Abstract
Plants Nicotiana tabacum L. with the choline oxidase gene (codA) responsible for the synthesis of glycine-betaine by agrobacterial transformation were obtained. In order to identify possible environmental consequences during the cultivation of transformants, microbial complexes in the rhizosphere were studied. Soil actinomycetes were used as a bioindication group of microorganisms. The abundance, taxonomic composition, and functional structure of the rhizosphere complexes of the original Samsun variety and independent transgenic lines CodA7 and CodA17 with the different codA gene were expressed. There were no significant differences in the taxonomic structure or the occurrence of phytopathogenic fungal antagonists or cellulolytic agents in the rhizosphere of the original plants and transformants. The structure of actinomycete complexes of transformants was characterized by variability comparable in magnitude with variability due to the stress effect of the soil background.
Similar content being viewed by others
REFERENCES
Agarwal, P.K. and Jha, B., Transcription factors in plants and ABA dependent and independent abiotic stress signaling, Biol. Plant., 2010, vol. 54, pp. 201–212.
Bhatti, A.A., Haq, S., and Bhat, R.A., Actinomycetes benefaction role in soil and plant health, Microb. Pathog., 2017, vol. 111, pp. 458–467.
Brookes, G. and Barfoot, P., GM Crops: Global Socio-Economic and Environmental Impacts 1996–2015, UK: PG Eeconomics LTD, 2017.
Egorov, N.S., Osnovy ucheniya ob antibiotikakh (Fundamentals of the Teaching of Antibiotics), Moscow: Nauka, 2004.
Gauze, G.F., Preobrazhenskaya, T.P., Sveshnikova, M.A., Terekhova, L.P., and Maksimova, T.S., Opredelitel’ aktinomitsetov. Rody Sreptomyces, Streptoverticillium, Chainia (Keys to Actinomycetes. Genera Sreptomyces, Streptoverticillium, and Chainia), Moscow: Nauka, 1983.
de Jesus Sousa, J.A. and Olivares, F.L., Plant growth promotion by Streptomycetes: ecophysiology, mechanisms and applications, Chem. Biol. Technol. Agricult., 2016, vol. 3, no. 1, p. 24.
Kochetov, A.V. and Shumnyi, V.K., Transgenic plants as genetic models for studying the functions of plant genes, Vavilov. Zh. Genet. Selekts., 2016, vol. 20, no. 4, pp. 476–481.
Kremer, R.J. and Means, N.E., Glyphosate and glyphosate-resistant crop interactions with rhizosphere microorganisms, Eur. J. Agron., 2009, vol. 31, no. 3, pp. 153–161.
Labeda, D.P., Taxonomic evaluation of putative Streptomyces scabiei strains held in the ARS Culture Collection (NRRL) using multi-locus sequence analysis, Antonie van Leeuwenhoek, 2016, vol. 109, no. 3, pp. 349–356.
Labeda, D.P., Dunlap, C.A., Rong, X., Huang, Y., Doroghazi, J.R., Ju, K.S., and Metcalf, W.W., Phylogenetic relationships in the family Streptomycetaceae using multi-locus sequence analysis, Antonie van Leeuwenhoek, 2017, vol. 110, no. 4, pp. 563–583.
Ladics, G.S., Bartholomaeus, A., Bregitzer, P., Doerrer, N.G., Gray, A., Holzhauser, T., and Parrott, W., Genetic basis and detection of unintended effects in genetically modified crop plants, Transgenic Res., 2015, vol. 24, no. 4, pp. 587–603.
Li, Z., Cui, J., Mi, Z., Tian, D., Wang, J., Ma, Z., and Niu, S., Responses of soil enzymatic activities to transgenic Bacillus thuringiensis (Bt) crops—a global meta-analysis, Sci. Total Environ., 2019, vol. 651, pp. 1830–1838.
Meriles, J.M., Vargas Gil, S., Haro, R.J., March, G.J., and Guzman, C.A., Glyphosate and previous crop residue effect on deleterious and beneficial soil-borne fungi from a peanut-corn-soybean rotations, J. Phytopath., 2006, vol. 154, no. 5, pp. 309–316.
Murashige, T. and Skoog, F., A revised medium for rapid growth and bioassays with tobacco tissue culture, Physiol. Plant., 1962, vol. 15, pp. 473–497.
