Potential plant benefits of endophytic microorganisms associated with halophyte <i>Glycyrrhiza glabra</i> L.

Gulsanam Mardonova; Vyacheslav Shurigin; Farkhod Eshboev; Dilfuza Egamberdieva; Gulsanam Mardonova; Vyacheslav Shurigin; Farkhod Eshboev; Dilfuza Egamberdieva

doi:10.3934/microbiol.2024037

AIMS Microbiology

2024, Volume 10, Issue 4: 859-879. doi: 10.3934/microbiol.2024037

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Research article

Potential plant benefits of endophytic microorganisms associated with halophyte Glycyrrhiza glabra L.

1.
Faculty of Biology, National University of Uzbekistan, Tashkent 100174, Uzbekistan
2.
State Key Laboratory of Desert and Oasis Ecology, Xinjiang Key Laboratory of Biodiversity Conservation and Application in Arid Lands, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi 830011, Xinjiang, China
3.
S. Yu. Yunusov Institute of the Chemistry of Plant Substances, Academy of Sciences of the Republic of Uzbekistan, Tashkent 100170, Uzbekistan
4.
School of Chemical Engineering, New Uzbekistan University, Movarounnahr Street 1, Mirzo Ulugbek District, Tashkent, 100000, Uzbekistan
5.
Institute of Fundamental and Applied Research, National Research University TIIAME, Tashkent 100000, Uzbekistan

Received: 11 April 2024 Revised: 14 August 2024 Accepted: 11 September 2024 Published: 30 September 2024

In this study, bacteria associated with licorice (Glycyrrhiza glabra L.) were characterized through 16S rRNA gene analysis. Profiling of endophytic bacteria isolated from Glycyrrhiza glabra tissues revealed 18 isolates across the following genera: Enterobacter (4), Pantoea (3), Bacillus (2), Paenibacillus (2), Achromobacter (2), Pseudomonas (1), Escherichia (1), Klebsiella (1), Citrobacter (1), and Kosakonia (1). Furthermore, the beneficial features of bacterial isolates for plants were determined. The bacterial isolates showed the capacity to produce siderophores, hydrogen cyanide (HCN), indole-3-acetic acid (IAA), chitinase, protease, glucanase, lipase, and other enzymes. Seven bacterial isolates showed antagonistic activity against F. culmorum, F. solani, and R. solani. According to these results, licorice with antimicrobial properties may serve as a source for the selection of microorganisms that have antagonistic activity against plant fungal pathogens and may be considered potential candidates for the control of plant pathogens. The selected bacterial isolates, P. polymyxa GU1, A. xylosoxidans GU6, P. azotoformans GU7, and P. agglomerans GU18, increased root and shoot growth of licorice and were able to colonize the plant root. They can also serve as an active part of bioinoculants, improving plant growth.
- licorice,
- plant beneficial bacteria,
- antagonism,
- endophytes
Citation: Gulsanam Mardonova, Vyacheslav Shurigin, Farkhod Eshboev, Dilfuza Egamberdieva. Potential plant benefits of endophytic microorganisms associated with halophyte Glycyrrhiza glabra L.[J]. AIMS Microbiology, 2024, 10(4): 859-879. doi: 10.3934/microbiol.2024037

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Abstract

In this study, bacteria associated with licorice (Glycyrrhiza glabra L.) were characterized through 16S rRNA gene analysis. Profiling of endophytic bacteria isolated from Glycyrrhiza glabra tissues revealed 18 isolates across the following genera: Enterobacter (4), Pantoea (3), Bacillus (2), Paenibacillus (2), Achromobacter (2), Pseudomonas (1), Escherichia (1), Klebsiella (1), Citrobacter (1), and Kosakonia (1). Furthermore, the beneficial features of bacterial isolates for plants were determined. The bacterial isolates showed the capacity to produce siderophores, hydrogen cyanide (HCN), indole-3-acetic acid (IAA), chitinase, protease, glucanase, lipase, and other enzymes. Seven bacterial isolates showed antagonistic activity against F. culmorum, F. solani, and R. solani. According to these results, licorice with antimicrobial properties may serve as a source for the selection of microorganisms that have antagonistic activity against plant fungal pathogens and may be considered potential candidates for the control of plant pathogens. The selected bacterial isolates, P. polymyxa GU1, A. xylosoxidans GU6, P. azotoformans GU7, and P. agglomerans GU18, increased root and shoot growth of licorice and were able to colonize the plant root. They can also serve as an active part of bioinoculants, improving plant growth.

Acknowledgments

This research was supported by the grant funded by Innovation Development Agency of Uzbekistan.

