تأثیر قارچ فانلی فورمیس موسه و اسیدی تیوباسیلوس بر برخی متابولیت‌های بیوشیمیایی ذرت (Zea mays L.) تحت تنش شوری

نوع مقاله : مقالات پژوهشی

نویسندگان

گروه علوم خاک، دانشکده کشاورزی، دانشگاه فردوسی مشهد، مشهد، ایران

10.22067/jsw.2023.84667.1339

چکیده

دستیابی به امنیت غذایی یک هدف بسیار ضروری برای تغذیه جمعیت رو به رشد جهان است، توسعه تکنیک‌های مناسب و کارآمد برای احیای خاک‌های متأثر از نمک بسیار ضروری است. استفاده از روش­های بیولوژیکی مانند کاربرد ریزجانداران مفید به‌عنوان اصلاح‌کننده‌های زیستی پتانسیل زیادی در بهبود شرایط رشد گیاه در خاک‌های شور دارد. هدف این مطالعه بررسی تأثیر کاربرد همزمان باکتری­های اسیدی­تیوباسیلوس و قارچ میکوریزی فانلی فورمیس موسه بر برخی متابولیت­های فتوسنتزی و بیوشیمیایی ذرت بود. برای این منظور یک آزمایش گلخانه­ای در قالب طرح کاملا تصادفی با آرایش فاکتوریل انجام شد. در این تحقیق اثر تیمارهای بیولوژیکی شامل: دو سطح قارچ میکوریزا (تلقیح و عدم تلقیح)، دو سطح شوری (96/0 و 6 دسی‌زیمنس بر متر) و چهار سطح تلقیح باکتری­های اسیدی تیوباسیلوس شامل شاهد (C)، تیوباسیلوس تیواکسیدانس (T)، تیوباسیلوس فرواکسیدانس (F)، تیوباسیلوس تیواکسیدانس و تیوباسیلوس فرواکسیدانس (T+F) در یک خاک بررسی شد. نتایج نشان داد که شوری غلظت کلروفیل a، b و کارتنوئید برگ را به‌ترتیب90/27،42/68 و 50 درصد در مقایسه با شاهد کاهش داد. شوری باعث افزایش، غلظت پرولین (62/42 درصد)، نشت الکترولیت (30/33 درصد)، غلظت آنتوسیانین­ها (36/96 درصد) و فلاونوئیدهای برگ (73/84 درصد) در مقایسه با خاک شاهد شد. تلقیح با قارچ میکوریزا در مقایسه با عدم تلقیح اثر قابل توجه و معنی‌داری بر همه پارامترهای مورد بررسی در هر دو خاک شور و شاهد داشت. در خاک شور تلقیح قارچ میکوریزا موجب کاهش نشت الکترولیت (75/56 درصد) و افزایش کلروفیل a (2/3 برابر)، کلروفیل b (6/6 برابر) کارتنوئید (3/1 برابر)، غلظت پرولین (39/24 درصد)، مقدار آنتوسیانین­ها (07/24 درصد) و فلاونوئیدها (40/20 در صد) در گیاه شد. تاثیر تیمارهای باکتریایی بر پارامترهای مورد بررسی در گیاهان تلقیح شده با قارچ میکوریزا بیشتر از گیاهان تلقیح نشده بود. اثرگذاری بر مقدار پرولین، کلروفیل­ها، آنتوسیانین و فلاونوئیدها در کاربرد توأم هر دو گونه باکتری بیشتر از تأثیر هر کدام به تنهایی بود. در خاک شور تلقیح همزمان قارچ میکوریزا با هر دو گونه باکتری موجب کاهش نشت الکترولیت (72/14 درصد) و افزایش کلروفیل a (80/39 درصد)، کلروفیل b (106 درصد)، کارتنوئید (50 درصد)، غلظت پرولین (12/10 درصد)، مقدار آنتوسیانین‌ها (17/14 درصد) و فلاونوئیدها (06/4 درصد) در گیاه در مقایسه با تیمار قارچ میکوریزا به تنهایی شد. نتایج نشان داد که این باکتری‌ها احتمالا می‌توانند به‌عنوان باکتری­های کمک کننده میکوریزا در نظر گرفته شوند.

