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Current Microbiology

, Volume 76, Issue 11, pp 1345–1354 | Cite as

Prospecting Plant Growth-Promoting Bacteria Isolated from the Rhizosphere of Sugarcane Under Drought Stress

  • Leticia B. Pereira
  • Gabriela S. Andrade
  • Silvana P. Meneghin
  • Renato Vicentini
  • Laura M. M. OttoboniEmail author
Article

Abstract

In the rhizosphere, the soil bacteria and the plants are closely related, with the plant-associated microbiota playing an important role in promoting plant growth under both normal and stress conditions. In this study, the cultivable bacteria in the sugarcane rhizosphere under different levels of drought stress were characterized and screened for plant growth activities. The results suggested that the microbial community associated with the sugarcane rhizosphere was strongly affected by drought, but some important genera of bacteria such as Arthrobacter, Pseudomonas, Microbacterium, and Bacillus remained present during the entire experiment, indicating the adaptability of these organisms and their importance in the rhizosphere community. Many isolates exhibited positive results for one or more plant growth activity, and they were also capable of growing under simulated drought stress, suggesting that the microorganisms isolated from the sugarcane rhizosphere could be explored for uses such as biofertilizers or biocontrol agents in agriculture.

Notes

Funding

This work was supported by the São Paulo State Research Foundation (FAPESP, Grant Number 2015/00408-5). L.B.P. received a fellowship from FAPESP/CAPES (Grant Number 2014/05929-0) and National Council for Scientific and Technological Development (CNPq, Grant Number 140547/2014-2).

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

284_2019_1749_MOESM1_ESM.docx (24 kb)
Electronic supplementary material 1 (DOCX 24 kb)

