Abstract
Background and aims
Plant growth-promoting rhizobacteria (PGPR) can function as biofertilizers to enhance plant growth and crop yield in an environmentally sustainable manner. However, when PGPR are introduced into agricultural soils, their survival is restricted due to limited nutrients available in the rhizosphere. It has been demonstrated that selected Bacillus velezensis (Bv) strains can use pectin-rich orange peel (OP) as a growth substrate, but results have been scarce due to lack of strain screening. Therefore, it is important to select Bv strains for their capability to utilize OP and to test their ability to promote soybean growth with OP as an amendment.
Methods
Six Bv strains were selected by their growth in OP media and then tested for their ability to promote soybean growth in combination with OP in greenhouse and field experiments.
Results
Among six Bv strains tested in a greenhouse experiment, strains AP191, AP215, and AP216 showed the best results in plant growth promotion when supplemented with OP, where only AP191 with OP significantly enhanced pod dry weight by 15.9%. Inoculation with AP191 + OP showed the greatest yield under field conditions, being the only treatment significantly different from the control treatment (+ 0.5 ton ha−1, 9.4% yield increase).
Conclusions
These results support the conclusion that soybean seed treatment with PGPR strains in conjunction with orange peel can produce a yield advantage under field conditions. This research opens the opportunity for more consistent yield increases when using biologics as a seed treatment for the biofertilizer industry.
Similar content being viewed by others
Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
Abbreviations
- Brad:
-
Bradyrhizobium japonicum
- Bv:
-
Bacillus velezensis
- CFU:
-
Colony forming unit
- EVS:
-
E.V. Smith Research Center
- M9OP:
-
M9 medium containing 0.5% orange peel
- Ndfa:
-
Nitrogen derived from the air
- OD600 :
-
Optical density of a sample measured at a wavelength of 600 nm
- OP:
-
Orange peel
- PGPR:
-
Plant growth-promotion rhizobacteria
References
Addo S, Carrias AA, Williams MA et al (2017) Effects of Bacillus subtilis strains and the prebiotic Previda ® on growth, immune parameters and susceptibility to Aeromonas hydrophila infection in Nile tilapia, Oreochromis niloticus. Aquac Res 48:4798–4810. https://doi.org/10.1111/are.13300
Arif MS, Riaz M, Shahzad SM et al (2017) Phosphorus-mobilizing rhizobacterial strain bacillus cereus gs6 improves symbiotic efficiency of soybean on an aridisol amended with phosphorus-enriched compost. Pedosphere 27:1049–1061. https://doi.org/10.1016/S1002-0160(17)60366-7
Barea JM, Brown ME (1974) Effects on plant growth produced by Azotobacter paspali related to synthesis of plant growth regulating substances. J Appl Bacteriol 37:583–593. https://doi.org/10.1111/j.1365-2672.1974.tb00483.x
Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350. https://doi.org/10.1007/s11274-011-0979-9
Buensanteai N, Yuen GY, Prathuangwong S (2008) The biocontrol bacterium Bacillus amyloliquefaciens KPS46 produces auxin, surfactin and extracellular proteins for enhanced growth of soybean plant. Thai J Agric Sci 41(3–4):101–116
Calvo P, Nelson L, Kloepper JW (2014) Agricultural uses of plant biostimulants. Plant Soil 383:3–41. https://doi.org/10.1007/s11104-014-2131-8
Cassán F, Perrig D, Sgroy V et al (2009) Azospirillum brasilense Az39 and Bradyrhizobium japonicum E109, inoculated singly or in combination, promote seed germination and early seedling growth in corn (Zea mays L.) and soybean (Glycine max L.). Eur J Soil Biol 45:28–35. https://doi.org/10.1016/j.ejsobi.2008.08.005