Conflict of interest

The authors declare no conflict of interest.

Author contributions

DE designed the experiment. GM conducted the laboratory experiments. VS and FE analyzed the results of experiments. DE, VS, and FE wrote the manuscript. All authors read and approved the manuscript.

References

[1]	Santos MLD, Berlitz DL, Wiest SLF, et al. (2018) Benefits associated with the interaction of endophytic bacteria and plants. Braz Arch Biol Technol 61: 1-11. https://doi.org/10.1590/1678-4324-2018160431
[2]	Egamberdieva D, Alimov J, Shurigin V, et al. (2022) Diversity and plant growth-promoting ability of endophytic, halotolerant bacteria associated with Tetragonia tetragonioides (Pall.) Kuntze. Plants 11: 49. https://doi.org/10.3390/plants11010049
[3]	Egamberdieva D, Ma H, Reckling M, et al. (2022) Interactive effects of biochar and N and P nutrients on the symbiotic performance, growth, and nutrient uptake of soybean (Glycine max L.). Agronomy 12: 27. https://doi.org/10.3390/agronomy12010027
[4]	Weyens N, van der Lelie D, Taghavi S, et al. (2009) Phytoremediation: Plant–endophyte partnerships take the challenge. Curr Opin Biotechnol 20: 248-254. https://doi.org/10.1016/j.copbio.2009.02.012
[5]	Shurigin V, Alaylar B, Davranov K, et al. (2021) Diversity and biological activity of culturable endophytic bacteria associated with marigold (Calendula officinalis L.). AIMS Microbiol 7: 336-353. https://doi.org/10.3934/microbiol.2021021
[6]	Shurigin V, Egamberdieva D, Li L, et al. (2020) Endophytic bacteria associated with halophyte Seidlitzia rosmarinus Ehrenb. ex Boiss. from saline soil of Uzbekistan and their plant beneficial traits. J Arid Land 12: 730-740. https://doi.org/10.1007/s40333-020-0019-4
[7]	Marui A, Nagafuchi T, Shinogi Y, et al. (2012) Soil physical properties to grow the wild licorice at semi-arid area in Mongolia. J Arid Land Studies 22: 33-36.
[8]	Lewis G, Schrire B, Mackinder B, et al. (2005) Legumes of the world. London: Royal Botanic Gardens, Kew Publishing.
[9]	Hayashi H, Hattori S, Inoue K, et al. (2003) Field survey of Glycyrrhiza plants in Central Asia (1). Characterization of G. uralensis, G. glabra and the putative intermediate collected in Kazakhstan. Biol Pharm Bull 26: 867-871. https://doi.org/10.1248/bpb.26.867
[10]	Patil SM, Patil MB, Sapkale GN (2009) Antimicrobial activity of Glycyrrhiza glabra Linn. roots. Int J Chem Sci 7: 585-591.
[11]	Sharma V, Agrawal RC, Pandey S (2014) Phytochemical screening and determination of anti-bacterial and anti-oxidant potential of Glycyrrhiza glabra root extracts. J Envir Res Devel 7: 1552-1558.
[12]	Chao H, Wang W, Hou J (2019) Plant growth and soil microbial impacts of enhancing licorice with inoculating dark septate endophytes under drought stress. Front Microbiol 10: 2277. https://doi.org/10.3389/fmicb.2019.02277
[13]	Li L, Sinkko H, Montonen L, et al. (2012) Biogeography of symbiotic and other endophytic bacteria isolated from medicinal Glycyrrhiza species in China. FEMS Microbiol Ecol 79: 46-68. https://doi.org/10.1111/j.1574-6941.2011.01198.x
[14]	Cao XM, Cai J, Li SB, et al. (2013) Fusarium solani and Fusarium oxysporum associated with root rot of Glycyrrhiza uralensis in China. Plant Dis 97: 1514. https://doi.org/10.1094/PDIS-12-12-1111-PDN
[15]	Parray J, Egamberdieva D, Abd_Allah E, et al. (2023) Editorial: Soil microbiome metabolomics: A way forward to sustainable intensification. Front Sustain Food Syst 7: 1251054. https://doi.org/10.3389/fsufs.2023.1251054
[16]	Abdullaeva Y, Mardonova G, Eshboev F, et al. (2024) Harnessing chickpea bacterial endophytes for improved plant health and fitness. AIMS Microbiol 10: 489-506. https://doi.org/10.3934/microbiol.2024024
[17]	Egamberdieva D, Wirth S, Alqarawi AA, et al. (2017) Phytohormones and beneficial microbes: Essential components for plants to balance stress and fitness. Front Microbiol 8: 2104. https://doi.org/10.3389/fmicb.2017.02104
