https://doi.org/10.4081/ija.2022.2006

Plant growth-promoting bacteria isolated from sugarcane improve the survival of micropropagated plants during acclimatisation

Vol. 17 No. 2 (2022)
Submitted: 12 November 2021
Accepted: 24 May 2022
Published: 29 June 2022
Bacillus, Paenibacillus, plant growth-promoting bacteria, Pseudomonas, Saccharum hybrids.
Abstract Views: 1175
PDF: 525
Appendix: 61
HTML: 14
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

Authors

  • Gabriela Michavila Instituto de Tecnología Agroindustrial del Noroeste Argentino (ITANOA), Estación Experimental Agroindustrial Obispo Colombres (EEAOC) - Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) - CONICET NOA Sur, Las Talitas, Tucuman, Argentina.
  • Pasquale Alibrandi Department of Life Sciences and Systems Biology, University of Turin, Italy.
  • Paolo Cinà ABIEL srl c/o Arca Incubatore di imprese, Palermo, Italy.
  • Bjorn Welin Instituto de Tecnología Agroindustrial del Noroeste Argentino (ITANOA), Estación Experimental Agroindustrial Obispo Colombres (EEAOC) - Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) - CONICET NOA Sur, Las Talitas, Tucuman, Argentina.
  • Atilio Pedro Castagnaro Instituto de Tecnología Agroindustrial del Noroeste Argentino (ITANOA), Estación Experimental Agroindustrial Obispo Colombres (EEAOC) - Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) - CONICET NOA Sur, Las Talitas, Tucuman, Argentina.
  • Nadia Regina Chalfoun Instituto de Tecnología Agroindustrial del Noroeste Argentino (ITANOA), Estación Experimental Agroindustrial Obispo Colombres (EEAOC) - Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) - CONICET NOA Sur, Las Talitas, Tucuman, Argentina.
  • Aldo Sergio Noguera Instituto de Tecnología Agroindustrial del Noroeste Argentino (ITANOA), Estación Experimental Agroindustrial Obispo Colombres (EEAOC) - Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) - CONICET NOA Sur, Las Talitas, Tucuman, Argentina.
  • Anna Maria Puglia ABIEL srl c/o Arca Incubatore di imprese, Palermo, Italy.
  • Mirella Ciaccio Institute for Biomedical Research and Innovation, National Research Council, Palermo, Italy.
  • Josefina Racedo • joracedo@gmail.com https://orcid.org/0000-0001-6874-1778 Instituto de Tecnología Agroindustrial del Noroeste Argentino (ITANOA), Estación Experimental Agroindustrial Obispo Colombres (EEAOC) - Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) - CONICET NOA Sur, Las Talitas, Tucuman, Argentina.

The plant microbiome plays an important role in nutrient acquisition and buffering plant hosts against abiotic and biotic stress. During in vitro propagation of sugarcane, pathogenic microorganisms are eliminated and most of the beneficial endophytic microorganisms. The objective of this study was to isolate and characterise potential plant growth-promoting bacteria (PGPB) from sugarcane and to analyse their ability to improve the survival of micropropagated sugarcane plantlets during the acclimatisation stage. First, bacterial isolates from sugarcane were identified by partial 16S rDNA sequencing and tested for plant growth-promoting (PGP) features, such as inorganic and organic phosphate solubilisation nitrogen fixation, siderophore synthesis, indole-3-acetic acid production, tolerance to abiotic stress and antibiotics production. Then three bacterial strains with multiple PGP traits were independently applied to micropropagated seedlings of the sugarcane variety TUC 03-12 when the plants were transferred to a nursery for ex vitro acclimatisation. The effect of selected PGPB on survival rates of micropropagated plantlets was evaluated in three independent assays, using different batches of seedlings. Thirty days after inoculation, 182-Bacillus and 336-Pseudomonas isolates significantly improved the transferred plants survival rate. High variability in plant survival among independent experiments was observed, but treatments with the 336-Pseudomonas strain showed a low mortality rate (20%) in all assays. This procedure constitutes a biological tool to improve the survival of micropropagated plants during greenhouse acclimatisation. Furthermore, it provides an initial tool for selecting bacteria with possible PGP effects in the field.