References

  1. 1.
    Compant S, Van Der Heijden MGA, Sessitsch A (2010) Climate change effects on beneficial plant-microorganism interactions. FEMS Microbiol Ecol 73(2):197–214PubMedGoogle Scholar
  2. 2.
    Bal HB, Da S, Dangar TK, Adhya TK (2013) ACC deaminase and IAA producing growth promoting bacteria from the rhizosphere soil of tropical rice plants. J Basic Microbiol 53(12):972–984CrossRefPubMedGoogle Scholar
  3. 3.
    Someya N, Akutsu K (2005) Biocontrol of plant diseases by genetically modified microorganisms: current status and future prospects. In: Siddiqui ZA (ed) PGPR: biocontrol and biofertilization. Springer, Dordrecht, pp 297–312Google Scholar
  4. 4.
    Ribeiro CM, Cardoso EJBN (2012) Isolation, selection and characterization of root-associated growth promoting bacteria in Brazil Pine (Araucaria angustifolia). Microbiol Res 167(2):69–78CrossRefPubMedGoogle Scholar
  5. 5.
    Paungfoo-Lonhienne C, Lonhienne TGA, Yeoh YK, Webb RI (2014) A new species of Burkholderia isolated from sugarcane roots promotes plant growth. Microb Biotechnol 7(2):142–154CrossRefPubMedGoogle Scholar
  6. 6.
    Aroca R, Ruiz-Lozano J (2009) Sustainable agriculture reviews. In: Lichtfouse E (ed) Climate change, intercropping, pest control and beneficial microorganisms, sustainable agriculture reviews. Springer, New York, pp 121–135CrossRefGoogle Scholar
  7. 7.
    Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci 166(2):525–530CrossRefGoogle Scholar
  8. 8.
    Papadakis EN, Vryzas Z, Kotopoulou A, Kintzikoglou K (2015) A pesticide monitoring survey in rivers and lakes of northern Greece and its human and ecotoxicological risk assessment. Ecotoxicol Environ Saf 116:1–9CrossRefPubMedGoogle Scholar
  9. 9.
    Vurukonda SSKP, Vardharajula S, Shrivastava MSKZA (2016) Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol Res 184:13–24CrossRefPubMedGoogle Scholar
  10. 10.
    Carvalho-Netto OV, Bressiani JA, Soriano HL, Fiori CS (2014) The potential of the energy cane as the main biomass crop for the cellulosic industry. Chem Biol Technol Agric 1(1):20CrossRefGoogle Scholar
  11. 11.
    Davies WJ (2006) Responses of plant growth and functioning to changes in water supply in a changing climate. In: Morison JIL, Morecroft MD (eds) Plant growth and climate change. Blackwell Publishing, Oxford, pp 96–117CrossRefGoogle Scholar
  12. 12.
    dos Santos SG, Chaves VA, da Silva Ribeiro F, Alves GC, Reis VM (2019) Rooting and growth of pre-germinated sugarcane seedlings inoculated with diazotrophic bacteria. Appl Soil Ecol 133:12–23CrossRefGoogle Scholar
  13. 13.
    Kruasuwan W, Thamchaipenet A (2018) 1-aminocyclopropane-1-carboxylate (ACC) deaminase-producing endophytic diazotrophic Enterobacter sp. EN-21 modulates salt–stress response in sugarcane. J Plant Growth Regul 37(3):849–858CrossRefGoogle Scholar
  14. 14.
    Cane Technology Center—CTC (2012) Varieties CTC: varieties highlights. CTC, PiracicabaGoogle Scholar
  15. 15.
    Sambrook E, Fritsch TM, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  16. 16.
    D’Onofrio A, Crawford JM, Stewart EJ, Witt K (2010) Siderophores from neighboring organisms promote the growth of uncultured bacteria. Chem Biol 17(3):254–264CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Bric JM, Bostock RM, Silverstone SE (1991) Rapid in situ assay for indoleacetic acid production by bacteria immobilized on a nitrocellulose membrane. Appl Environ Microbiol 57:535–538PubMedPubMedCentralGoogle Scholar
  18. 18.
    Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol Plant 118(1):10–15CrossRefPubMedGoogle Scholar
  19. 19.
    Gupta R, Singal R, Shankar A, Kuhad RC (1994) A modified plate assay for screening phosphate solubilizing microorganisms. J Gen Appl Microbiol 40(3):255–260CrossRefGoogle Scholar
  20. 20.
    Park M, Kim C, Yang J, Lee H (2005) Isolation and characterization of diazotrophic growth promoting bacteria from rhizosphere of agricultural crops of Korea. Microbiol Res 160(2):127–133CrossRefPubMedGoogle Scholar
  21. 21.
    Ortiz N, Armada E, Duque E, Roldán A (2015) Contribution of arbuscular mycorrhizal fungi and/or bacteria to enhancing plant drought tolerance under natural soil conditions: effectiveness of autochthonous or allochthonous strains. J Plant Physiol 174:87–96CrossRefPubMedGoogle Scholar
