Arbuscular Mycorrhizal Fungi Modulate Photosynthetic Gene Expression (rbcl, rbcs, psbA, psbD) to Enhance Salinity Tolerance in Pistacia vera
Subject Areas : Plant Physiology
Hanieh Hamzehzadeh
1
,
Hossein Abbaspour
2
*
,
Akbar Safipour Afshar
3
,
Seyed Mohammad Mahdi Hamdi
4
1 - Department of Biology, Damghan Branch, Islamic Azad University, Damghan, Iran
2 - Department of Biology, North Tehran Branch, Department of Biology, North Tehran Branch, Islamic Azad University, Tehran, Iran, Tehran, Iran
3 - Department of Biology, Neyshabur Branch, Islamic Azad University, Neyshabur, Iran
4 - Department of Biology, Central Tehran Branch, Islamic Azad University, Tehran, Iran
Keywords: Pistachio, Mycorrhizae, photosynthesis, gene expression ,
Abstract :
This study investigated the role of arbuscular mycorrhizal fungi (AMF) in mitigating salinity stress in Pistacia vera L. cv. Ohadi. A greenhouse pot experiment was conducted using a randomized complete block design with two factors: Glomus mosseae inoculation (inoculated or non-inoculated) and salinity (control or 12 dS m⁻¹ NaCl). While salinity reduced AMF colonization from 67% to 43%, AMF-inoculated plants consistently exhibited superior performance compared to non-mycorrhizal plants. Salinity stress significantly decreased shoot and root biomass, total chlorophyll content, and net photosynthetic rate (Pn) in both groups. However, AMF symbiosis significantly ameliorated these negative effects, resulting in higher biomass, chlorophyll content, and a notably higher Pn (38.8% increase) under saline conditions. Furthermore, AMF inoculation altered the chlorophyll a/b ratio under salinity, suggesting an adaptive response in light-harvesting. Molecular analysis revealed that while salinity downregulated psbA, psbD, rbcL, and rbcS expression, AMF differentially upregulated psbA (under both conditions), psbD (specifically under salinity), and rbcL (under both conditions). Additionally, AMF improved shoot potassium (K) content and upregulated the expression of the SKOR gene, involved in K+ transport, under both control and saline conditions. These findings demonstrate that AMF symbiosis enhances salinity tolerance in pistachio by improving K nutrition, modulating photosynthetic gene expression, and consequently, maintaining photosynthetic efficiency under stress.
Afshar, A. S. and H. Abbaspour. 2023. Mycorrhizal symbiosis alleviate salinity stress in pistachio plants by altering gene expression and antioxidant pathways. Physiology and Molecular Biology of Plants, 29, (2) 263-276.
Bhantana, P., M. S. Rana, X.-C. Sun, M. G. Moussa, M. H. Saleem, M. Syaifudin, A. Shah, A. Poudel, A. B. Pun and M. A. Bhat. 2021. Arbuscular mycorrhizal fungi and its major role in plant growth, zinc nutrition, phosphorous regulation and phytoremediation. Symbiosis, 84, 19-37.
Biermann, B. and R. Linderman. 1981. Quantifying vesicular‐arbuscular mycorrhizae: a proposed method towards standardization. New phytologist, 87, (1) 63-67.
Chen, J., H. Zhang, X. Zhang and M. Tang. 2017. Arbuscular mycorrhizal symbiosis alleviates salt stress in black locust through improved photosynthesis, water status, and K+/Na+ homeostasis. Frontiers in plant science, 8, 1739.
Diagne, N., M. Ngom, P. I. Djighaly, D. Fall, V. Hocher and S. Svistoonoff. 2020. Roles of arbuscular mycorrhizal fungi on plant growth and performance: Importance in biotic and abiotic stressed regulation. Diversity, 12, (10) 370.
Fan, L., C. Zhang, J. Li and Y. Liu. 2024. The use of Arbuscular mycorrhizal fungi to alleviate the growth and photosynthetic characteristics of strawberry under salt stress. Acta Physiologiae Plantarum, 46, (12) 1-9.
Ghorbani, A., V. O. G. Omran, S. M. Razavi, H. Pirdashti and M. Ranjbar. 2019. Piriformospora indica confers salinity tolerance on tomato (Lycopersicon esculentum Mill.) through amelioration of nutrient accumulation, K+/Na+ homeostasis and water status. Plant Cell Reports, 38, 1151-1163.
