Abstract
Salinity is considered as one of the most destructive abiotic stresses for plants, and its prevalence is growing globally. This study assayed the impacts of single inoculation with the arbuscular mycorrhizal fungi (AMF) Rhizophagus irregularis (Ri) or Funneliformis mosseae (Fm), and co-inoculation of Ri and Fm, on rosemary plants exposed to long-term salinity stress [0, 50, 100, 150 mM NaCl] with three replications under controlled conditions of greenhouse. The results exhibited that Ri and Ri + Fm differentially colonized the roots of rosemary plants under moderate NaCl stress (50 and 100 mM) compared to Fm. Under non-saline conditions, AMF symbiosis increased plant growth, promoted biomass and chlorophyll contents, and improved the nutrient uptake and antioxidant capacity of the host plant. However, long-term salinity stress, even at a low level (50 mM), adversely affected the growth parameters of rosemary plants. Furthermore, AMF inoculation improved plant growth and alleviated ion toxicity under NaCl stress. Plants inoculated with single and consortia AMF species had high values of photosynthetic pigments, Fv/Fm index (0.80 for Fm + Ri), proline content (4.69 µM.g−1 FW for Fm), total phenolic content (58.38 mg GA.g−1 DW for Ri), K (9.46 mg.g−1 DW for Ri), P, and K: Na ratio (0.88 for Ri), but had low values of electrolyte leakage (42.34% for Ri), Na+ concentration in the shoot (11.56 mg.g−1 DW for Ri), and malondialehyde content (3.62 µM.g−1 FW for Fm) under high salinity levels, as compared to non-inoculated plants. Further, shoot fresh weight, root length, and Zn content in Fm inoculated plants under NaCl stress were higher compared to non-inoculated plants. Specifically, the results of this study suggest that the utilization of consortia AMF species does not necessarily lead to better capacity to compensate for hazardous effects of salinity compared to single species. Finally, this study indicated that arbuscular mycorrhizal symbiosis could improve the growth, ion homeostasis, osmoregulation, and reactive oxygen species scavenging capabilities of rosemary plants under salinity stress.
Graphical Abstract
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
The datasets used and/or analyzed during the current study available from the corresponding author on reasonable request.
References
Aalipour H, Nikbakht A, Etemadi N, Rejali F, Soleimani M (2020) Biochemical response and interactions between arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria during establishment and stimulating growth of Arizona cypress (Cupressus arizonica G.) under drought stress. Sci Hortic 261:108923
Aebi, HE (1983) Catalase. In: Bergmayer HU (ed) Methods of Enzymatic Analysis. Verlag Chemie, Weinheim, pp 273–286
Abbaspour H, Pour FSN, Abdel-Wahhab MA (2021) Arbuscular mycorrhizal symbiosis regulates the physiological responses, ion distribution and relevant gene expression to trigger salt stress tolerance in pistachio. Physiol Mol Biol Plants 27:1765–1778. https://doi.org/10.1007/s12298-021-01043-w
Abdel-Fattah GM, Asrar AWA (2012) Arbuscular mycorrhizal fungal application to improve growth and tolerance of wheat (Triticum aestivum L.) plants grown in saline soil. Acta Physiol Plant 34:267–277. https://doi.org/10.1007/s11738-011-0825-6
Alguacil MM, Hernandez JA, Caravaca F, Portillo B, Roldan A (2003) Antioxidant enzyme activities in shoots from three mycorrhizal shrub species afforested in a degraded semi-arid Soil. Physiol Plant 118:562–570. https://doi.org/10.1034/j.1399-3054,2003.00149.x
