The combination of multiple plant growth promotion and hydrolytic enzyme producing rhizobacteria and their effect on Jerusalem artichoke growth improvement

Natthawat Sritongon; Sophon Boonlue; Wiyada Mongkolthanaruk; Sanun Jogloy; Nuntavun Riddech

doi:10.1038/s41598-023-33099-x

journal article Open Access Apr 11, 2023

The combination of multiple plant growth promotion and hydrolytic enzyme producing rhizobacteria and their effect on Jerusalem artichoke growth improvement

Natthawat Sritongon Sophon Boonlue Wiyada Mongkolthanaruk

Sanun Jogloy Nuntavun Riddech

Scientific Reports Vol. 13 No. 1 · Springer Science and Business Media LLC

View at Publisher Save 10.1038/s41598-023-33099-x

Abstract

AbstractRhizobacteria are well recognized for their beneficial multifunctions as key promoters of plant development, suppressing pathogens, and improving soil health. In this study, experiments focused on characterizing the plant growth promotion (PGP) and extracellular hydrolase production traits of rhizobacteria, and their impact on Jerusalem artichoke growth. A total of 50 isolates proved capable of either direct PGP or hydrolase-producing traits. Two promising strains (Enterobactercloacae S81 and Pseudomonasazotoformans C2-114) showed potential on phosphate and potassium solubilization, IAA production, and 1-aminocyclopropane-1-carboxylic acid deaminase activity and hydrolase production. A hydrolase-producing strain (Bacillussubtilis S42) was able to generate cellulase, protease, amylase, β-glucosidase, and phosphatase. These three selected strains also gave positive results for indirect PGP traits such as siderophore, ammonia, oxalate oxidase, polyamine, exopolysaccharide, biofilm, motility, and tolerance to salinity and drought stress. Colonization was observed using a scanning electron microscope and rhizobacteria appeared at the root surface. Interestingly, inoculation with consortia strains (S42, S81, and C2-114) significantly increased all plant parameters, including height, biomass, root (length, surface, diameter, and volume), and tuber fresh weight. Therefore, we recommend that potential consortia of PGP and hydrolase-producing rhizobacteria be employed as a biofertilizer to improve soil and boost crop productivity.

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References

59

[1]

Nacoon, S. et al. Interaction between phosphate solubilizing bacteria and arbuscular mycorrhizal fungi on growth promotion and tuber inulin content of Helianthus tuberosus L. Sci. Rep. 10, 4916 (2020). 10.1038/s41598-020-61846-x

[2]

Khaekhum, S. et al. The first member of Exserohilum rostratum beneficial for promoting growth and yield of sunchoke (Helianthus tuberosus L.). Rhizosphere 19, 100379 (2021). 10.1016/j.rhisph.2021.100379

[3]

Khamwan, S., Boonlue, S., Riddech, N., Jogloy, S. & Mongkolthanaruk, W. Characterization of endophytic bacteria and their response to plant growth promotion in Helianthus tuberosus L. Biocatal. Agric. Biotechnol. 13, 153–159 (2018). 10.1016/j.bcab.2017.12.007

[4]

Ruttanaprasert, R. et al. Genotypic variability for tuber yield, biomass, and drought tolerance in Jerusalem artichoke germplasm. Turk. J. Agric. For. 38, 570–580 (2014). 10.3906/tar-1310-43

[5]

Puangbut, D., Jogloy, S., Vorasoot, N. & Patanothai, A. Response of growth, physiological traits and tuber yield in Helianthus tuberosus to seasonal variations under tropical area. Sci. Hortic. 195, 108–115 (2015). 10.1016/j.scienta.2015.09.008

[6]

Puangbut, D., Jogloy, S., Vorasoot, N. & Songsri, P. Photosynthetic and physiological response to drought of Jerusalem artichoke genotypes differing in drought resistance. Agric. Water Manag. 259, 107252 (2022). 10.1016/j.agwat.2021.107252

[7]

Nacoon, S. et al. Combination of arbuscular mycorrhizal fungi and phosphate solubilizing bacteria on growth and production of Helianthus tuberosus under field condition. Sci. Rep. 11, 6501 (2021). 10.1038/s41598-021-86042-3

[8]

Potential Use of Beneficial Microorganisms for Soil Amelioration, Phytopathogen Biocontrol, and Sustainable Crop Production in Smallholder Agroecosystems

Gilbert Koskey, Simon Wambui Mburu, Richard Awino et al.

