Skip to main content
SpringerLink
Log in

Isolation and identification of Ammodendron bifolium endophytic bacteria and the action mechanism of selected isolates-induced seed germination and their effects on host osmotic-stress tolerance

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

This study aimed to identify Ammodendron bifolium endophytic bacteria, and to evaluate promoting mechanism of selected isolates on seed germination and their effects on host osmotic-stress tolerance. Forty-five strains were isolated from A. bifolium and were classified into 13 different genera by 16S rDNA gene sequence analysis. AY3, AY9 and AG18, which were identified as Staphylococcus, Kocuria, Bacillus sp., promoted host seed ethylene release during germination. Ethrel and 1-aminocyclopropane-1-carboxylic acid (ACC) imitated the effect of AY3, AY9 and AG18 on seed germination. The data suggest that ethylene mediates AY3-, AY9-, AG18-induced A. bifolium seed germination. In addition, osmotic stress prevented seed germination and radicle elongation. However, the inhibitory effect of osmotic stress on seed germination and radicle elongation were rescued by AY3, AY9 and AG18. The results show that AY3, AY9 and AG18 increased osmotic-stress tolerance in A. bifolium. AY3, AY9, AG18 induced A. bifolium seed germination through promoting ethylene production during endophytic bacteria–plant interaction, and increase osmotic-stress tolerance in A. bifolium. AY3, AY9 and AG18 are potential candidates for the protection of A. bifolium.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ali S, Charles TC, Glick BR (2014a) Amelioration of high salinity stress damage by plant growth-promoting bacterial endophytes that contain ACC deaminase. Plant Physiol Biochem 80:160–167

    Article  CAS  PubMed  Google Scholar 

  • Ali SZ, Sandhya V, Rao LV (2014b) Isolation and characterization of drought-tolerant ACC deaminase and exopolysaccharide-producing fluorescent Pseudomonas sp. Ann Microbiol 64:493–502

    Article  CAS  Google Scholar 

  • Araújo WL, Maccheroni W Jr, Aguilar-Vildoso CI, Barroso PAV, Saridakis HO, Azevedo JL (2001) Variability and interactions between endophytic bacteria and fungi isolated from leaf tissues of citrus rootstocks. Can J Microbiol 47:229–236

    Article  PubMed  Google Scholar 

  • Arc E, Sechet J, Corbineau F, Rajjou L, Marion-Poll A (2013) ABA crosstalk with ethylene and nitric oxide in seed dormancy and germination. Front Plant Sci 4:63. https://doi.org/10.3389/fpls.2013.00063

    Article  PubMed  PubMed Central  Google Scholar 

  • Azevedo JL, Maccheroni W Jr, Pereira JO, Araújo WL (2000) Endophytic microorganisms: a review on insect control and recent advances on tropical plants. Electron J Biotechnol 3:40–65

    Article  Google Scholar 

  • Bernardr G, Cheng Z, Jennifer C, Duan J (2007) Promotion of plant growth by ACC deaminase-producing soil bacteria. Eur J Plant Pathol 119:329–339

    Article  CAS  Google Scholar 

  • Bhore SJ, Ravichantar N, Loh CY (2010) Screening of endophytic bacteria isolated from leaves of Sambung Nyawa [Gynura procumbens (Lour.) Merr.] for cytokinin-like compounds. Bioinformation 5:191–197

    Article  PubMed  PubMed Central  Google Scholar 

  • Byers HK, Stackebrandt E, Hayward C, Blackall LL (1998) Molecular investigation of a microbial mat associated with the great artesian basin. FEMS Microbiol Ecol 25:391–403

    Article  CAS  Google Scholar 

  • Chen L, Luo SL, Xiao X, Guo HJ, Chen JL, Wan Y, Li B, Xu TY, Xi Q, Rao C, Liu CB, Zeng GM (2010) Application of plant growth-promoting endophytes (PGPE) isolated from Solanum nigrum L. for phytoextraction of Cd-polluted soils. Appl Soil Ecol 46:383–389