[18]	Rezaei-Chiyaneh E, Mahdavikia H, Subramanian S, et al. (2021) Co-inoculation of phosphate-solubilizing bacteria and mycorrhizal fungi: Effect on seed yield, physiological variables, and fixed oil and essential oil productivity of ajowan (Carum copticum L.) under water deficit. J Soil Sci Plant Nutr 21: 3159-3179. https://doi.org/10.1007/s42729-021-00596-9
[19]	Pawlik M, Cania B, Thijs S, et al. (2017) Hydrocarbon degradation potential and plant growth-promoting activity of culturable endophytic bacteria of Lotus corniculatus and Oenothera biennis from a long-term polluted site. Environ Sci Pollut Res 24: 19640-19652. https://doi.org/10.1007/s11356-017-9496-1
[20]	Chamkhi I, Sbabou L, Aurag J (2023) Improved growth and quality of saffron (Crocus sativus L.) in the field conditions through inoculation with selected native plant growth-promoting rhizobacteria (PGPR). Ind Crops Prod 197: 116606. https://doi.org/10.1016/j.indcrop.2023.116606
[21]	Egamberdieva D, Shurigin V, Alaylar B, et al. (2020) Bacterial endophytes from horseradish (Armoracia rusticana G. Gaertn., B. Mey. & Scherb.) with antimicrobial efficacy against pathogens. Plant Soil Environ 66: 309-316. https://doi.org/10.17221/137/2020-PSE
[22]	Egamberdieva D, Shurigin V, Alaylar B, et al. (2020) The effect of biochars and endophytic bacteria on growth and root rot disease incidence of Fusarium infested narrow-leafed lupin (Lupinus angustifolius L.). Microorganisms 8: 496. https://doi.org/10.3390/microorganisms8040496
[23]	Egamberdieva D, Wirth S, Behrendt U, et al. (2017) Antimicrobial activity of medicinal plants correlates with the proportion of antagonistic endophytes. Front Microbiol 8: 199. https://doi.org/10.3389/fmicb.2017.00199
[24]	Nejatzadeh-Barandozi F (2013) Antibacterial activities and antioxidant capacity of Aloe vera. Bioorganic Med Chem Lett 3: 1-8. https://doi.org/10.1186/2191-2858-3-5
[25]	Bafana A, Lohiya R (2013) Diversity and metabolic potential of culturable root-associated bacteria from Origanum vulgare in sub-Himalayan region. World J Microbiol Biotechnol 29: 63-74. https://doi.org/10.1007/s11274-012-1158-3
[26]	Phetcharat P, Duangpaeng A (2012) Screening of endophytic bacteria from organic rice tissue for indole acetic acid production. Procedia Eng 32: 177-183. https://doi.org/10.1016/j.proeng.2012.01.1254
[27]	Katoch M, Pull S (2017) Endophytic fungi associated with Monarda citriodora, an aromatic and medicinal plant and their biocontrol potential. Pharm Biol 55: 1528-1535. https://doi.org/10.1080/13880209.2017.1309054
[28]	Farhaoui A, El Alami N, Khadiri M, et al. (2023) Biological control of diseases caused by Rhizoctonia solani AG-2-2 in sugar beet (Beta vulgaris L.) using plant growth-promoting rhizobacteria (PGPR). Physiol Mol Plant Pathology 124: 101966. https://doi.org/10.1016/j.pmpp.2023.101966
[29]	Rustamova N, Wubulikasimu A, Mukhamedov N, et al. (2020) Endophytic bacteria associated with medicinal plant Baccharoides anthelmintica diversity and characterization. Curr Microbiol 77: 1457-1465. https://doi.org/10.1007/s00284-020-01924-5
[30]	Mora-Ruiz MDR, Font-Verdera F, Díaz-Gil C, et al. (2015) Moderate halophilic bacteria colonizing the phylloplane of halophytes of the subfamily Salicornioideae (Amaranthaceae). Syst Appl Microbiol 38: 406-416. https://doi.org/10.1016/j.syapm.2015.05.004
[31]	Dashti AA, Jadaon MM, Abdulsamad AM, et al. (2009) Heat treatment of bacteria: A simple method of DNA extraction for molecular techniques. Kuwait Med J 41: 117-122.
[32]	Lane DJ (1991) 16S/23S rRNA Sequencing. Nucleic Acid Techniques in Bacterial Systematic. New York: John Wiley and Sons 115-175.
[33]	Jinneman KC, Wetherington JH, Adams AM, et al. (1996) Differentiation of Cyclospora sp. and Eimeria spp. by using the polymerase chain reaction amplification products and restriction fragment length polymorphisms. Food and Drug Administration Laboratory Information Bulletin LIB no 4044 .
