Skip to main content

Advertisement

SpringerLink
Log in

Characteristics of endophytic bacteria from Polygonum hydropiper and their use in enhancing P-phytoextraction

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

Endophytes are significant for their ecological role in plants and potential applications in phytoremediation. Endophytic bacteria with plant-growth-promoting (PGP) characteristics are isolated as inoculants to enhance phytoremediation efficiency; however, few attempts have been made to isolate bacteria from phosphorus (P)-accumulating plants and study their roles in P-phytoextraction.

Method

Endophytic bacteria of P-accumulating herb Polygonum hydropiper were isolated and identified. The PGP traits including indole-3-acetic acid (IAA), siderophores, phosphate-solubilization etc. were characterized. Some endophytes were selected as the inoculants for a pot experiment in high P soil to investigate their role in P-phytoextraction.

Results

Thirty-five isolates were tolerant of high P and classified into 10 taxonomic groups. The production of indole-3-acetic acid into IAA acid and siderophores was dependent on strain species. Tricalcium phosphate (TCP)-solubilizing activity of these strains was associated with a decrease of pH but increases of organic acids production, while phytin-solubilizing activity was associated with a decrease of pH but increases of acid and alkaline phosphatase activities. In the six inoculants, five strains promoted stem and leaf growth of Polygonum hydropiper except for SLs08. P. hydropiper with inoculation of SLr02, SLr15, SLs13 and SLs18 showed significantly higher root length and surface area than the control plants. The inoculation with SLr15, SLs13 and SLs18 significantly enhanced stem and leaf P accumulation of P. hydropiper.

Conclusions

Endophytic bacteria with PGP traits exist in Polygonum hydropiper and strains SLr15, SLs13 and SLs18 greatly promoted plant growth and shoot P accumulation, offering the most potential as PGP inoculants for assisting P. hydropiper in P-phytoextraction.

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Allison SD, Vitousek PM (2005) Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biol Biochem 37:937–944

    CAS  Google Scholar 

  • Amaresan N, Jayakumar V, Kumar K, Thajuddin N (2012) Isolation and characterization of plant growth promoting endophytic bacteria and their effect on tomato (Lycopersicon esculentum) and chilli (Capsicum annuum) seedling growth. Ann Microbiol 62:805–810

    CAS  Google Scholar 

  • Balseiro-Romero M, Gkorezis P, Kidd PS, Van HJ, Weyens N, Monterroso C, Vangronsveld J (2017) Use of plant growth promoting bacterial strains to improve Cytisus striatus and Lupinus luteus development for potential application in phytoremediation. Sci Total Environ 581-582:676–688

    PubMed  CAS  Google Scholar 

  • Bashan Y, Kamnev AA, De-Bashan LE (2013) Tricalcium phosphate is inappropriate as a universal selection factor for isolating and testing phosphate-solubilizing bacteria that enhance plant growth: a proposal for an alternative procedure. Biol Fertil Soils 49:465–579

    CAS  Google Scholar 

  • Braud A, Jézéquel K, Bazot S, Lebeau T (2009) Enhanced phytoextraction of an agricultural Cr- and Pb-contaminated soil by bioaugmentation with siderophore-producing bacteria. Chemosphere 74:280–286

    PubMed  Google Scholar 

  • Busato J, Lima LS, Aguiar NO, Canellas LP, Olivares FL (2012) Changes in labile phosphorus forms during maturation of vermicompost enriched with phosphorus-solubilizing and diazotrophic bacteria. Bioresour Technol 110:390–395

    PubMed  CAS  Google Scholar 

  • Chen L, Luo S, Chen J, Wan Y, Liu C, Liu Y, Pang XY, Lai C, Zeng GM (2012) Diversity of endophytic bacterial populations associated with cd-hyperaccumulator plant Solanum nigrum L. grown in mine tailings. Appl Soil Ecol 62:24–30

    Google Scholar 

  • Chen L, Luo S, Li X, Wan Y, Chen J, Liu C (2014a) Interaction of cd-hyperaccumulator Solanum nigrum L. and functional endophyte Pseudomonas sp. Lk9 on soil heavy metals uptake. Soil Biol Biochem 68:300–308