    Article  Google Scholar 

  • Cheng Z, Park E, Glick BR (2007) 1-Aminocyclopropane-1-carboxylate deaminase from Pseudomonas putida UW4 facilitates the growth of canola in the presence of salt. Can J Microbiol 53:912–918

    Article  CAS  PubMed  Google Scholar 

  • Cherif H, Marasco R, Rolli E, Ferjani R, Fusi M, Soussi A, Mapelli F, Blilou I, Borin S, Boudabous A, Cherif A, Daffonchio D, Ouzari H (2015) Oasis desert farming selects environment-specific date palm root endophytic communities and cultivable bacteria that promote resistance to drought. Env Microbiol Rep 7:668–678

    Article  CAS  Google Scholar 

  • Claus D (1992) A standardized Gram staining procedure. World J Microb Biot 8:451–452

    Article  CAS  Google Scholar 

  • Compant S, Mitter B, Colli-Mull JG, Gangl H, Sessitsch A (2011) Endophytes of grapevine flowers, berries, and seeds: identification of cultivable bacteria, comparison with other plant parts, and visualization of niches of colonization. Microb Ecol 62:188–197

    Article  PubMed  Google Scholar 

  • Corbineau F, Xia Q, Bailly C, El-Maarouf-Bouteau H (2014) Ethylene, a key factor in the regulation of seed dormancy. Front Plant Sci 5:1–13

    Article  Google Scholar 

  • Creus CM, Sueldo RJ, Barassi CA (1998) Water relations in Azospirillum-inoculated wheat seedlings under osmotic stress. Can J Bot 76:238–244

    Google Scholar 

  • De Jesus Santos AF, Martins CYS, Santos PO, Corrêa ÉB, Barbosa HR, Sandoval APS, Oliveira LM, De Souza JT, Soares ACF (2014) Diazotrophic bacteria associated with sisal (Agave sisalana Perrine ex Engelm): potential for plant growth promotion. Plant Soil 385:37–48

    Article  CAS  Google Scholar 

  • Deivanai S, Bindusara AS, Prabhakaran G, Bhore SJ (2014) Culturable bacterial endophytes isolated from Mangrove tree (Rhizophora apiculata Blume) enhance seedling growth in Rice. J Nat Sci Biol Med 5:437–444

    Article  PubMed  PubMed Central  Google Scholar 

  • Deng ZS, Zhao LF, Kong ZY, Yang WQ, Lindström K, Wang ET, Wei GH (2011) Diversity of endophytic bacteria within nodules of the Sphaerophysa salsula in different regions of Loess Plateau in China. FEMS Microbiol Ecol 76:463–475

    Article  CAS  PubMed  Google Scholar 

  • Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA 103:626–631

    Article  CAS  PubMed  Google Scholar 

  • Hallmann J, Quadt-Hallmann A, Mahaffee WF, Kloepper JW (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43:895–914

    Article  CAS  Google Scholar 

  • Hinton DM, Bacon CW (1995) Enterobacter cloacae is an endophytic symbiont of corn. Mycopathologia 129:117–125

    Article  CAS  PubMed  Google Scholar 

  • Huang ZY, Wu H, Hu ZH (1995) An anatomical study on xeromorphic structures of the psammophytes in Xinjiang. Acta Bot Boreal 15:56–61

    Google Scholar 

  • Hurek T, Handley LL, Reinhold-Hurek B, Piché Y (2002) Azoarcus grass endophytes contribute fixed nitrogen to the plant in an unculturable state. Mol Plant Microbe Interact 15:233–242

    Article  CAS  PubMed  Google Scholar 

  • Indiragandhi P, Anandham R, Kim K, Yim W, Madhaiyan M, Sa T (2008) Induction of defense responses in tomato against Pseudomonas syringae pv. tomato by regulating the stress ethylene level with Methylobacterium oryzae CBMB20 containing 1-aminocyclopropane-1-carboxylate deaminase. World J Microbiol Biotechnol 24:1037–1045