[34]	Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci USA 101: 11030-11035. https://doi.org/10.1073/pnas.0404206101
[35]	Kumar S, Stecher G, Li M, et al. (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35: 1547-1549. https://doi.org/10.1093/molbev/msy096
[36]	Castric PA (1975) Hydrogen cyanide, a secondary metabolite of Pseudomonas aeruginosa. Can J Microbiol 21: 613-618. https://doi.org/10.1139/m75-088
[37]	Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160: 47-56. https://doi.org/10.1016/0003-2697(87)90612-9
[38]	Brown MRW, Foster JHS (1970) A simple diagnostic milk medium for Pseudomonas aeruginosa. J Clin Pathol 23: 172-177. https://doi.org/10.1136/jcp.23.2.172
[39]	Walsh GA, Murphy RA, Killeen GF, et al. (1995) Technical note: Detection and quantification of supplemental fungal b-glucanase activity in animal feed. J Anim Sci 73: 1074-1076. https://doi.org/10.2527/1995.7341074x
[40]	Malleswari D, Bagyanarayan G (2017) In vitro screening of rhizobacteria isolated from the rhizosphere of medicinal and aromatic plants for multiple plant growth promoting activities. J Microbiol Biotechnol Res 3: 84-91.
[41]	Howe TG, Ward JM (1976) The utilization of tween 80 as carbon source by Pseudomonas. J Gen Microbiol 92: 234-235. https://doi.org/10.1099/00221287-92-1-234
[42]	Bano N, Musarrat J (2003) Characterization of a new Pseudomonas aeruginosa strain NJ-15 as a potential biocontrol agent. Curr Microbiol 46: 324-328. https://doi.org/10.1007/s00284-002-3857-8
[43]	Egamberdieva D, Kucharova Z (2009) Selection for root colonising bacteria stimulating wheat growth in saline soils. Biol Fertil Soils 45: 561-573. https://doi.org/10.1007/s00374-009-0366-y
[44]	Egamberdieva D, Wirth SJ, Shurigin VV, et al. (2017) Endophytic bacteria improve plant growth, symbiotic performance of chickpea (Cicer arietinum L.) and induce suppression of root rot caused by Fusarium solani under salt stress. Front Microbiol 8: 1887. https://doi.org/10.3389/fmicb.2017.01887
[45]	Simons M, van der Bij AJ, Brand I, et al. (1996) Gnotobiotic system for studying rhizosphere colonization by plant growth-promoting Pseudomonas bacteria. Mol Plant Microbe Interact 9: 600-607. https://doi.org/10.1094/mpmi-9-0600
[46]	Makuwa SC, Motadi LR, Choene M, et al. (2023) Bacillus dicomae sp. nov., a new member of the Bacillus cereus group isolated from medicinal plant Dicoma anomala. Int J Syst Evol Microbiol 73: 006112. https://doi.org/10.1099/ijsem.0.006112
[47]	Khan MS, Gao J, Chen X, et al. (2020) Isolation and characterization of plant growth-promoting endophytic bacteria Paenibacillus polymyxa SK1 from Lilium lancifolium. Biomed Res Int 27: 8650957. https://doi.org/10.1155/2020/8650957
[48]	Anandan K, Vittal RR (2019) Endophytic Paenibacillus amylolyticus KMCLE06 extracted dipicolinic acid as antibacterial agent derived via dipicolinic acid synthetase gene. Curr Microbiol 76: 178-186. https://doi.org/10.1007/s00284-018-1605-y
[49]	Shurigin V, Alimov J, Davranov K, et al. (2022) The diversity of bacterial endophytes from Iris pseudacorus L. and their plant beneficial traits. Curr Res Microb Sci 3: 100133. https://doi.org/10.1016/j.crmicr.2022.100133
[50]	Egamberdieva D, Kamilova F, Validov S, et al. (2008) High incidence of plant growth-stimulating bacteria associated with the rhizosphere of wheat grown in salinated soil in Uzbekistan. Environ Microbiol 19: 1-9. https://doi.org/10.1111/j.1462-2920.2007.01424.x
[51]	Lim JA, Lee DH, Heu S (2014) The interaction of human enteric pathogens with plants. Plant Pathol J 30: 109-116. https://doi.org/10.5423/PPJ.RW.04.2014.0036
[52]	Cho ST, Chang HH, Egamberdieva D, et al. (2015) Genome analysis of Pseudomonas fluorescens PCL1751: A rhizobacterium that controls root diseases and alleviates salt stress for its plant host. PLoS ONE 10: e0140231. https://doi.org/10.1371/journal.pone.0140231
