Abstract
The objective of the current study was to identify native bacterial strains with potential to mitigate abiotic stress, caused by the topical application of the herbicide imazethapyr, as well as promoting growth of alfalfa (Medicago sativa). The initial investigation involved the isolation of bacteria from the rhizosphere of field-grown alfalfa, which were subsequently screened for their ability to fix nitrogen, synthesize auxin, solubilize phosphate and potassium, and produce lipase, protease, and cellulase enzymes, in addition to their tolerance to imazethapyr. Among the selected isolates, Serratia rubidaea (A), Pseudomonas putida (B), and Serratia sp. (C) were found to have highest potential for these growth-promoting traits. However, auxin production was only detected in S. rubidaea. In the second phase of the study, the effects of soil inoculation with bacterial species A, B, and C and Sinorhizobium meliloti (R) on the growth and development of alfalfa were assessed in pot and field experiments. The results of these experiments indicated that herbicide application decreased both crop yield and photosynthetic pigments. In most cases, the herbicide was shown to have less impact upon the growth of the inoculated plants compared to the control. However, increase in yield traits, photosynthetic pigments, and microbial population only occurred in plants treated by AB, AR, and ABR bacterial inoculations. Thus, alleviation of herbicide stress in conjunction with growth promotion has been achieved by using native rhizosphere-associated bacterial isolates. These findings open new avenues of research to develop potent biofertilizers that are effective under herbicide-stressed conditions.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
The data is available by request.
References
Ahemad M, Khan MS (2010) Ameliorative effects of Mesorhizobium sp. MRC4 on chickpea yield and yield components under different doses of herbicide stress. Pestic Biochem Physiol 98:183–190. https://doi.org/10.1016/J.PESTBP.2010.06.005
Akbar S, Sultan S (2016) Soil bacteria showing a potential of chlorpyrifos degradation and plant growth enhancement. Brazilian J Microbiol 47:563–570. https://doi.org/10.1016/J.BJM.2016.04.009
Al-Garni SMS, Khan MMA, Bahieldin A (2019) Plant growth-promoting bacteria and silicon fertilizer enhance plant growth and salinity tolerance in Coriandrum sativum. J Plant Interact 14:386–396. https://doi.org/10.1080/17429145.2019.1641635
Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (1989) Short protocols in molecular biology: a compendium of methods from Current protocols in molecular biology, 2rd edn. Wiley-Interscience, 410
Barnawal D, Maji D, Bharti N, Chanotiya CS, Kalra A (2013) ACC deaminase-containing bacillus subtilis reduces stress ethylene-induced damage and improves mycorrhizal colonization and rhizobial nodulation in trigonella foenum-graecum under drought stress. J Plant Growth Regul 32:809–822. https://doi.org/10.1007/s00344-013-9347-3
Barton LL, Nurthub DE (2011) Microbial ecology. First edition, Wiley-Blackwell
Bocker T, Mohring N, Finger R (2019) Herbicide free agriculture? A bio-economic modelling application to Swiss wheat production. Agric Syst 173:378–392. https://doi.org/10.1016/j.agsy.2019.03.001
Carabias-Martinez R, Rodriguez-Gonzalo E, Fernandez-Laespada ME, Sanchez-San-Roman FJ (2000) Evaluation of surface- and ground-water pollution due to herbicides in agricultural areas of Zamora and Salamanca (Spain). J Chromatogr A 869:471–480. https://doi.org/10.1016/S0021-9673(99)01188-7
Carrillo-Castaeda G, Juarez Muos J, Peralta-Videa JR, Gomez E, Tiemannb KJ, Duarte-Gardea M, Gardea-Torresdey JL (2002) Alfalfa growth promotion by bacteria grown under iron limiting conditions. Adv Environ Res 6:391–399. https://doi.org/10.1016/S1093-0191(02)00054-0
Chauhan A, Guleria S, Balgir PP, Walia A, Mahajan R, Mehta P, Shirkot CK (2017) Tricalcium phosphate solubilization and nitrogen fixation by newly isolated Aneurinibacillus aneurinilyticus CKMV1 from rhizosphere of Valeriana jatamansi and its growth promotional effect. Brazilian J Microbiol 48:294–304. https://doi.org/10.1016/j.bjm.2016.12.001
Cycon M, Wojcik M, Borymski S, Piotrowska-Seget Z (2013) Short-term effects of the herbicide napropamide on the activity and structure of the soil microbial community assessed by the multi-approach analysis. Appl Soil Ecol 66:8–18. https://doi.org/10.1016/J.APSOIL.2013.01.014
de Souza LS, Oliveira M, Ferraz TM, De SSA (2016) Endophytic colonization of Arabidopsis thaliana by gluconacetobacter diazotrophicus and its effect on plant growth promotion, plant physiology, and activation of plant defense. Plant Soil 399:257–270. https://doi.org/10.1007/S11104-015-2672-5
Dobereiner J, Day JM, Dart PJ (1972) Nitrogenase activity and oxygen sensitivity of the Paspalum notatum-Azotobacter paspali association. J Gen Microbiol 71:103–116. https://doi.org/10.1099/00221287-71-1-103
Elsas JD van, Trevors JT, Rosado AS, Nannipieri P (2019) Modern soil microbiology. 3rd edn. CRC Press.
