Alleviating Salinity Stress in Almond Plants through Rhizophagus irregularis Inoculation: A Greenhouse Study

Otabek Bobojonov ¹ (Lecturer of the Department of Fruits and Vegetables at the Urganch State University, Khorazm Region, Uzbekistan ) Uday Abdul-Reda Hussein ² (Colleges of Pharmacy, University of Al-Ameed, Karbala, Iraq ) Ali Obaid Hajray ³ (Department of Dentistry, Al-Manara College for Medical Sciences, (Maysan), Iraq )
Mohaned Mohammed Hani ⁴ (Department of Medical Instrumentation Engineering Techniques, Imam Ja'afar Al-Sadiq University, Al‐Muthanna, 66002, Iraq) Salam Ahjel ⁵ (Department of Pharmacy, Al-Zahrawi University College, Karbala, Iraq ) Amran Mezher Lawas ⁶ (Mazaya university college , Iraq) Abed J. Kadhim ⁷ (Al-Nisour University College,Iraq) Sada Ghalib Al- Musawi ⁸ (college of pharmacy, National University of Science and Technology, Dhi Qar, Iraq) Manzura Kamalova ⁹ (Candidate of Biological Sciences, Associate Professor of the Department of Environmental Monitoring, National University of Uzbekistan named after Mirzo Ulugbek, Tashkent city,Uzbekistan) H.F. Hamroev ¹⁰ (Tashkent State Agrarian University, Tashkent Region Kibray District, University Street 2, Tashkent, Uzbekistan ) Jurabekova Khabiba ¹¹ (Andijan machine-building institute, Andijan, Uzbekistan, Western Caspian University, Scientific Researcher, Baku, Azerbaijan ) A.K. Mukhiddin Ugli ¹² (International School of Finance and Technology, Tashkent, Uzbekistan)

تاریخ ارسال : 1402/07/21 تاریخ تایید : 1403/03/21

کلید واژه: Antioxidant enzymes, Rhizophagus irregulari, Salinity levels,

چکیده مقاله :

Soil salinity significantly limits crop productivity. This study explores the role of the mycorrhizal fungus Rhizophagus irregularis (Ri) in enhancing the antioxidant system and pigment concentrations in almond plants (Prunus dulcis) under salinity stress, aiming to reduce salt-induced toxicity and offer potential solutions for saline agriculture. The experiment used almond seeds grown under varying salinity levels (0, 25, 50, and 100 mM NaCl) and Ri inoculation. Parameters including root colonization percentage, growth parameters, plant pigment concentrations, and antioxidant enzyme activity were analyzed. Results revealed that salinity significantly impacted all parameters, with a notable reduction in both wet and dry weights of shoots and roots as salinity increased. Shoot dry weight decreased from 1.87 g to 0.58 g in Ri plants and from 1.39 g to 0.60 g in non-Ri plants as salinity increased from 0 to 100 mM NaCl. Additionally, root colonization by Ri showed a significant decrease from 47.12% under non-saline conditions to 8.23% under high salinity (100 mM NaCl). Ri treatment had a significant effect on several parameters except for carotenoid levels and catalase enzyme activity. For instance, Ri inoculation resulted in increased chlorophyll levels (from 3.57 mg g-1 to 4.78 mg g-1 in control plants and from 1.58 mg g-1 to 2.21 mg g-1 under high salinity) and flavonoid quantities (from 4.78 mg g-1 to 5.80 mg g-1 in control plants and from 6.46 mg g-1 to 6.68 mg g-1 under high salinity) compared to non-inoculated plants, irrespective of salinity conditions. The data also demonstrated that salinity was the primary determinant of catalase enzyme activity in both shoot and root tissues, with a corresponding increase in catalase activity as salinity increased. For instance, shoot catalase activity increased from 1.30 mg protein min-1 to 2.35 mg protein min-1 in Ri plants and from 1.16 mg protein min-1 to 2.24 mg protein min-1 in non-Ri plants with increasing salinity. In conclusion, Ri inoculation can potentially mitigate the adverse effects of salinity in almond plants by enhancing certain growth parameters and antioxidant activity, as indicated by the statistically significant interactions between salinity and Ri.

