Evaluation of the application of endophytic bacteria Micromonospora echinaurantiaca and Sphingomonas aquatilis in enhancing wheat tolerance to salinity stress

Articles in Press

Document Type : Original Article

Authors

1 Postdoctoral Researcher, Department of Biological Control Research, Iranian Research Institute of Plant Protection, Agricultural Research, Education and Extension Organization (AREEO), Tehran, Iran

2 Associate Professor, Department of Biological Control Research, Iranian Research Institute of Plant Protection, Agricultural Research, Education and Extension Organization (AREEO), Tehran, Iran

3 Associate Professor, Faculty of Bioscience, University of Tarbiat Modares, Tehran, Iran

Abstract

Introduction
Climate change is a major concern for sustainable agriculture in the twenty-first century, as it negatively affects crop production and soil fertility, thereby increasing the risk of famine. Among the various issues associated with climate change, salt stress is one of the most significant factors affecting crop production worldwide. Many biotic and abiotic factors can limit wheat yield. Abiotic stress is one of the main limitations that inhibit plant growth and productivity by disrupting physiological processes and suppressing defense mechanisms. Seed germination is a critical life stage for the survival of plants and the timely establishment of seedlings, especially in stressful environments. However, several mitigation strategies are also used to cope with the adverse effects of salt stress. Microbial-based solutions, in particular, are highly desirable in sustainable agriculture as they provide a natural, cost-effective, and environmentally safe approach to improve plant growth and yield.
 
Materials and methods
A study was conducted to investigate the effect of the endophytic bacteria Micromonospora echinaurantiaca and Sphingomonas aquatilis on the salinity tolerance of the Sardari wheat variety under laboratory and greenhouse conditions. The experiments were designed in a factorial arrangement based on a completely randomized design (CRD). Treatments included endophytic bacteria (1 × 10⁸ cells ml-1, λ = 600 n) and salt stress levels of 50, 100, and 150 mM NaCl, with three replications.
 
Results and discussion
The results showed that the endophytic bacteria M. echinaurantiaca and S. aquatilis enhanced wheat seed germination compared to the control. The presence of the endophyte M. echinaurantiaca at concentrations of 50 and 100 mM, and S. aquatilis at 50 mM, improved wheat seed germination by 100% compared to the control. The most significant increases in shoot and root length under 150 mM salt stress were observed in wheat inoculated with M. echinaurantiaca compared to the control. M. echinaurantiaca increased the fresh weight of wheat seedlings by 4.32% under 150 mM salinity stress compared to uninoculated plants. However, this bacterium caused a 19.90% decrease in dry weight. A significant 15.07% increase in root lenght tolerance index was observed in the presence of M. echinaurantiaca under 50 mM salinity stress compared to the control. Evaluation of salinity tolerance indices revealed that the highest tolerance indices for shoot length, root length, dry weight, and germination were observed in plants inoculated with M. echinaurantiaca and S. aquatilis under control (non-saline) conditions. Wheat inoculated with M. echinaurantiaca showed a 63.92% increase in stem length tolerance under 150 mM salinity stress. The endophytic bacterium M. echinaurantiaca increased root stress tolerance by 62.25% under 150 mM salinity stress. The wet weight tolerance index increased in response to inoculation with M. echinaurantiaca. Evaluation of the dry weight tolerance index showed that M. echinaurantiaca increased this index by 129.01%. The germination tolerance index increased by 108.70% following wheat inoculation with M. echinaurantiaca. Under greenhouse conditions and 150 mM salt stress, M. echinaurantiaca and S. aquatilis increased chlorophyll a content by 12.95% and 6.39%, respectively. Additionally, S. aquatilis increased chlorophyll b content by 48.54% and carotenoid content by 80.42% compared to the control. Under 150 mM salinity stress, S. aquatilis also increased relative leaf water content by 81.60%, and enhanced antioxidant activity and flavonoid content by 81.23% and 46.11%, respectively. Moreover, the endophytes enhanced catalase activity and modulated hydrogen peroxide levels, indicating their crucial role in improving wheat tolerance to salt stress. Based on these results, using the endophytic bacteria M. echinaurantiaca and S. aquatilis for biological seed priming is an effective strategy to mitigate salinity stress and enhance wheat salinity tolerance.
 