Highlights
- A total of 162 isolates obtained from the rhizosphere, rhizoplane, roots, and stems of sugarcane were characterised for plant growthpromoting features and identified by partial 16S rDNA sequencing.
- Two PGPBs strains isolated from sugarcane (182-Bacillus and 336-Pseudomonas) significantly improved survival rates of micropropagated seedlings during the acclimatisation stage.
- Under different stress conditions, the 336-Pseudomonas strain improved the survival of micropropagated plants during the acclimatisation stage.

Erratum in: 10.4081/ija.2022.2150

Dimensions

Altmetric

PlumX Metrics

Downloads

Download data is not yet available.

Citations

Crossref
Scopus
Google Scholar
Europe PMC
Alibrandi P, Cardinale M, Mahafizur Rahman MD, Strati F, Ciná P, de Viana ML, Giamminola EM, Gallo G, Schnell S, De Filippo C, Ciaccio M, Puglia AM, 2018. The seed endosphere of Anadenanthera colubrina is inhabited by a complex microbiota, including Methylobacterium spp. and Staphylococcus spp. with potential plant-growth promoting activities. Plant Soil. 422:81-99. DOI: https://doi.org/10.1007/s11104-017-3182-4
Beneduzi A, Ambrosini A, Passaglia LMP, 2012. Plant growth-promoting rhizobacteria (PGPR): Their potential as antagonists and biocontrol agents. Genet. Mol. Biol. 35:1044-51. DOI: https://doi.org/10.1590/S1415-47572012000600020
Bhardwaj G, Shah R, Joshi B, Patel P, 2017. Klebsiella pneumoniae VRE36 as a PGPR isolated from Saccharum officinarum cultivar Co99004. J. Appl. Biol. Biotechnol. 5:047-52. DOI: https://doi.org/10.7324/JABB.2017.50108
Boddey RM, de Oliveira OC, Urquiaga S, Reis VM, de Olivares FL, Baldani VLD, Dobereiner J, 1995. Biological nitrogen fixation associated with sugar cane and rice: contributions and prospects for improvement. Plant Soil. 174:195-209. DOI: https://doi.org/10.1007/978-94-011-0053-3_9
OECD-FAO Agricultural Outlook, 2018. OECD Agricultur estatistics (data base). Available from: http://dx.doi.org/10.1787/agr-outl-data-en DOI: https://doi.org/10.1787/agr-outl-data-en
Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW. InfoStat versión 2020. Centro de Transferencia InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. Available from: http://www.infostat.com.ar
Di Rienzo JA, Guzmán AW, Casanoves F, 2002. A multiple comparisons method based on the distribution of the root node distance of a binary tree. JABES. 7:1-14. DOI: https://doi.org/10.1198/10857110260141193
Díaz ME, Perera MF, Paz NV, Insaurralde Rocco P, Ovejero SN, Cerviño AM, Castagnaro AP, Noguera AS, 2020. Proceso de producción de vitroplantas de caña de azúcar de pureza genética y sanidad garantizadas en etapa de laboratorio en la EEAOC. Revi Ind y Agrí de Tucumán. 97:39-44.
Díaz Romero C, Chavanne E, Cuenya MI, Berardinelli A, Noguera AS, 2005. Proyecto vitroplantas de caña de azúcar: resultados obtenidos entre 2001 y 2004 en las áreas de crianza en invernáculo y de manejo de semillero básico. Avance Agroindustrial. 26:8-12.
Figueiredo GGO, Lopes VR, Fendrich RC, Szilagyi-Zecchin VJ, 2017. Interaction between beneficial bacteria and sugarcane. In: D. Singh, H. Singh, R. Prabha (Eds.), Plant-microbe interactions in agro-ecological perspectives. Springer, Singapore, pp 1-27. DOI: https://doi.org/10.1007/978-981-10-6593-4_1