    CAS  Google Scholar 

  • Chen B, Shen JG, Zhang XC, Pan FS, Yang XE, Feng Y (2014b) The endophytic bacterium, Sphingomonas SaMR12, improves the potential for zinc phytoremediation by its host, Sedum alfredii. PLoS One 9:e106826

    PubMed  PubMed Central  Google Scholar 

  • Chimwamurombe PM, Grönemeyer JL, Reinhold-Hurek B (2016) Isolation and characterization of culturable seed-associated bacterial endophytes from gnotobiotically grown Marama bean seedlings. FEMS Microbiol Ecol 92:fiw083

    PubMed  Google Scholar 

  • Croes S, Weyens N, Colpaert J, Vangronsveld J (2015) Characterization of the cultivable bacterial populations associated with field grown Brassica napus L.: an evaluation of sampling and isolation protocols. Environ Microbiol 17:2379–2392

    PubMed  CAS  Google Scholar 

  • Deng ZJ, Cao LX (2017) Fungal endophytes and their interactions with plants in phytoremediation: a review. Chemosphere 168:1100–1106

    PubMed  CAS  Google Scholar 

  • Forchetti G, Masciarelli O, Alemano S, Alvarez D, Abdala G (2007) Endophytic bacteria in sunflower (Helianthus annuus L.): isolation, characterization, and production of jasmonates and abscisic acid in culture medium. Appl Microbiol Biotechnol 76:1145–1152

    PubMed  CAS  Google Scholar 

  • Friedrich J, Eder W, Castaneda J, Doss M, Huber E, Ebner R, Kunz-Schughart LA (2007) A reliable tool to determine cell viability in complex 3-d culture: the acid phosphatase assay. J Biomol Screen 12:925–937

    PubMed  CAS  Google Scholar 

  • Gulati A, Sharma N, Vyas P, Sood S, Rahi P, Pathania V, Prasad R (2010) Organic acid production and plant growth promotion as a function of phosphate solubilization by Acinetobacter rhizosphaerae strain BIHB 723 isolated from the cold deserts of the trans-Himalayas. Arch Microbiol 192:975–983

    PubMed  CAS  Google Scholar 

  • Huang X, Li TX, Zhang XZ, Zheng ZC, Yu HY (2012) Growth, P accumulation, and physiological characteristics of two ecotypes of Polygonum hydropiper as affected by excess P supply. J Plant Nutr Soil Sci 175:293–302

    CAS  Google Scholar 

  • Kukla M, Płociniczak T, Piotrowska-Seget Z (2014) Diversity of endophytic bacteria in Lolium perenne and their potential to degrade petroleum hydrocarbons and promote plant growth. Chemosphere 117:40–46

    PubMed  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

    PubMed  CAS  Google Scholar 

  • Li HY, Wei DQ, Shen M, Zhou ZP (2012) Endophytes and their role in phytoremediation. Fungal Divers 54:11–18

    Google Scholar 

  • Li X, Geng XY, Xie RR, Fu L, Jiang JX, Gao L, Sun JZ (2016) The endophytic bacteria isolated from elephant grass (Pennisetum purpureum Schumach) promote plant growth and enhance salt tolerance of Hybrid pennisetum. Biotechnol Biofuel 9:190

    Google Scholar 

  • Liu FP, Liu HQ, Zhou HL, Dong ZG, Bai XH, Bai P, Qiao JJ (2014) Isolation and characterization of phosphate-solubilizing bacteria from betel nut (Areca catechu) and their effects on plant growth and phosphorus mobilization in tropical soils. Biol Fertil Soils 50:927–937

    CAS  Google Scholar 

  • Liu Z, Li YC, Zhang S, Fu Y, Fan X, Patel JS, Zhang M (2015) Characterization of phosphate-solubilizing bacteria isolated from calcareous soils. Appl Soil Ecol 96:217–224

    Google Scholar 

  • Liu D, Ye DH, Li TX, Zheng ZC, Zhang XZ (2017) Practicability of using Polygonum japonicum as a P accumulator for P phytoextraction from soil amended with swine manure. Appl Soil Ecol 112:11–17

    Google Scholar 

  • Lu RK (ed) (1999) Analysis of soil Agrochemistry. Chinese Agricultural Science and Technology Press, Beijing (in Chinese)

    Google Scholar 

  • Marques APGC, Moreira H, Franco AR, Rangel AOSS, Castro PML (2013) Inoculating Helianthus annuus (sunflower) grown in zinc and cadmium contaminated soils with plant growth promoting bacteria – Effects on phytoremediation strategies. Chemosphere 92:74–83