Conclusion
These results highlight the importance of further research on biological priming using endophytic bacteria. In the future, enhancing crop performance through microbiome-based approaches could contribute to significant advances in sustainable agriculture under changing climatic conditions.

Keywords

Main Subjects

References

 Ali, A., Shahzad, R., Khan, A.L., Halo, B.A., Al-Yahyai, R., Al-Harrasi, A., Al-Rawahi, A. and Lee, I.J., 2017. Endophytic bacterial diversity of Avicennia marina helps to confer resistance against salinity stress in Solanum lycopersicum. Journal of Plant Interactions, 12(1), 312-322. https://doi.org/10.1080/17429145.2017.1362051
Abd-Allah, E.F., Alqarawi, A.A., Hashem, A., Radhakrishnan, R., Al-Huqail, A.A., Al-Otibi, F.O.N., Malik, J.A., Alharbi, R.I., Egamberdieva, D., 2018. Endophytic bacterium Bacillus subtilis (BERA 71) improves salt tolerance in chickpea plants by regulating the plant defense mechanisms. Journal of Plant Interactions. 13, 37-44. https://doi.org/10.1080/17429145.2017.1414321 
Abdellatif, L., Bouzid, S., Kaminskyj, S., Vujanovic, V., 2009. Endophytic hyphal compartmentalization is required for successful symbiotic Ascomycota association with root cells. Mycological Research, 113, 782-791. https://doi.org/10.1016/j.mycres.2009.02.013
Albdaiwi, R., Al-Sayaydeh, R., Al-Rifaee, M.K., Alhindi, T., Ashraf, M., Al-Abdallat, A.M., 2024. Halotolerant endophytic bacteria regulate growth and field performance of two durum wheat genotypes with contrasting salinity tolerance potential. Plants, 13, 1179. https://doi.org/10.3390/plants13091179
Abdul‐Baki, A.A., Anderson, J.D., 1973. Relationship between decarboxylation of glutamic acid and vigor in soybean seed 1. Crop Science. 13, 227-232. https://doi.org/10.2135/cropsci1973.0011183X001300020023x
Abideen, Z., Cardinale, M., Zulfiqar, F., Koyro, H.W., Rasool, S.G., Hessini, K., Darbali, W., Zhao, F., Siddique, K.H., 2022. Seed endophyte bacteria enhance drought stress tolerance in Hordeum vulgare by regulating, physiological characteristics, antioxidants and minerals uptake. Frontiers in Plant Science. 13, 980046. https://doi.org/10.3389/fpls.2022.980046
Afridi, M.S., Mahmood, T., Salam, A., Mukhtar, T., Mehmood, S., Ali, J., Khatoon, Z., Bibi, M., Javed, M.T., Sultan, T., Chaudhary, H.J., 2019. Induction of tolerance to salinity in wheat genotypes by plant growth promoting endophytes: Involvement of ACC deaminase and antioxidant enzymes. Plant Physiology and Biochemistry. 139, 569-577. https://doi.org/10.1016/j.plaphy.2019.03.041
Aghaei Dargiri, S., Samsampour, D., Askari Seyahooei, M., Bagheri, A., 2021. Evaluation of the effect of fungal Penicillium chrysogenum and bacterial Exigubacteium aurantiacum endophytes on improvement of the morpho-physiological characteristics of tomato seedlings. Journal of Plant Process and Function. 10, 251-266. [In Persian]. http://dorl.net/dor/20.1001.1.23222727.1400.10.42.17.9
Aghaei Dargiri, S., Samsampour, D., Askari Seyahooei, M., Bagheri, A., 2019. Investigation of endophyte diversity of some Amaranthacea species in Hormozgan province and their role to salinity tolerance in tomato plant. PhD thesis, Hormozgan University. [In Persian].