de Lorenzo G, Castoria R, Bellincampi D, Cervone F (1997) Fungal invasion enzymes and their inhibition. In: Plant relationships. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 61–83. https://doi.org/10.1007/978-3-662-10370-8_5
di Cello F, Bevivino A, Chiarini L et al (1997) Biodiversity of a Burkholderia cepacia population isolated from the maize rhizosphere at different plant growth stages. Appl Environ Microbiol 63:4485–4493. https://doi.org/10.1128/aem.63.11.4485-4493.1997
Farquhar GD, Ehleringer JR, Hubic KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537. https://doi.org/10.1146/annurev.pp.40.060189.002443
Fehr WR, Caviness CE, Burmood DT, Pennington JS (1971) Stage of development descriptions for soybeans, Glycine Max (L.) Merrill 1. Crop Sci 11:929–931. https://doi.org/10.2135/cropsci1971.0011183X001100060051x
Gopalakrishnan S, Sathya A, Vijayabharathi R et al (2015) Plant growth promoting rhizobia: challenges and opportunities. 3 Biotech 5:355–377. https://doi.org/10.1007/s13205-014-0241-x
Goswami D, Thakker JN, Dhandhukia PC (2016) Portraying mechanics of plant growth promoting rhizobacteria (PGPR): A review. Cogent Food Agric 2:. https://doi.org/10.1080/23311932.2015.1127500
Govindasamy V, Senthilkumar M, Magheshwaran V et al (2010) Bacillus and Paenibacillus spp.: potential PGPR for sustainable agriculture. In: Plant growth and health promoting bacteria. Microbiology monographs, vol 18. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-13612-2_15
Gray EJ, Smith DL (2005) Intracellular and extracellular PGPR: commonalities and distinctions in the plant–bacterium signaling processes. Soil Biol Biochem 37:395–412. https://doi.org/10.1016/j.soilbio.2004.08.030
Grover M, Bodhankar S, Sharma A et al (2021) PGPR mediated alterations in root traits: way toward sustainable crop production. Front Sustain Food Syst 4:. https://doi.org/10.3389/fsufs.2020.618230
Hartmann A, Rothballer M, Schmid M (2008) Lorenz Hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research. Plant Soil 312:7–14. https://doi.org/10.1007/s11104-007-9514-z
Hassan MK (2016) The role of pectin utilization in root colonization and plant growth-promotion by Bacillus amyloliquefaciens subsp. plantarum (Bap). Master Thesis, Auburn University, Alabama USA
Hassan MK, McInroy JA, Jones J et al (2019) Pectin-rich amendment enhances soybean growth promotion and nodulation mediated by bacillus Velezensis strains. Plants 8:120. https://doi.org/10.3390/plants8050120
Hiltner L (1904) Über neuere Erfahrungen und Probleme auf dem Gebiete der Bodenbakteriologie und unter Berücksichtigung der Gründüngung und Brache. Deutsche Landwirtschafts-Gesellschaft, Berlin, Arbeiten Der DLG 98:59–78
Hossain MJ, Ran C, Liu K et al (2015) Deciphering the conserved genetic loci implicated in plant disease control through comparative genomics of Bacillus amyloliquefaciens subsp. plantarum. Front Plant Sci 6:. https://doi.org/10.3389/fpls.2015.00631
Hungria M, Mendes IC (2015) Nitrogen fixation with soybean: the perfect symbiosis? In: Biological nitrogen fixation. John Wiley & Sons, Inc, Hoboken, pp 1009–1024. https://doi.org/10.1002/9781119053095.ch99
Kang UG, Somasegaran P, Hoben HJ, Bohlool BB (1991) Symbiotic potential, competitiveness, and serological properties of Bradyrhizobium japonicum indigenous to Korean soils. Appl Environ Microbiol 57:1038–1045. https://doi.org/10.1128/aem.57.4.1038-1045.1991
Kloepper JW (1994) Plant growth-promoting rhizobacteria (other systems). Azospirillum/Plant Assoc 187:137–166