کلیدواژه‌ها

موضوعات


عنوان مقاله [English]

The Effect of Funneliformis mosseae Fungus and Acidithiobacillus Application on Some Biochemical Metabolites of Maize (Zea mays L.) Exposed to Salinity Stress

نویسندگان [English]

  • J. Al-Jomah
  • A. Halajnia
  • A. Lakzian
  • A.R. Astaraei
Department of Soil Science, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran
چکیده [English]

Introduction
Saline soils resulting from natural and/or anthropogenic processes are very diverse and widely distributed under all climates. Soil salinity as a serious environmental problem has negative effects on plant growth and development in arid and semi-arid as well as humid regions. Since increasing global food security is a fundamental goal to feed the growing world population, it is necessary to develop suitable and efficient techniques for the rehabilitation of salt-affected soils and their exploitation. Chemical fertilizers are usually used to provide nutrients required for plant growth in order to increase crop yield, but application of these chemical components has negative environmental effects and reduces the quality of soils and agricultural products. The use of beneficial microorganisms (bacteria and fungi) as fertilizers and biological amendments has a high potential to improve productivity in saline soils. The aim of this study was to investigate the effect of using Acidithiobacillus bacteria along with mycorrhiza on the production of some photosynthetic and biochemical metabolites in maize under salt stress and comparing it with control conditions.
 
Materials and Methods
To perform this experiment, a surface soil sample was collected from a depth of 30 cm from the campus of Ferdowsi University of Mashhad, and some physical and chemical properties of the soil were measured by usual laboratory methods. To prepare saline soil a mixture of four compounds MgSO4.7H2O, Na2SO4, NaCl, and CaCl2. 2H2O were used. The mycorrhizal fungus (Funneliformis mosseae) and mesophilic Acidithiobacillus bacteria species two types of bacteria, Acidithiobacillus thiooxidans PTCC No: 1692 (DSM 504) and Acidithiobacillus ferrooxidans PTCC No: 1646 (DSM 583), were purchased from Turan Biotechnology Company (Semnan Science and Technology Park) and Iran Microbial Scientific and Industrial Research Center (PTCC), respectively. In this research, the effect of biological treatments including: two levels of mycorrhiza (inoculation and non-inoculation), two levels of salinity (0.96 and 6 d/m) and four levels of Acidithiobacillus control (C), Acidithiobacillus thiooxidans (T), Acidithiobacillus Ferrooxidans (F), Acidithiobacillus thiooxidans and Ferrooxidans (T+F) were compared with each other on some photosynthetic and biochemical characteristics of Zea mays under greenhouse conditions in the form of a completely randomized design with factorial arrangement with three replications. 10 gr of salt mixture (this amount of salt was obtained to reach electrical conductivity of 6 in the pre-experiment) was added to 5 kg of soil and the soil moisture of the pots was kept for one month in the field capacity. Bacterial treatments were inoculated with 30 mL of cell suspension per pot (approximately 107 CFU mL-1). In the simultaneous use of two bacteria, 15 ml of each bacterial cell suspension (15+15) was added to each pot. Single-cross 704 variety of maize was grown in pots and soil moisture was maintained during the growth period in the field capacity by weighing. Chlorophyll a, b and carotenoid, concentrations of flavonoids, anthocyanins and proline and electrical leakage were measured in fresh leaf samples (third leaf on the stem).
 