Fan X, Chang W, Feng F, Song F (2018) Responses of photosynthesis-related parameters and chloroplast ultrastructure to atrazine in alfalfa (Medicago sativa L.) inoculated with arbuscular mycorrhizal fungi. Ecotoxicol Environ Saf 166:102–108. https://doi.org/10.1016/J.ECOENV.2018.09.030
Fox JE, Gulledge J, Engelhaupt E, Burow ME, McLachlan JA (2007) Pesticides reduce symbiotic efficiency of nitrogen-fixing rhizobia and host plants. Proc Natl Acad Sci USA 104:10282–10287. https://doi.org/10.1073/pnas.0611710104
Gholami A, Shahsavani S, Nezarat S (2009) The effect of plant growth promoting rhizobacteria (PGPR) on germination, seedling growth and yield of maize. World Acad Sci Eng Technol 37:19–24
Glickmann E, Dessaux Y (1995) A critical examination of the specificity of the Salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Appl Environ Microbiol 61:793–796
Gomez-Godinez LJ, Fernandez-Valverde SL, Martinez Romero JC, Martinez-Romero E (2019) Metatranscriptomics and nitrogen fixation from the rhizoplane of maize plantlets inoculated with a group of PGPRs. Syst Appl Microbiol 42:517–525. https://doi.org/10.1016/j.syapm.2019.05.003
Hanson CH (2015) Alfalfa science and technology. Alfalfa Sci Technol 15:1–812. https://doi.org/10.2134/AGRONMONOGR15
Hawes MC, Bengough AG, Cassab GI, Ponce G (2003) Root caps and rhizosphere. J Plant Growth Regul 21:352–367
Ju W, Liu L, Fang L, Cui Y, Duan C, Wu H (2019) Impact of co-inoculation with plant-growth-promoting rhizobacteria and rhizobium on the biochemical responses of alfalfa-soil system in copper contaminated soil. Ecotoxicol Environ Saf 167:218–226. https://doi.org/10.1016/j.ecoenv.2018.10.016
Kalsi A, Celin SM, Bhanot P, Sahai S, Sharma JG (2020) Microbial remediation approaches for explosive contaminated soil: critical assessment of available technologies, Recent innovations and Future prospects. Environ Technol Innov 18:100721. https://doi.org/10.1016/J.ETI.2020.100721
Lazali M, Boudsocq S, Taschen E, Farissi M, Hamdi W, Ralli P, Sentenac H (2021) Crosymed project: enhancing nutrient use efficiency through legumes in agroecosystems of the mediterranean basin. Sustain 13(9):1–10. https://doi.org/10.3390/su13094695
Li H, Qiu Y, Yao T, Ma Y, Zhang H, Yang X (2020) Effects of PGPR microbial inoculants on the growth and soil properties of Avena sativa, Medicago sativa, and Cucumis sativus seedlings. Soil Tillage Res 199:104577. https://doi.org/10.1016/j.still.2020.104577
Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592. https://doi.org/10.1042/BST0110591
Liu H, Wu XQ, Ren JH, Ye JR (2011) Isolation and identification of phosphobacteria in poplar rhizosphere from different regions of China. Pedosphere 21:90–97. https://doi.org/10.1016/S1002-0160(10)60083-5
Lu P, Li Q, Liu H, Feng Z, Yan X, Hong Q, Li S (2013) Biodegradation of chlorpyrifos and 3,5,6-trichloro-2-pyridinol by Cupriavidus sp. DT-1. Bioresour Technol 127:337–342. https://doi.org/10.1016/J.BIORTECH.2012.09.116
Nosratti I, Sabeti P, Chaghamirzaee G, Heidari H (2020) Weed problems, challenges, and opportunities in Iran. Crop Prot 134:104371. https://doi.org/10.1016/j.cropro.2017.10.007
Parween T, Jan S, Mahmooduzzafar S, Fatma T, Siddiqui ZH (2016) Selective effect of pesticides on plant: a review. Crit Rev Food Sci Nutr 56:160–179. https://doi.org/10.1080/10408398.2013.787969
Pereira SIA, Castro PML (2014) Diversity and characterization of culturable bacterial endophytes from Zea mays and their potential as plant growth-promoting agents in metal-degraded soils. Environ Sci Pollut Res 21:14110–14123. https://doi.org/10.1007/S11356-014-3309-6
Pertile M, Sousa RMS, Mendes LW, Antunes JEL, de Oliveira LMS, de Araujo FF, Melo VMM, Araujo ASF (2021) Response of soil bacterial communities to the application of the herbicides imazethapyr and flumyzin. Eur J Soil Biol 102:7195253. https://doi.org/10.1016/j.ejsobi.2020.103252
