Skip to main content

Advertisement

Log in

Endophytic bacterium Buttiauxella sp. SaSR13 improves plant growth and cadmium accumulation of hyperaccumulator Sedum alfredii

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Inoculation with endophytic bacterium has been considered as a prospective application to improve the efficiency of phytoextraction. In this study, the effect of Buttiauxella sp. SaSR13 (SaSR13), a novel endophytic bacterium isolated from the root of hyperaccumulator Sedum alfredii, on plant growth and cadmium (Cd) accumulation in S. alfredii was investigated. Laser scanning confocal microscopic (LSCM) images showed that SaSR13 was mainly colonized in the root elongation and mature zones. The inoculation with SaSR13 to Cd-treated plants significantly enhanced plant growth (by 39 and 42% for shoot and root biomass, respectively), chlorophyll contents (by 38%), and Cd concentration in the shoot and root (by 32 and 22%, respectively). SaSR13 stimulated the development of roots (increased root length, surface area, and root tips number) due to an increase in the indole-3-acid (IAA) concentrations and a decrease in the concentrations of superoxide anion (O2.−) in plants grown under Cd stress. Furthermore, inoculation with SaSR13 enhanced the release of root exudates, especially malic acid and oxalic acid, which might have facilitated the uptake of Cd by S. alfredii. It is suggested that inoculation with endophytic bacterium SaSR13 is a promising bioaugmentation method to enhance the Cd phytoextraction efficiency by S. alfredii.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Abou-Shanab RA, Ghozlan H, Ghanem K, Moawad H (2005) Behaviour of bacterial populations isolated from rhizosphere of Diplachne fusca dominant in industrial sites. World J Microbiol Biotechnol 21:1095–1101

    Article  CAS  Google Scholar 

  • Babu AG, Shea PJ, Sudhakar D, Jung IB, Oh BT (2015) Potential use of Pseudomonas koreensis AGB-1 in association with Miscanthus sinensis to remediate heavy metal(loid)-contaminated mining site soil. J Environ Manag 151:160–166

    Article  CAS  Google Scholar 

  • Bonnet M, Camares O, Veisseire P (2000) Effects of zinc and influence of Acremonium lolii on growth parameters, chlorophyll a fluorescence and antioxidant enzyme activities of ryegrass (Lolium perenne L. cv Apollo). J Exp Bot 51:945–953

    CAS  Google Scholar 

  • Chelius MK, Triplett EW (2000) Immunolocalization of dinitrogenase reductase produced by Klebsiella pneumoniae in association with Zea mays L. Appl Environ Microbiol 66:783–787

    Article  CAS  Google Scholar 

  • Chen B, Zhang Y, Rafiq MT, Khan KY, Pan F, Yang X, Feng Y (2014a) Improvement of cadmium uptake and accumulation in Sedum alfredii by endophytic bacteria Sphingomonas SaMR12: effects on plant growth and root exudates. Chemosphere 117:367–373

    Article  CAS  Google Scholar 

  • Chen L, Luo SL, Li XJ, Wan Y, Chen JL, Liu CB (2014b) Interaction of Cd-hyperaccumulator Solanum nigrum L. and functional endophyte Pseudomonas sp. Lk9 on soil heavy metals uptake. Soil Biol Biochem 68:300–308

    Article  CAS  Google Scholar 

  • Cunningham SD, Ow DW (1996) Promises and prospects of phytoremediation. Plant Physiol 110:715–719

    Article  CAS  Google Scholar 

  • Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245:35–47

    Article  CAS  Google Scholar 

  • Elbeltagy A, Nishioka K, Sato T, Suzuki H, Ye B, Hamada T, Isawa T, Mitsui H, Minamisawa K (2001) Endophytic colonization and in planta nitrogen fixation by a Herbaspirillum sp. isolated from wild rice species. Appl Environ Microbiol 67:5285–5293

    Article  CAS  Google Scholar 

  • Fan L-M, Ma Z-Q, Liang J-Q, Li H-F, Wang E-T, Wei G-H (2011) Characterization of a copper-resistant symbiotic bacterium isolated from Medicago lupulina growing in mine tailings. Bioresour Technol 102:703–709

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hardoim PR, van Overbeek LS, van Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471

    Article  CAS  Google Scholar 

  • He H, Ye Z, Yang D, Yan J, Xiao L, Zhong T, Yuan M, Cai X, Fang Z, Jing Y (2013) Characterization of endophytic Rahnella sp. JN6 from Polygonum pubescens and its potential in promoting growth and Cd, Pb, Zn uptake by Brassica napus. Chemosphere 90:1960–1965

    Article  CAS  Google Scholar 

  • Hinsinger P, Plassard C, Tang C, Jaillard B (2003) Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review. Plant Soil 248:43–59

    Article  CAS  Google Scholar 

  • Hou S, Zhu J, Ding M, Lv G (2008) Simultaneous determination of gibberellic acid, indole-3-acetic acid and abscisic acid in wheat extracts by solid-phase extraction and liquid chromatography-electrospray tandem mass spectrometry. Talanta 76:798–802

  • Jin XF, Yang XE, Islam E, Liu D, Mahmood Q (2008) Effects of cadmium on ultrastructure and antioxidative defense system in hyperaccumulator and non-hyperaccumulator ecotypes of Sedum alfredii Hance. J Hazard Mater 156:387-397