Frontiers in Sustainable Food Systems 2021 10.3389/fsufs.2021.606308

[9]

Plant growth-promoting rhizobacteria and root system functioning

Jordan Vacheron, Guilhem Desbrosses, Marie-Lara Bouffaud et al.

Frontiers in Plant Science 2013 10.3389/fpls.2013.00356

[10]

Chandwani, S. & Ameresan, N. Role of ACC deaminase producing bacteria for abiotic stress management and sustainable agriculture production. Environ. Sci. Pollut. Res. 29, 22843–22859 (2022). 10.1007/s11356-022-18745-7

[11]

Fan, D. & Smith, D. L. Characterization of selected plant growth-promoting rhizobacteria and their non-host growth promotion effects. Microbiol. Spectr. 9, 1–20 (2021). 10.1128/spectrum.00279-21

[12]

Kavamura, V. N. et al. Screening of Brazilian cacti rhizobacteria for plant growth promotion under drought. Microbiol. Res. 168, 183–191 (2013). 10.1016/j.micres.2012.12.002

[13]

Passari, A. K., Mishra, V. K., Saikia, R., Gupta, V. K. & Singh, B. P. Isolation, abundance and phylogenetic affiliation of endophytic actinomycetes associated with medicinal plants and screening for their in vitro antimicrobial biosynthetic potential. Front. Microbiol. 6, 273 (2015). 10.3389/fmicb.2015.00273

[14]

Hazarika, S. N., Saikia, K., Borah, A. & Thakur, D. Prospecting endophytic bacteria endowed with plant growth promoting potential isolated from Camellia sinensis. Front. Microbiol. 12, 738058 (2021). 10.3389/fmicb.2021.738058

[15]

Makoi, J. H. J. R. & Ndakidemi, P. Selected soil enzymes: Example of their potential roles in the ecosystem. Afr. J. Biotechnol. 7, 181–191 (2008).

[16]

Namwongsa, J. et al. Endophytic bacteria improve root traits, biomass and yield of Helianthus tuberosus L. under normal and deficit water conditions. J. Microbiol. Biotechnol. 29, 1777–1789 (2019). 10.4014/jmb.1903.03062

[17]

Suebrasri, T. et al. Novel endophytic fungi with fungicidal metabolites suppress sclerotium disease. Rhizosphere 16, 100250 (2020). 10.1016/j.rhisph.2020.100250

[18]

Miao, Y. et al. Long-term compost amendment spurs cellulose decomposition by driving shifts in fungal community composition and promoting fungal diversity and phylogenetic relatedness. MBio 13, 1–12 (2022). 10.3391/mbi.2022.13.1.01

[19]

El-Deeb, B., Bazaid, S., Gherbawy, Y. & Elhariry, H. Characterization of endophytic bacteria associated with rose plant (Rosa damascene trigintipeta) during flowering stage and their plant growth promoting traits. J. Plant Interact. 7, 248–253 (2012). 10.1080/17429145.2011.637161

[20]

Magotra, S. et al. Field evaluation of PGP Bacillus sp. strain D5 native to Crocus sativus, in traditional and non-traditional areas, and mining of PGP genes. Sci. Rep. 11, 1–16 (2021). 10.1038/s41598-021-84585-z

[21]

Dinesh, R. et al. Isolation, characterization, and evaluation of multi-trait plant growth promoting rhizobacteria for their growth promoting and disease suppressing effects on ginger. Microbiol. Res. 173, 34–43 (2015). 10.1016/j.micres.2015.01.014

[22]

Contribution of Zinc Solubilizing Bacteria in Growth Promotion and Zinc Content of Wheat

Sana Kamran, Izzah Shahid, Deeba N. Baig et al.