Results and Discussion
The results showed that salinity decreased the percentage of root colonization and chlorophyll a and b content in leaves. Salinity decreased chlorophyll a, b and carotenoid in leaves by 27.9, 68.42% and 50%, respectively. Salinity increased proline concentration (42.62%), electrolyte leakage (33.30%), anthocyanins concentration (96.36%) and leaf flavonoids (84.73%) compared to control soil. Inoculation with mycorrhiza compared to no inoculation had a remarkable and significant effect on all investigated parameters in both saline and control soils. In saline soil, mycorrhizal inoculation reduces electrolyte leakage (56.75%) and increases chlorophyll a (2.3 times), chlorophyll b (6.6 times), carotenoid (1.3 times), proline concentration (24.39%), anthocyanins amount (24.07) and flavonoids (20.4%) in the plant. The effect of bacterial treatments on the investigated parameters in plants inoculated with mycorrhiza was greater than non-inoculated treatments. The effectiveness of the simultaneous application of both bacteria was greater than the effect of each of them alone. In saline soil, simultaneous inoculation of mycorrhizae with both bacteria species reduces electrolyte leakage (14.72%) and increases chlorophyll a (39.80%), chlorophyll b (106%), carotenoid (50%), proline concentration (10.12%), the amount of anthocyanins (14.17%) and flavonoids (4.06%) compared to mycorrhiza treatment alone. The results showed that these bacteria can probably be considered as helping mycorrhizal bacteria.
 
Conclusion
The objective of this study was to examine the impact of simultaneous inoculation of mycorrhizae and Acidithiobacillus bacteria on select photosynthetic and biochemical metabolites of maize subjected to salinity stress conditions. Confirming the results of other studies, the results of this research also showed the clear and distinct effect of mycorrhiza on increasing chlorophyll and producing metabolites effective in increasing plant resistance to salt stress. In addition, the results showed that although the use of each species of Acidithiobacillus ferrooxidans and Acidithiobacillus thiooxidans alone was effective on the measured parameters in both saline and control soils, the simultaneous inoculation of both Acidithiobacillus bacteria species and mycorrhiza had the greatest effect on increasing chlorophyll, production of proline, anthocyanins and flavinoids and reducing electrolyte leakage and as a result, increasing tolerance to salt stress. In other words, these bacteria can be considered as mycorrhiza helper bacteria, whose activity can improve the function of mycorrhiza. On the other hand, mycorrhiza symbiosis may have increased the efficiency of these bacteria by changing the soil conditions and the environment around the roots. However, further greenhouse and field experiments with other plant species are necessary to confirm these findings.

کلیدواژه‌ها [English]

  • Biofertilizer
  • Mycorrhizal helping bacteria
  • Mycorrhizal symbiosis
  • Proline
  • Salt affected soils

©2023 The author(s). This is an open access article distributed under Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source.