Hao, S., Y. Wang, Y. Yan, Y. Liu, J. Wang and S. Chen. 2021. A review on plant responses to salt stress and their mechanisms of salt resistance. Horticulturae, 7, (6) 132.
Igwegbe, C. A., J. O. Ighalo, S. Ghosh, S. Ahmadi and V. I. Ugonabo. 2023. Pistachio (Pistacia vera) waste as adsorbent for wastewater treatment: a review. Biomass Conversion and Biorefinery, 13, (10) 8793-8811.
Karima, B., H. Amima, M. Ahlam, B. Zoubida, T. Benoît, D. Yolande and L.-H. S. Anissa. 2023. Native arbuscular mycorrhizal inoculum modulates growth, oxidative metabolism and alleviates salinity stresses in legume species. Current Microbiology, 80, (2) 66.
Kashaninejad, M., A. Mortazavi, A. Safekordi and L. Tabil. 2006. Some physical properties of Pistachio (Pistacia vera L.) nut and its kernel. Journal of Food Engineering, 72, (1) 30-38.
Kumar, A., J. F. Dames, A. Gupta, S. Sharma, J. A. Gilbert and P. Ahmad. 2015. Current developments in arbuscular mycorrhizal fungi research and its role in salinity stress alleviation: a biotechnological perspective. Critical Reviews in Biotechnology, 35, (4) 461-474.
Liu, M.-Y., Q.-S. Li, W.-Y. Ding, L.-W. Dong, M. Deng, J.-H. Chen, X. Tian, A. Hashem, A.-B. F. Al-Arjani and M. M. Alenazi. 2023. Arbuscular mycorrhizal fungi inoculation impacts expression of aquaporins and salt overly sensitive genes and enhances tolerance of salt stress in tomato. Chemical and biological technologies in agriculture, 10, (1) 5.
Livak, K. J. and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. methods, 25, (4) 402-408.
Mandalari, G., D. Barreca, T. Gervasi, M. A. Roussell, B. Klein, M. J. Feeney and A. Carughi. 2021. Pistachio nuts (Pistacia vera L.): Production, nutrients, bioactives and novel health effects. Plants, 11, (1) 18.
Mukai, K., X. Qiu, Y. Takai, S. Yasuo, Y. Oshima and Y. Shimasaki. 2024. Diurnal-Rhythmic Relationships between Physiological Parameters and Photosynthesis-and Antioxidant-Enzyme Genes Expression in the Raphidophyte Chattonella marina Complex. Antioxidants, 13, (7) 781.
Peng, Z., T. Zulfiqar, H. Yang, M. Wang and F. Zhang. 2024. Effect of Arbuscular Mycorrhizal Fungi (AMF) on photosynthetic characteristics of cotton seedlings under saline-alkali stress. Scientific Reports, 14, (1) 8633.
Phillips, J. and D. Hayman. 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, (1) 158-IN118.
Rashad, Y. M., W. M. Fekry, M. M. Sleem and N. T. Elazab. 2021. Effects of mycorrhizal colonization on transcriptional expression of the responsive factor JERF3 and stress-responsive genes in banana plantlets in response to combined biotic and abiotic stresses. Frontiers in Plant Science, 12, 742628.
Razvi, S. M., N. Singh, A. Mushtaq, D. Shahnawaz and S. Hussain. 2023. Arbuscular mycorrhizal fungi for salinity stress: Anti-stress role and mechanisms. Pedosphere, 33, (1) 212-224.
Ren, C.-G., C.-C. Kong, K. Yan and Z.-H. Xie. 2019. Transcriptome analysis reveals the impact of arbuscular mycorrhizal symbiosis on Sesbania cannabina expose to high salinity. Scientific reports, 9, (1) 2780.
Sadhana, B. 2014. Arbuscular Mycorrhizal Fungi (AMF) as a biofertilizer-a review. Int J Curr Microbiol App Sci, 3, (4) 384-400.
Santander, C., R. Aroca, P. Cartes, G. Vidal and P. Cornejo. 2021. Aquaporins and cation transporters are differentially regulated by two arbuscular mycorrhizal fungi strains in lettuce cultivars growing under salinity conditions. Plant Physiology and Biochemistry, 158, 396-409.
