Biochem 41:1173–1179. https://doi.org/10.1016/j.soilbio.2009.02.027
Nafady NA, Abdel-Azeem AM, Salem FM (2016) A checklist of Egyptian fungi: II Glomeromycota. Microb Biosyst 1:40–49
Olsen SR, Cole CV, Watanabe FS et al (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. Washington DC
Porcel R, Gómez M, Kaldenhoff R, Ruiz-Lozano JM (2005) Impairment of NtAQP1 gene expression in tobacco plants does not affect root colonisation pattern by arbuscular mycorrhizal fungi but decreases their symbiotic efficiency under drought. Mycorrhiza 15:417–423. https://doi.org/10.1007/s00572-005-0346-5
Requena N, Perez Soliz E, Azcon Aguilar C et al (2001) Management of indigenous plant microbe symbiosis aids restoration of desertified ecosystems. Appl Environ Microbiol 67:495–498
Rillig MC, Ramsey PW, Morris S, Paul EA (2003) Glomalin, an arbuscular-mycorrhizal fungal soil protein, responds to land-use change. Plant Soil 253:293–299. https://doi.org/10.1023/A:1024807820579
Rivera D, Obón C, Alcaraz F et al (2015) Date Palm Status and Perspective in Spain En: Date Palm Genetic Resources and Utilization. Volume 2: Asia and Europe, Eds Al-Khayri J.M,Jain SM, Johnson DV. Springer, Dordrecht, Paises Bajos, pp 489–526. https://doi.org/10.1007/978-94-017-9707-8_15
Roda JJ, Díaz G, Torres P (2008) Spatial distribution of Arbuscular Mycorrhizal Fungi in the Rhizosphere of the salt Marsh Plant Inula crithmoides L. along a salinity gradient. Arid Land Res Manag 22:310–319. https://doi.org/10.1080/15324980802388199
Schwartz MW, Hoeksema JD, Gehring CA, Johnson NC, Klironomos JN, Abbott LK, Pringle A (2006) The promise and the potential consequences of the global transport of mycorrhizal fungal inoculum. Ecol Lett 9:501–515. https://doi.org/10.1111/j.1461-0248.2006.00910.x
Sghir F, Touati J, Chliyeh M, Ouazzani Touhami A et al (2014) Int J Pure Appl Biosci 2:1–11
Sharif AO, Sanduk M, Taleb HM (2010) The date palm and its role in reducing soil salinity and global warming. Acta Hortic 882:59–64. https://doi.org/10.17660/actahortic.2010.882.5
Sharma A, Batra N (2014) Diversity of arbuscular mycorrhizal fungi associated with the rhizosphere of Phoenix dactylifera L in semi-arid soils. Int J Pharm Bio Sci 5:819–826
Shukla A, Kumar A, Jha A, Salunkhe O, Vyas D (2012) Soil moisture levels affect mycorrhization during early stages of development of agroforestry plants. Biol Fertil Soils 49:545–554. https://doi.org/10.1007/s00374-012-0744-8
Sieverding E (1991)Vesicular-arbuscular mycorrhiza management in tropical agrosystems Deutsche Gesellschaft für Technische Zusammenarbeit Nr 224 Hartmut Bremer Verlag, Friedland
Sieverding E, Da Silva GA, Berndt R et al (2014) Rhizoglomus, a new genus in the Glomeraceae. Mycotaxon 129:373–386. https://doi.org/10.5248/129.373
Silva-Flores P, Bueno CG, Neira J, Palfner G (2019) Factors affecting Arbuscular Mycorrhizal Fungi spore density in the Chilean Mediterranean-type ecosystem. J Soil Sci Plant Nutr 19:42–50. https://doi.org/10.1007/s42729-018-0004-6
Symanczik S, Błaszkowski J, Koegel S, Boller T, Wiemken A, al-Yahya’Ei MN (2014) Isolation and identification of desert habituated arbuscular mycorrhizal fungi newly reported from the Arabian peninsula. J Arid Land 6:488–497. https://doi.org/10.1007/s40333-013-0213-8
Symanczik S, Courty PE, Boller T, Wiemken A, al-Yahya’ei MN (2015) Impact of water regimes on an experimental community of four desert arbuscular mycorrhizal fungal (AMF) species, as affected by the introduction of a non-native AMF species. Mycorrhiza 25:639–647. https://doi.org/10.1007/s00572-015-0638-3
Tchabi A, Coyne D, Hountondji F, Lawouin L, Wiemken A, Oehl F (2010) Efficacy of indigenous arbuscular mycorrhizal fungi for promoting white yam (Dioscorea rotundata) growth in West Africa. Appl Soil Ecol 45:92–100. https://doi.org/10.1016/j.apsoil.2010.03.001
Treseder KK, Turner KM (2007) Glomalin in ecosystems. Soil Sci Soc Am J 71:1257–1266. https://doi.org/10.2136/sssaj2006.0377
Tressner HD, Hayes JA (1971) Sodium chloride tolerance of terrestrial fungi. Appl Microbiol 22:210–213
Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorrhization VA d’un systeme radiculaire Recherche de methodes d’estimation ayant Une signification fonctionnelle in: Gianinazzi-Pearson V and Gianinazzi, S, Eds, physiological and Genetical aspects of Mycorrhizae. INRA edition, Paris, pp 217–221
USDA (2013) Soil classification: a comprehensives system (prepared by) soil survey staff USDA Washington, DC USA
VDLUFA (1991) Die Untersuchung von Böden Methodenbuch Nr. 1 VDLUFA Verlag Darmstadt, Germany. [VDLUFA = Verband Deutscher Landwirtschaftlicher Untersuchungs- und Forschungsanstalten]
Verner D (2013) Tunisia in a changing climate: assessment and actions for increased resilience and development. The World Bank, Washington DC
Verzeaux J, Nivelle E, Roger D, Hirel B, Dubois F, Tetu T (2017) Spore density of arbuscular mycorrhizal fungi is fostered by six years of a no-till system and is correlated with environmental parameters in a silty loam soil. Agronomy 7:38. https://doi.org/10.3390/agronomy7020038
White T, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In "PCR protocols: a guide to methods and applications" (M. Innis, D. Gelfand, J. Shinsky and T. White, eds.), academic press, 315–322
Wright SF, Upadhyaya A (1996) Extraction of an abundant and unusual protein from soil and comparison with hyphal protein of arbuscular mycorrhizae fungi. Soil Sci 161:575–586. https://doi.org/10.1097/00010694-199609000-00003
Wu QS, Srivastava A, Wang S et al (2015) Exogenous application of EE-GRSP and changes in citrus rhizosphere properties. Indian J Agric Sci 85:802–806
Yang X, Zhang Q, Li X, Jia X, Wei X, Shao M' (2015) Determination of soil texture by laser diffraction method. Soil Sci Soc Am J 79:1556–1566. https://doi.org/10.2136/sssaj2015.04.0164
Zaller JG, Frank T, Drapela T (2011) Soil sand content can alter effects of different taxa of mycorrhizal fungi on plant biomass production of grassland species. Eur J Soil Biol 47:175–181. https://doi.org/10.1016/j.ejsobi.2011.03.001
Zhang T, Yang X, Guo R, Guo J (2016). Response of AM fungi spore population to elevated temperature and nitrogen addition and their influence on the plant community composition and productivity. Scientific Reports 6. https://doi.org/10.1038/srep24749
Zhang Y, He X, Zhao L, Zhang J, Xu W (2017a) Dynamics of arbuscular mycorrhizal fungi and glomalin under Psammochloa villosa along a typical dune in desert, North China. Symbiosis 73:145–153. https://doi.org/10.1007/s13199-017-0488-1
Zhang Z, Wang Q, Wang H, Nie S, Liang Z (2017b) Effects of soil salinity on the content, composition, and ion binding capacity of glomalin-related soil protein. Sci Total Environ 581-582:657–665. https://doi.org/10.1016/j.scitotenv.2016.12.176
Zougari-Elwedi B, Issami W, Msetra A et al (2016) Monitoring the evolution of the arbuscular mycorrhizal fungi associated with date palm. J New Sci Agricul Biotechnol 31:1822–1831
Acknowledgements
This work was partly supported by the r4d project “Application of organic bio-fertilizer technology to improve the sustainability of date palm production and cultivation” with the grand number IZ07Z0_160904 funded by the r4d program, the Swiss Programme for Research on global Issues for Development, a partnership of the Agency for Development and Cooperation and the Swiss National Science Foundation.
We would like to thank the two anonymous reviewers for their constructive comments, which have contributed to the improved quality of the manuscript.
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This work was partly supported by the r4d project “Application of organic bio-fertilizer technology to improve the sustainability of date palm production and cultivation” with the grand number IZ07Z0_160904 funded by the r4d program, the Swiss Programme for Research on global Issues for Development, a partnership of the Agency for Development and Cooperation and the Swiss National Science Foundation.
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Chebaane, A., Symanczik, S., Oehl, F. et al. Arbuscular mycorrhizal fungi associated with Phoenix dactylifera L. grown in Tunisian Sahara oases of different salinity levels. Symbiosis 81, 173–186 (2020). https://doi.org/10.1007/s13199-020-00692-x
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DOI: https://doi.org/10.1007/s13199-020-00692-x