Effects of treating wheat (Triticum aestivum) seedling roots with Azospirillum lectins to improve abiotic stress tolerance
Svetlana A. Alen’kina
A
Abstract
While the effects of plant growth-promoting rhizobacterium, Azospirillum, on abiotic stress tolerance in plants are widely reported, the mechanisms that underlie this process remain elusive. Surface lectins of strains A. brasilense Sp7 and A. baldaniorum Sp245 are capable of attaching to specific carbohydrates and ensure the binding of bacteria to the surface of the plant root. They exhibit multifunctionality, and the effects induced by lectins are dose-dependent. This work investigated mechanisms by which lectins improved drought tolerance in wheat (Triticum aestivum) plants. In the roots of wheat seedlings under drought stress, lectins with varying intensities increased the activity of peroxidase (POD), superoxide dismutase (SOD), and catalase (CAT). Lectins caused a decrease in lipid peroxidation, but increased the content of secondary metabolites such as total phenolics and flavonoids. In the roots of stressed seedlings, lectins increased the total protein content and caused a dose-dependent change in the electrophoretic spectra of low molecular weight proteins. It was concluded that Azospirillum lectins, due to their ability to influence the metabolism of the host plant, are involved in adaptive changes in the roots of wheat seedlings. Lectins can regulate the relationship between bacteria and their hosts when soil and climatic factors change.
Keywords: bacterial proteins, drought stress, plant-growth-promoting rhizobacteria, plants, stress metabolites.
References
Ahmad Z, Waraich EA, Akhtar S, Anjum S, Ahmad T, Mahboob W, Hafeez OBA, Tapera T, Labuschagne M, Rizwan M (2018) Physiological responses of wheat to drought stress and its mitigation approaches. Acta Physiologiae Plantarum 40(4), 80.
| Crossref | Google Scholar |
Alen’kina SA, Kupryashina MA (2024) Dose-dependent effects of Azospirilla lectin on the growth of wheat seedlings under salt stress. Applied Biochemistry and Microbiology 60, 73-79.
| Crossref | Google Scholar |
Alen’kina SА, Nikitina VЕ (2017) Change in the ratio between the activities of different types of proteases and their inhibitors in plant roots exposed to Azospirillum lectins. Journal of Plant Growth Regulation 36, 522-527.
| Crossref | Google Scholar |
Alen’kina SА, Nikitina VЕ (2020) Effect of Azospirillum lectins on the ascorbate peroxidase activity and ascorbic acid content in wheat seedling roots exposed to abiotic stresses. Applied Biochemistry and Microbiology 56, 211-218.
| Crossref | Google Scholar |
Alen’kina SА, Nikitina VЕ (2021) Stimulating effect from lectins of associative bacteria of the genus Azospirillum on the germination and morphometric characteristics of spring wheat sprouts in simulated abiotic stress. Russian Journal of Plant Physiology 68, 315-321.
| Crossref | Google Scholar |
Alen’kina SA, Payusova OA, Nikitina VE (2006) Effect of Azospirillum lectins on the activities of wheat-root hydrolytic enzymes. Plant and Soil 283, 147-151.
| Crossref | Google Scholar |
Alen’kina SA, Bogatyrev VA, Matora LY, Sokolova MK, Chernyshova MP, Trutneva KA, Nikitina VE (2014) Signal effects of the lectin from the associative nitrogen-fixing bacterium Azospirillum brasilense Sp7 in bacterial–plant root interactions. Plant and Soil 381, 337-349.
| Crossref | Google Scholar |
Alen’kina SА, Romanov NI, Nikitina VЕ (2018) Regulation by Azospirillum lectins of the activity of antioxidant enzymes in wheat seedling roots under short-term stresses. Brazilian Journal of Botany 41, 579-587.
| Crossref | Google Scholar |
Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. Journal of Experimental Botany 53, 1331-1341.
| Crossref | Google Scholar | PubMed |
Antonyuk LP, Evseeva NV (2006) Wheat lectin as a factor in plant–microbial communication and a stress response protein. Microbiology 75, 470-475.
| Crossref | Google Scholar |
Arzanesh MH, Alikhani HA, Khavazi K, Rahimian HA, Miransari M (2009) In vitro growth of wheat (Triticum aestivum L.) seedlings, inoculated with Azospirillum sp., under drought stress. International Journal of Botany 5, 244-249.