Ali S, Moon YS, Hamayun M, Khan MA, Bibi K, Lee IJ (2022) Pragmatic role of microbial plant biostimulants in abiotic stress relief in crop plants. J Plant Interact 17:705–718
Alqarawi AA, Hashem A, Abd_Allah EF, Alshahrani TS, Huqail AA (2014) Effect of salinity on moisture content, pigment system, and lipid composition in Ephedra alata Decne. Acta Biol Hung 65:61–71https://doi.org/10.1556/ABiol.65.2014.1.6
Amanifar S, Toghranegar Z (2020) The efficiency of arbuscular mycorrhiza for improving tolerance of Valeriana officinalis L. and enhancing valerenic acid accumulation under salinity stress. Ind Crops Prod 147:112234
Amiri R, Nikbakht A, Etemadi N (2015) Alleviation of drought stress on rose geranium [Pelargonium graveolens (L.) Herit.] in terms of antioxidant activity and secondary metabolites by mycorrhizal inoculation. Sci Hortic 197:373–380. https://doi.org/10.1016/j.scienta.2015.09.062
Aroca R, Del Mar AM, Vernieri P, Ruiz-Lozano JM (2008) Plant responses to drought stress and exogenous ABA application are modulated differently by mycorrhization in tomato and an ABA-deficient mutant (sitiens). Microbial Ecol 56:704. https://doi.org/10.1007/s00248-008-9390-y
Aslani Z, Hassani A, Rasouli-Sadaghiani M, Esmailpour B, Rohi Z (2014) Effects of arbuscular mycorrhizal (AM) fungi on essential oil content and nutrients uptake in basil under drought stress. J Med Plants By-Products. 3:147–153 https://doi.org/10.22092/jmpb.2014.108727
Bahonar A, Mehrafarin A, Abdousi V, Radmanesh E, Ladan Moghadam AR, Naghdi Badi H (2016) Quantitative and qualitative changes of rosemary (Rosemarinus officinalis L.) in response to mycorrhizal fungi (Glomus intraradices) inoculation under saline environments. J Med Plant 15:25–37
Baltazar-Bernal O, Spinoso-Castillo JL, Mancilla-Álvarez E, Bello-Bello JJ (2022) arbuscular mycorrhizal fungi induce tolerance to salinity stress in Taro plantlets (Colocasia esculenta L. Schott) during acclimatization. Plants 11:1780
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207. https://doi.org/10.1007/BF00018060
Bozdogan Sert E, Turkmen M, Cetin M (2019) Heavy metal accumulation in rosemary leaves and stems exposed to traffic-related pollution near Adana-İskenderun Highway (Hatay, Turkey). Environ Monit Assess 191:1–12
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Burleigh SH, Kristensen BK, Bechmann IE (2003) A plasma membrane zinc transporter from Medicago truncatula is up-regulated in roots by Zn fertilization, yet down-regulated by arbuscular mycorrhizal colonization. Plant Mol Biol 52:1077–1088. https://doi.org/10.1023/A:1025479701246
Cantrell IC, Linderman RG (2001) Preinoculation of lettuce and onion with VA mycorrhizal fungi reduces deleterious effects of soil salinity. Plant Soil 233:269–281. https://doi.org/10.1023/A:1010564013601
Chen J, Zhang H, Zhang X, Tang M (2017) Arbuscular mycorrhizal symbiosis alleviates salt stress in black locust through improved photosynthesis, water status, and K+/Na+ homeostasis. Front Plant Sci 8:1739. https://doi.org/10.3389/fpls.2017.01739
Crossay T, Cavaloc Y, Majorel C, Redecker D, Medevielle V, Amir H (2020) Combinations of different arbuscular mycorrhizal fungi improve fitness and metal tolerance of sorghum in ultramafic soil. Rhizosphere 14:100204. https://doi.org/10.1016/j.rhisph.2020.100204
Dastogeer KM, Zahan MI, Tahjib-Ul-Arif M, Akter MA, Okazaki S (2020) Plant Salinity Tolerance Conferred by Arbuscular Mycorrhizal Fungi and Associated Mechanisms: A Meta-Analysis. Front Plant Sci 11:1927. https://doi.org/10.3389/fpls.2020.588550
