Bacteria associated with grapevine (Vitis vinifera L.) rhizosphere and their efficacy in plant growth promotion

Authors

  • Djalolova Bakhora Department of Microbiology and Biotechnology, National University of Uzbekistan, Tashkent 100 174, Uzbekistan https://orcid.org/0009-0001-8346-7540
  • Abdusamatov Sokhibjon Department of Microbiology and Biotechnology, National University of Uzbekistan, Tashkent 100 174, Uzbekistan https://orcid.org/0000-0001-8696-7973
  • Shurigin Vyacheslav State Key Laboratory of Desert and Oasis Ecology, Key Laboratory of Ecological Safety and Sustainable Development in Arid Lands, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi 830 011, China https://orcid.org/0000-0002-5495-0373
  • Jabborova Dilfuza Laboratory of Genetics, Breeding and Selection of Pulses, Oilseeds and Medicinal Plants, Institute of Genetics and Plant Experimental Biology of the Academy of Sciences of the Republic of Uzbekistan, Tashkent 111 215, Uzbekistan https://orcid.org/0000-0003-2327-9545
  • Turaeva Bakhora Laboratory of Microbiology and Biotechnology of Probiotics, Institute of Microbiology of the Academy of Sciences of the Republic of Uzbekistan, Tashkent 100 128, Uzbekistan https://orcid.org/0000-0002-7828-7692
  • Kutlieva Guzal Laboratory of Microbiology and Biotechnology of Probiotics, Institute of Microbiology of the Academy of Sciences of the Republic of Uzbekistan, Tashkent 100 128, Uzbekistan https://orcid.org/0000-0001-6480-1817
  • Davranov Kakhramon Laboratory of Enzymology, Institute of Microbiology of the Academy of Sciences of the Republic of Uzbekistan, Tashkent 100 128, Uzbekistan https://orcid.org/0000-0002-4265-5561

DOI:

https://doi.org/10.14719/pst.3338

Keywords:

Pantoea agglomerans, PGPR, Priestia megaterium, rhizosphere, Vitis vinifera L, grapevine

Abstract

Plant growth, development, and stress resistance depend on the presence of plant growth-promoting rhizobacteria (PGPR) in its rhizosphere. The detection of the highly active PGPR is of high importance due to their possible application as microbial inoculants for plant growth promotion (PGP) in agriculture. In this study, we report on PGPR from the rhizosphere of grapevine (Vitis vinifera L.) growing in Uzbekistan, as it was not studied before. Based on the screening of 37 isolates from grapevine rhizosphere for stimulation of wheat seed germination, just two isolates, BDI-1 and BDI-2 were chosen as the most active. In laboratory conditions, the isolates BDI-1 and BDI-2 increased wheat root length up to 1.48 and 1.5 times and shoot length up to 1.59 and 1.64 times, respectively, as compared to the control. Based on 16S rRNA gene analysis and comparison with the relative strains registered in GenBank of the National Center for Biotechnology Information (NCBI), the isolates BDI-1 and BDI-2 were identified as Pantoea agglomerans and Priestia megaterium, accordingly. Their 16S rRNA gene nucleotide sequences were deposited to GenBank under the accession numbers OP727725 for BDI-1 and OP782582 for BDI-2. Both isolates were phenotypically characterized and demonstrated phosphate-solubilizing and nitrogen-fixing abilities, producing indole-3-acetic acid (IAA) in a high amount; however, BDI-1 also produced siderophores and BDI-2 - 1-aminocyclopropane-1-carboxylate (ACC) - deaminase. Due to these features, the bacteria showed their high activity in the promotion of plant growth and seed germination. In conclusion, according to our results, P. agglomerans BDI-1 and P. megaterium BDI-2 are promising PGPR, which can be applied as microbial inoculants for plant growth improvement.

Downloads

References

FAO. FAOSTAT. Crops and livestock products [Internet]. 2022 [cited 22 May 2024]. Available from: http://www.fao.org/faostat/en/#data/QC.