Araújo, S., Balestrazzi, A., 2016. New Challenges in Seed Biology - Basic and Translational Research Driving Seed Technology. IntechOpen. Available at: http://dx.doi.org/10.5772/61583.
Bashan, Y., de-Bashan, L.E., 2005. Fresh-weight measurements of roots provide inaccurate estimates of the effects of plant growth-promoting bacteria on root growth: a critical examination. Soil biology and biochemistry, 37, 1795-1804. https://doi.org/10.1016/j.soilbio.2005.02.013
Chakraborty, U., Roy, S., Chakraborty, A.P., Dey, P., Chakraborty, B., 2011. Plant growth promotion and amelioration of salinity stress in crop plants by a salt-tolerant bacterium. Recent Research in Science and Technology. 3.(11):61-70.
Cui, J., Nie, F., Zhao, Y., Zhang, D., Zhou, D., Wu, J., Qu, L., Xiao, L., Liu, L., 2024. A review on plant endophytes in response to abiotic stress. Environmental Pollutants and Bioavailability. 36, 2323123. https://doi.org/10.1080/26395940.2024.2323123
Djanaguiraman, M., Narayanan, S., Erdayani, E., Prasad, P.V., 2020. Effects of high temperature stress during anthesis and grain filling periods on photosynthesis, lipids and grain yield in wheat. BMC Plant Biology. 20, 1-12. https://doi.org/10.1186/s12870-020-02479-0
Eid, A.M., Fouda, A., Abdel-Rahman, M.A., Salem, S.S., Elsaied, A., Oelmüller, R., Hijri, M., Bhowmik, A., Elkelish, A., Hassan, S.E.D., 2021. Harnessing bacterial endophytes for promotion of plant growth and biotechnological applications: an overview. Plants. 10, 935. https://doi.org/10.3390/plants10050935
Ellis, R.H., Roberts, E.H., 1980. Towards a rational basis for testing seed quality. In: Hebblethwaite, P.D. (Ed), Seed Production. Butterworths, London. 605-635.
Emami, S., Alikhani, H.A., Pourbabaei, A.A., Etesami, H., Sarmadian, F., Motessharezadeh, B., 2019. Effect of rhizospheric and endophytic bacteria with multiple plant growth promoting traits on wheat growth. Environmental Science and Pollution Research. 26, 19804-19813. https://doi.org/10.1007/s11356-019-05284-x
Etesami, H., Adl, S.M., 2020. Plant growth-promoting rhizobacteria (PGPR) and their action mechanisms in availability of nutrients to plants. Environmental and Microbial Biotechnology Phyto-Microbiome in Stress Regulation, p. 147-203. https://doi.org/10.1007/978-981-15-2576-6_9
Etesami, H., Maheshwari, D.K., 2018. Use of plant growth promoting rhizobacteria (PGPRs) with multiple plant growth promoting traits in stress agriculture: Action mechanisms and future prospects. Ecotoxicology and Environmental Safety. 156, 225-246. https://doi.org/10.1016/j.ecoenv.2018.03.013
FAO, 2021. Crops: Food and Agriculture Organization of the United Nations. https://www.fao.org/faostat/en/#data
Fouda, A., Hassan, S.E.D., Eid, A.M., El-Din Ewais, E., 2019. The interaction between plants and bacterial endophytes under salinity stress. Endophytes and Secondary Metabolites. 1-12. https://doi.org/10.1007/978-3-319-90484-9_15
Gholizadeh, F., Mirzaghaderi, G., Danish, S., Farsi, M., Marashi, S.H., 2021. Evaluation of morphological traits of wheat varieties at germination stage under salinity stress. Plos One. 16, e0258703. https://doi.org/10.1371/journal.pone.0258703