  22. 22.
    Huse SM, Welch DBM (2011) Accuracy and quality of massively parallel DNA pyrosequencing. Genome Biol 8(7):R143CrossRefGoogle Scholar
  23. 23.
    Masoud W, Takamiya M, Vogensen FK, Lillevang S (2011) Characterization of bacterial populations in Danish raw milk cheeses made with different starter cultures by denaturating gradient gel electrophoresis and pyrosequencing. Int Dairy J 21(3):142–148CrossRefGoogle Scholar
  24. 24.
    Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12), 2725–2729.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):1–9Google Scholar
  27. 27.
    Zahir ZA, Munir A, Asghar HN, Shaharoona B (2008) Effectiveness of rhizobacteria containing acc deaminase for growth promotion of peas (Pisum sativum) under drought conditions. J Microbiol Biotechnol 18:958–963PubMedGoogle Scholar
  28. 28.
    Griffiths RI, Whiteley AS, Anthony G, Donnell O (2003) Physiological and community responses of established grassland bacterial populations to water stress physiological and community responses of established grassland bacterial populations to water stress. Appl Environ Microbiol 69(12):6961–6968CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Bogino P, Abod A, Nievas F, Giordano W (2013) Water-limiting conditions alter the structure and biofilm-forming ability of bacterial multispecies communities in the alfalfa rhizosphere. PLoS ONE 8(11):e79614CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Mehnaz S (2013) Microbes - friends and foes of sugarcane. J Basic Microbiol 53(12):954–971CrossRefPubMedGoogle Scholar
  31. 31.
    Dhanraj BN (2013) Bacterial diversity in sugarcane (Saccharum officinarum) rhizosphere of saline soil. Int Res J Biol Sci 2:60–64Google Scholar
  32. 32.
    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 App Sci 5:1072–1083CrossRefGoogle Scholar
  33. 33.
    Lin L, Guo W, Xing Y, Zhang X (2012) The actinobacterium Microbacterium sp. 16SH accepts pBBR1-based pPROBE vectors, forms biofilms, invades roots, and fixes N2 associated with micropropagated sugarcane plants. Appl Microbiol Biotechnol 93:1185–1195CrossRefPubMedGoogle Scholar
  34. 34.
    Velázquez E, Rojas M, Lorite MJ, Rivas R (2008) Genetic diversity of endophytic bacteria which could be find in the apoplastic sap of the medullary parenchym of the stem of healthy sugarcane plants. J Basic Microbiol 48:118–124CrossRefPubMedGoogle Scholar
  35. 35.
    Upadhyay SK, Singh DP, Saikia R (2009) Genetic diversity of plant growth promoting rhizobacteria isolated from rhizospheric soil of wheat under saline condition. Curr Microbiol 59(5):489–496CrossRefPubMedGoogle Scholar
  36. 36.
    Singh GY, Singh US, Sharma AK (2015) Bacterial mediated amelioration of drought stress in drought tolerant and susceptible cultivars of rice (Oryza sativa L.). Afr J Biotechnol 14(9):764–773CrossRefGoogle Scholar
  37. 37.
    Kumar G, Kanaujia N, Bafana A (2012) Functional and phylogenetic diversity of root-associated bacteria of Ajuga bracteosa in Kangra valley. Microbiol Res 167(4):220–225CrossRefPubMedGoogle Scholar
  38. 38.
    Kruasuwan W, Thamchaipenet A (2016) Diversity of culturable plant growth-promoting bacterial endophytes associated with sugarcane roots and their effect of growth by co-inoculation of diazotrophs and actinomycetes. J Plant Growth Regul 35(4):1074–1087CrossRefGoogle Scholar
  39. 39.
    Rau N, Mishra V, Sharma M, Das MK (2009) Evaluation of functional diversity in rhizobacterial taxa of a wild grass (Saccharum ravennae) colonizing abandoned fly ash dumps in Delhi urban ecosystem. Soil Biol Biochem 41(4):813–821CrossRefGoogle Scholar
  40. 40.
    Turnbull AL, Liu Y, Lazarovits G (2012) Isolaton of bacteria from the rhizosphere and rhizoplane of potato (Solanum tuberosum) grown in two distinct soils using semi selective media and characterization of their biological properties. Am J Potato Res 89(4):294–305CrossRefGoogle Scholar
  41. 41.
    Akhtar N, Ali A, Bashir U, Haider MS (2011) Morphological and biochemical studies on bacterial microfauna from lahore soils. Pak J Phytopathol 25:137–140Google Scholar
  42. 42.