  1. Abbas, A., Khan, S., Hussain, N., Hanjra, M.A., & Akbar, S. (2013). Characterizing soil salinity in irrigated agriculture using a remote sensing approach. Physics and Chemistry of the Earth, 55–57, 43–52. https://doi.org/ 10.1016/j.pce.2010.12.004
  2. Abdel Latef, A.A., Shaddad, M.A.K., Ismail, A.M., & Abu Alhmad, M.F.A. (2009). Benzyladenine can alleviate saline injury of two Roselle (Hibiscus sabdariffa) cultivars via equilibration of cytosolutes including anthocyanins. International Journal of Agriculture and Biology, 11, 151–157
  3. Abdel Latef, A.A.H., & Chaoxing, H. (2014). Does inoculation with Glomus mosseae improve salt tolerance in pepper plants? Journal of Plant Growth Regulation, 33, 644–653. https://doi.org/10.1007/s00344-014-9414-4
  4. Ai, Y., & Jane, J.L. (2016). Macronutrients in corn and human nutrition. Comprehensive Reviews in Food Science and Food Safety, 15, 581–598. https://doi.org/10.1111/1541-4337.12192
  5. Amanifar, S., Khodabandeloo, M., Mohseni Fard, E., Askari, M.S., & Ashrafi, M. (2019). Alleviation of Salt Stress and Changes in Glycyrrhizin Accumulation by Arbuscular Mycorrhiza in Liquorice (Glycyrrhiza glabra) Grown Under Salinity Stress. Environmental and Experimental Botany, 160, 25–34. https://doi.org/10.1016/ j.envexpbot.2019.01.001
  6. Armada, E., Probanza, A., Roldán, A., &. Azcón, R. (2016). Native Plant Growth Promoting Bacteria Bacillus thuringiensis and Mixed or Individual Mycorrhizal Species Improved Drought Tolerance and Oxidative Metabolism in Lavandula dentata Journal of Plant Physiology,192, 1–12. https://doi.org/10.1016/j.jplph.2015.11.007
  7. Arnon, A.N. (1967). Method of Extraction of Chlorophyll in the Plants. Agronomy Journal, 23, 112–12.1
  8. Asad, S.Q., Tesfaye, E., & Melese, M. (2018). Prospects of Alternative Copping Systems for Salt-Affected Soils in Ethiopia. Journal of Soil Science and Environmental Management, 9, 98–107. https://doi.org/10.5897/jssem2018. 0686
  9. Augé, R.M. (2001). Water Relations, Drought and Vesicular-Arbuscular Mycorrhizal Symbiosis. Mycorrhiza, 11, 3–42. https://doi.org/10.1007/s005720100097
  10. Barea, J.M., Pozo, M.J., Azcon, R., & Azcon-Aguilar, C. (2005). Microbial Co-Operation in the Rhizosphere. Journal of Experimental Botany, 56, 1761–1778. https://doi.org/10.1093/jxb/eri197
  11. Barin, M., Ali, A.N., & Samadi, A. (2006). Effects of NaCl-Induced and Salts Mixture Salinity on Leaf Proline and Growth of Tomato in Symbiosis with Arbuscular Mycorrhizal Fungi. ranian Journal of Agriculture Science, 37(1), 139-147. (In Persian).
  12. Bates, L.S., Waldren, R.P., & Teare, I.D. (1973). Rapid determination of free Proline for Water-Stress Studies. Plant and Soil, 39, 205–207. https://doi.org/10.1007/BF00018060
  13. Bharti, N., & Barnawal, D. (2019). Amelioration of salinity stress by PGPR. In: PGPR amelioration in sustainable agriculture. Food Security and Environmental Management, 85–106. https://doi.org/10.1016/B978-0-12-815879-1.00005-7
  14. Bothe, H. (2012). Arbuscular mycorrhiza and salt tolerance of plants. Symbiosis, 58, 7–16. https://doi.org/10.1007/s13199-012-0196-9
  15. Bourles, A., Guentas, L., Charvis, C., Gensous, S., Majorel, C., Crossay, T., Cavaloc, Y., Burtet-Sarramegna, V., Jourand, P., & Amir, H. (2020). Co-inoculation with a bacterium and arbuscular mycorrhizal fungi improves root colonization, plant mineral nutrition, and plant growth of a Cyperaceae plant in an ultramafic soil. Mycorrhiza, 30, 121–131. https://doi.org/10.1007/s00572-019-00929-8