    Article  CAS  Google Scholar 

  • Iniguez AL, Dong Y, Triplett EW (2004) Nitrogen fixation in wheat provided by Klebsiella pneumoniae. Mol Plant Microbe Interact 342:1078–1085

    Article  Google Scholar 

  • Ishibashi Y, Koda Y, Zheng SH, Yuasa T, Iwaya-Inoue M (2013) Regulation of soybean seed germination through ethylene production in response to reactive oxygen species. Ann Bot 111:95–102

    Article  CAS  PubMed  Google Scholar 

  • Jasim B, Joseph AA, John CJ, Mathew J, Radhakrishnan EK (2014) Isolation and characterization of plant growth promoting endophytic bacteria from the rhizome of Zingiber officinale. 3 Biotech 4:197–204

    Article  CAS  PubMed  Google Scholar 

  • Ji SH, Gururani MA, Chun SC (2014) Isolation and characterization of plant growth promoting endophytic diazotrophic bacteria from Korean rice cultivars. Microbiol Res 169:83–98

    Article  CAS  PubMed  Google Scholar 

  • Kang SM, Joo GJ, Hamayun M, Na CI, Shin DH, Kim HY, Hong JK, Lee IJ (2009) Gibberellin production and phosphate solubilization by newly isolated strain of Acinetobacter calcoaceticus and its effect on plant growth. Biotechnol Lett 31:277–281

    Article  CAS  PubMed  Google Scholar 

  • Kerry BR (2000) Rhizosphere interactions and the exploitation of microbial agents for the biological control of plant-parasitic nematodes. Ann Rev Phytopath 38:423–441

    Article  CAS  Google Scholar 

  • Kuklinsky-Sobral J, Araújo WL, Mendes R, Geraldi IO, Pizzirani-Kleiner AA, Azevedo JL (2004) Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ Microbiol 6:1244–1251

    Article  CAS  PubMed  Google Scholar 

  • Kuklinsky-Sobral J, Araújo WL, Mendes R, Pizzirani-Kleiner AA, Azevedo JL (2005) Isolation and characterization of endophytic bacteria from soybean (Glycine max) grown in soil treated with glyphosate herbicide. Plant Soil 273:91–99

    Article  CAS  Google Scholar 

  • Li L, Sinkko H, Montonen L, Wei GH, Lindström K, Räsänen LA (2012) Biogeography of symbiotic and other endophytic bacteria isolated from medicinal Glycyrrhiza species in China. FEMS Microbiol Ecol 79:46–68

    Article  CAS  PubMed  Google Scholar 

  • Li J, Huang LP, Lü HY, Wang XA (2013a) Distribution patterns of main populations of Ammodendron argenteum communities in the Takeermohuer Desert. Arid Zone Res 30:634–639

    CAS  Google Scholar 

  • Li J, Wang XA, Lü HY, Wang SX (2013b) Interspecific relationships of major species in Ammodendron argenteum communities of Takeermohuer Desert. Guihaia 33:482–487

    CAS  Google Scholar 

  • Lichter A, Barash I, Valinsky L, Manulis S (1995) The genes involved in cytokinin biosynthesis in Erwinia herbicola pv. gypsophilae: characterization and role in gall formation. J Bacteriol 177:4457–4465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo XY, Deng YB (1986) Anatomical observation of leaves and assimilative branches on several xerophytes structure in Xinjiang. J Xinjiang Univ 1:77–84

    Google Scholar 

  • Luo SL, Xu TY, Chen L, Chen JL, Rao C, Xiao X, Wan Y, Zeng GM, Long F, Liu CB, Liu YT (2012) Endophyte-assisted promotion of biomass production and metal-uptake of energy crop sweet sorghum by plant-growth-promoting endophyte Bacillus sp. SLS18. Appl Microbiol Biotechnol 93:1745–1753

