Title:

First record of the endophytic bacteria of Deschampsia antarctica Ė. Desv. from two distant localities of the maritime Antarctic

Authors Name:   

Olga Podolich, Ievgeniia Prekrasna, Ivan Parnikoza, Tamara Voznyuk, Ganna Zubova, Iryna Zaets, Natalia Miryuta, Ganna Myryuta, Oksana Poronnik, Iryna Kozeretska, Viktor Kunakh, Anna Maria Pirttila, Evgen Dykyi, Natalia Kozyrovska

Journal: Czech Polar Reports
Issue: 11
Volume: 1
Page Range: 134-153
No. of Pages: 20
Year: 2021
DOI:

10.5817/CPR2021-1-10

Publishers: muniPress Masaryk University Brno
ISSN:    1805-0689 (Print), 1805-0697 (On-line)
Language: English
Subject:  
Abstract:

Endophytic bacteria, recognized for their beneficial effects on plant development and adaptation, can facilitate the survival of Antarctic plants in severe environments. Here we studied endophytes of the vascular plant Deschampsia antarctica Ė. Desv. from two distantly located regions in the maritime Antarctic: King George Island (South Shetland Islands) and Galindez Island (Argentine Islands). Bacterial group-specific PCR indicated presence of Alphaproteobacteria, Betaproteobacteria, Gammaproteobacteria, Firmicutes, Cytophaga-Flavobacteria and Actinobacteria in root and leaf endosphere of D. antarctica sampled at four distinct sites of both locations. The diversity of endophytic bacteria was significantly higher in the leaves compared to the roots in plants from Galindez Island. Similarly, the diversity of endophytes was higher in the leaves rather than roots of plants from the King George Island. Twelve bacterial species were isolated from roots of D. antarctica of Galindez Island (the Karpaty Ridge and the Meteo Point) and identified by sequencing the 16S rRNA gene. Isolates were dominated by the Pseudomonas genus, followed by the genera Bacillus and Micrococcus. The vast majority of the isolates exhibited cellulase and pectinase activities, however, Bacillus spp. expressed neither of them, suggesting lack of genetic flow of these traits in endophytic bacilli in the maritime Antarctic. Pseudomonas sp. IMBG305 promoted an increase in the leaf number in most of the treated plant genotypes when compared with non-inoculated plants, and a rapid vegetation period of D. antarctica cultured in vitro, albeit the length of leaves in the treated plants was significantly lower, and flavonoid content leveled off in all treated plants. D. antarctica is known to develop diverse ecotypes with regard to ecological conditions, such as organic input, moisture or wind exposition. The D. antarctica phenotype could be extended further through the endophyte colonization, since phenotypic changes were observed in the inoculated D. antarctica plants grown in vitro in our study. Herewith, endophytes can contribute to plant phenotypic plasticity, potentially beneficial for adaptation of D. antarctica.

 

Keywords: endophytic bacteria, Antarctic hairgrass, Antarctica, plant growth promotion
 

References:

Affendy, H., Aminuddin, M., Arifin, A., Mandy, M., Julius, K. and Tamer, A. T. (2010): Effects of light intensity on Orthosiphon stamineus Benth. seedlings treated with different organic fertilizers. International Journal of Agricultural Research, 5(4): 201-207. doi: 10.3923/ijar.2010.201.207.

Alain, K., Querellou, J. (2009): Cultivating the uncultured: Limits, advances and future challenges. Extremophiles, 3: 583-594. doi: 10.1007/s00792-009-0261-3.

Alberdi, M., Bravo, L. A., Gutiérrez A., Gidekel M. and Corcuera, L. J. (2002): Ecophysiology of Antarctic vascular plants. Physiologia Plantarum, 115: 479-486. doi: 10.1034/j.1399-3054.2002.1150401.x.

Ardanov, P., Ovcharenko, L., Zaets, I., Kozyrovska, N. and Pirttilä, A. M. (2011): Endophytic bacteria enhancing growth and disease resistance of potato (Solanum tuberosum L.). Biological Control, 5(1): 43-49. doi: 10.1016/j.biocontrol.2010.09.014.

Bayman, P., Lebrón, L. L., Tremblay, R. L. and Lodge, D. J. (1997): Variation in endophytic fungi from roots and leaves of Lepanthes (Orchidaceae). New Phytologist, 135(1): 143-149. doi: 10.1046/j.1469-8137.1997.00618.x.