  16. Camejo, D., Jiménez, A., Alarcón, J.J., Torres, W., Gómez, J.M., & Sevilla, F. (2006). Changes in photosynthetic parameters and antioxidant activities following heat-shock treatment in tomato plants. Functional Plant Biology, 33, 177–187. https://doi.org/10.1071/FP05067
  17. Campos, P.S., Quartin, V., Ramalho, J.C., & Nunes, M.A. (2003). Electrolyte leakage and lipid degradation account for cold sensitivity in leaves of Coffea plants. Journal of Plant Physiology, 160, 283–292. https://doi.org/10.1078/ 0176-1617-00833
  18. Carter, M.R., & Gregorich, E.G. (2007). Soil sampling and methods of analysis. CRC press. https://doi.org/ 10.1201/9781420005271
  19. Chen, M., Wang, Y., Chen, G., Ji, R., & Shi, W. (2021a). Effects of nitrogen fertilizer levels on nitrogen balance index and yield of hybrid super rice. Soils, 53, 700–706. https://doi.org/10.13758/j.cnki.tr.2021.04.005
  20. Chen, M., Zhang, S., Liu, L., Wu, L., & Ding, X. (2021b). Combined organic amendments and mineral fertilizer application increase rice yield by improving soil structure, P availability and root growth in saline-alkaline soil. Soil and Tillage Research, 212, 105060. https://doi.org/10.1016/j.still.2021.105060
  21. Chon, S.U., Boo, HO., Heo, B.G., & Gorinstein, S. (2012). Anthocyanin content and the activities of polyphenol oxidase, peroxidase and phenylalanine ammonia-lyase in lettuce cultivars. International Journal of Food Sciences and Nutrition, 63, 45–48. https://doi.org/10.3109/09637486.2011.595704
  22. Chu, T.N., Tran, B.T.H., Van Bui, L., & Hoang, M.T.T. (2019). Plant growth-promoting rhizobacterium Pseudomonas PS01 induces salt tolerance in Arabidopsis thaliana. BMC Research Notes, 12, 1–7. https://doi.org/ 10.1186/s13104-019-4046-1
  23. Csonka, L.N. (1989). Physiological and genetic responses of bacteria to osmotic stress. Microbiology Reviews, 53, 121–147. https://doi.org/10.1128/mmbr.53.1.121-147.1989
  24. Cui, Q., Xia, J., Yang, H., Liu, J., & Shao, P. (2021). Biochar and effective microorganisms promote Sesbania cannabina growth and soil quality in the coastal saline-alkali soil of the yellow river Delta, China. Science of the Total Environment, 756, 143801. https://doi.org/10.1016/j.scitotenv.2020.143801
  25. Daliran, T., Halajnia, A., & Lakzian, A. (2022). Thiobacillus bacteria-enhanced iron biofortification of soybean in a calcareous soil enriched with ferrous sulfate, mill scale, and Pyrite. Journal of Soil Science and Plant Nutrition, 22, 2221–2234. https://doi.org/10.1007/s42729-022-00804-0
  26. Demidchik, V., Straltsova, D., Medvedev, S.S., Pozhvanov, G.A., Sokolik, A., & Yurin V. (2014). Stress-induced electrolyte leakage: The role of K+-Permeable channels and involvement in programmed cell death and metabolic adjustment. Journal of Experimental Botany, 65, 1259–1270. https://doi.org/10.1093/jxb/eru004
  27. Duc, N.H., Csintalan, Z., & Posta, K. (2018). Arbuscular mycorrhizal fungi mitigate negative effects of combined drought and heat stress on tomato plants. Plant Physiology and Biochemistry, 132, 297–307. https://doi.org/ 10.1016/j.plaphy.2018.09.011
  28. Eren, E. (2022). The effect of plant growth promoting rhizobacteria (PGPRs) on yield and some guality parameters during shelf life in white button mushroom (Agaricus bisporus ). Journal of Fungi, 27, 10-16. https://doi.org/10.3390/jof8101016
  29. Eroğlu, G., Cabral, C., Ravnskov, S., Bak Topbjerg, H., & Wollenweber, B. (2020). Arbuscular mycorrhiza influences carbon-use efficiency and grain yield of wheat grown under pre- and post-anthesis salinity stress. Plant Biology, 22, 863–871. https://doi.org/10.1111/plb.13123
  30. FAO. (1947). Food and agriculture organization of the United Nations. International Organization, 1, 350–353. https://doi.org/10.1017/S0020818300006160