Ghonaim, M.M., Mohamed, H.I., Omran, A.A., 2021. Evaluation of wheat (Triticum aestivum L.) salt stress tolerance using physiological parameters and retrotransposon-based markers. Genetic Resources and Crop Evolution. 68, 227-242. https://doi.org/10.1007/s10722-020-00981-w
Golparyan, F., Azizi, A., Soltani, J., 2018. Endophytes of Lippia citriodora (Syn. Aloysia triphylla) enhance its growth and antioxidant activity. European Journal of Plant Pathology. 152, 759-768. https://doi:10.1007/s10658-018-1520-x
Gururani, M.A., Upadhyaya, C.P., Baskar, V., Venkatesh, J., Nookaraju, A., Park, S.W., 2013. Plant growth-promoting rhizobacteria enhance abiotic stress tolerance in Solanum tuberosum through inducing changes in the expression of ROS-scavenging enzymes and improved photosynthetic performance. Journal of Plant Growth Regulation. 32, 245-258. https://doi.org/10.1007/s00344-012-9292-6
Hadj Brahim, A., Ben Ali, M., Daoud, L., Jlidi, M., Akremi, I., Hmani, H., Feto, N.A., Ben,
Ha-Tran, D.M., Nguyen, T.T.M., Hung, S.H., Huang, E., Huang, C.C., 2021. Roles of plant growth-promoting rhizobacteria (PGPR) in stimulating salinity stress defense in plants: A review. International Journal of Molecular Sciences. 22, 3154. https://doi.org/10.3390/ijms22063154
Hasanuzzaman, M. and Fujita, M., 2013. Exogenous sodium nitroprusside alleviates arsenic-induced oxidative stress in wheat (Triticum aestivum L.) seedlings by enhancing antioxidant defense and glyoxalase system. Ecotoxicology, 22(3), 584-596. https://doi.org/10.1007/s10646-013-1050-4
Hamilton, C.E., Gundel, P.E., Helander, M. and Saikkonen, K., 2012. Endophytic mediation of reactive oxygen species and antioxidant activity in plants: a review. Fungal Diversity, 54(1), 1-10. https://doi.org/10.1007/s13225-012-0158-9
Hualpa-Ramirez, E., Carrasco-Lozano, E.C., Madrid-Espinoza, J, Tejos., R, Ruiz-Lara, S., Stange, C., Norambuena, L., 2024. Stress salinity in plants: New strategies to cope with in the foreseeable scenario. Plant Physiology and Biochemistry. https://doi.org/10.1016/j.plaphy.2024.108507
Hubbard, M., Germida, J., Vujanovic, V., 2012. Fungal endophytes improve wheat seed germination under heat and drought stress. Botany. 90, 137-149. https://doi.org/10.1139/b11-091
Hunter, E.A., Glasbey, C.A., Naylor, R.E.L., 1984. The analysis of data from germination tests. The Journal of Agricultural Science. 102, 207-213. https://doi.org/10.1017/S0021859600041642
Jha, Y., 2019. Endophytic bacteria as a modern tool for sustainable crop management under stress. Biofertilizers for Sustainable Agriculture and Environment. 203-223. https://doi.org/10.1007/978-3-030-18933-4_9
Kandel, S.L., Joubert, P.M., Doty, S.L., 2017. Bacterial endophyte colonization and distribution within plants. Microorganisms. 5, 77. https://doi.org/10.3390/microorganisms5040077
Kaymak, H.Ç., Güvenç, İ., Yarali, F., Dönmez, M.F., 2009. The effects of bio-priming with PGPR on germination of radish (Raphanus sativus L.) seeds under saline conditions. Turkish Journal of Agriculture and Forestry. 33, 173-179. https://doi.org/10.3906/tar-0806-30
Khan, M.A., Asaf, S., Khan, A.L., Adhikari, A., Jan, R., Ali, S., Imran, M., Kim, K.M., Lee, I.J., 2020. Plant growth‐promoting endophytic bacteria augment growth and salinity tolerance in rice plants. Plant Biology. 22, 850-862. https://doi.org/10.1111/plb.13124