Di Vecchi-Staraz M, Laucou V, Bruno G, Lacombe T, Gerber S, Bourse T, et al. Low level of pollen-mediated gene flow from cultivated to wild grapevine: consequences for the evolution of the endangered subspecies Vitis vinifera L. subsp. silvestris. J Hered. 2009;100(1):66-75. https://doi.org/10.1093/jhered/esn084

Shurigin V, Alaylar B, Davranov K, Wirth S, Bellingrath-Kimura SD, Egamberdieva D. Diversity and biological activity of culturable endophytic bacteria associated with marigold (Calendula officinalis L.). AIMS Microbiol. 2021;7(3):336-53. https://doi.org/10.3934/microbiol.2021021

Shurigin V, Li L, Alaylar B, Egamberdieva D, Liu Y-H, Li W-J. Plant beneficial traits of endophytic bacteria associated with fennel (Foeniculum vulgare Mill.). AIMS Microbiol. 2024;10(2):449-67. https://doi.org/10.3934/microbiol.2024022

Rijavec T, Lapanje A. Hydrogen cyanide in the rhizosphere: not suppressing plant pathogens, but rather regulating availability of phosphate. Front Microbiol. 2016;7:1785. https://doi.org/10.3389/fmicb.2016.01785

Darriaut R, Lailheugue V, Masneuf-Pomarede I, Marguerit E, Martins G, Compant S, et al. Grapevine rootstock and soil microbiome interactions: Keys for a resilient viticulture. Hortic Res. 2022;9,uhac019. https://doi.org/10.1093/hr/uhac019

Rilling JI, Acuna JJ, Sadowsky MJ, Jorquera MA. Putative nitrogen-fixing bacteria associated with the rhizosphere and root endosphere of wheat plants grown in an andisol from southern Chile. Front Microbiol. 2018;9:2710. https://doi.org/10.3389/fmicb.2018.02710

Baldan E, Nigris S, Romualdi C, D’Alessandro S, Clocchiatti A, Zottini M, et al. Beneficial bacteria isolated from grapevine inner tissues shape Arabidopsis thaliana roots. Plos One. 2015;10(10):e0140252. https://doi.org/10.1371/journal.pone.0140252

Ma H, Shurigin V, Jabborova D, dela Cruz JA, dela Cruz TE, Wirth S, et al. The integrated effect of microbial inoculants and biochar types on soil biological properties and plant growth of lettuce (Lactuca sativa L.). Plants. 2022;11(3):423. https://doi.org/10.3390/plants11030423

Mardanov AV, Chizhevskaya EP, Lazarev AM, Rakitin AL, Beletsky AV, Chebotar VK, Ravin NV. Complete genome sequences of endophytic bacilli isolated from grapevine plants. Microbiol Resour Announc. 2019;8(48):e01265-19. https:// org/10.1128/MRA.01265-19

Shurigin V, Alimov J, Davranov K, Gulyamova T, Egamberdieva D. The diversity of bacterial endophytes from Iris pseudacorus L. and their plant beneficial traits. Curr Res Microb Sci. 2022;3:100133. https://doi.org/10.1016/j.crmicr.2022.100133

Marasco R, Rolli E, Fusi M, Michoud G, Daffonchio D. Grapevine rootstocks shape underground bacterial microbiome and networking but not potential functionality. Microbiome. 2018;6:3. https://doi.org/10.1186/s40168-017-0391-2

Gavande SS, Maurya A, Sharma S. Isolation and characterization of plant growth promoting rhizobacteria (PGPR) from rhizosphere of major crops grown in Marathwada region of Maharashtra, India. Vegetos. 2024;37:637-48. https://doi.org/10.1007/s42535-023-00779-y

Agunbiade VF, Fadiji AE, Agbodjato NA, Babalola OO. Isolation and characterization of plant-growth-promoting, drought-tolerant rhizobacteria for improved maize productivity. Plants. 2024;13(10):1298. https://doi.org/10.3390/plants13101298

Karagoz K, Ates F, Karagoz H, Kotan R, Cakmakci R. Characterization of plant growth-promoting traits of bacteria isolated from the rhizosphere of grapewine grown in alkaline and acidic soils. Eur J Soil Biol. 2012;50:144-50. https://doi.org/10.1016/j.ejsobi.2012.01.007

Labouyrie M, Ballabio C, Romero F, et al. Patterns in soil microbial diversity across Europe. Nat Commun. 2023;14:3311.

https://doi.org/10.1038/s41467-023-37937-4

Fouda A, Eid AM, Elsaied A, El-Belely EF, Barghoth MG, Azab E, et al. Plant growth promoting endophytic bacterial community inhabiting the leaves of Pulicaria incisa (Lam.) DC inherent to arid regions. Plants. 2021;10:76. https://doi.org/10.3390/plants10010076