Frontiers in Microbiology 2017 10.3389/fmicb.2017.02593

[23]

Mumtaz, M. Z., Ahmad, M., Jamil, M. & Hussain, T. Zinc solubilizing Bacillus spp. potential candidates for biofortification in maize. Microbiol. Res. 202, 51–60 (2017). 10.1016/j.micres.2017.06.001

[24]

Goswami, M. & Deka, S. Isolation of a novel rhizobacteria having multiple plant growth promoting traits and antifungal activity against certain phytopathogens. Microbiol. Res. 240, 1–17 (2020). 10.1016/j.micres.2020.126516

[25]

Boubekri, K. et al. The screening of potassium and phosphate solubilizing actinobacteria and the assessment of their ability to promote wheat growth parameters. Microorganisms 9, 1–16 (2021). 10.3390/microorganisms9030470

[26]

Ribeiro, C. M. & Cardoso, E. J. B. N. Isolation, selection and characterization of root-associated growth promoting bacteria in Brazil Pine (Araucaria angustifolia). Microbiol. Res. 167, 69–78 (2012). 10.1016/j.micres.2011.03.003

[27]

Gupta, S. & Pandey, S. ACC deaminase producing bacteria with multifarious plant growth promoting traits alleviates salinity stress in French Bean (Phaseolus vulgaris) plants. Front. Microbiol 10, 1506 (2019). 10.3389/fmicb.2019.01506

[28]

Bist, V. et al. Silicon-solubilizing media and its implication for characterization of bacteria to mitigate biotic stress. Front. Microbiol. 11, 28 (2020). 10.3389/fmicb.2020.00028

[29]

Sritongon, K. et al. Rhizobacterial candidates isolated from Jerusalem artichoke (Helianthus tuberosus L.) rhizosphere for host plant growth promotion. Chiang Mai J. Sci. 44, 83–93 (2017).

[30]

Rangjaroen, C., Rerkasem, B., Teaumroong, N., Noisangiam, R. & Lumyong, S. Promoting plant growth in a commercial rice cultivar by endophytic diazotrophic bacteria isolated from rice landraces. Ann. Microbiol. 65, 253–266 (2015). 10.1007/s13213-014-0857-4

[31]

Glick, B. R. Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol. Res. 169, 30–39 (2014). 10.1016/j.micres.2013.09.009

[32]

Penrose, D. M. & Glick, B. R. Methods for isolating characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol. Plant 118, 10–15 (2003). 10.1034/j.1399-3054.2003.00086.x

[33]

Zarei, T., Moradi, A., Kazemeini, S. A., Akhgar, A. & Rahi, A. A. The role of ACC deaminase producing bacteria in improving sweet corn (Zea mays L. var saccharata) productivity under limited availability of irrigation water. Sci. Rep. 10, 20361 (2020). 10.1038/s41598-020-77305-6

[34]

Indole acetic acid and ACC deaminase from endophytic bacteria improves the growth of Solanum lycopersicum

Abdul Latif Khan, Boshra Ahmed Halo, Ali Elyassi et al.

Electronic Journal of Biotechnology 2016 10.1016/j.ejbt.2016.02.001

[35]

Ali, S. Z., Sandhya, V. & Rao, L. V. Isolation and characterization of drought-tolerant ACC deaminase and exopolysaccharide-producing fluorescent Pseudomonas sp. Ann. Microbiol. 64, 493–502 (2014). 10.1007/s13213-013-0680-3

[36]

Kumar, P., Dubey, R. C. & Maheshwari, D. K. Bacillus strains isolated from rhizosphere showed plant growth promoting and antagonistic activity against phytopathogens. Microbiol. Res. 167, 493–499 (2012). 10.1016/j.micres.2012.05.002