  • Marra LM, Soares CRFS, Oliveira SMD, Ferreira PAA, Soares BL, Carvalho RDF, Lima JMD, Moreira FMDS (2012) Biological nitrogen fixation and phosphate solubilization by bacteria isolated from tropical soils. Plant Soil 357:289–307

    CAS  Google Scholar 

  • Mendes GDO, Freitas ALMD, Pereira OL, Silva IRD, Vassilev NB, Costa MD (2014) Mechanisms of phosphate solubilization by bacterial isolates when exposed to different P sources. Ann Microbiol 64:239–249

    CAS  Google Scholar 

  • Mohammadi K (2012) Phosphorus solubilizing bacteria: occurrence, mechanisms and their role in crop production. Resour Environ 2:80–85

    Google Scholar 

  • Murphy J, Riley JP (1962) A modified solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    CAS  Google Scholar 

  • Oliveira CA, Alves VMC, Marriel IE, Gomes EA, Scotti MR, Carneiro CT, Guimarães CT, Schaffert RE, Sá NMH (2009) Phosphate solubilizing microorganisms isolated from rhizosphere of maize cultivated in an oxisol of the Brazilian Cerrado biome. Soil Biol Biochem 41:1782–1787

    CAS  Google Scholar 

  • Pagliari PH, Laboski CA (2012) Investigation of the inorganic and organic phosphorus forms in animal manure. J Environ Qual 41:901–910

    PubMed  CAS  Google Scholar 

  • Patten CL, & Glick BR (2002) Regulation of indoleacetic acid production in pseudomonas putida GR12-2 by tryptophan and the stationary-phase sigma factor Rpos. Can J Microbiol 48:635–642

  • Pikovskaya RI (1948) Mobilization of phosphorous in soil in connection with vital activity of some microbial species. Mikrobiologya 17:362–370

    CAS  Google Scholar 

  • Rajkumar M, Ae N, Freitas H (2009) Endophytic bacteria and their potential to enhance heavy metal phytoextraction. Chemosphere 77:153–160

    PubMed  CAS  Google Scholar 

  • Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28:142–149

    PubMed  CAS  Google Scholar 

  • Rajkumar M, Sandhya S, Prasad MNV, Freitas H (2012) Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol Adv 30:1562–1574

    PubMed  CAS  Google Scholar 

  • Richardson AE, Hadobas PA, Hayes JE (2001) Extracellular secretion of Aspergillus phytase from Arabidopsis roots enables plants to obtain phosphorus from phytate. Plant J 25:641–649

    PubMed  CAS  Google Scholar 

  • Scervino JM, Prieto MM, Della MI (2010) Soil fungal isolates produce different organic acid patterns involved in phosphates salts solubilization. Biol Fertil Soils 46:755–763

    CAS  Google Scholar 

  • Schalk IJ, Hannauer M, Braud A (2011) New roles for bacterial siderophores in metal transport and tolerance. Environ Microbiol 13:2844–2854

    PubMed  CAS  Google Scholar 

  • Schwyn R, Neilands JB (1987) Universal chemical assay for detection and estimation of siderophores. Anal Biochem 160:47–56

    PubMed  CAS  Google Scholar 

  • Sharma NC, Starnes DL, Sahi SV (2007) Phytoextraction of excess soil phosphorus. Environ Pollut 146:120–127

    PubMed  CAS  Google Scholar 

  • Shen J, Yuan L, Zhang J, Li HG, Bai ZH, Chen XP, Zhang WF, Zhang FS (2011) Phosphorus dynamics: from soil to plant. Plant Physiol 156:997–1005

    PubMed  PubMed Central  CAS  Google Scholar 

  • Sheng XF, Xia JJ, Jiang CY, He LY, Qian M (2008) Characterization of heavy metal-resistant endophytic bacteria from rape (Brassica napus) roots and their potential in promoting the growth and lead accumulation of rape. Environ Pollut 156:1164–1170

    PubMed  CAS  Google Scholar 

  • Shi YN, Xie HR, Cao LX, Zhang RD, Xu ZC, Wang ZY, Deng ZJ (2017) Effects of cd-and Pb-resistant endophytic bacteria on growth and phytoextraction of Brassica napus in metal-contaminated soils. Environ Sci Pollut Res 24:417–426