    Article  CAS  PubMed  Google Scholar 

  • M’piga P, Bélanger RR, Paulitz TC, Benhamou N (1997) Increased resistance to Fusarium oxysporum f. sp. radicis-lycopersici in tomato plants treated with the endophytic bacterium Pseudomonas fluorescens strain 63-28. Physiol Mol Plant Pathol 50:301–320

    Article  Google Scholar 

  • Marasco R, Rolli E, Ettoumi B, Vigani G, Mapelli F, Borin S, Abou-Hadid AF, El-Behairy UA, Sorlini C, Cherif A, Zocchi G, Daffonchio D (2012) A drought resistance-promoting microbiome is selected by root system under desert farming. PLoS One 7:e0048479

    Article  CAS  Google Scholar 

  • Marasco R, Rolli E, Fusi M, Cherif A, Abou-Hadid A, El-Bahairy U, Borin S, Sorlini C, Daffonchio D (2013) Plant growth promotion potential is equally represented in diverse grapevine root-associated bacterial communities from different biopedoclimatic environments. BioMed Res Int 2013:491091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matilla AJ, Matilla-Vázquez MA (2008) Involvement of ethylene in seed physiology. Plant Sci 175:87–97

    Article  CAS  Google Scholar 

  • Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci 166:525–530

    Article  CAS  Google Scholar 

  • Michel BE, Kaufmann MR (1973) The osmotic potential of polyethylene glycol 6000. Plant Physiol 51:914–916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nair DN, Padmavathy S (2014) Impact of endophytic microorganisms on plants, environment and humans. Sci World J 2014:250693

    Article  Google Scholar 

  • Palaniappan P, Chauhan PS, Saravanan VS, Anandham R, Sa T (2010) Isolation and characterization of plant growth promoting endophytic bacterial isolates from root nodule of Lespedeza sp. Biol Fertil Soils 46:807–816

    Article  Google Scholar 

  • Petruzzelli L, Coraggio I, Leubner-Metzger G (2000) Ethylene promotes ethylene biosynthesis during pea seed germination by positive feedback regulation of 1-aminocyclo-propane-1-carboxylic acid oxidase. Planta 211:144–149

    Article  CAS  PubMed  Google Scholar 

  • Powell GK, Morris RO (1986) Nucleotide sequence and expression of a Pseudomonas savastanoi cytokinin biosynthetic gene: homology with Agrobacterium tumefaciens tmr and tzs loci. Nucleic Acids Res 14:2555–2565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pritchard SL, Charlton WL, Baker A, Graham IA (2002) Germination and storage reserve mobilization are regulated independently in Arabidopsis. Plant J 31:639–647

    Article  CAS  PubMed  Google Scholar 

  • Queiroz SEE, Da-Silva EAA, Davide AC, José AC, Silva AT, Fraiz ACR, Faria JMR, Hilhorst HWM (2012) Mechanism and control of Genipa americana seed germination. Physiol Plantarum 144:263–276

    Article  CAS  Google Scholar 

  • Rashid S, Charles TC, Glick BR (2012) Isolation and characterization of new plant growth-promoting bacterial endophytes. Appl Soil Ecol 61:217–224

    Article  Google Scholar 

  • Rolli E, Marasco R, Vigani G, Ettoumi B, Mapelli F, Deangelis ML, Gandolfi C, Casati E, Previtali F, Gerbino R, Cei FP, Borin S, Sorlini C, Zocchi G, Daffonchio D (2014) Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait. Environ Microbiol 17:316–331

    Article  PubMed  Google Scholar 

  • Rolli E, Marasco R, Saderi S, Corretto E, Mapelli F, Cherif A, Borin S, Valenti L, Sorlini C, Daffonchio D (2017) Root-associated bacteria promote grapevine growth: from the laboratory to the field. Plant Soil 410:369–382