Berríos, G., Cabrera, G., Gidekel, M. and Gutiérrez-Moraga, A. (2013): Characterization of a novel antarctic plant growth-promoting bacterial strain and its interaction with antarctic hair grass (Deschampsia antarctica Desv.). Polar Biology, 36: 349-362. doi: 10.1007/s00300-012-1264-6.

Bertani, G. (1951): Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. Journal of Bacteriology, 62(3): 293-300. doi: 10.1128/JB.62.3.293-300.1951.

Bodenhausen, N., Horton, M. W. and Bergelson, J. (2013): Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. PLOS ONE, 8(2): e56329. doi: 10.1371/journal.pone.0056329.

Brader, G., Compant, S., Mitter, B., Trognitz, F. and Sessitsch, A. (2014): Metabolic potential of endophytic bacteria. Current Opinion in Biotechnology, 27: 30-37. doi: 10.1016/j.copbio.2013.09.012.

Chamam, A., Sanguin, H., Bellvert, F., Meiffren, G., Comte, G., Wisniewski-Dyé, F., Bertrand, C. and Prigent-Combaret, C. (2013): Plant secondary metabolite profiling evidences strain-dependent effect in the Azospirillum-Oryza sativa association. Phytochemistry, 87: 65-77. doi: 10.1016/j.phytochem.2012.11.009.

Chen, X., Zeng, Y. and Jiao, N. (2008): Characterization of Cytophaga-Flavobacteria community structure in the Bering Sea by cluster-specific 16S rRNA gene amplification analysis. Journal of Microbiology and Biotechnology, 18: 194-198.

Cheng, D., Tian, Z., Feng, L., Xu, L. and Wang, H. (2019): Diversity analysis of the rhizospheric and endophytic bacterial communities of Senecio vulgaris L. (Asteraceae) in an invasive range. PeerJ, 6(3): e6162. doi: 10.7717/peerj.6162.

Chong, C. W., Dunn, M. J., Convey, P., Tan, G. Y. A., Wong, R. C. S. and Tan, I. K. P. (2009): Environmental influences on bacterial diversity of soils on Signy Island, maritime Antarctic. Polar Biology, 32: 1571-1582. doi: 10.1007/s00300-009-0656-8.

Cid, F. P., Inostroza, N. G., Graether, S. P., Bravo, L. A. and Jorquera, M. A. (2017): Bacterial community structures and ice recrystallization inhibition activity of bacteria isolated from the phyllosphere of the Antarctic vascular plant Deschampsia antarctica. Polar Biology, 40: 1319-1331. doi: 10.1007/s00300-016-2036-5.

Convey, P. (1996): The influence of environmental characteristics on life history attributes of Antarctic terrestrial biota. Biological Reviews, 71: 191-225. doi: 10.1111/j.1469-185X.1996. tb00747.x.

Devi, K. A., Pandey, G., Rawat, A. K. S., Sharma, G. D. and Pandey, P. (2017): The endophytic symbiont-Pseudomonas aeruginosa stimulates the antioxidant activity and growth of Achyranthes aspera L. Frontiers in Microbiology, 8: 1897  doi: 10.3389/fmicb.2017.01897.

Felsenstein, J. (1985): Confidence limits on phylogenies: An approach using the bootstrap. Evolution, 39(4): 783-791. doi: 10.2307/2408678.

Fredriksson, N. J., Hermansson, M. and Wilén, B. M. (2013): The choice of PCR primers has great impact on assessments of bacterial community diversity and dynamics in a wastewater treatment plant. PLoS ONE, 8(10): e76431. doi: 10.1371/journal.pone.0076431.

Gie³wanowska, I., Szczuka, E. (2005): New ultrastructural features of organelles in leaf cells of Deschampsia antarctica Desv. Polar Biology, 28: 951-955. doi: 10.1007/s00300-005-0024-2.

Gran-Scheuch, A., Ramos-Zuñiga, J., Fuentes, E., Bravo, D. and Pérez-Donoso, J. M. (2020): Effect of Co-contamination by PAHs and Heavy Metals on Bacterial Communities of  Diesel Contaminated Soils of South Shetland Islands, Antarctica. Microorganisms, 8(11): 1749. doi: 10.3390/microorganisms8111749.

Gupta, M., Sharma, M., Singh, S., Gupta, P. and Bajaj, B. K. (2015): Enhanced production of cellulase from Bacillus licheniformis k-3 with potential for saccharification of rice straw. Energy Technology, 3: 216-224. doi: 10.1002/ente.201402137.