    CAS  Google Scholar 

  • Sun LN, Zhang YF, He LY, Chen ZJ, Wang QY, Qian M, Sheng XF (2010) Genetic diversity and characterization of heavy metal-resistant-endophytic bacteria from two copper-tolerant plant species on copper mine wasteland. Bioresour Technol 101:501–509

    PubMed  CAS  Google Scholar 

  • Tao GC, Tian SJ, Cai MY, Xie GH (2008) Phosphate-solubilizing and -mineralizing abilities of bacteria isolated from soils. Pedosphere 18:515–523

    CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The clustal-x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    PubMed  PubMed Central  CAS  Google Scholar 

  • Tiwari S, Sarangi BK, Thul ST (2016) Identification of arsenic resistant endophytic bacteria from Pteris vittata roots and characterization for arsenic remediation application. J Environ Manag 180:359–365

    CAS  Google Scholar 

  • Vangronsveld J, Herzig R, Weyens N, Boulet J, Adriaensen K, Ruttens A, Thewys T, Vassilev A, Meers E, Nehnevajova E, Lelie DVD, Mench M (2009) Phytoremediation of contaminated soils and groundwater: lessons from the field. Environ Sci Pollut Res 16:765–794

    CAS  Google Scholar 

  • Vazquez P, Holguin G, Puente ME, Lopezcortez A, Bashan Y (2000) Phosphate-solubilizing microorganisms associated with the rhizosphere of mangroves in a semiarid coastal lagoon. Biol Fertil Soils 30:460–468

    CAS  Google Scholar 

  • Wang D, Marschner P, Solaiman Z, Rengel Z (2007) Growth, P uptake and rhizosphere properties of intercropped wheat and chickpea in soil amended with iron phosphate or phytate. Soil Biol Biochem 39:249–256

    CAS  Google Scholar 

  • Weisburg WG, Barns SW, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    PubMed  PubMed Central  CAS  Google Scholar 

  • Xia Y, Debolt S, Dreyer J, Scott D, Williams MA (2015) Characterization of culturable bacterial endophytes and their capacity to promote plant growth from plants grown using organic or conventional practices. Front Plant Sci 6:490

    PubMed  PubMed Central  Google Scholar 

  • Xiao GL, Li TX, Zhang XZ, Yu HY, Huang HG, Gupta DK (2009) Uptake and accumulation of phosphorus by dominant plant species growing in a phosphorus mining area. J Hazard Mater 171:542–550

    PubMed  CAS  Google Scholar 

  • Yi YHW, Ge Y (2008) Exopolysaccharide: a novel important factor in the microbial dissolution of tricalcium phosphate. World J Microbiol Biotechnol 24:1059–1065

    CAS  Google Scholar 

  • Zhu J, Li M, Whelan M (2018) Phosphorus activators contribute to legacy phosphorus availability in agricultural soils: a review. Sci Total Environ 612:522–537

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was funded by grant from the National Natural Science Foundation of China (41671323) and the Sichuan Science and Technology Support Project (2013NZ0044). We appreciate Prof. Hans Lambers and Dr. Ann Hamblin in The University of Western Australia for their edit on this manuscript.

Author information

Authors and Affiliations

  1. College of Resources, Sichuan Agricultural University, 211 Huimin Road, Chengdu, 611130, Sichuan, China

    Daihua Ye, Tingxuan Li, Yuanjun Yi, Likou Zou, Xizhou Zhang & Min Xie

  2. College of Economics, Sichuan Agricultural University, 211 Huimin Road, Chengdu, 611130, Sichuan, China

    Jiangbo Liu

Authors
  1. Daihua Ye
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tingxuan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jiangbo Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yuanjun Yi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Likou Zou
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xizhou Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Min Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tingxuan Li.

Ethics declarations

Conflict of interest

We declare no conflicts of interest.

Additional information

Responsible Editor: Tim S. George.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 160 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ye, D., Li, T., Liu, J. et al. Characteristics of endophytic bacteria from Polygonum hydropiper and their use in enhancing P-phytoextraction. Plant Soil 448, 647–663 (2020). https://doi.org/10.1007/s11104-020-04456-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-020-04456-w

Keywords

Search

Navigation