Frank JA, Reichm CI, Sharma S, Weisbaum JS, Wilson BA, Olsen GJ, 2008. Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl Environ Microbiol. 74:2461-70. DOI: https://doi.org/10.1128/AEM.02272-07
Fuentes-Ramirez LE, Jimenez-Salgado T, Abarca-Ocampo IR, Caballero-Mellado J, 1993. Acetobacter diazotrophicus, an indoleacetic acid producing bacterium isolated from sugarcane cultivars of México. Plant Soil. 154:145-50. DOI: https://doi.org/10.1007/BF00012519
Gallo G, Baldi F, Renzone G, Gallo M, Cordaro A, Scaloni A, Puglia AM, 2012. Adaptative biochemical pathways and regulatory networks in Klebsiella oxytoca BAS-10 producing a biotechnologically relevant exopolysaccharide during Fe (III)-citrate fermentation. Microb. Cell Fact. 11:152. DOI: https://doi.org/10.1186/1475-2859-11-152
Garcia JAL, Probanza A, Ramos B, Palomino MR, Manero FJG, 2004. Effect of inoculation of Bacillus licheniformis on tomato and pepper. Agron Sustain Dev. 24:169-76. DOI: https://doi.org/10.1051/agro:2004020
Glickmann E, Dessaux Y, 1995. A critical examination of the specificity of the Salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Appl. Environ. Microbiol. 61:793-6. DOI: https://doi.org/10.1128/aem.61.2.793-796.1995
Inui-Kishi RN, Takeshi Kishi L, Picchi SC, Barbosa JC, Olivério Lemos MT, Marcondes J, Macedo Lemos EG, 2012. Phosphorus solubilizing and IAA production activities in plant growth promoting rhizobacteria from Brazilian soils under sugarcane cultivation. ARPN J. Eng. Appl. Sci. 7:1446-54.
Jaizme-Vega MDC, Rodríguez-Romero AS, Guerra MSP, 2004. Potential use of rhizobacteria from the Bacillus genus to stimulate the plant growth of micropropagated bananas. Fruits. 59:83-90. DOI: https://doi.org/10.1051/fruits:2004008
Jensen HL, 1942. Nitrogen fixation in leguminous plants. II. Is symbiotic nitrogen fixation influenced by Azobacter. Proc Linn Soc NSW. 67:205-12.
Jibu T, Ajay D, Raj Kumar R, Mandal AKA, 2010. Influence of beneficial microorganisms during in vivo acclimatization of in vitro-derived tea (Camellia sinensis) plants. Plant. Cell Tissue Organ. Cult. 101:365-70. DOI: https://doi.org/10.1007/s11240-010-9687-7
Kaur R, Putatunda C, 2018. In vitro phosphate solubilization by sugarcane (Saccharum officinarum) rhizosphere bacteria. Int. J. Curr. Microbiol. Appl. Sci. 7:1557-64. DOI: https://doi.org/10.20546/ijcmas.2018.706.186
Kozai T, Xiao Y, Nguyen QT, Afreen F, Zobayed, SMA, 2005. Photoautotrophic (sugar-free medium) micropropagation systems for large-scale commercialization. Propag. Ornam. Plants. 5:23-34.
Kumar S, Stecher G, Li M, Knyaz C, Tamura K, 2018. MEGA x: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35:1547-9. DOI: https://doi.org/10.1093/molbev/msy096
Kumar A, Singh S, Gaurav AK, Srivastava S, Verma JP, 2020. Growth-promoting bacteria: biological tools for the mitigation of salinity stress in plants. Front Microbiol. 11:1216. DOI: https://doi.org/10.3389/fmicb.2020.01216