Selvakumar, G., C. C. Shagol, K. Kim, S. Han and T. Sa. 2018. Spore associated bacteria regulates maize root K+/Na+ ion homeostasis to promote salinity tolerance during arbuscular mycorrhizal symbiosis. BMC plant biology, 18, 1-13.
Seutra Kaba, J., A. A. Abunyewa, J. Kugbe, G. K. Kwashie, E. Owusu Ansah and H. Andoh. 2021. Arbuscular mycorrhizal fungi and potassium fertilizer as plant biostimulants and alternative research for enhancing plants adaptation to drought stress: Opportunities for enhancing drought tolerance in cocoa (Theobroma cacao L.). Sustainable Environment, 7, (1) 1963927.
Sheng, M., M. Tang, H. Chen, B. Yang, F. Zhang and Y. Huang. 2008. Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza, 18, 287-296.
Sun, D., X. Shang, H. Cao, S.-J. Lee, L. Wang, Y. Gan and S. Feng. 2024. Physio-Biochemical Mechanisms of Arbuscular Mycorrhizal Fungi Enhancing Plant Resistance to Abiotic Stress. Agriculture, 14, (12) 2361.
Thangavel, P., N. A. Anjum, T. Muthukumar, G. Sridevi, P. Vasudhevan and A. Maruthupandian. 2022. Arbuscular mycorrhizae: natural modulators of plant–nutrient relation and growth in stressful environments. Archives of Microbiology, 204, (5) 264.
Vineeth, T., G. Krishna, P. Pandesha, L. Sathee, S. Thomas, D. James, K. Ravikiran, S. Taria, C. John and N. Vinaykumar. 2023. Photosynthetic machinery under salinity stress: Trepidations and adaptive mechanisms. Photosynthetica, 61, (1) 73.
Wahab, A., M. Muhammad, A. Munir, G. Abdi, W. Zaman, A. Ayaz, C. Khizar and S. P. P. Reddy. 2023. Role of arbuscular mycorrhizal fungi in regulating growth, enhancing productivity, and potentially influencing ecosystems under abiotic and biotic stresses. Plants, 12, (17) 3102.
Wang, F., Y. Sun and Z. Shi. 2019. Arbuscular mycorrhiza enhances biomass production and salt tolerance of sweet sorghum. Microorganisms, 7, (9) 289.
Wang, H., L. Liang, B. Liu, D. Huang, S. Liu, R. Liu, K. H. Siddique and Y. Chen. 2020. Arbuscular mycorrhizas regulate photosynthetic capacity and antioxidant defense systems to mediate salt tolerance in maize. Plants, 9, (11) 1430.
Wei, H., W. He, Y. Kuang, Z. Wang, Y. Wang, W. Hu, M. Tang and H. Chen. 2023a. Arbuscular mycorrhizal symbiosis and melatonin synergistically suppress heat-induced leaf senescence involves in abscisic acid, gibberellin, and cytokinin-mediated pathways in perennial ryegrass. Environmental and Experimental Botany, 213, 105436.
Wei, H., X. Li, W. He, Y. Kuang, Z. Wang, W. Hu, M. Tang and H. Chen. 2023b. Arbuscular mycorrhizal symbiosis enhances perennial ryegrass growth during temperature stress through the modulation of antioxidant defense and hormone levels. Industrial Crops and Products, 195, 116412.
Winicov, I. and J. D. Button. 1991. Accumulation of photosynthesis gene transcripts in response to sodium chloride by salt-tolerant alfalfa cells. Planta, 183, (4) 478-483.
Xu, S., L. Meng and Y. Bao. 2024. Molecular evolution of the rbcS multiple gene family in Oryza punctata. Journal of Systematics and Evolution, 62, (5) 903-914.
Zhao, S., Q. Zhang, M. Liu, H. Zhou, C. Ma and P. Wang. 2021. Regulation of plant responses to salt stress. International Journal of Molecular Sciences, 22, (9) 4609.
Zhou, H., H. Shi, Y. Yang, X. Feng, X. Chen, F. Xiao, H. Lin and Y. Guo. 2024. Insights into plant salt stress signaling and tolerance. Journal of Genetics and Genomics, 51, (1) 16-34.
Zong, J., Z. Zhang, P. Huang and Y. Yang. 2023. Arbuscular mycorrhizal fungi alleviates salt stress in Xanthoceras sorbifolium through improved osmotic tolerance, antioxidant activity, and photosynthesis. Frontiers in Microbiology, 14, 1138771.