Hardoim, P. R., van Overbeek, L. S., Berg, G., Pirttilä, A. M., Compant, S., Campisano, A., Döring, M. and Sessitsch, A. (2015): The Hidden World within Plants: Ecological and Evolutionary Considerations for Defining Functioning of Microbial Endophytes. Microbiology and Molecular Biology Reviews, 79(3): 293-320. doi: 10.1128/mmbr.00050-14.

Hereme, R., Morales-Navarro, S., Ballesteros, G., Barrera, A., Ramos, P., Gundel, P. E. and Molina-Montenegro, M. A. (2020): Fungal endophytes exert positive effects on Colobanthus quitensis under water stress but neutral under a projected climate change scenario in Antarctica. Frontiers in Microbiology, 11: 264. doi: 10.3389/fmicb.2020.00264.

Higuera-Llantén, S., Vásquez-Ponce, F., Núñez-Gallegos, M., Pavlov, M. S., Marshall, S. and Olivares-Pacheco, J. (2018): Phenotypic and genotypic characterization of a novel multi-antibiotic-resistant, alginate hyperproducing strain of Pseudomonas mandelii isolated in Antarctica. Polar Biology, 41(3): 469-480. doi: 10.1007/s00300-017-2206-0.

Huang, J. (1986): Ultrastructure of bacterial penetration in plants. Annual Review of Phytopathology, 24(1): 141-157. doi: 10.1146/annurev.py.24.090186.001041.

James, E. K., Gyaneshwar, P., Mathan, N., Barraquio, W. L., Reddy, P. M., Iannetta, P. P. M., Olivares, F. L. and Ladha, J. K. (2002): Infection and colonization of rice seedlings by the plant growth-promoting bacterium Herbaspirillum seropedicae Z67. Molecular Plant-Microbe Interactions, 15(9): 894-906. doi: 10.1094/MPMI.2002.15.9.894.

Jasim, B., John Jimtha, C., Jyothis, M. and Radhakrishnan, E. K. (2013): Plant growth promoting potential of endophytic bacteria isolated from Piper nigrum. Plant Growth Regulation. 71: 1-11. doi: 10.1007/s10725-013-9802-y.

Jha, Y. (2019): Endophytic bacteria-mediated regulation of secondary metabolites for the growth induction in Hyptis suaveolens under stress. In: D. Egamberdieva, A. Tiezzi (eds): Medically Important Plant Biomes: Source of Secondary Metabolites. Microorganisms for Sustainability, vol 15. Springer, Singapore, pp. 277–292. doi: 10.1007/978-981-13-9566-6_12.

Jones, C. G., Hartley, S. E. (1999): A protein competition model of phenolic allocation. Oikos, 86(1): 27-44. doi: 10.2307/3546567.

King, E. O., Ward, M. K. and Raney, D. E. (1954): Two simple media for the demonstration of pyocyanin and fluorescin. The Journal of Laboratory and Clinical Medicine, 44(2): 301-307. doi: 10.5555/uri:pii:002221435490222X.

Khan, S. S., Verma, V. and Shafaq, R. (2020): Diversity and the role of endophytic bacteria: A review. Botanica Serbica, 44(2): 103-120. doi: 10.2298/BOTSERB2002103K.

Kozyrovska, N. O. (2013): Crosstalk between endophytes and a plant host within information processing networks. Biopolymers and Cell, 29(3): 234-243. doi: 10.7124/bc.00081D.

Kumar, S., Stecher, G., Li, M., Knyaz, C. and Tamura, K. (2018): MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6): 1547-1549. doi: 10.1093/molbev/msy096.

Lally, R. D., Galbally, P., Moreira, A. S., Spink, J., Ryan, D., Germaine, K. J. and Dowling, D. N. (2017): Application of endophytic Pseudomonas fluorescens and a bacterial consortium to Brassica napus can increase plant height and biomass under greenhouse and field conditions. Frontiers in Plant Science, 8: 2193. doi: 10.3389/fpls.2017.02193.

Li, J. L., Sun, X., Zheng, Y., Lü, P. P., Wang, Y. L. and Guo, L. D. (2020): Diversity and community of culturable endophytic fungi from stems and roots of desert halophytes in northwest China. MycoKeys, 62: 75-95. doi: 10.3897/mycokeys.62.38923.

Mano, H., Tanaka, F., Watanabe, A., Kaga, H., Okunishi, S. and Morisaki, H. (2006): Culturable surface and endophytic bacterial flora of the maturing seeds of rice plants (Oryza sativa) cultivated in a paddy field. Microbes and Environments, 21(2): 86-100. doi: 10.1264/ jsme2.21.86.