    Article  CAS  Google Scholar 

  • Rosenblueth M, Martínez-Romero E (2004) Rhizobium etli maize populations and their competitiveness for root colonization. Arch Microbiol 181:337–344

    Article  CAS  PubMed  Google Scholar 

  • Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1–9

    Article  CAS  PubMed  Google Scholar 

  • Saravanakumar D, Kavino M, Raguchander T, Subbian P, Samiyappan R (2011) Plant growth promoting bacteria enhance water stress resistance in green gram plants. Acta Physiol Plant 33:203–209

    Article  CAS  Google Scholar 

  • Seghers D, Wittebolle L, Top EM, Verstraete W, Siciliano SD (2004) Impact of agricultural practices on the Zea mays L. endophytic community. Appl Environ Microbiol 70:1475–1482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sgroy V, Cassán F, Masciarelli O, Del Papa MF, Lagares A, Luna V (2009) Isolation and characterization of endophytic plant growth-promoting (PGPB) or stress homeostasis-regulating (PSHB) bacteria associated to the halophyte Prosopis strombulifera. Appl Microbiol Biotechnol 85:371–381

    Article  CAS  PubMed  Google Scholar 

  • Shelef O, Helman Y, Friedman ALL, Behar A, Rachmilevitch S (2013) Tri-party underground symbiosis between a weevil, bacteria and a desert plant. PloS One 8:e76588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi CY, Qi C, Ren HY, Huang AX, Hei SM, She XP (2015) Ethylene mediates brassinosteroid-induced stomatal closure via Gα protein-activated hydrogen peroxide and nitric oxide production in Arabidopsis. Plant J 82:280–301

    Article  CAS  PubMed  Google Scholar 

  • Soussi A, Ferjani R, Marasco R, Guesmi A, Cherif H, Rolli E, Mapelli F, Ouzari HI, Daffonchio D, Cherif A (2016) Plant-associated microbiomes in arid lands: diversity, ecology and biotechnological potential. Plant Soil 405:357–370

    Article  CAS  Google Scholar 

  • Sturz AV, Christie BR, Matheson BG, Nowak J (1997) Biodiversity of endophytic bacteria which colonize red clover nodules, roots, stems and foliage and their influence on host growth. Biol Fertil Soils 25:13–19

    Article  Google Scholar 

  • Sturz AV, Christie BR, Nowak J (2000) Bacterial endophytes: potential role in developing sustainable systems of crop production. Crit Rev Plant Sci 19:1–30

    Article  Google Scholar 

  • Surette MA, Sturz AV, Lada RR, Nowak J (2003) Bacterial endophytes in processing carrots (Daucus carota L. var. sativus): their localization, population density, biodiversity and their effects on plant growth. Plant Soil 253:381–390

    Article  CAS  Google Scholar 

  • Van Buren AM, Andre C, Ishimaru CA (1993) Biological control of the bacterial ring rot pathogen by endophytic bacteria isolated from potato. Phytopathology 83:1406 (Abstr.)

    Google Scholar 

  • Verma SC, Ladha JK, Tripathi AK (2001) Evaluation of plant growth promoting and colonization ability of endophytic diazotrophs from deep water rice. J Biotechnol 91:127–141

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Knill E, Glick BR, Défago G (2000) Effect of transferring 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase genes into Pseudomonas fluorescens strain CHA0 and its gac A derivative CHA96 on their growth-promoting and disease-suppressive capacities. Can J Microbiol 46:898–907

    Article  CAS  PubMed  Google Scholar 

  • Wang ET, Tan ZY, Guo XW, Rodríguez-Duran R, Boll G, Martínez-Romero E (2006) Diverse endophytic bacteria isolated from a leguminous tree Conzattia multiflora grown in Mexico. Arch Microbiol 186:251–259