Zucol F, Ammann RA, Berger C, Aebi C, Altwegg M, Niggli FK, Nadal D. Real-time quantitative broad-range PCR assay for detection of the 16S rRNA gene followed by sequencing for species identification. J Clin Microbiol. 2006;44(8):2750-59. https://doi.org/10.1128/JCM.00112-06

Saitou N, Nei M. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4(4):406-25. https://doi.org/10.1093/oxfordjournals.molbev.a040454

Felsenstein J. Confidence limits on phylogenies: An approach using the bootstrap. Evolution. 1985;39(4):783-91. https://doi.org/10.2307/2408678

Tamura K, Nei M, Kumar S. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci USA. 2004;101(30):11030-35. https://doi.org/10.1073/pnas.0404206101

Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35(6):1547-49. https://doi.org/10.1093/molbev/msy096

Bashan Y, Holguin G, Lifshitz R. Isolation and characterization of plant growth-promoting rhizobacteria. In: Glick BR, Thompson JE, editors. Methods in Plant Molecular Biology and Biotechnology. USA, FL, Boca Raton: CRC Press; 1993. p. 331-45.

Sarwar M, Kremer RJ. Determination of bacterially derived auxins using a microplate method. Lett Appl Microbiol. 1995;20:282-85. https://doi.org/10.1111/j.1472-765X.1995.tb00446.x

Kuklinsky-Sobral J, Araújo WL, Mendes R, Geraldi IO, Pizzirani-Kleiner AA, Azevedo JL. Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ Microbiol. 2004;6:1244-51. https://doi.org/10.1111/j.1462-2920.2004.00658.x.

Mehta S, Nautiyal CS. An efficient method for qualitative screening of phosphate-solubilizing bacteria. Curr Microbiol. 2001;43:51-56. https://doi.org/10.1007/s002840010259

Egamberdieva D, Kucharova Z, Davranov K, Berg G, Makarova N, Azarova T, et al. Bacteria able to control foot and root rot and to promote growth of cucumber in salinated soils. Biol Fertil Soils. 2011;47:197-205. https://doi.org/10.1007/s00374-010-0523-3

Schwyn B, Neilands JB. Universal chemical assay for the detection and determination of siderophores. Anal Biochem. 1987;160:45-46. https://doi.org/10.1016/0003-2697(87)90612-9.

Logan NA, De Vos P. Genus I. Bacillus Cohn 1872, 174AL. In: De Vos P, Garrity GM, Jones D, Krieg NR, Ludwig W, Rainey FA, Schleifer KH, Whitman WB, editors. Bergey’s Manual of Systematic Bacteriology, 2nd Edition. New York: Springer; 2009. 3. p. 21-128.

Egamberdieva D, Shurigin V, Gopalakrishnan S, Ram S. Microbial strategies for the improvement of legume production in hostile environments. In: Azooz MM, Ahmad P, editors. Legumes Under Environmental Stress: Yield, Improvement and Adaptations. UK: John Wiley and Sons Ltd; 2015. p. 133-44. https://doi.org/10.1002/9781118917091.ch9

Aasfar A, Meftah Kadmiri I, Azaroual SE, Lemriss S, Mernissi NE, Bargaz A, et al. Agronomic advantage of bacterial biological nitrogen fixation on wheat plant growth under contrasting nitrogen and phosphorus regimes. Front Plant Sci. 2024;15:1388775. https://doi.org/10.3389/fpls.2024.1388775

Shurigin V, Alikulov B, Davranov K, Ismailov Z. Bacterial endophytes from halophyte black saxaul (Haloxylon aphyllum Minkw.) and their plant growth-promoting properties. J Appl Biol Biotech. 2022;10(1):45-53. https://doi.org/10.7324/JABB.2021.100106

Kondracka A, Rychter AM. The role of Pi recycling processes during photosynthesis in phosphate-deficient bean plants. J Exp Bot. 1997;48:1461-68. https://doi.org/10.1093/jxb/48.7.1461

Ma Z, Bielenberg DG, Brown KM, Lynch JP. Regulation of root hair density by phosphorus availability in Arabidopsis thaliana. Plant Cell Environ. 2001;24:459-67. https://doi.org/10.1111/pce.12059