Mano, H., Tanaka, F., Nakamura, C., Kaga, H. and Morisaki, H. (2007): Culturable endophytic bacterial flora of the maturing leaves and roots of rice plants (Oryza sativa) cultivated in a paddy field. Microbes and Environments, 22 (2): 175-185. doi: 10.1264/jsme2.22.175.

Mano, H., Morisaki, H. (2008): Endophytic bacteria in the rice plant. Microbes and Environments, 23(2): 109-117. doi: 10.1264/jsme2.23.109.

Meyer, S., Cerovic, Z. G., Goulas, Y., Montpied, P., Demotes-Mainard, S., Bidel, L. P. R., Moya, I. and Dreyer, E. (2006): Relationships between optically assessed polyphenols and chlorophyll contents, and leaf mass per area ratio in woody plants: A signature of the carbon-nitrogen balance within leaves? Plant, Cell and Environment, 29: 1338-1348. doi: 10.1111/ j.1365-3040.2006.01514.x.

Miliute, I., Buzaite, O., Gelvonauskiene, D., Sasnauskas, A., Stanys, V. and Baniulis, D. (2016): Plant growth promoting and antagonistic properties of endophytic bacteria isolated from domestic apple. Zemdirbyste, 103(1): 77-82. doi: 10.13080/z-a.2016.103.010.

Miller, J. (1972): Experiments in molecular genetics. Cold Spring Harbor Laboratory, New York, 466 p.

Molina-Montenegro, M. A., Acuña-Rodríguez, I. S., Torres-Díaz, C., Gundel, P. E. and Dreyer, I. (2020): Antarctic root endophytes improve physiological performance and yield in crops under salt stress by enhanced energy production and Na+ sequestration. Scientific Reports, 10: 5819. doi: 10.1038/s41598-020-62544-4.

Mühling, M., Woolven-Allen, J., Murrell, J. C. and Joint, I. (2008): Improved group-specific PCR primers for denaturing gradient gel electrophoresis analysis of the genetic diversity of complex microbial communities. ISME Journal, 2: 379-392. doi: 10.1038/ismej.2007.97.

Müller, H., Berg, C., Landa, B. B., Auerbach, A., Moissl-Eichinger, C. and Berg, G. (2015): Plant genotype-specific archaeal and bacterial endophytes but similar Bacillus antagonists colonize Mediterranean olive trees. Frontiers in Microbiology, 6: 138. doi: 10.3389/fmicb. 2015.00138.

Navrotska, D. O., Andreev, I. O., Parnikoza, I. Y., Spiridonova, K. V., Poronnik, O. O., Miryuta, N. Y., Myryuta, G. Y., Zahrychuk, O. M., Drobyk, N. M. and Kunakh, V. A. (2017): Comprehensive characterization of cultivated in vitro Deschampsia antarctica E. Desv. plants with different chromosome numbers. Cytology and Genetics, 51: 422-431. doi: 10.3103/ S009545271706010X.

Nuzhyna, N., Parnikoza, I., Poronnik, O., Kozeretska, I. and Kunakh, V. (2019): Anatomical variations of Deschampsia antarctica É. Desv.plants from distant Antarctic regions, in vitro culture, and in relations to Deschampsia caespitosa (L.) P. Beauv. Polish Polar Research, 40(4): 361-383.

Ozheredova, I. P., Parnikoza, I. Y., Poronnik, O. O., Kozeretska, I. A., Demidov, S. V. and Kunakh, V. A. (2015): Mechanisms of antarctic vascular plant adaptation to abiotic environmental factors. Cytology and Genetics, 49: 139-145. doi.org/10.3103/S00954527150 20085.

Parnikoza, I., Kozeretska, I. and Kunakh, V. (2011a): Vascular plants of the maritime Antarctic: Origin and adaptation. American Journal of Plant Sciences, 2(3): 381-395. doi: 10.4236/ajps.2011.23044.

Parnikoza, I. Y., Loro, P., Miryuta, N. Y., Kunakh, V. A. and Kozeretska, I. A. (2011b): The influence of some environmental factors on cytological and biometric parameters and chlorophyll content of Deschampsia antarctica Desv. in the maritime Antarctic. Cytology and Genetics, 45: 170. doi: 10.3103/S0095452711030078.