Khan, T.A., Mazid, M., Quddusi, S., 2014. Role of Organic and Inorganic Chemicals in Plant-Stress Mitigation. In: Gaur, R., Sharma, P. (eds) Approaches to Plant Stress and their Management. Springer, New Delhi. https://doi.org/10.1007/978-81-322-1620-9_3
Khezri, M., Abbaspour Anbi, A., Mohammad Sour, F., 2018. Evaluation of seed biopriming on tomato leaf spot biocontrol and plant growth factors. Biological Control of Pests and Plant Disease. 7, 1-16. https://doi.org/10.22059/jbioc.2018.263489.237
Kushwaha, P., Kashyap, P.L., Bhardwaj, A.K., Kuppusamy, P., Srivastava, A.K., Tiwari, R.K., 2020. Bacterial endophyte mediated plant tolerance to salinity: growth responses and mechanisms of action. World Journal of Microbiology and Biotechnology. 36, 26. https://doi.org/10.1007/s11274-020-2804-9
Lastochkina, O., Pusenkova, L., Yuldashev, R., Babaev, M., Garipova, S., Blagova, D.Y., Khairullin, R., Aliniaeifard, S., 2017. Effects of Bacillus subtilis on some physiological and biochemical parameters of Triticum aestivum L.(wheat) under salinity. Plant Physiology and Biochemistry. 121, 80-88. https://doi.org/10.1016/j.plaphy.2017.10.020
Liang, Q., Tan, D., Chen, H., Guo, X., Afzal, M., Wang, X., Tan, Z., Peng, G., 2024. Endophyte-mediated enhancement of salt resistance in Arachis hypogaea L. by regulation of osmotic stress and plant defense-related genes. Frontiers in Microbiology. 15, 1383545. https://doi.org/10.3389/fmicb.2024.1383545
Lichtenthaler, H.K., 1987. Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. Methods Enzymol. 148: 350 382. https://doi.org/10.1002/0471142913.faf0403s01
Liu, B., Asseng, S., Müller, C., Ewert, F., Elliott, J., Lobell, D.B., Martre, P., Ruane, A.C., Wallach, D., Jones, J.W., Rosenzweig, C., 2016. Similar estimates of temperature impacts on global wheat yield by three independent methods. Nature Climate Change. 6, 1130-1136. https://doi.org/10.1038/nclimate3115
Manjunatha, N., Manjunatha, N., Li, H., Sivasithamparam, K., Jones, M.G., Edwards, I., Wylie, S.J., Agarrwal, R., 2022. Fungal endophytes from salt-adapted plants confer salt tolerance and promote growth in wheat (Triticum aestivum L.) at early seedling stage. Microbiology. 168, 001225. https://doi.org/10.1099/mic.0.001225
Moradi, A., Piri, R., 2018. Plant growth promoting rhizobactria enhance salinity stress tolerance in Cumin (Cuminum cyminum L.) during germination stage. Journal of Plant Process and Function. 6, 47-54. https://dorl.net/dor/20.1001.1.23222727.1396.6.22.8.2
Nanjo, F., Goto, K., Seto, R., Suzuki, M., Sakai, M., Hara, Y., 1996. Scavenging effects of tea catechins and their derivatives on 1, 1-diphenyl-2-picrylhydrazyl radical. Free Radical Biology and Medicine. 21, 895-902. https://doi.org/10.1016/0891-5849(96)00237-7
Nawaz, F., Rafeeq, R., Majeed, S., Ismail, M.S., Ahsan, M., Ahmad, K.S., Akram, A., Haider, G., 2023. Biochar amendment in combination with endophytic bacteria stimulates photosynthetic activity and antioxidant enzymes to improve soybean yield under drought stress. Journal of Soil Science and Plant Nutrition. 23, 746-760. https://doi.org/10.1007/s42729-022-01079-1
Otlewska, A., Migliore, M., Dybka-Stępień, K., Manfredini, A., Struszczyk-Świta, K., Napoli, R., Białkowska, A., Canfora, L., Pinzari, F., 2020. When salt meddles between plant, soil, and microorganisms. Frontiers in Plant Science. 11, 553087. https://doi.org/10.3389/fpls.2020.553087