Lam LL, Verbanov PS, Klemes J, 2010. Optimisation of regional supply chains utilising renewable: P-graph approach. Comput. Chem. Eng. 34:782-92. DOI: https://doi.org/10.1016/j.compchemeng.2009.11.020
Lamizadeh E, Enayatizamir N, Motamedi H, 2016. Isolation and identification of plant growth-promoting rhizobacteria (PGPR) from the rhizosphere of sugarcane in saline and non-saline soil. Int. J. Curr Microbiol. Appl. Sci. 5:1072-83. DOI: https://doi.org/10.20546/ijcmas.2016.510.113
Lane D J. 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M, editors. Nucleic acid techniques in bacterial systematics. John Wiley and Sons, New York, NY, USA, pp. 115-148.
Milanesi C, Cresti M, Costantini L, Gallo M, Gallo G, Crognale S, Faleri C, Gradi A, Baldi F, 2015. Spoilage of oat bran by sporogenic microorganisms revived from soil buried 4000 years ago in Iranian archaeological site. Int. Biodeterior. Biodegrad. 104:83-91. DOI: https://doi.org/10.1016/j.ibiod.2015.05.016
Mirza MS, Ahmad W, Latif F, Haurat J, Bally R, Normand P, Malik KA, 2001. Isolation, partial characterization, and the effect of plant growth-promoting bacteria (PGPB) on micro-propagated sugarcane in vitro. Plant Soil. 237:47-54. DOI: https://doi.org/10.1023/A:1013388619231
Murashige T, 1974. Plant propagation through tissue cultures. Annu Rev Plant Physiol. 25:135-66. DOI: https://doi.org/10.1146/annurev.pp.25.060174.001031
Nautiyal CS, 1999. An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol. Lett. 170:265-70. DOI: https://doi.org/10.1111/j.1574-6968.1999.tb13383.x
Neves LA, Rodrigues JM, Daroda RJ, Silva PR, Ferreira AA, Aranda DA, Eberlin MN, Fasciotti M, 2015. The influence of different referencing methods on the accuracy of δ (13) C value measurement of ethanol fuel by gas chromatography/combustion/isotope ratio mass spectrometry. Rapid Commun Mass Spectrom. 29:1938-46. DOI: https://doi.org/10.1002/rcm.7298
Noguera A, Enrique R, Perera MP, Ostengo S, Racedo J, Costilla D, Zossi S, Cuenya MI, Filippone MP, Welin B, Castagnaro AP, 2015. Genetic characterization and field evaluation to recover parental phenotype in transgenic sugarcane: a step toward commercial release. Mol Breed. 35:115. DOI: https://doi.org/10.1007/s11032-015-0300-y
Noguera AS, Paz NV, Díaz ME, Perera MF, Díaz-Romero C, García MB, Filippone MP, Welin B, Cuenya MI, Digonzelli PA, Castagnaro AP, 2013. Production of healthy seed cane in Tucumán, Argentina. Proc. Int. Soc. Sugar Cane Technol. 28:1-9.
Numan M, Bashir S, Khan Y, Mumtaz R, Khan Shinwari Z, Latif Khan A, Khan A, AL-Harrasi A, 2018. Plant growth promoting bacteria as an alternative strategy for salt tolerance in plants: A review. Microbiol Res. 209:21-32. DOI: https://doi.org/10.1016/j.micres.2018.02.003
Oliveira ALM, Urquiaga S, Döbereiner J, Baldani JI, 2002. The effect of inoculating endophytic N2 fixing bacteria on micro propagated sugarcane plants. Plant Soil. 2:205-15. DOI: https://doi.org/10.1023/A:1016249704336
Patel P, Shah R, Joshi B, Ramar K, Natarajan A, 2019. Molecular identification and biocontrol activity of sugarcane rhizosphere bacteria against red rot pathogen Colletotrichum falcatum. Biotechnol Rep. 21:e00317. DOI: https://doi.org/10.1016/j.btre.2019.e00317