Pollard, J. H. P. (1982): A handbook of numerical and statistical techniques. Finances and Statistics, Moscow, 454 p. (In Russian).

Poosakkannu, A., Nissinen, R. and Kytöviita, M. M. (2015): Culturable endophytic microbial communities in the circumpolar grass, Deschampsia flexuosa in a sub-Arctic inland primary succession are habitat and growth stage specific. Environmental Microbiology Reports, 7: 111-122. doi: 10.1111/1758-2229.12195.

Ramos, P., Rivas, N., Pollmann, S., Casati, P. and Molina-Montenegro, M. A. (2018): Hormonal and physiological changes driven by fungal endophytes increase Antarctic plant performance under UV-B radiation. Fungal Ecology, 34: 76-82. doi: 10.1016/j.funeco.2018. 05.006.

Reinhold-Hurek, B., Maes, T., Gemmer, S., Van Montagu, M. and Hurek, T. (2006): An endoglucanase is involved in infection of rice roots by the not-cellulose-metabolizing endophyte Azoarcus sp. strain BH72. Molecular Plant-Microbe Interactions, 19(2): 181-188. doi: 10.1094/MPMI-19-0181.

Robinson, S. A., Wasley, J. and Tobin, A. K. (2003): Living on the edge – plants and global change in continental and maritime Antarctica. Global Change Biology, 9: 1681-1717. doi: 10.1046/j.1365-2486.2003.00693.x.

Rosa, L. H., Vaz, A. B. M., Caligiorne, R. B., Campolina, S. and Rosa, C. A. (2009): Endophytic fungi associated with the Antarctic grass Deschampsia antarctica Desv. (Poaceae). Polar Biology, 32: 161-167. doi: 10.1007/s00300-008-0515-z.

Rosenblueth, M., Martínez-Romero, E. (2006): Bacterial endophytes and their interactions with hosts. Molecular Plant-Microbe Interactions, 19(8): 827-37. doi: 10.1094/MPMI-19-0827.

Saitou, N., Nei, M. (1987): The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4(4): 406-425. doi: 10.1093/ oxfordjournals.molbev.a040454.

Sanger, F., Nicklen, S. and Coulson, A. R. (1977): DNA sequencing with chain-terminating inhibitors. PNAS, 74(12): 5463-5467. doi: 10.1073/pnas.74.12.5463.

Santiago, I. F., Rosa, C. A. and Rosa, L. H. (2017): Endophytic symbiont yeasts associated with the Antarctic angiosperms Deschampsia antarctica and Colobanthus quitensis. Polar Biology, 40: 177-183. doi: 10.1007/s00300-016-1940-z.

Santoyo, G., Moreno-Hagelsieb, G., del Carmen Orozco-Mosqueda, M. and Glick, B. R. (2016): Plant growth-promoting bacterial endophytes. Microbiological Research, 183: 92-99. doi: 10.1016/j.micres.2015.11.008.

Scheible, W.-R., Morcuende, R., Czechowski, T., Fritz, C., Osuna, D., Palacios-Rojas, N., Schindelasch, D., Thimm, O., Udvardi, M. K. and Stitt, M. (2004): Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiology, 136(1): 2483-2499. doi: 10.1104/pp.104.047019.

Sessitsch, A., Hardoim, P., Döring, J., Weilharter, A., Krause, A., Woyke, T., Mitter, B., Hauberg-Lotte, L., Friedrich, F., Rahalkar, M., Hurek, T., Sarkar, A., Bodrossy, L., Van Overbeek, L., Brar, D., Van Elsas, J. D. and Reinhold-Hurek, B. (2012): Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Molecular Plant-Microbe Interactions, 25(1): 28-36. doi: 10.1094/MPMI-08-11-0204.

Soares, M. M. C. N., Da Silva, R. and Gomes, E. (1999): Screening of bacterial strains for pectinolytic activity: Characterization of the polygalacturonase produced by Bacillus sp. Revista de Microbiologia, 30(4): 299-303. doi: 10.1590/S0001-37141999000400002.

Stach, J. E. M., Maldonado, L. A., Ward, A. C., Goodfellow, M. and Bull, A. T. (2003): New primers for the class Actinobacteria: Application to marine and terrestrial environments. Environmental Microbiology, 5(10): 828-841. doi: 10.1046/j.1462-2920.2003.00483.x.

Starr, M. P., Chatterjee, A. K., Starr, P. B. and Buchanan, G. E. (1977): Enzymatic degradation of polygalacturonic acid by Yersinia and Klebsiella species in relation to clinical laboratory procedures. Journal of Clinical Microbiology, 6(4): 379-386.