De Azevedo Neto AD, Prisco JT, Enéas-Filho J, de Abreu CEB, Gomes-Filho E (2006) Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environ Exp Bot 56:87–94
De Oliveira VH, Ullah I, Dunwell JM, Tibbett M (2020) Mycorrhizal symbiosis induces divergent patterns of transport and partitioning of Cd and Zn in Populus trichocarpa. Environ Exp Bot 171:103925
Evelin H, Devi TS, Gupta S, Kapoor R (2019) Mitigation of salinity stress in plants by arbuscular mycorrhizal symbiosis: current understanding and new challenges. Front Plant Sci 10:470
Fileccia V, Ruisi P, Ingraffia R, Giambalvo D, Salvatore Frenda A, Martinelli F (2017) Arbuscular mycorrhizal symbiosis mitigates the negative effects of salinity on durum wheat. PLoS ONE 12:1–15. https://doi.org/10.1371/journal.pone.0184158
Gericke S, Kurmies B (1952) Die kolorimetrische phosphorsäure bestimmung mit ammonium-vanadat-molybdat und ihre anwendung in der pflanzenanalyse. Düngg Pflanzenernähr Bodenk 59:235–247. https://doi.org/10.12691/plant-5-1-4
Giannopolitis CN, Ries SK (1977) Superoxide dismutase: occurrence in higher plants. Plant Physiol 59:309–314. https://doi.org/10.1104/pp.59.2.309
Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500. https://doi.org/10.1111/j.1469-8137.1980.tb04556.x
Hanato T, Kagawa H, Yasuhara T, Okuda T (1988) Two new flavonoids and other constituents in licorice root: their relative astringency and radical scavenging effect. Chem Pharm Bull 36:1090–1097. https://doi.org/10.1248/cpb.36.2090
Hart MM, Forsythe J, Oshowski B, Bücking H, Jansa J (2013) Hiding in a crowd—does diversity facilitate persistence of a low-quality fungal partner in the mycorrhizal symbiosis? Symbiosis 59:47–56. https://doi.org/10.1007/s13199-012-0197-8
Hashem A, Abd-Allah EF, Alqarawi AA, Aldubise A, Egamberdieva D (2015) Arbuscular mycorrhizal fungi enhances salinity tolerance of Panicum turgidum Forssk by altering photosynthetic and antioxidant pathways. J Plant Intract 10:230–242. https://doi.org/10.1080/17429145.2015.1052025
Hassena AB, Zouari M, Trabelsi L, Decou R, Amar FB, Chaari A, Zouari N (2021) Potential effects of arbuscular mycorrhizal fungi in mitigating the salinity of treated wastewater in young olive plants (Olea europaea L. cv. Chetoui). Agri Water Manage 245:106635. https://doi.org/10.1016/j.agwat.2020.106635
Huang YC, Chang YH, Shao YY (2006) Effects of genotype and treatment on the antioxidant activity of sweet potato in Taiwan. Food Chem 98:529–538. https://doi.org/10.1016/j.foodchem.2005.05.083
Jugran AK, Bahukhandi A, Dhyani P, Bhatt ID, Rawal RS, Nandi SK, Palni LMS (2015) The effect of inoculation with mycorrhiza: AM on growth, phenolics, tannins, phenolic composition and antioxidant activity in Valeriana jatamansi Jones. J Soil Sci Plant Nut 15:1036–1049. https://doi.org/10.4067/S0718-95162015005000072
Lattanzio V, Kroon PA, Quideau S, Treutter D (2008) Plant phenolics—secondary metabolites with diverse functions. Recent Adv Polyphenol Res 1:1–35
Li T, Liu RJ, He XH, Wang BS (2012) Enhancement of superoxide dismutaseand catalase activities and NaCl tolerance of euhalophyte Suaeda salsa L. by mycorrhizal fungus Glomus mosseae. Pedosphere 22:217–224. https://doi.org/10.1016/S1002-0160(12)60008-3
Lichtenthaler HK (1987) Chlorophylls and carotenoids, the pigmants of photosynthetic biomembranes. In: Douce R and Pacher L (eds) Methods Enzymol. Academic press Inc, New York, pp 350–382
Lutts S, Bouharmont J (1996) NaCl-induced senescence in leaves of rice (oryza sativa L.) cultivars differing in salinity resistance. Ann Bot 78:389–398. https://doi.org/10.1006/anbo.1996.0134