Pedula RO, Schultz N, Monteiro RC, Pereira W, Araujo AP, Urquiaga S, Reis VM, 2016. Growth analysis of sugarcane inoculated with diazotrophic bacteria and nitrogen fertilization. Afr. J. Agric. Res. 11:2786-95. DOI: https://doi.org/10.5897/AJAR2016.11141
Perera MF, Racedo J, García MG, Pardo EM, Rocha CML, Orce IG, Chiesa MA, Filippone MP, Welin B, Castagnaro AP, 2015. Use of molecular markers to improve the agro-industrial productivity in the North West of Argentina. Mol Biol. 5:2.
Pirhadi M, Enayatizamir N, Motamedi H, Sorkheh K, 2018. Impact of soil salinity on diversity and community of sugarcane endophytic plant growth promoting bacteria (Saccharum officinarum l. Var. Cp48). Appl. Ecol. Environ. Res. 16:725-39. DOI: https://doi.org/10.15666/aeer/1601_725739
Rilling JI, Acun JA, Nannipieri P, Cassan FD, Maruyam F, Jorquer M, 2019. Current opinion and perspectives on the methods for tracking and monitoring plant growth-promoting bacteria. Soil Biol. Biochem. 130:205-19. DOI: https://doi.org/10.1016/j.soilbio.2018.12.012
Rocha PSGD, Oliveira RPD, Scivittaro WB, 2013. Sugarcane micropropagation using light emitting diodes and adjustment in growth-medium sucrose concentration. Ciência Rural. 43:1168-73. DOI: https://doi.org/10.1590/S0103-84782013000700005
Russo A, Vettori L, Felici C, Fiaschi G, Morini S, Toffanin A, 2008. Enhanced micropropagation response and biocontrol effect of Azospirillum brasilense Sp245 on Prunus cerasifera L. clone Mr. S 2/5 plants. J. Biotechnol. 134:312-9. DOI: https://doi.org/10.1016/j.jbiotec.2008.01.020
Sezonov G, Joseleau-Petit D, D’Ari R, 2007. Escherichia coli physiology in Luria-Bertani broth. J. Bacteriol. 189:8746-9. DOI: https://doi.org/10.1128/JB.01368-07
Tortora ML, Díaz Ricci JC, Pedraza RO, 2011. Azospirillum brasilense siderophores with antifungal activity against Colletotrichum acutatum. Arch. Microbiol. 193:275-86. DOI: https://doi.org/10.1007/s00203-010-0672-7
Yadav A, Kothari SL, Kachhwaha S, Joshi A, 2019. In vitro propagation of chia (Salvia hispanica L.) and assessment of genetic fidelity using random amplified polymorphic DNA and intersimple sequence repeat molecular markers. J. Appl. Biol. Biotechnol. 7:42-7. DOI: https://doi.org/10.7324/JABB.2019.70108
Zayed MS, El-Moneim Hegazi GA, Salem HM, Ali Adas WMI, 2017. Role of endomycorrhizae and Pseudomonas fluorescens on the acclimatization of micropropagated Stevia rebaudiana Bert. plantlets. Afr. J. Plant Sci. 11:38-47. DOI: https://doi.org/10.5897/AJPS2016.1494

How to Cite

Michavila, G., Alibrandi, P., Cinà, P. ., Welin, B. ., Castagnaro, A. P., Chalfoun, N. R., Noguera, A. S., Puglia, A. M., Ciaccio, M. ., & Racedo, J. (2022). Plant growth-promoting bacteria isolated from sugarcane improve the survival of micropropagated plants during acclimatisation. Italian Journal of Agronomy, 17(2). https://doi.org/10.4081/ija.2022.2006
Copyright (c) 2022 The Author(s) Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

PAGEPress has chosen to apply the Creative Commons Attribution NonCommercial 4.0 International License (CC BY-NC 4.0) to all manuscripts to be published.