[37]

Gu, S. et al. Competition for iron drives phytopathogen control by natural rhizosphere microbiomes. Nat. Microbiol. 5, 1002–1010 (2020). 10.1038/s41564-020-0719-8

[38]

Gill, S. S. & Tuteja, N. Polyamines and abiotic stress tolerance in plants. Plant Signal. Behav. 5, 26–33 (2010). 10.4161/psb.5.1.10291

[39]

Ansari, F. A. & Ahmad, I. Biofilm development, plant growth promoting traits and rhizosphere colonization by Pseudomonas entomophila FAP1: A promising PGPR. Adv. Appl. Microbiol. 8, 235–251 (2018). 10.4236/aim.2018.83016

[40]

Dias, A. C. F. et al. Isolation of micropropagated strawberry endophytic bacteria and assessment of their potential for plant growth promotion. World J. Microbiol. Biotechnol. 25, 189–195 (2009). 10.1007/s11274-008-9878-0

[41]

Santiago, C. D. et al. Bacterial compatibility in combined inoculation enhances the growth of potato seedlings. Microbes Environ. 32, 14–23 (2017). 10.1264/jsme2.me16127

[42]

Nayana, A. R., Joseph, B. J., Jose, A. & Radhakrishnan, E. K. Nanotechnological advances with PGPR applications. In Sustainable Agriculture Reviews 41 (eds Hayat, S. et al.) 163–180 (Springer, 2020). 10.1007/978-3-030-33996-8_9

[43]

Bunt, J. S. & Rovira, A. D. Microbiological studies of some subantarctic soils. J. Soil Sci. 6, 199–288 (1955). 10.1111/j.1365-2389.1955.tb00836.x

[44]

Atlas, R. M. Handbook of Microbiological Media (CRC Press, 2004). 10.1201/9781420039726

[45]

Nautiyal, C. S. An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol. Lett. 170, 265–270 (1999). 10.1111/j.1574-6968.1999.tb13383.x

[46]

Hu, X. F., Chen, J. S. & Guo, J. F. Two phosphate and potassium solubilizing bacteria isolated from Tianmu mountain, Zhejiang, China. World J. Microbiol. Biotechnol. 22, 983–990 (2006). 10.1007/s11274-006-9144-2

[47]

COLORIMETRIC ESTIMATION OF INDOLEACETIC ACID

Solon A. Gordon, Robert P. Weber

Plant Physiology 1951 10.1104/pp.26.1.192

[48]

Dworkin, M. & Foster, J. Experiments with some microorganisms which utilize ethane and hydrogen. J. Bacteriol. 75, 592–601 (1958). 10.1128/jb.75.5.592-603.1958

[49]

Barton, C. J. Photometric analyses of phosphate rock. Anal. Chem. 20, 1068–1073 (1948). 10.1021/ac60023a024

[50]

A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding

Marion M. Bradford

Analytical Biochemistry 1976 10.1016/0003-2697(76)90527-3

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Published: Apr 11, 2023
Vol/Issue: 13(1)
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Authors

Department of Microbiology, Faculty of Science, Khon Kaen University, Khon Kaen, Thailand

W

Wiyada Mongkolthanaruk

Funding

the research fund for supporting lecturers to admit a student with high potential to study and do research on his expert program in 2017, graduate school, Khon Kaen University, Thailand Award: 602JT212

Cite This Article

Natthawat Sritongon, Sophon Boonlue, Wiyada Mongkolthanaruk, et al. (2023). The combination of multiple plant growth promotion and hydrolytic enzyme producing rhizobacteria and their effect on Jerusalem artichoke growth improvement. Scientific Reports, 13(1). https://doi.org/10.1038/s41598-023-33099-x

The combination of multiple plant growth promotion and hydrolytic enzyme producing rhizobacteria and their effect on Jerusalem artichoke growth improvement

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