[53]	Koberl M, Ramadan EM, Adam M, et al. (2013) Bacillus and Streptomyces were selected as broad-spectrum antagonists against soilborne pathogens from arid areas in Egypt. FEMS Microbiol Lett 342: 168-178. https://doi.org/10.1111/1574-6968.12089
[54]	Egamberdiyeva D, Hoflich G (2004) Effect of plant growth-promoting bacteria on growth and nutrient uptake of cotton and pea in a semi-arid region of Uzbekistan. J Arid Environ 56: 293-301. https://doi.org/10.1016/S0140-1963(03)00050-8
[55]	Medison RG, Tan L, Medison MB, et al. (2022) Use of beneficial bacterial endophytes: A practical strategy to achieve sustainable agriculture. AIMS Microbiol 8: 624-643. https://doi.org/10.3934/microbiol.2022040
[56]	Ali S, Duan J, Charles TC, et al. (2014) A bioinformatics approach to the determination of genes involved in endophytic behavior in Burkholderia spp. J Theor Biol 343: 193-198. https://doi.org/10.1016/j.jtbi.2013.10.007
[57]	Goryluk A, Rekosz-Burlaga H, Blaszczyk M (2009) Isolation and characterization of bacterial endophytes of Chelidonium majus L. Pol J Microbiol 58: 355-361.
[58]	Akinsanya MA, Goh JK, Lim SP, et al. (2015) Metagenomics study of endophytic bacteria in Aloe vera using next-generation technology. Genom Data 6: 159-163. https://doi.org/10.1016/j.gdata.2015.09.004
[59]	Liu Y, Mohamad OAA, Salam N, et al. (2019) Diversity, community distribution and growth promotion activities of endophytes associated with halophyte Lycium ruthenicum Murr. 3 Biotech 9: 144. https://doi.org/10.1007/s13205-019-1678-8
[60]	Rana KL, Kour D, Yadav AH (2019) Endophytic microbiomes: Biodiversity, ecological significance and biotechnological applications. Res J Biotechnol 14: 142-162.
[61]	Michelsen CF, Stougaard P (2012) Hydrogen cyanide synthesis and antifungal activity of the biocontrol strain Pseudomonas fluorescens In5 from Greenland is highly dependent on growth medium. Can J Microbiol 58: 381-390. https://doi.org/10.1139/w2012-004
[62]	Wozniak M, Gałazka A, Tyskiewicz R, et al. (2019) Endophytic bacteria potentially promote plant growth by synthesizing different metabolites and their phenotypic/physiological profiles in the Biolog GEN III MicroPlateTM Test. Int J Mol Sci 20: 1-24. https://doi.org/10.3390/ijms20215283
[63]	Musa Z, Ma J, Egamberdieva D, et al. (2020) Diversity and antimicrobial potential of cultivable endophytic actinobacteria associated with medicinal plant Thymus roseus. Front Microbiol 11: 191. https://doi.org/10.3389/fmicb.2020.00191
[64]	Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169: 30-39. https://doi.org/10.1016/j.micres.2013.09.009
[65]	Yadav A, Yadav K (2019) Plant growth-promoting endophytic bacteria and their potential to improve agricultural crop yields. Microbial Interventions in Agriculture and Environment. Singapore: Springer 143-169. https://doi.org/10.1007/978-981-32-9084-6_7
[66]	Fouda A, Eid AM, Elsaied A, et al. (2021) Plant growth promoting endophytic bacterial community inhabiting the leaves of Pulicaria incisa (Lam.) DC inherent to arid regions. Plants 10: 76. https://doi.org/10.3390/plants10010076
[67]	Shurigin V, Li L, Alaylar B, et al. (2024) Plant beneficial traits of endophytic bacteria associated with fennel (Foeniculum vulgare Mill.). AIMS Microbiol 10: 449-467. https://doi.org/10.3934/microbiol.2024022
[68]	Sudarshna, Sharma N (2024) Endophytic bacteria associated with critically endangered medicinal plant Trillium govanianum (Wall ex. Royle) and their potential in soil nutrition alleviation. Plant Stress 11: 100349. https://doi.org/10.1016/j.stress.2024.100349
[69]	Deepa N, Chauhan Sh, Singh A (2024) Unraveling the functional characteristics of endophytic bacterial diversity for plant growth promotion and enhanced secondary metabolite production in Pelargonium graveolens. Microbiol Res 283: 127673. https://doi.org/10.1016/j.micres.2024.127673

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