Oguchi, T., Kashimura, Y., Mimura, M., Yu, X., Matsunaga, E., Nanto, K., Shimada, T., Kikuchi, A., and Watanabe, K.N., A multi-year assessment of the environmental impact of transgenic eucalyptus trees harboring a bacterial choline oxidase gene on biomass, precinct vegetation and the microbial community, Transgenic Res., 2014, vol. 23, pp. 767–777.
Bergey’s Manual of Determinative Bacteriology, Holt, J.G., Krieg, N.R., Sneath, P.H.A., Staley, J.T., and Williams, S.T., Eds., Baltimore: Williams and Wilkins, 1993, 9th ed.
Prasad, K.V.S.K., Sharmila, P., Kumar, P.A., and Saradhi, P.P., Transformation of Brassica juncea (L.) Czern with bacterial coda gene enhances its tolerance to salt stress, Mol. Breed., 2000, vol. 6, pp. 489–499.
Sakamoto, A. and Murata, N., Genetic engineering of glycine-betaine synthesis in plants: current status and implications for enhancement of stress tolerance, J. Exp. Bot., 2000, vol. 51, no. 342, pp. 81–88.
Shirokikh, I.G., Zenova, G.M., and Zvyagintsev, D.G., Actinomycetes in the rhizosphere of barley grown on acid soddy podzolic soil, Microbiology, 2002, vol. 71, no. 4, pp. 455–459.
Shirokikh, I.G., Shirokikh, A.A., Merzaeva, O.V., and Tumasova, M.I., Actinomycetes in the rhizosphere of red clover on a soddy-podzolic soil, Eur. Soil Sci., 2004, vol. 37, no. 7, pp. 762–768.
Singh, A.K. and Dubey, S.K., Current trends in Bt crops and their fate on associated microbial community dynamics: a review, Protoplasma, 2016, vol. 253, no. 3, pp. 663–681.
Teather, R.M. and Wood, P.J., Use of Congo red–polysaccharide interaction in enumeration and characterization of cellulozalytic bacteria the bovine rumen, Appl. Environ. Microbiol., 1982, vol. 43, pp. 777–780.
Tran, N.-H.T., Oguchi, T., Matsunaga, E., Kawaoka, A., Watanabe, K.N., and Kikuchi, A., Environmental risk assessment of impacts of transgenic Eucalyptus camaldulensis events highly expressing bacterial choline oxidase A gene, Plant Biotechnol., 2018, vol. 35, pp. 393–397.
Turrini, A., Sbrana, C., and Giovannetti, M., Belowground environmental effects of transgenic crops: a soil microbial perspective, Res. Microbiol., 2015, vol. 166, no. 3, pp. 121–131.
Viaene, T., Langendries, S., Beirinckx, S., Maes, M., and Goormachtig, S., Streptomyces as a plant’s best friend?, FEMS Microbiol. Ecol., 2016, vol. 92, no. 8, pp. 1–10. https://doi.org/10.1093/femsec/fiw119
Vurukonda, S.S.K.P., Giovanardi, D., and Stefani, E., Plant growth promoting and biocontrol activity of Streptomyces spp. as endophytes, Int. J. Mol. Sci., 2018, vol. 19, no. 4, p. 952.
You, L., Song, Q., Wu, Y., Li, S., Jiang, C., Chang, L., and Zhang, J., Accumulation of glycine betaine in transplastomic potato plants expressing choline oxidase confers improved drought tolerance, Planta, 2019, vol. 249, no. 6, pp. 1963–1975.
Zablotowicz, R.M. and Reddy, K.N., Nitrogenase activity, nitrogen content, and yield responses to glyphosate in glyphosate-resistant soybean, Crop. Protect., 2007, vol. 26, pp. 370–376.
Zhang, Y.J., Xie, M., and Peng, D.L., Effects of the transgenic CrylAc and CpTI insect-resistant cotton SGK321 on rhizosphere soil microorganism populations in northern China, Plant, Soil Environ., 2014, vol. 60, no. 6, pp. 285–289.
Funding
This work was carried out within the framework of State Assignments (project nos. 0767-2019-0090 and 0574-2019-0002) and was supported in part by the Russian Foundation for Basic Research, project no. 19-016-00207_a.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The authors declare that they have no conflicts of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.
Rights and permissions
About this article
Cite this article
Shirokikh, I.G., Nasarova, Y.I., Raldugina, G.N. et al. Analysis of Actinobiota in the Tobacco Rhizosphere with a Heterologous Choline Oxidase Gene from Arthrobacter globiformis. Biol Bull Russ Acad Sci 49, 713–720 (2022). https://doi.org/10.1134/S1062359022010137
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1062359022010137