چکیده انگلیسی :

Soil salinity significantly limits crop productivity. This study explores the role of the mycorrhizal fungus Rhizophagus irregularis (Ri) in enhancing the antioxidant system and pigment concentrations in almond plants (Prunus dulcis) under salinity stress, aiming to reduce salt-induced toxicity and offer potential solutions for saline agriculture. The experiment used almond seeds grown under varying salinity levels (0, 25, 50, and 100 mM NaCl) and Ri inoculation. Parameters including root colonization percentage, growth parameters, plant pigment concentrations, and antioxidant enzyme activity were analyzed. Results revealed that salinity significantly impacted all parameters, with a notable reduction in both wet and dry weights of shoots and roots as salinity increased. Shoot dry weight decreased from 1.87 g to 0.58 g in Ri plants and from 1.39 g to 0.60 g in non-Ri plants as salinity increased from 0 to 100 mM NaCl. Additionally, root colonization by Ri showed a significant decrease from 47.12% under non-saline conditions to 8.23% under high salinity (100 mM NaCl). Ri treatment had a significant effect on several parameters except for carotenoid levels and catalase enzyme activity. For instance, Ri inoculation resulted in increased chlorophyll levels (from 3.57 mg g-1 to 4.78 mg g-1 in control plants and from 1.58 mg g-1 to 2.21 mg g-1 under high salinity) and flavonoid quantities (from 4.78 mg g-1 to 5.80 mg g-1 in control plants and from 6.46 mg g-1 to 6.68 mg g-1 under high salinity) compared to non-inoculated plants, irrespective of salinity conditions. The data also demonstrated that salinity was the primary determinant of catalase enzyme activity in both shoot and root tissues, with a corresponding increase in catalase activity as salinity increased. For instance, shoot catalase activity increased from 1.30 mg protein min-1 to 2.35 mg protein min-1 in Ri plants and from 1.16 mg protein min-1 to 2.24 mg protein min-1 in non-Ri plants with increasing salinity. In conclusion, Ri inoculation can potentially mitigate the adverse effects of salinity in almond plants by enhancing certain growth parameters and antioxidant activity, as indicated by the statistically significant interactions between salinity and Ri.

منابع و مأخذ:

Akca Y, Sahin U (2022) Responses of ‘Chandler’ walnut variety grafted onto different rootstocks to salt stress. International Journal of Horticultural Science and Technology. 9, 1-13.
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. Scientia Horticulturae 253, 429–438.
Ali I, Tawaha AR, Khan MD, Samir R, Sachan K, Devgon I, Karnwal A (2022) Biochemical and Molecular Mechanism of Wheat to Diverse Environmental Stresses. In: Roychoudhury, A., Aftab, T., Acharya, K. (Eds.), Omics Approach to Manage Abiotic Stress in Cereals. Springer Nature Singapore, Singapore. 435–446. doi: 10.1007/978-981-19-0140-9_16
Benton TG, Bieg C, Harwatt H, Pudasaini R, Wellesley L (2021) Food system impacts on biodiversity loss. Three Levers for Food System Transformation in Support of Nature. Chatham House, London. 02–03.
Beyk-Khormizi A, Sarafraz-Ardakani MR, Hosseini Sarghein S, Moshtaghioun SM, Mousavi-Kouhi SM, Taghavizadeh Yazdi ME (2023) Effect of Organic Fertilizer on the Growth and Physiological Parameters of a Traditional Medicinal Plant under Salinity Stress Conditions. Horticulturae. 9, 701.
Bukhari SAH, Peerzada AM, Javed MH, Dawood M, Hussain N, Ahmad S (2019) Growth and Development Dynamics in Agronomic Crops Under Environmental Stress. In: Hasanuzzaman, M. (Ed.), Agronomic Crops. Springer Singapore, Singapore, 83–114. doi: 10.1007/978-981-32-9151-5_6
Chaudhry S, Sidhu GPS (2022) Climate change regulated abiotic stress mechanisms in plants: a comprehensive review. Plant Cell Reports. 41, 1–31. doi: 10.1007/s00299-021-02759-5.
Chaudhry UK, Gökçe ZNÖ, Gökçe AF (2021) The influence of salinity stress on plants and their molecular mechanisms. Biology and Life Sciences Forum. 11, 1, 31.
Chourasia KN, Lal MK, Tiwari RK, Dev D, Kardile HB, Patil VU, Kumar A, Vanishree G, Kumar D, Bhardwaj V (2021) Salinity stress in potato: Understanding physiological, biochemical and molecular responses. Life. 11, 545.
Dowarah B, Gill SS, Agarwala N (2022) Arbuscular Mycorrhizal Fungi in Conferring Tolerance to Biotic Stresses in Plants. Journal of Plant Growth Regulation. 41, 1429–1444. doi: 10.1007/s00344-021-10392-5
Fayaz F, Zahedi M (2022) Beneficial effects of arbuscular mycorrhizal fungi on wheat (Triticum aestivum L.) nutritional status and tolerance indices under soil salinity stress. Journal of Plant Nutrition. 45, 185–201. doi: 10.1080/01904167.2021.1952228
Gao Y, Huang S, Wang Y, Lin H, Pan Z, Zhang S, Zhang J, Wang W, Cheng S, Chen Y (2023) Analysis of the molecular and biochemical mechanisms involved in the symbiotic relationship between Arbuscular mycorrhiza fungi and Manihot esculenta Crantz. Frontiers in Plant Science. 14, 1130924.
Gardner B (2013) Global food futures: feeding the world in 2050. Bloomsbury Publishing.
Garg N, Singla P (2016) Stimulation of nitrogen fixation and trehalose biosynthesis by naringenin (Nar) and arbuscular mycorrhiza (AM) in chickpea under salinity stress. Plant Growth Regulation. 80, 5–22. doi: 10.1007/s10725-016-0146-2
Gong M, Bai N, Wang P, Su J, Chang Q, Zhang Q (2023) Co-Inoculation with Arbuscular Mycorrhizal Fungi and Dark Septate Endophytes under Drought Stress: Synergistic or Competitive Effects on Maize Growth, Photosynthesis, Root Hydraulic Properties and Aquaporins? Plants. 12, 2596.
Haghighi TM, Saharkhiz MJ, Kavoosi G, Zarei M (2023) Adaptation of Glycyrrhiza glabra L. to water deficiency based on carbohydrate and fatty acid quantity and quality. Scientific Reports. 13, 1766.
He W, Fan X, Zhou Z, Zhang H, Gao X, Song F, Geng G (2020) The effect of Rhizophagus irregularis on salt stress tolerance of Elaeagnus angustifolia roots. Journal of Forestry Research. 31, 2063–2073. doi: 10.1007/s11676-019-01053-1
Heidarianpour MB, Aliasgharzad N, Olsson PA (2020) Positive effects of co-inoculation with Rhizophagus irregularis and Serendipita indica on tomato growth under saline conditions, and their individual colonization estimated by signature lipids. Mycorrhiza 30, 455–466. doi: 10.1007/s00572-020-00962-y
Hopmans JW, Qureshi AS, Kisekka I, Munns R, Grattan SR, Rengasamy P, Ben-Gal A, Assouline S, Javaux M, Minhas PS (2021) Critical knowledge gaps and research priorities in global soil salinity. Advances in Agronomy. 169, 1–191.
Ishtiaq M, Mazhar MW, Maqbool M, Hussain T, Hussain SA, Casini R, Abd-ElGawad AM, Elansary HO (2023) Seed priming with the selenium nanoparticles maintains the redox status in the water stressed tomato plants by modulating the antioxidant defense enzymes. Plants. 12)7(, 1556.