Kloepper JW, Gutiérrez-Estrada A, McInroy JA (2007) Photoperiod regulates elicitation of growth promotion but not induced resistance by plant growth-promoting rhizobacteria. Can J Microbiol 53:159–167. https://doi.org/10.1139/w06-114
Kumar R, Chandra R (2008) Influence of PGPR and PSB on Rhizobium leguminosarum bv. viciae strain competition and symbiotic performance in lentil. World J Agric Sci 4:297–301
Kumar A, Prakash A, Johri BN (2011) Bacillus as PGPR in crop ecosystem. In: Maheshwari D (ed) Bacteria in agrobiology: crop ecosystems. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-18357-7_259
Lionetti V, Cervone F, Bellincampi D (2012) Methyl esterification of pectin plays a role during plant–pathogen interactions and affects plant resistance to diseases. J Plant Physiol 169:1623–1630. https://doi.org/10.1016/j.jplph.2012.05.006
Liu K, Newman M, McInroy JA et al (2017) Selection and assessment of plant growth-promoting rhizobacteria for biological control of multiple plant diseases. Phytopathology 107:928–936. https://doi.org/10.1094/PHYTO-02-17-0051-R
Mageshwaran V, Inmann F, Holmes LD (2014) Growth kinetics of Bacillus subtilis in lignocellulosic carbon sources. Int J Microbiol Res 6:570–574
McNear DH Jr (2013) The rhizosphere-roots, soil and everything in between. Nat Educ Knowl 4:1
Mekjian KR, Bryan EM, Beall BW, Moran CP (1999) Regulation of hexuronate utilization in Bacillus subtilis. J Bacteriol 181:426–433. https://doi.org/10.1128/JB.181.2.426-433.1999
Mohammadi K, Sohrabi Y, Heidari G et al (2012) Effective factors on biological nitrogen fixation. Afr J Agric Res 7:1782–1788. https://doi.org/10.5897/AJARX11.034
Morrissey JP, Dow JM, Mark GL, O’Gara F (2004) Are microbes at the root of a solution to world food production? EMBO Rep 5:922–926. https://doi.org/10.1038/sj.embor.7400263
Murphey Coy R, Held DW, Kloepper JW (2017) Bacterial inoculant treatment of Bermudagrass alters ovipositional behavior, larval and pupal weights of the fall armyworm (Lepidoptera: Noctuidae). Environ Entomol 46:831–838. https://doi.org/10.1093/ee/nvx102
Pacheco da Silva ML, Moen FS, Liles MR et al (2022) The response to inoculation with PGPR plus orange peel amendment on soybean is cultivar and environment dependent. Plants 11:1138. https://doi.org/10.3390/plants11091138
Ran C, Carrias A, Williams MA et al (2012) Identification of Bacillus strains for biological control of catfish pathogens. PLoS One 7:e45793. https://doi.org/10.1371/journal.pone.0045793
Riedell WE, Catangui MA, Beckendorf EA (2009) Nitrogen fixation, Ureide, and nitrate accumulation responses to soybean aphid injury in Glycine max. J Plant Nutr 32:1674–1686. https://doi.org/10.1080/01904160903150925
Saeki Y, Akagi I, Takaki H, Nagatomo Y (2000) Diversity of indigenous Bradyrhizobium strains isolated from three different Rj -soybean cultivars in terms of randomly amplified polymorphic DNA and intrinsic antibiotic resistance. Soil Sci Plant Nutr 46:917–926. https://doi.org/10.1080/00380768.2000.10409157
Sanz-sáez Á, Heath KD, Burke PV, Ainsworth EA (2015) Inoculation with an enhanced N 2 -fixing B radyrhizobium japonicum strain (USDA110) does not alter soybean ( G lycine max Merr.) response to elevated [CO 2 ]. Plant Cell Environ 38:2589–2602. https://doi.org/10.1111/pce.12577
Seethepalli A, Guo H, Liu X et al (2020) RhizoVision crown: an integrated hardware and software platform for root crown phenotyping. Plant Phenomics 2020:1–15. https://doi.org/10.34133/2020/3074916
Shahab S, Ahmed N, Khan NS (2009) Indole acetic acid production and enhanced plant growth promotion by indigenous PSBs. Afr J Agric Res 4:1312–1316