Vance CP, Uhde-Stone C, Allan DL. Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol. 2003;157(3):423-47. https://doi.org/10.1046/j.1469-8137.2003.00695.x

Egamberdieva D, Ma H, Shurigin V, Alimov J, Wirth S, Bellingrath-Kimura SD. Biochar additions alter the abundance of p-cycling-related bacteria in the rhizosphere soil of Portulaca oleracea L. under salt stress. Soil Syst. 2022;6:64. https://doi.org/10.3390/soilsystems6030064

Chandra S, Askari K, Kumari M. Optimization of indole acetic acid production by isolated bacteria from Stevia rebaudiana rhizosphere and its effects on plant growth. J Genet Eng Biotechnol. 2018;16(2):581-86. https://doi.org/10.1016/j.jgeb.2018.09.001

Fierro-Coronado RA, Quiroz-Figueroa FR, Garcia-Perez LM, Ramirez-Chavez E, Molina-Torres J, Maldonado-Mendoza IE. IAA-producing rhizobacteria from chickpea (Cicer arietinum L.) induce changes in root architecture and increase root biomass. Can J Microbiol. 2014;60(10):639-48. https://doi.org/10.1139/cjm-2014-0399

Jaiswal A, Das K, Koli DK, Pabbi S. Characterization of cyanobacteria for IAA and siderophore production and their effect on rice seed germination. Int J Curr Microbiol App Sci. 2018;5:212-22.

Ramos Solano B, Maicas JB, Pereyra De La Iglesia MT, Domenech J, Gutierrez Manero FJ. Systemic disease protection elicited by plant growth promoting rhizobacteria strains: relationship between metabolic responses, systemic disease protection and biotic elicitors. Am Phytopath Soc. 2008;98(4):451-57. https://doi.org/10.1094/PHYTO-98-4-0451

Gu S, Wei Z, Shao Z, Friman VP, Cao K, Yang T, et al. Competition for iron drives phytopathogen control by natural rhizosphere microbiomes. Nat Microbiol. 2020;5:1002-10. https://doi.org/10.1038/s41564-020-0719-8

Khan A, Singh P, Srivastava A. Synthesis, nature and utility of universal iron chelator - Siderophore: a review. Microbiol Res. 2018;212-213:103-11. https://doi.org/10.1016/j.micres.2017.10.012

Kramer J, Ozkaya O, Kummerli R. Bacterial siderophores in community and host interactions. Nat Rev Microbiol. 2020;18:152-63. https://doi.org/10.1038/s41579-019-0284-4

Pan YJ, Liu L, Lin YC, Zu YG, Li LP, Tang ZH. Ethylene antagonizes salt-induced growth retardation and cell death process via transcriptional controlling of ethylene-, BAG- and senescence-associated genes in Arabidopsis. Front Plant Sci. 2016;7:696. https://doi.org/10.3389/fpls.2016.00696

Subhan D, Muhammad Z, Fauzia M, Mubshar H. ACC-deaminase producing plant growth promoting rhizobacteria and biochar mitigate adverse effects of drought stress on maize growth. Plos One. 2020;16:e0250286. https://doi.org/10.1371/journal.pone.0250286

Singh RP, Shelke GM, Kumar A, Jha PN. Biochemistry and genetics of ACC deaminase: a weapon to “stress ethylene” produced in plants. Front Microbiol. 2015;6:937. https://doi.org/10.3389/fmicb.2015.00937

Tiwari G, Duraivadivel P, Sharma S, Hariprasad P. 1-Aminocyclopropane-1-carboxylic acid deaminase producing beneficial rhizobacteria ameliorate the biomass characters of Panicum maximum Jacq. by mitigating drought and salt stress. Sci Rep. 2018;8:17513. https://doi.org/10.1038/s41598-018-35565-3

Published

29-12-2024 — Updated on 29-12-2024

Versions

How to Cite

1.
Bakhora D, Sokhibjon A, Vyacheslav S, Dilfuza J, Bakhora T, Guzal K, Kakhramon D. Bacteria associated with grapevine (Vitis vinifera L.) rhizosphere and their efficacy in plant growth promotion. Plant Sci. Today [Internet]. 2024 Dec. 29 [cited 2025 Apr. 11];11(4). Available from: https://horizonepublishing.com/journals/index.php/PST/article/view/3338

Issue

Section

Research Articles