Maathuis FJM, Amtmann A (1999) K+ nutrition and Na+ toxicity: the basis of cellular K+/Na+ ratios. Ann Bot 84:123–133. https://doi.org/10.1006/anbo.1999.0912
Mahouachi J (2018) Long-term salt stress influence on vegetative growth and foliar nutrient changes in mango (Mangifera indica L.) seedlings. Sci Hortic 234:95–100. https://doi.org/10.1016/j.scienta.2018.02.028
Marxen K, Vanselow KH, Lippemeier S, Hintze R, Ruser A, Hansen UP (2007) Determination of DPPH radical oxidation caused by methanolic extracts of some microalgal species by linear regression analysis of spectrophotometric measurements. Sensors 7:2080–2095. https://doi.org/10.3390/s7102080
Matamoros MA, Dalton DA, Ramos J, Clemente MR, Rubio MC, Becana M (2003) Biochemistry and molecular biology of antioxidants in the rhizobia-legume symbiosis. Plant Physiol 133:499–509. https://doi.org/10.1104/pp.103.025619
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence a practical guide. J Expt Bot 51:659–668. https://doi.org/10.1093/jexbot/51.345.659
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410. https://doi.org/10.1016/S1360-1385(02)02312-9
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
Parihar M, Rakshit A, Rana K, Meena RP, Joshi DC (2020) A consortium of arbuscular mycorrizal fungi improves nutrient uptake, biochemical response, nodulation and growth of the pea (Pisum sativum L.) under salt stress. Rhizosphere 15:100235. https://doi.org/10.1016/j.rhisph.2020.100235
Parvin S, Van Geel M, Yeasmin T, Lievens B, Honnay O (2019) Variation in arbuscular mycorrhizal fungal communities associated with lowland rice (Oryza sativa) along a gradient of soil salinity and arsenic contamination in Bangladesh. Sci Total Environ 686:546–554. https://doi.org/10.1016/j.scitotenv.2019.05.450
Parvin S, Van Geel M, Yeasmin T, Verbruggen E, Honnay O (2020) Effects of single and multiple species inocula of arbuscular mycorrhizal fungi on the salinity tolerance of a Bangladeshi rice (Oryza sativa L.) cultivar. Mycorrhiza 30:431–444. https://doi.org/10.1007/s00572-020-00957-9
Pedone-Bonfim MVL, da Silva DKA, da Silva-Batista AR, de Oliveira AP, da Silva Almeida JRG, Yano-Melo AM, Maia LC (2018) Mycorrhizal inoculation as an alternative for the sustainable production of Mimosa tenuiflora seedlings with improved growth and secondary compounds content. Fungal Biol 122:918–927. https://doi.org/10.1016/j.funbio.2018.05.009
Pellegrino E, Bedini S (2014) Enhancing ecosystem services in sustainable agriculture: biofertilization and biofortification of chickpea (Cicer arietinum L.) by arbuscular mycorrhizal fungi. Soil Biol Biochem 68:429–439. https://doi.org/10.1016/j.soilbio.2013.09.030
Phillips JM, Hayman DS (1970) Improved procedures for clearing roots andstaining parasitic and vesicular–arbuscular mycorrhizal fungi for rapidassessment of infection. Trans Br Mycol Soc 55:158–161. https://doi.org/10.1016/S0007-1536(70)80110-3
Porcel R, Aroca R, Azcon R, Ruiz-Lozano JM (2016) Regulation of cation transporter genes by the arbuscular mycorrhizal symbiosis in rice plants subjected to salinity suggests improved salt tolerance due to reduced Na+ root-to-shoot distribution. Mycorrhiza 26:673–684. https://doi.org/10.1007/s00572-016-0704-5
Porras-Soriano A, Soriano-Martin ML, Porras-Piedra A, Azcon R (2009) Arbuscular mycorrhizal fungi increased growth, nutrient uptake and tolerance to salinity in olive trees under nursery conditions. J Plant Physiol 166:1350–1359. https://doi.org/10.1016/j.jplph.2009.02.010
Putter J (1974) Peroxidases. In: Methods of enzymatic analysis Vol. II. Ed. H. U. Bergmeyer, Academic Press, pp 685–690 https://doi.org/10.1016/B978-0-12-091302-2.50033-5