Oukala, N., Aissat, K., Pastor, V., 2021. Bacterial endophytes: The hidden actor in plant immune responses against biotic stress. Plants. 10, 1012. https://doi.org/10.3390/plants10051012
Pan, Y., Wu, L.J., Yu, Z.L., 2006. Effect of salt and drought stress on antioxidant enzymes activities and SOD isoenzymes of liquorice (Glycyrrhiza uralensis Fisch). Plant Growth Regulation. 49, 157-165. https://doi.org/10.1007/s10725-006-9101-y
Paśmionka, I.B., Bulski, K., Boligłowa, E., 2021. The participation of microbiota in the transformation of nitrogen compounds in the soil—A review. Agronomy. 11, 977. https://doi.org/10.3390/agronomy11050977
Porcel, R., Aroca, R., Ruiz-Lozano, J.M., 2012. Salinity stress alleviation using arbuscular mycorrhizal fungi. A review. Agronomy for Sustainable Development. 32, 181-200. https://doi.org/10.1007/s13593-011-0029-x
Posada, F., Aime, M.C., Peterson, S.W., Rehner, S.A., Vega, F.E., 2007. Inoculation of coffee plants with the fungal entomopathogen Beauveria bassiana (Ascomycota: Hypocreales). Mycological Research, 111, 748-757. https://doi.org/10.1016/j.mycres.2007.03.006
Rocha, I., Ma, Y., Souza-Alonso, P., Vosátka, M., Freitas, H., Oliveira, R.S., 2019. Seed coating: a tool for delivering beneficial microbes to agricultural crops. Frontiers in Plant Science. 10, 1357. https://doi.org/10.3389/fpls.2019.01357
Sadak, M.S., Abd El-Hameid, A.R., Zaki, F.S., Dawood, M.G., El-Awadi, M.E., 2020. Physiological and biochemical responses of soybean (Glycine max L.) to cysteine application under sea salt stress. Bulletin of the National Research Centre. 44, 1-10. https://doi.org/10.1186/s42269-019-0259-7
Saddiq, M.S., Iqbal, S., Hafeez, M.B., Ibrahim, A.M., Raza, A., Fatima, E.M., Baloch, H., Jahanzaib, Woodrow, P., Ciarmiello, L.F., 2021. Effect of salinity stress on physiological changes in winter and spring wheat. Agronomy. 11, 1193. https://doi.org/10.3390/agronomy11061193
Sarkar, D., Singh, S., Parihar, M., Rakshit, A., 2021. Seed bio-priming with microbial inoculants: A tailored approach towards improved crop performance, nutritional security, and agricultural sustainability for smallholder farmers. Current Research in Environmental Sustainability. 3, 100093. https://doi.org/10.1016/j.crsust.2021.100093
Shahid, M., Zeyad, M.T., Syed, A., Singh, U.B., Mohamed, A., Bahkali, A.H., Elgorban, A.M., Pichtel, J., 2022. Stress-tolerant endophytic isolate Priestia aryabhattai BPR-9 modulates physio-biochemical mechanisms in wheat (Triticum aestivum L.) for enhanced salt tolerance. International Journal of Environmental Research and Public Health. 19, 10883. https://doi.org/10.3390/ijerph191710883
Shakirova, F.M., Sakhabutdinova, A.R., Bezrukova, M.V., Fatkhutdinova, R.A., Fatkhutdinova, D.R., 2003. Changes in the hormonal status of wheat seedlings induced by salicylic acid and salinity. Plant Science. 164, 317-322. https://doi.org/10.1016/S0168-9452(02)00415-6
Singh, P., Kumar, A., Borthakur, A., 2019. Abatement of environmental pollutants: trends and strategies. Elsevier Science and Technology. https://doi.org/10.1016/C2018-0-03174-6