  31. Fazal, A., & Bano, A. (2016). Role of plant growth-promoting rhizobacteria (PGPR), biochar, and chemical fertilizer under salinity stress. Communications in Soil Science and Plant Analysis, 47, 1985–1993. https://doi.org/10.1080/00103624.2016.1216562
  32. Frey-Klett, P., Garbaye, J., & Tarkka, M. (2007). The mycorrhiza helper bacteria revisited. New Phytologist, 176, 22–36. https://doi.org/10.1111/j.1469-8137.2007.02191.x
  33. Garbaye, J. (1994). Tansley Review No. 76 Helper Bacteria: A new dimension to the mycorrhizal symbiosis. New Phytologist, 128, 197–210. https://doi.org/10.1111/j.1469-8137.1994.tb04003.x
  34. Garcia Junior, O. (1992). O enxofre e suas transformações microbianas. Microbiol do solo, 319–329
  35. Geetha, S., Sai Ram, M., Mongia, S.S., Singh, V., Ilavazhagan, G., & Sawhney, R.C. (2003). Evaluation of antioxidant activity of leaf extract of Seabuckthorn (Hippophae rhamnoides ) on chromium (VI) induced oxidative stress in albino rats. Journal of Ethnopharmacology, 87, 247–251. https://doi.org/10.1016/S0378-8741(03)00154-5
  36. Giovannetti, M., & Mosse, B. (1980). An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytologist, 84, 489–500. https://doi.org/10.1111/j.1469-8137.1980.tb04556.x
  37. Hajiboland, R. (2013). Role of arbuscular mycorrhiza in amelioration of salinity. In: Ahmad, P., Azooz, M.M., Prasad, M.N.V. (eds) Salt Stress in Plants. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-6108-1_13
  38. Hameed, A., Dilfuza, E., Abd-Allah, E.F., Hashem, A., Kumar, A., & Ahmad, P. (2014). Salinity stress and arbuscular mycorrhizal symbiosis in plants. In: Miransari, M. (eds) Use of Microbes for the Alleviation of Soil Stresses, Volume 1. Springer, New York, NY. 139–159. https://doi.org/10.1007/978-1-4614-9466-9_7
  39. Hamidian, M., Movahhedi-Dehnavi, M., Sayyed, R.Z., Almalki, W.H., Gafur, A., & Fazeli-Nasab, B. (2023). Author correction: Co-application of mycorrhiza and methyl jasmonate regulates morpho-physiological and antioxidant responses of Crocus sativus (Saffron) under salinity stress conditions. Scientific Reports, 13, 73-78. https://doi.org/ 10.1038/s41598-023-35118-3
  40. He, Z.Q,. He, C.X., Zhang, Z.B., Zou, Z.R., & Wang, H.S. (2007). Changes of antioxidative enzymes and cell membrane osmosis in tomato colonized by arbuscular mycorrhizae under NaCl stress. Colloids Surfaces B: Biointerfaces, 59, 128–133. https://doi.org/10.1016/j.colsurfb.2007.04.023
  41. Heydari, S., & Pirzad, A. (2021a). Improvement of the yield-related response of mycorrhized Lallemantia iberica to salinity through sulfur-oxidizing bacteria. Journal of the Science of Food and Agriculture, 101, 3758–3766. https://doi.org/10.1002/jsfa.11007
  42. Heydari, S., & Pirzad, A. (2021b). Efficiency of Funneliformis mosseae and Thiobacillus sp. on the secondary metabolites (essential oil, seed oil and mucilage) of Lallemantia iberica under salinity stress. Journal of Horticultural Science and Biotechnology, 96, 249–259. https://doi.org/10.1080/14620316.2020.1833764
  43. Heydari, S., & Pirzad, A. (2020). Mycorrhizal fungi and Thiobacillus co-inoculation improve the physiological indices of Lallemantia iberica under salinity stress. Current Microbiology, 77, 2523–2534. https://doi.org/10.1007/s00284-020-02034-y
  44. Jahantigh, O., Najafi, F., Naghdi Badi, H.A., Khavari-Nejad, R.A., & Sanjarian, F. (2016). Changes in antioxidant enzymes activities and proline, total phenol and anthocyanine contents in Hyssopus officinalis plants under salt stress. Biologia Futura, 67, 195–204. https://doi.org/10.1556/018.67.2016.2.7