Ribeiro-Santos R, Carvalho-Costa D, Cavaleiro C, Costa HS, Albuquerque TG, Castilho MC, Ramos F, Melo NR, Sanches-Silva A (2015) A novel insight on an ancient aromatic plant: The rosemary (Rosmarinus officinalis L.). Trends Food Sci Technol 45:355–368
Roy SJ, Negrão S, Tester M (2014) Salt resistant crop plants. Curr Opin Biotech 26:115–124. https://doi.org/10.1016/j.copbio.2013.12.004
Santander C, Sanhueza M, Olave J, Borie F, Valentine A, Cornejo P (2019) Arbuscular mycorrhizal colonization promotes the tolerance to salt stress in lettuce plants through an efficient modification of ionic balance. J Soil Sci Plant Nut 19:321–331. https://doi.org/10.1007/s42729-019-00032-z
Sato T, Ezawa T, Cheng W, Tawaraya K (2015) Release of acid phosphatase from extraradical hyphae of arbuscular mycorrhizal fungus Rhizophagus clarus. J Soil Sci Plant Nutr 61:269–274 https://doi.org/10.1080/00380768.2014.993298
Sharma D, Dubey A, Srivastav M (2011) Effect of putrescine and paclobutrazol on growth, physiochemical parameters and nutrient acquisition of salt-sensitive citrus rootstock Karna khatta (Citrus karna Raf.) under NaCl Stress. J Plant Growth Regul 30:301–311. https://doi.org/10.1007/s00344-011-9192-1
Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Viticul 16:144–158
Tawaha K, Alali FQ, Gharaibeh M, Mohammad M, El-Elimat T (2007) Antioxidant activity and total phenolic content of selected Jordanian plant Species. Food Chem 104:1372–1378. https://doi.org/10.1016/j.foodchem.2007.01.064
Treutter D (2010) Managing phenol contents in crop plants by phytochemical farming and breeding—visions and constraints. Int J Mol Sci 11:807–857
Turner NC (1981) Techniques and experimental approaches for the measurement of plant water status. Plant Soil 58:339–366. https://doi.org/10.1007/BF02180062
Van Geel M, De Beenhouwer M, Lievens B, Honnay O (2016) Crop-specific and single-species mycorrhizal inoculation is the best approach to improve crop growth in controlled environments. Agron Sustain Dev 36:37. https://doi.org/10.1007/s13593-016-0373-y37
Van Zelm E, Zhang Y, Testerink C (2020) Salt tolerance mechanisms of plants. Annu Rev Plant Biol 71:403–433. https://doi.org/10.1146/annurev-arplant-050718-100005
Wang Y, Wang M, Li Y, Wu A, Huang J (2018) Effects of arbuscular mycorrhizal fungi on growth and nitrogen uptake of Chrysanthemum morifolium under salt stress. Plose One 13:1–14. https://doi.org/10.1371/journal.pone.0196408
Wang J, Yuan J, Ren Q, Zhang B, Zhang J, Wang HR, GG, (2022) Arbuscular mycorrhizal fungi enhanced salt tolerance of Gleditsia sinensis by modulating antioxidant activity, ion balance and P/N ratio. Plant Growth Regul 97:33–49
Xu H, Lu Y, Tong S (2018) Effects of arbuscular mycorrhizal fungi on photosynthesis and chlorophyll fluorescence of maize seedlings under salt stress. Emirates J Food Agric 30:199–204. https://doi.org/10.9755/ejfa.2018.v30.i3.1642
Author information
Authors and Affiliations
Contributions
M. Abdal, N. Etemadi, and A. Nikbakht conceived and designed research. M. Abdal and N. Etemadi conducted experiments. M. Abdal and R. Amirikhah wrote the manuscript. All authors read and approved the manuscript.
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Abdal, M., Etemadi, N., Nikbakht, A. et al. The arbuscular mycorrhizal symbiosis alleviating long-term salt stress through the modulation of nutrient elements, osmolytes, and antioxidant capacity in rosemary. Biologia 78, 993–1010 (2023). https://doi.org/10.1007/s11756-022-01285-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11756-022-01285-3