    Article  CAS  PubMed  Google Scholar 

  • Weitbrecht K, Müller K, Leubner-Metzger G (2011) First off the mark: early seed germination. J Exp Bot 62:3289–3309

    Article  CAS  PubMed  Google Scholar 

  • Xinjiang Flora Editorial Committee (2011) Ammodendron bifolium (Pall.) Yakovl. In: Xinjiang flora, vol III. Xinjiang Science and Technology Press, Urumqi, pp 5–6

    Google Scholar 

  • Yaish MW, Antony I, Glick BR (2015) Isolation and characterization of endophytic plant growth-promoting bacteria from date palm tree (Phoenix dactylifera L.) and their potential role in salinity tolerance. Antonie Van Leeuwenhoek 107:1519–1532

    Article  CAS  PubMed  Google Scholar 

  • Yang SS, Bellogín RA, Buendía A, Camacho M, Chen M, Cubo T, Daza A, Díaz CL, Espuny MR, Gutiérrez R, Harteveld M, Li XH, Lyra MCCP, Madinabeitia N, Medina C, Miao L, Ollero FJ, Olsthoorn MMA, Rodríguez DN, Santamaría C, Schlaman HRM, Spaink HP, Temprano F, Thomas-Oates JE, Van Brussel AAN, Vinardell JM, Xie F, Yang J, Zhang HY, Zhen J, Zhou J, Ruiz-Sainz JE (2001) Effect of pH and soybean cultivars on the quantitative analyses of soybean rhizobia populations. J Biotechnol 91:243–255

    Article  CAS  PubMed  Google Scholar 

  • Yu X, Liu X, Zhu TH, Liu GH, Mao C (2011) Isolation and characterization of phosphate-solubilizing bacteria from walnut and their effect on growth and phosphorus mobilization. Biol Fertil Soils 47:437–446

    Article  CAS  Google Scholar 

  • Yu Y, Wang J, Shi H, Gu J, Dong J, Deng XW, Huang R (2016) Salt stress and ethylene antagonistically regulate nucleocytoplasmic partitioning of COP1 to control seed germination. Plant Physiol 170:2340–2350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zahir ZA, Munir A, Asghar HN, Shaharoona B, Arshad M (2008) Effectiveness of rhizobacteria containing ACC deaminase for growth promotion of peas (Pisum sativum) under drought conditions. J Microbiol Biotechnol 18:958–963

    CAS  PubMed  Google Scholar 

  • Zahir ZA, Ghani U, Naveed M, Nadeem SM, Asghar HN (2009) Comparative effectiveness of Pseudomonas and Serratia sp. containing ACC-deaminase for improving growth and yield of wheat (Triticum aestivum L.) under salt-stressed conditions. Arch Microbiol 191:415–424

    Article  CAS  PubMed  Google Scholar 

  • Zhu YL, She XP (2018) Evaluation of the plant-growth-promoting abilities of endophytic bacteria from the psammophyte Ammodendron bifolium. Can J Microbiol 64:253–264

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The work described here was supported by a grant from the National Natural Science Foundation of China (no. 31260060).

Author information

Authors and Affiliations

  1. College of Life Sciences, Xinjiang Normal University, Urumqi, 830054, Xinjiang, China

    Yanlei Zhu

  2. College of Life Sciences, Shaanxi Normal University, Xi’an, 710119, Shaanxi, China

    Yanlei Zhu

Authors
  1. Yanlei Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yanlei Zhu.

Ethics declarations

Conflict of interest

The author declares that there is no conflict of interest.

Additional information

Communicated by Erko Stackebrandt.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhu, Y. Isolation and identification of Ammodendron bifolium endophytic bacteria and the action mechanism of selected isolates-induced seed germination and their effects on host osmotic-stress tolerance. Arch Microbiol 201, 431–442 (2019). https://doi.org/10.1007/s00203-018-1582-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-018-1582-3

Keywords

Search

Navigation