  45. Jaleel, C.A., Manivannan, P., Lakshmanan, G.M.A., Sridharan, R., & Panneerselvam, R. (2007). NaCl as a physiological modulator of proline metabolism and antioxidant potential in Phyllanthus amarus. Comptes Rendus Biologies, 330, 806–813. https://doi.org/10.1016/j.crvi.2007.08.009
  46. Kandpal, G. (2021). Review on impact of chemical fertilizers on environment. International Journal of Modern Agriculture, 10(1), 758–763.
  47. Karlidag, H., Yildirim, E., Turan, M., Pehluvan, M., & Donmez, F. (2013). Plant growth-promoting rhizobacteria mitigate deleterious effects of salt stress on strawberry plants (Fragaria ananassa). HortScience, 48, 563–567. https://doi.org/10.21273/hortsci.48.5.563
  48. Kaur, S., Tiwari, V., Kumari, A., Chaudhary, E,m Sharma, A., Ali, U., & Garg, M. (2023). Protective and defensive role of anthocyanins under plant abiotic and biotic stresses: An emerging application in sustainable agriculture. Journal of Biotechnology, 361, 12–29. https://doi.org/10.1016/j.jbiotec.2022.11.009
  49. Koç, A., Balcı, G., Ertürk, Y., Keles, H., Bakoğlu, N., & Ercişli, S. (2016). Influence of arbuscular mycorrhizae and plant growth promoting rhizobacteria on proline content, membrane permeability and growth of strawberry (Fragaria x ananassa Duch.) under salt stress. Journal of Applied Botany and Food Quality, 89, 89-97. https://doi.org/10.5073/JABFQ.2016.089.011
  50. Krizek, D.T., Britz, S.J., & Mirecki, R.M. (1998). Inhibitory effects of ambient levels of solar UV-A and UV-B radiation on growth of CV. new red fire lettuce. Plant Physiology, 103, 1–7. https://doi.org/10.1034/j.1399-3054.1998.1030101.x
  51. Kumar, S. (2012). Assay guided comparison for enzymatic and non-enzymatic antioxidant activities with special reference to medicinal plants. Antioxidant Enzyme, 14, 382–400. https://doi.org/10.5772/50782
  52. Labbé, J.L., Weston, D.J., Dunkirk, N., Pelletier, D.A., & Tuskan, G.A. (2014). Newly identified helper bacteria stimulate ectomycorrhizal formation in populus. Front Plant Science, 5, 579. https://doi.org/10.3389/fpls.2014.00579
  53. Lei, P., Xu, Z., Liang, J., Luo, X., Zhang, Y., Feng, X., & Xu, H. (2016). Poly (γ-glutamic acid) enhanced tolerance to salt stress by promoting proline accumulation in Brassica napus Plant Growth Regulation, 78, 233–241. https://doi.org/10.1007/s10725-015-0088-0
  54. Li, P., Qian, H., Howard, K.W.F., & Wu, J. (2015). Building a new and sustainable ‘silk road economic Belt’ Environmental Earth Sciences, 74, 7267–7270. https://doi.org/10.1007/s12665-015-4739-2
  55. Liu, H., Tang, H., Ni, X., Zhang, Y., & Wang,Y. (2022). Impact of an arbuscular mycorrhizal fungal inoculum and exogenous methyl jasmonate on the performance of tall fescue under saline-alkali condition. Frontiers in Microbiology, 13, 902667. https://doi.org/10.3389/fmicb.2022.902667
  56. Mamba, S.F., Salam, A., & Peter, G. (2016). Farmers’ perception of climate change a case study in Swaziland. Journal of Food Security, 3, 47–61. https://doi.org/10.12691/jfs-3-2-3
  57. Mcfarland, J. (1907). The nephelometer: An instrument for estimating the number of bacteria in suspensions used for calculating the opsonic index and for vaccines. The Journal of the American Medical Association, XLIX, 1176–1178. https://doi.org/10.1001/jama.1907.25320140022001f
  58. Mohamed, A.A., Eweda, W.E.E., Heggo, A.M., & Hassan, E.A. (2014). Effect of dual inoculation with arbuscular mycorrhizal fungi and sulphur-oxidising bacteria on onion (Allium cepa ) and maize (Zea mays L.) grown in sandy soil under green house conditions. Annals of Agricultural Sciences, 59, 109–118. https://doi.org/10.1016/ j.aoas.2014.06.015