Shantharaj D, Williams MA, Potnis NS, Liles MR (2021) Burkholderia gladioli C101 metabolites protect tomato plants against Xanthomonas perforans infection. J Plant Dis Prot 128:379–390. https://doi.org/10.1007/s41348-020-00416-9
Shearer G, Kohl D (1986) N2-fixation in field settings: estimations based on natural 15N abundance. Funct Plant Biol 13:699. https://doi.org/10.1071/PP9860699
Sibponkrung S, Kondo T, Tanaka K et al (2020) Co-Inoculation of Bacillus velezensis strain S141 and Bradyrhizobium strains promotes nodule growth and nitrogen fixation. Microorganisms 8:678. https://doi.org/10.3390/microorganisms8050678
Thakur BR, Singh RK, Handa AK, Rao MA (1997) Chemistry and uses of pectin — A review. Crit Rev Food Sci Nutr 37:47–73. https://doi.org/10.1080/10408399709527767
Tilman D, Balzer C, Hill J, Befort BL (2011) Global food demand and the sustainable intensification of agriculture. Proc Natl Acad Sci 108:20260–20264. https://doi.org/10.1073/pnas.1116437108
Tiwari AK, Saha SN, Yadav VP et al (2017) Extraction and characterization of pectin from orange peels. Int J Biotechnol Biochem 13:39–47
Vacheron J, Desbrosses G, Bouffaud M-L et al (2013) Plant growth-promoting rhizobacteria and root system functioning. Front Plant Sci 4:356. https://doi.org/10.3389/fpls.2013.00356
van Loon LC (2007) Plant responses to plant growth-promoting rhizobacteria. Eur J Plant Pathol 119:243–254. https://doi.org/10.1007/s10658-007-9165-1
van Veen JA, van Overbeek LS, van Elsas JD (1997) Fate and activity of microorganisms introduced into soil. Microbiol Mol Biol Rev 61:121–135. https://doi.org/10.1128/mmbr.61.2.121-135.1997
Yeoh S, Shi J, Langrish TAG (2008) Comparisons between different techniques for water-based extraction of pectin from orange peels. Desalination 218:229–237. https://doi.org/10.1016/j.desal.2007.02.018
Zeffa DM, Fantin LH, Koltun A et al (2020) Effects of plant growth-promoting rhizobacteria on co-inoculation with Bradyrhizobium in soybean crop: a meta-analysis of studies from 1987 to 2018. PeerJ 8:e7905. https://doi.org/10.7717/peerj.7905
Acknowledgements
The authors would like to thank the technical help from graduate and undergraduate students in Dr. Alvaro Sanz-Saez’s and Dr. Mark Liles’s laboratory at Auburn University.
Funding
This research was financially supported by the Alabama Agricultural Experiment Station grant to Sanz, entitled "Improved soybean and peanut growth, drought resistance and nodulation using rhizobacteria and pectin amendments”.
Author information
Authors and Affiliations
Contributions
M.L.P.D Experimentation, curation of the data, formal analysis, writing original draft. F.M. Experimentation, curation of data, review and editing. Y.F. supervision, review and editing. M.L. Conceptualization, experimentation, data curation, resource managing, supervision, project administration, review and editing. A.S.S. Conceptualization, experimentation, data curation, resource managing, formal analysis, supervision, project administration, writing original draft.
Corresponding author
Ethics declarations
Competing interests
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Additional information
Responsible Editor: Didier Lesueur.
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
da Silva, M.L.P., Moen, F.S., Liles, M.R. et al. Orange peel in combination with selected PGPR strains as seed treatment can improve soybean yield under field conditions. Plant Soil 491, 401–420 (2023). https://doi.org/10.1007/s11104-023-06121-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-023-06121-4