| Crossref | Google Scholar |
Bashan Y, de-Bashan LE, Prabhu SR, Hernandez J-P (2014) Advances in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (1998–2013). Plant and Soil 378, 1-33.
| Crossref | Google Scholar |
Batool T, Ali S, Seleiman MF, Naveed NH, Ali A, Ahmed K, Abid M, Rizwan M, Shahid MR, Alotaibi M, Al-Ashkar I, Mubushar M (2020) Plant growth promoting rhizobacteria alleviates drought stress in potato in response to suppressive oxidative stress and antioxidant enzymes activities. Scientific Reports 10(1), 16975.
| Crossref | Google Scholar |
Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World Journal of Microbiology and Biotechnology 28, 1327-1350.
| Crossref | Google Scholar | PubMed |
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248-254.
| Crossref | Google Scholar | PubMed |
Cassán F, Diaz-Zorita M (2016) Azospirillum sp. in current agriculture: from the laboratory to the field. Soil Biology and Biochemistry 103, 117-130.
| Crossref | Google Scholar |
Castellanos T, Ascencio F, Bashan Y (1998) Cell-surface lectins of Azospirillum spp. Current Microbiology 36, 241-244.
| Crossref | Google Scholar | PubMed |
Cheng G, Basha E, Wysocki VH, Vierling E (2008) Insights into small heat shock protein and substrate structure during chaperone action derived from hydrogen/deuterium exchange and mass spectrometry. Journal of Biological Chemistry 283, 26634-26642.
| Crossref | Google Scholar | PubMed |
Darkó É, Fodor J, Dulai S, Ambrus H, Szenzenstein A, Király Z, Barnabás B (2011) Improved cold and drought tolerance of doubled haploid maize plants selected for resistance to prooxidant tert-butyl hydroperoxide. Journal of Agronomy and Crop Science 197(6), 454-465.
| Crossref | Google Scholar |
Dwibedi V, Rath SK, Joshi M, Kaur R, Kaur G, Singh D, Kaur G, Kaur SJ (2022) Microbial endophytes: application towards sustainable agriculture and food security. Applied Microbiology and Biotechnology 106, 5359-5384.
| Crossref | Google Scholar | PubMed |
Georgiadou EC, Ntourou T, Goulas V, Manganaris GA, Kalaitzis P, Fotopoulos V (2015) Temporal analysis reveals a key role for VTE5 in vitamin E biosynthesis in olive fruit during on-tree development. Frontiers in Plant Science 6, 871.
| Crossref | Google Scholar |
Ghatak A, Chaturvedi P, Bachmann G, Valledor L, Ramšak Ž, Bazargani MM, Bajaj P, Jegadeesan S, Li W, Sun X, Gruden K, Varshney RK, Weckwerth W (2021) Physiological and proteomic signatures reveal mechanisms of superior drought resilience in pearl millet compared to wheat. Frontiers in Plant Science 11(1), 600278.
| Crossref | Google Scholar |
Guidi L, Tattini M (2021) Antioxidant defenses in plants: a dated topic of current interest. Antioxidants 10(6), 855.
| Crossref | Google Scholar |
Hartmann A, James EK, deBruijn FJ, Schwab S, Rothballer M, Schmid M (2015) In situ localization and strain-specific quantification of Azospirillum and other diazotrophic plant growth-promoting rhizobacteria using antibodies and molecular. In ‘Handbook for Azospirillum, technical issues and protocols’. (Eds FD Cassán, Y Okon, CM Creus) pp. 45–64. (Springer International Publishing: Switzerland)
Horváth E, Pál M, Szalai G, Páldi E, Janda T (2007) Exogenous 4-hydroxybenzoic acid and salicylic acid modulate the effect of short-term drought and freezing stress on wheat plants. Biologia Plantarum 51(3), 480-487.
| Crossref | Google Scholar |
Huseynova IM (2012) Photosynthetic characteristics and enzymatic antioxidant capacity of leaves from wheat cultivars exposed to drought. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1817(8), 1516-1523.
| Crossref | Google Scholar | PubMed |
Ishikawa T, Takahara K, Hirabayashi T, Matsumura H, Fujisawa S, Terauchi R, Uchimiya H, Kawai-Yamada M (2010) Metabolome analysis of response to oxidative stress in rice suspension cells overexpressing cell death suppressor Bax inhibitor-1. Plant and Cell Physiology 51(1), 9-20.