  59. Heidari, M. (2011). Effects of salinity stress on growth, chlorophyll content and osmotic components of two Basil (Ocimum basilicum ) genotypes. African Journal of Biotechnology, 11, 379–384. https://doi.org/10.5897/ ajb11.2572
  60. Mostafavian, S.R., Pirdashti, H., Ramzanpour, M.R., Andarkhor, A.A., & Shahsavari, A. (2008). Effect of mycorrhizae, Thiobacillus and sulfur nutrition on the chemical composition of soybean [Glycine max (L.)] Merr. Seed. Pakistan Journal of Biological Sciences, 11, 826–835. https://doi.org/10.3923/pjbs.2008.826.835
  61. Oliveira, M de S., da Silva Campos, M.A., de Albuquerque, U.P., & da Silva, F.S.B. (2013). Arbuscular Mycorrhizal Fungi (AMF) Affects Biomolecules Content in Myracrodruon urundeuva Industrial Crops and Products, 50, 244–247. https://doi.org/10.1016/j.indcrop.2013.07.041
  62. Phillips, J.M., & Hayman, D.S. (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-IN18. https://doi.org/10.1016/s0007-1536(70)80110-3
  63. Pirzad, A., & Mohammadzadeh, S. (2018). Water use efficiency of three mycorrhizal Lamiaceae species (Lavandula officinalis, Rosmarinus officinalis and Thymus vulgaris). Agricultural Water Management, 204, 1–10. https://doi. org/10.1016/j.agwat.2018.03.020
  64. Pokorna, D., & Zabranska, J. (2015). Sulfur-oxidizing bacteria in environmental technology. Biotechnology Advances, 33, 1246–1259. https://doi.org/10.1016/j.biotechadv.2015.02.007
  65. Rahimzadeh, S., Sohrabi, Y., Heidari, G., Pirzad, A., & Ghassemi Golezani, K. (2016). Effect of bio-fertilizers on the essential oil yield and components isolated from Dracocephalum moldavica using nanoscale injection method. Journal of Essential Oil Bearing Plants, 19, 529–541. https://doi.org/10.1080/0972060X.2014.935057
  66. Ratti, N., Verma, H.N., & Gautam, S.P. (2010). Effect of Glomus species on physiology and biochemistry of Catharanthus roseus. Indian Journal of Microbiology, 50, 355–360. https://doi.org/10.1007/s12088-010-0012-2
  67. 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. Journal of Soil Science and Plant Nutrition, 19, 321–331. https://doi.org/10.1007/s42729-019-00032-z
  68. Sarker, U., Islam, M.T., & Oba, S. (2019). Salinity Stress Accelerates Nutrients, Dietary Fiber, Minerals, Phytochemicals and Antioxidant Activity in Amaranthus tricolor PLoS One, 13, e0206388. https://doi.org/ 10.1371/journal.pone.0206388
  69. Singh, J., & Thakur, J.K. (2018). Photosynthesis and Abiotic Stress in Plants. In: Vats, S. (eds) Biotic and Abiotic Stress Tolerance in Plants. Springer, Singapore. https://doi.org/10.1007/978-981-10-9029-5_2
  70. Wagner, G.J. (1979). Content and Vacuole/Extravacuole Distribution of Neutral Sugars, Free Amino Acids, and Anthocyanin in Protoplasts. Plant Physiology, 64, 88–93. https://doi.org/10.1104/pp.64.1.88
  71. Wang, Y.F., Wang, S.P., Cui, X.Y., Chen, Z.Z., Schnug, E., & Haneklau, S. (2003). Effects of sulphur supply on the morphology of shoots and roots of alfalfa (Medicago sativa L.). Grass and Forage Science, 58, 160–167. https:// doi.org/10.1046/j.1365-2494.2003.00366.x
  72. Zhang, T., Hu, Y., Zhang, K., Tian, C., & Guo, J. (2018) Arbuscular mycorrhizal fungi improve plant growth of Ricinus communis by altering photosynthetic properties and increasing pigments under drought and salt stress. Industrial Crops and Products, 117, 13–19. https://doi.org/10.1016/j.indcrop.2018.02.087
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دوره 38، شماره 1 - شماره پیاپی 93
فروردین و اردیبهشت 1403
صفحه 85-104
  • تاریخ دریافت: 08 مهر 1402
  • تاریخ بازنگری: 22 آبان 1402
  • تاریخ پذیرش: 23 آبان 1402
  • تاریخ اولین انتشار: 24 آبان 1402