Singh, S., Singh, U.B., Malviya, D., Paul, S., Sahu, P.K., Trivedi, M., Paul, D., Saxena, A.K., 2020. Seed biopriming with microbial inoculant triggers local and systemic defense responses against Rhizoctonia solani causing banded leaf and sheath blight in maize (Zea mays L.). International Journal of Environmental Research and Public Health. 17, 1396. https://doi.org/10.3390/ijerph17041396
Singh, V., Upadhyay, R.S., Sarma, B.K., Singh, H.B., 2016. Seed bio-priming with Trichoderma asperellum effectively modulate plant growth promotion in pea. International Journal of Agriculture, Environment and Biotechnology. 9, 361-365. http://dx.doi.org/10.5958/2230 732X.2016.00047.4
Singleton, V.L., Rossi, J.A., 1965. Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. American Journal of Enology and Viticulture. 16, 144-158. https://doi.org/10.5344/ajev.1965.16.3.144
Sofy, M.R., Aboseidah, A.A., Heneidak, S.A. and Ahmed, H.R., 2021. ACC deaminase containing endophytic bacteria ameliorate salt stress in Pisum sativum through reduced oxidative damage and induction of antioxidative defense systems. Environmental Science and Pollution Research, 28(30), 40971-40991. https://doi.org/10.1007/s11356-021-13585-3
Soltani, J., Samavati, R., Jalili, B., Bagheri, H., Hamzei, J., 2024. Halotolerant endophytic bacteria from desert-adapted halophyte plants alleviate salinity stress in germinating seeds of the common wheat Triticum aestivum L. Cereal Research Communications, 52, 165-175 https://doi.org/10.1007/s42976-023-00377-3
Sturz, A.V., Christie, B.R., Nowak, J., 2000. Bacterial endophytes: potential role in developing sustainable systems of crop production. Critical Reviews in Plant Sciences. 19, 1-30. https://doi.org/10.1080/07352680091139169
Tang, M.J., Lu, F., Yang, Y., Sun, K., Zhu, Q., Xu, F.J., Zhang, W., Dai, C.C., 2022. Benefits of endophytic fungus Phomopsis liquidambaris inoculation for improving mineral nutrition, quality, and yield of rice grains under low nitrogen and phosphorus condition. Journal of Plant Growth Regulation. 41, 2499-2513. https://doi.org/10.1007/s00344-021-10462-8
Tao, R., Ding, J., Li, C., Zhu, X., Guo, W., Zhu, M., 2021. Evaluating and screening of agro-physiological indices for salinity stress tolerance in wheat at the seedling stage. Frontiers in Plant Science. 12, 646175. https://doi.org/10.3389/fpls.2021.646175
Toor, R.K., Savage, G.P., 2005. Antioxidant activity in different fractions of tomatoes. Food Research International. 38, 487-494. https://doi.org/10.1016/j.foodres.2004.10.016
Torabian, S., Shakiba, M.R., Dabbagh Mohammadi Nasab, A., Toorchi, M., 2018. Leaf gas exchange and grain yield of common bean exposed to spermidine under water stress. Photosynthetica. 56, 1387-1397. https://doi.org/10.1007/s11099-018-0834-4
Vaishnav, A., Shukla, A.K., Sharma, A., Kumar, R., Choudhary, D.K., 2019. Endophytic bacteria in plant salt stress tolerance: current and future prospects. Journal of Plant Growth Regulation. 38, 650-668. https://doi.org/10.1007/s00344-018-9880-1
Verma, H., Kumar, D., Kumar, V., Kumari, M., Singh, S.K., Sharma, V.K., Droby, S., Santoyo, G., White, J.F., Kumar, A., 2021. The potential application of endophytes in management of stress from drought and salinity in crop plants. Microorganisms, 9. 1729. https://doi.org/10.3390/microorganisms9081729