| Crossref | Google Scholar | PubMed |
Khairullin RM, Yarullina LG, Troshina NB, Akhmetova IE (2001) Chitooligosaccharide-induced activation of o-phenylenediamine oxidation by wheat seedlings in the presence of oxalic acid. Biochemistry 66, 286-289.
| Crossref | Google Scholar | PubMed |
Kosmala A, Bocian A, Rapacz M, Jurczyk B, Zwierzykowski Z (2009) Identification of leaf proteins differentially accumulated during cold acclimation between Festuca pratensis plants with distinct levels of frost tolerance. Journal of Experimental Botany 60, 3595-3609.
| Crossref | Google Scholar | PubMed |
Kotak S, Larkindale J, Lee U, von Koskull-Doring P, Vierling E, Scharf K-D (2007) Complexity of the heat stress response in plants. Current Opinion in Plant Biology 10, 310-316.
| Crossref | Google Scholar | PubMed |
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the read of bacteriophage T4. Nature 227(5259), 680-685.
| Crossref | Google Scholar | PubMed |
Lana MdC, Dartora J, Marini D, Hann JE (2012) Inoculation with Azospirillum, associated with nitrogen fertilization in maize. Revista Ceres Viçosa 59, 399-405.
| Crossref | Google Scholar |
Laus MC, Logman TJ, Lamers GE, Van Brussel AAN, Carlson RW, Kijne JW (2006) A novel polar surface polysaccharide from Rhizobium leguminosarum binds host plant lectin. Molecular Microbiology 59(6), 1704-1713.
| Crossref | Google Scholar | PubMed |
Makkar HPS, Siddhuraju P, Becker K (2007) ‘Plant secondary metabolites. Vol. 393.’ Methods in Molecular Biology. pp. 1–122. (Springer) 10.1007/978-1-59745-425-4_1
Marinova D, Ribarova F, Atanassova M (2005) Total phenolics and total flavonoids in bulgarian fruits and vegetables. Journal of the University of Chemical Technology Metallurgy 40, 255-260.
| Google Scholar |
Nag P, Shriti S, Das S (2020) Microbiological strategies for enhancing biological nitrogen fixation in nonlegumes. Journal of Applied Microbiology 129, 186-198.
| Crossref | Google Scholar | PubMed |
Oguz MC, Aycan M, Oguz E, Poyraz I, Yildiz M (2022) Drought stress tolerance in plants: interplay of molecular, biochemical and physiological responses in important development stages. Physiologia 2, 180-197.
| Crossref | Google Scholar |
Puente ML, Gualpa JL, Lopez GA, Molina RM, Carletti SM, Cassán FD (2018) The benefits of foliar inoculation with Azospirillum brasilense in soybean are explained by an auxin signaling model. Symbiosis 76, 41-49.
| Crossref | Google Scholar |
Rabara S, Vishwakarma NP, Patel S (2023) Isolation and biochemical identification of N2 fixing bacteria (Azospirillium Sp.) from Saurashtra Region. Current Agriculture Research Journal 11(1), 277-286.
| Crossref | Google Scholar |
Saeed Q, Xiukang W, Haider FU, Kučerik J, Mumtaz MZ, Holatko J, Naseem M, Kintl A, Ejaz M, Naveed M, Brtnicky M, Mustafa A (2021) Rhizosphere bacteria in plant growth promotion, biocontrol, and bioremediation of contaminated sites: a comprehensive review of effects and mechanisms. International Journal of Molecular Sciences 22(19), 10529.
| Crossref | Google Scholar |
Schloter M, Hartmann A (1998) Endophytic and surface colonization of wheat roots (Triticum aestivum) by different Azospirillum brasilense strains studied with strain-specific monoclonal antibodies. Symbiosis 25, 159-179.
| Google Scholar |
Takahashi F, Kuromori T, Urano K, Yamaguchi-Shinozaki K, Shinozaki K (2020) Drought stress responses and resistance in plants: from cellular responses to long-distance intercellular communication. Frontiers in Plant Science 11, 556972.
| Crossref | Google Scholar |
Wu H, Wu X, Li Z, Duan L, Zhang M (2012) Physiological evaluation of drought stress tolerance and recovery in cauliflower (Brassica oleracea L.) seedlings treated with methyl jasmonate and coronatine. Journal of Plant Growth Regulation 31, 113-123.
| Crossref | Google Scholar |