Tamošiūnė, I., Stanienė, G., Haimi, P., Stanys, V., Rugienius, R. and Baniulis, D. (2018): Endophytic Bacillus and Pseudomonas spp. modulate apple shoot growth, cellular redox balance, and protein expression under in vitro conditions. Frontiers in Plant Science, 9: 889. doi: 10.3389/fpls.2018.00889.

Tamura, K., Nei, M. and Kumar, S. (2004): Prospects for inferring very large phylogenies by using the neighbor-joining method. PNAS, 101(30): 11030-11035. doi: 10.1073/pnas. 0404206101.

Toju, H., Kurokawa, H. and Kenta, T. (2019): Factors influencing leaf- and root-associated communities of bacteria and fungi across 33 plant orders in a grassland. Frontiers in Microbiology, 10: 241. doi: 10.3389/fmicb.2019.00241.

Upson, R., Newsham, K. K., Bridge, P. D., Pearce, D. A. and Read, D. J. (2009): Taxonomic affinities of dark septate root endophytes of Colobanthus quitensis and Deschampsia antarctica, the two native Antarctic vascular plant species. Fungal Ecology, 2(4): 184-196. doi: 10.1016/j.funeco.2009.02.004.

Vásquez-Ponce, F., Higuera-Llantén, S., Pavlov, M. S., Marshall, S. H. and Olivares-Pacheco, J. (2018): Phylogenetic MLSA and phenotypic analysis identification of three probable novel Pseudomonas species isolated on King George Island, South Shetland, Antarctica. Brazilian Journal of Microbiology, 49(4): 695-702. doi: 10.1016/j.bjm.2018.02.005.

Wood, P. J. (1981): The use of dye-polysaccharide interactions in β-D-glucanase assay. Carbohydrate Research, 94(2): 19-23. doi: 10.1016/S0008-6215(00)80727-2.

Yang, R., Liu, P. and Ye, W. (2017): Illumina-based analysis of endophytic bacterial diversity of tree peony (Paeonia Sect. Moutan) roots and leaves. Brazilian Journal of Microbiology, 48(4): 695-705. doi: 10.1016/j.bjm.2017.02.009.

Yudakova, O. I., Tyrnov, V. S., Kunakh, V. A.,  Kozeretskaya, I. A. and Parnikoza, I. Yu. (2016): Adaptation of the seed reproduction system to conditions of maritime Antarctic in Deschampsia antarctica Ė. Desv. Russian Journal of Developmental Biology, 47: 138-146. doi: 10.1134/ S1062360416030073.

Zaets, I., Kozyrovska, N. (2012): Heavy metal resistance in plants: A putative role of endophytic bacteria. In: A. Zaidi, P. Wani, M. Khan (eds): Toxicity of heavy metals to legumes and bioremediation. Springer, Vienna. pp. 203–217. doi: 10.1007/978-3-7091-0730-0_12.

Zahrychuk, O. M., Drobyk, N. M., Kozeretska, I. A., Parnikoza, I. Y. and Kunakh, V. A. (2012): Introduction in culture in vitro of Deschampsia аntarctica Desv. (Poaceae) from two regions of Maritime Antarctica. Ukrainian Antarctic Journal, 10(11): 289-295. doi: 10.33275/ 1727-7485.10-11.2012.309.

Zhang, Q., Acuña, J. J., Inostroza, N. G., Mora, M. L., Radic, S., Sadowsky, M. J. and Jorquera, M. A. (2019): Endophytic bacterial communities associated with roots and leaves of plants growing in chilean extreme environments. Scientific Reports, 9: 4950. doi: 10.1038/ s41598-019-41160-x.

Zhang, Q., Acuña, J. J., Inostroza, N. G., Duran, P., Mora, M. L., Sadowsky, M. J. and Jorquera, M. A. (2020): Niche differentiation in the composition, predicted function, and co-occurrence networks in bacterial communities associated with antarctic vascular plants. Frontiers in Microbiology, 11: 1036. doi: 10.3389/fmicb.2020.01036.

Zhao, L., Xu, Y., Lai, X. H., Shan, C., Deng, Z. and Ji, Y. (2015): Screening and characterization of endophytic Bacillus and Paenibacillus strains from medicinal plant Lonicera japonica for use as potential plant growth promoters. Brazilian Journal of Microbiology, 46(4): 977-989. doi: 10.1590/S1517-838246420140024.

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