Karle SB, Guru A, Dwivedi P, Kumar K (2021) Insights into the Role of Gasotransmitters Mediating Salt Stress Responses in Plants. Journal of Plant Growth Regulation. 40, 2259–2275. doi: 10.1007/s00344-020-10293-z
Kumar A, Dames JF, Gupta A, Sharma S, Gilbert JA, Ahmad P (2015) Current developments in arbuscular mycorrhizal fungi research and its role in salinity stress alleviation: a biotechnological perspective. Critical Reviews in Biotechnology. 35, 461–474. doi: 10.3109/07388551.2014.899964
Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: Measurement and characterization by UV-VIS spectroscopy. Current Protocols in Food Analytical Chemistry. 1, F4-3.
Liu CY, Zou YN, Zhang DJ, Shu B, Wu QS (2019) Mycorrhizae and Tolerance of Abiotic Stress in Citrus Plants. In: Giri, B., Prasad, R., Wu, Q.-S., Varma, A. (Eds.), Biofertilizers for Sustainable Agriculture and Environment, Soil Biology. Springer International Publishing, Cham. 465–487. doi: 10.1007/978-3-030-18933-4_21
Lotfi N, Soleimani A, Çakmakçı R, Vahdati K, Mohammadi P (2022) Characterization of plant growth-promoting rhizobacteria (PGPR) in Persian walnut associated with drought stress tolerance. Scientific Report 12, 12725.
Lotfi N, Vahdati K, Kholdebarin B and Amiri R (2010) Drought-induced accumulation of sugars and proline in radicle and plumule of tolerant walnut varieties during germination phase. Acta Horticulturae. 861, 289-296.
Lotfi N, Vahdati K, Kholdebarin B, Ashrafi EN (2009) Germination, mineral composition, and ion uptake in walnut under salinity conditions. HortScience. 44(5), 1352–1357.
Ma Y, Dias MC, Freitas H (2020) Drought and salinity stress responses and microbe-induced tolerance in plants. Frontiers in Plant Science. 11, 591911.
Mariyam S, Bhardwaj R, Khan NA, Sahi SV, Seth CS (2023) Review on nitric oxide at the forefront of rapid systemic signaling in mitigation of salinity stress in plants: Crosstalk with calcium and hydrogen peroxide. Plant Science. 111835.
McGONIGLE TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular—arbuscular mycorrhizal fungi. New Phytologist. 115, 495–501. doi: 10.1111/j.1469-8137.1990.tb00476.x
Moradbeygi H, Jamei R, Heidari R, Darvishzadeh R (2020) Investigating the enzymatic and non-enzymatic antioxidant defense by applying iron oxide nanoparticles in Dracocephalum moldavica L. plant under salinity stress. Scientia Horticulturae. 272, 109537.
Mukhopadhyay R, Sarkar B, Jat HS, Sharma PC, Bolan NS (2021) Soil salinity under climate change: Challenges for sustainable agriculture and food security. Journal of Environmental Management. 280, 111736.
Munns R, Tester M (2008) Mechanisms of Salinity Tolerance. Annual Review of Plant Biology. 59, 651–681. doi: 10.1146/ annurev. arplant.59.032607.092911
Negrão S, Schmöckel SM, Tester M (2017) Evaluating physiological responses of plants to salinity stress. Annals of Botany. 119, 1–11.
Pandey R, Garg N (2017) High effectiveness of Rhizophagus irregularis is linked to superior modulation of antioxidant defence mechanisms in Cajanus cajan (L.) Millsp. genotypes grown under salinity stress. Mycorrhiza. 27, 669–682. doi: 10.1007/s00572-017-0778-8
Sarker U, Oba S, Daramy MA (2020) Nutrients, minerals, antioxidant pigments and phytochemicals, and antioxidant capacity of the leaves of stem amaranth. Scientific Reports. 10, 3892.
Singh A (2022) Soil salinity: A global threat to sustainable development. Soil Use and Management. 38, 39–67. doi: 10.1111/sum.12772
Singh N, Mansoori A, Dey D, Kumar R, Kumar A (2021) Potential of Metabolomics in Plant Abiotic Stress Management. In: Kumar A, Kumar R, Shukla P, Patel HK (Eds.), Omics Technologies for Sustainable Agriculture and Global Food Security (Vol II). Springer Singapore, Singapore. 193–214. doi: 10.1007/978-981-16-2956-3_7
Tran BT, Watts-Williams SJ, Cavagnaro TR (2019) Impact of an arbuscular mycorrhizal fungus on the growth and nutrition of fifteen crop and pasture plant species. Functional Plant Biology. 46, 732–742.
Zhu X, Song F, Liu S, Liu F (2016) Role of Arbuscular Mycorrhiza in Alleviating Salinity Stress in Wheat (Triticum aestivum L.) Grown Under Ambient and Elevated CO2. Journal of Agronomy and Crop Science. 202, 486–496. doi: 10.1111/jac.12175