    Mahmoud HM, Kalendar AA (2016) Coral-associated actinobacteria: diversity, abundance, and biotechnological potentials. Front Microbiol 7:204PubMedPubMedCentralGoogle Scholar
  43. 43.
    Marulanda A, Barea JM, Azcón R (2009) Stimulation of plant growth and drought tolerance by native microorganisms (AM Fungi and bacteria) from dry environments: mechanisms related to bacterial effectiveness. J Plant Growth Regul 28(2):115–124CrossRefGoogle Scholar
  44. 44.
    Tian Y, Gao L (2014) Bacterial diversity in the rhizosphere of cucumbers grown in soils covering a wide range of cucumber cropping histories and environmental conditions. Microb Ecol 68(4):794–806CrossRefPubMedGoogle Scholar
  45. 45.
    Schreiter S, Ding GC, Heuer H, Neumann G (2014) Effect of the soil type on the microbiome in the rhizosphere of field-grown lettuce. Front Microbiol 5:144CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Graham PH, Vance CP (2003) Legumes: importance and constraints to greater use. Plant Physiol 131(3):872–877CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Wang HF, Zhang YG, Li L, Liu WH (2015) Okibacterium endophyticum sp. nov. a novel endophytic actinobacterium isolated from roots of Salsola affinis CA Mey. Antonie Leeuwenhoek 107(3):835–843CrossRefPubMedGoogle Scholar
  48. 48.
    Idris R, Trifonova R, Puschenreiter M, Wenzel WW (2004) Bacterial communities associated with flowering plants of the Ni fyperaccumulator Thlaspi goesingense. Appl Environ Microbiol 70(5):2667–2677CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Vargas L, Brígida ABS, Mota Filho JP, de Carvalho TG (2014) Drought tolerance conferred to sugarcane by association with Gluconacetobacter diazotrophicus: a transcriptomic view of hormone pathways. PLoS ONE 9(12):e114744CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Urquiaga S, Xavier RP, de Morais RF, Batista RB (2012) Evidence from field nitrogen balance and 15N natural abundance data for the contribution of biological N2 fixation to Brazilian sugarcane varieties. Plant Soil 356:5–21CrossRefGoogle Scholar
  51. 51.
    Chaves VA, dos Santos SG, Schultz N, Pereira W (2015) Initial development of two sugarcane varieties inoculated with diazotrophic bacteria. Rev Bras Cienc do Solo 39(6):1595–1602CrossRefGoogle Scholar
  52. 52.
    Dos Santos SG, da Silva Ribeiro F, da Fonseca CS, Pereira W (2017) Development and nitrate reductase activity of sugarcane inoculated with five diazotrophic strains. Arch Microbiol 199(6):863–873CrossRefPubMedGoogle Scholar
  53. 53.
    Gtari M, Ghodhbane-Gtari F, Nouioui I, Beauchemin N (2012) Phylogenetic perspectives of nitrogen-fixing actinobacteria. Arch Microbiol 194:3–11CrossRefPubMedGoogle Scholar
  54. 54.
    Vasebi Y, Khakvar R, Faghihi MM, Vinatzer BA (2019) Genomic and pathogenic properties of Pseudomonas syringae pv. syringae strains isolated from apricot in East Azerbaijan province. Iran. Biocatal Agric Biotechnol 20:101167CrossRefGoogle Scholar
  55. 55.
    de Castro Gava GJ, Scarpare FV, Cantarella H, Kölln OT, Ruiz-Corrêa ST et al (2019) Nitrogen source contribution in sugarcane-inoculated plants with diazotrophic bacterias under urea-N fertigation management. Sugar Tech 21(3):462–470CrossRefGoogle Scholar
  56. 56.
    Pedula RO, Schultz N, Monteiro RC, Pereira W, de Araujo AP et al (2016) Growth analysis of sugarcane inoculated with diazotrophic bacteria and nitrogen fertilization. Afr J Agric 11(30):2786–2795CrossRefGoogle Scholar
  57. 57.
    Zerrouk IZ, Benchabane M, Khelifi L, Yokawa K, Ludwig-Müller J, Baluska F (2016) A Pseudomonas strain isolated from date-palm rhizospheres improves root growth and promotes root formation in maize exposed to salt and aluminum stress. J Plant Physiol 191:111–119CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Leticia B. Pereira
    • 1
  • Gabriela S. Andrade
    • 2
  • Silvana P. Meneghin
    • 2
  • Renato Vicentini
    • 3
  • Laura M. M. Ottoboni
    • 1
    Email author
  1. 1.Center for Molecular Biology and Genetic Engineering (CBMEG)State University of Campinas (UNICAMP)CampinasBrazil
  2. 2.Department of Biotechnology and Vegetal and Animal ProductionFederal University of São Carlos (UFSCar)ArarasBrazil
  3. 3.Department of Plant BiologyState University of Campinas (UNICAMP)CampinasBrazil

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