Verma, S.K., Kharwar, R.N., White, J.F., 2019. The role of seed-vectored endophytes in seedling development and establishment. Symbiosis. 78, 107-113. https://doi.org/10.1007/s13199-019-00619-1
Wani, A.S., Ahmad, A., Hayat, S., Tahir, I., 2019. Epibrassinolide and proline alleviate the photosynthetic and yield inhibition under salt stress by acting on antioxidant system in mustard. Plant Physiology and Biochemistry. 135, 385-394. https://doi.org/10.1016/j.plaphy.2019.01.002
Wei, H., He, W., Li, Z., Ge, L., Zhang, J., Liu, T., 2022. Salt-tolerant endophytic bacterium Enterobacter ludwigii B30 enhance bermudagrass growth under salt stress by modulating plant physiology and changing rhizosphere and root bacterial community. Frontiers in Plant Science. 13, 959427. https://doi.org/10.3389/fpls.2022.959427
Weller, D.M., Cook, R.J., 1983. Suppression of take-all of wheat by seed treatments with Fluorescent pseudomonads. Phytopathology. 73, 463-469
Wu, F.L., Li, Y., Tian, W., Sun, Y., Chen, F., Zhang, Y., Zhai, Y., Zhang, J., Su, H., Wang, L., 2020. A novel dark septate fungal endophyte positively affected blueberry growth and changed the expression of plant genes involved in phytohormone and flavonoid biosynthesis. Tree Physiology. 40, 1080-1094. https://doi.org/10.1093/treephys/tpaa047
Yañez-Yazlle, M.F., Romano-Armada, N., Acreche, M.M., Rajal, V.B., Irazusta, V.P., 2021. Halotolerant bacteria isolated from extreme environments induce seed germination and growth of chia (Salvia hispanica L.) and quinoa (Chenopodium quinoa Willd.) under saline stress. Ecotoxicology and Environmental safety. 218, 112273. https://doi.org/10.1016/j.ecoenv.2021.112273
Yang, S.L., Lan, S.S., Gong, M., 2009. Hydrogen peroxide-induced proline and metabolic pathway of its accumulation in maize seedlings. Journal of Plant Physiology. 166 1694-1699. https://doi.org/10.1016/j.jplph.2009.04.006
Youseif, S.H., 2018. Genetic diversity of plant growth promoting rhizobacteria and their effects on the growth of maize plants under greenhouse conditions. Annals of Agricultural Sciences. 63, 25-35. https://doi.org/10.1016/j.aoas.2018.04.002
Zandi, P., Schnug, E., 2022. Reactive oxygen species, antioxidant responses and implications from a microbial modulation perspective. Biology. 11, 155. https://doi.org/10.3390/biology11020155
Zhang, T., Fan, S., Xiang, Y., Zhang, S., Wang, J., Sun, Q., 2020. Non-destructive analysis of germination percentage, germination energy and simple vigour index on wheat seeds during storage by Vis/NIR and SWIR hyperspectral imaging. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy. 239, 118488. https://doi.org/10.1016/j.saa.2020.118488
Zhu, M., Shabala, S., Shabala, L., Fan, Y., Zhou, M.X., 2016. Evaluating predictive values of various physiological indices for salinity stress tolerance in wheat. Journal of Agronomy and Crop Science. 202, 115-124.  https://doi.org/10.1111/jac.12122 
Environmental Stresses in Crop Sciences

Articles in Press, Accepted Manuscript
Available Online from 26 October 2025

Files

History

  • Receive Date: 09 July 2024
  • Revise Date: 16 September 2024
  • Accept Date: 18 September 2024

Share

How to cite

Statistics