Pozo C, Salmeron V, Rodelas B, Martinez-Toledo MV, Gonzalez-Lopez J (1994) Effects of the herbicide alachlor on soil microbial activities. Ecotoxicol 3:4–10. https://doi.org/10.1007/BF00121384
Putnam DH, Orloff SB (2014) Forage crops. Encycl Agric Food Syst 381–405. https://doi.org/10.1016/B978-0-444-52512-3.00142-X
Radhakrishnan R, Lee IJ (2016) Gibberellins producing Bacillus methylotrophicus KE2 supports plant growth and enhances nutritional metabolites and food values of lettuce. Plant Physiol Biochem 109:181–189. https://doi.org/10.1016/j.plaphy.2016.09.018
Radosevich M, Traina SJ, Hao YL, Tuovinen OH (1995) Degradation and mineralization of atrazine by a soil bacterial isolate. Appl Environ Microbiol 61:297–302. https://doi.org/10.1128/AEM.61.1.297-302.1995
Radovic J, Sokolovic D, Markovic J (2009) Alfalfa-most important perennial forage legume in animal husbandry. Biotechnol Anim Husb 25:465–475. https://doi.org/10.2298/bah0906465r
Ramakrishna W, Yadav R, Li K (2019) Plant growth promoting bacteria in agriculture: two sides of a coin. Appl Soil Ecol 138:10–18. https://doi.org/10.1016/J.APSOIL.2019.02.019
Ramani V (2011) Effect of pesticides on phosphate solubilization by Bacillus sphaericus and Pseudomonas cepacia. Pestic Biochem Physiol 99:232–236. https://doi.org/10.1016/J.PESTBP.2011.01.001
Rose MT, Cavagnaro TR, Scanlan CA, Rose TJ, Vancov T, Kimber S, Kennedy IR, Kookana RS, Van Zwieten L (2016) Impact of herbicides on soil biology and function. Adv Agron 136:133–220. https://doi.org/10.1016/bs.agron.2015.11.005
Shahid M, Khan MS (2018) Glyphosate induced toxicity to chickpea plants and stress alleviation by herbicide tolerant phosphate solubilizing Burkholderia cepacia PSBB1 carrying multifarious plant growth promoting activities. 3 Biotech 8(2):131. https://doi.org/10.1007/S13205-018-1145-Y
Shahid M, Ahmed B, Khan MS (2018) Evaluation of microbiological management strategy of herbicide toxicity to greengram plants. Biocatal Agric Biotechnol 14:96–108. https://doi.org/10.1016/J.BCAB.2018.02.009
Singh VK, Singh AK, Singh PP, Kumar A (2018) Interaction of plant growth promoting bacteria with tomato under abiotic stress: a review. Agric Ecosyst Environ 267:129–140. https://doi.org/10.1016/J.AGEE.2018.08.020
Tirry N, Kouchou A, Laghmari G, Lemjereb M, Hnadi H, Amrani K, Bahafid W, El Ghachtouli N (2021) Improved salinity tolerance of Medicago sativa and soil enzyme activities by PGPR. Biocatal Agric Biotechnol 31:101914. https://doi.org/10.1016/j.bcab.2021.101914
Tyagi S, Mandal SK, Kumar R, Kumar S (2018) Effect of different herbicides on soil microbial population dynamics in Rabi maize (Zea mays L.). Int J Curr Microbiol App Sci 7:3751–3758
Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703. https://doi.org/10.1128/JB.173.2.697-703.1991
Zabalza A, Gaston S, Sandalio LM, del Río LA, Royuela M (2007) Oxidative stress is not related to the mode of action of herbicides that inhibit acetolactate synthase. Environ Exp Bot 59:150–159. https://doi.org/10.1016/j.envexpbot.2005.11.003
Zimdahl RL (2018) Fundamentals of weed science. Fundam Weed Sci. https://doi.org/10.1016/C2015-0-04331-3
Funding
This study was supported by a grant from the research council of Isfahan University of Technology.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing Interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Motamedi, M., Zahedi, M., Karimmojeni, H. et al. Rhizosphere-Associated Bacteria as Biofertilizers in Herbicide-Treated Alfalfa (Medicago sativa). J Soil Sci Plant Nutr 23, 2585–2598 (2023). https://doi.org/10.1007/s42729-023-01214-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42729-023-01214-6