  • Khan AG, Kuek C, Chaudhry TM, Khoo CS, Hayes WJ (2000) Role of plants, mycorrhizae and phytochelators in heavy metal contaminated land remediation. Chemosphere 41:197–207

  • Khan Z, Roman D, Kintz T, Alas MD, Yap R, Doty S (2014) Degradation, Phytoprotection and phytoremediation of phenanthrene by endophyte Pseudomonas putida, PD1. Environ Sci Technol 48:12221–12228

    Article  CAS  Google Scholar 

  • Kumar P, Dushenkov V, Motto H, Raskin I (1995) Phytoextraction—the use of plants to remove heavy-metals from soils. Environ Sci Technol 29:1232–1238

    Article  CAS  Google Scholar 

  • Lebeau T, Braud A, Jezequel K (2008) Performance of bioaugmentation-assisted phytoextraction applied to metal contaminated soils: a review. Environ Pollut 153:497–522

    Article  CAS  Google Scholar 

  • Li TQ, Di ZZ, Han X, Yang XE (2012) Elevated CO2 improves root growth and cadmium accumulation in the hyperaccumulator Sedum alfredii. Plant Soil 354:325–334

    Article  CAS  Google Scholar 

  • Li WC, Ye ZH, Wong MH (2010) Metal mobilization and production of short-chain organic acids by rhizosphere bacteria associated with a Cd/Zn hyperaccumulating plant, Sedum alfredii. Plant Soil 326:453–467

    Article  CAS  Google Scholar 

  • Lichtenthaler HK, Wellburn AR (1983) Determination of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592

    Article  CAS  Google Scholar 

  • Lin L, Guo W, Xing Y, Zhang X, Li Z, Hu C, Li S, Li Y, An Q (2012) The actinobacterium Microbacterium sp. 16SH accepts pBBR1-based pPROBE vectors, forms biofilms, invades roots, and fixes N(2) associated with micropropagated sugarcane plants. Appl Microbiol Biotechnol 93:1185–1195

    Article  CAS  Google Scholar 

  • Liu D, Islam E, Li T, Yang X, Jin X, Mahmood Q (2008) Comparison of synthetic chelators and low molecular weight organic acids in enhancing phytoextraction of heavy metals by two ecotypes of Sedum alfredii Hance. J Hazard Mater 153:114–122

    Article  CAS  Google Scholar 

  • Liu W, Zhang CJ, Hu P, Luo YM, Wu LH, Sale P, Tang C (2016) Influence of nitrogen forms on the phytoextraction of cadmium by a newly discovered hyperaccumulator Carpobrotusrossii. Environ Sci Pollut Res 23:1246–1253

  • Lodewyckx C, Vangronsveld J, Porteous F, Moore ERB, Taghavi S, Mezgeay M, van der Lelie D (2002) Endophytic bacteria and their potential applications. Crit Rev Plant Sci 21:583–606

    Article  Google Scholar 

  • Lu LL, Tian SK, Yang XE, Peng HY, Li TQ (2013) Improved cadmium uptake and accumulation in the hyperaccumulator Sedum alfredii: the impact of citric acid and tartaric acid. J Zhejiang University-SCIENCE B 14:106–114

  • Luo K, Ma T, Liu H, Wu L, Ren J, Nai F, Li R, Chen L, Luo Y, Christie P (2015) Efficiency of repeated phytoextraction of cadmium and zinc from an agricultural soil contaminated with sewage sludge. Int J Phytoremediation 17:575–582

    Article  CAS  Google Scholar 

  • Ma Y, Rajkumar M, Vicente JAF, Freitas H (2011) Inoculation of Ni-resistant plant growth promoting bacterium Psychrobacter sp. strain SRS8 for the improvement of nichel phytoextraction by energy crops. Int J Phytoremediation 13:126–139

    Article  CAS  Google Scholar 

  • Ma Y, Rajkumar M, Luo YM, Freitas H (2013) Phytoextraction of heavy metal polluted soils using Sedum plumbizincicola inoculated with metal mobilizing Phyllobacterium myrsinacearum RC6b. Chemosphere 93:1386–1392

    Article  CAS  Google Scholar 

  • McGrath SP, Zhao FJ (2003) Phytoextraction of metals and metalloids from contaminated soils. Curr Opin Biotechnol 14:277–282

    Article  CAS  Google Scholar 

  • Meers E, Tack FM, Van SS, Ruttens A, Du LG, Vangronsveld J, Verloo MG (2008) Chemically assisted phytoextraction: a review of potential soil amendments for increasing plant uptake of heavy metals. Int J Phytoremediation 10:390–414

    Article  CAS  Google Scholar 

  • Muratova A, Lyubun Y, German K, Turkovskaya O (2015) Effect of cadmium stress and inoculation with a heavy-metal-resistant bacterium on the growth and enzyme activity of Sorghum bicolor. Environ Sci Pollut Res 22:16098–16109

    Article  CAS  Google Scholar 

  • Park JH, Bolan N, Megharaj M, Naidu R (2011) Isolation of phosphate solubilizing bacteria and their potential for lead immobilization in soil. J Hazard Mater 185:829–836

    Article  CAS  Google Scholar 

  • Pavlo A, Leonid O, Iryna Z, Natalia K, Annamaria P (2011) Endophytic bacteria enhancing growth and disease resistance of potato (Solanum tuberosum L.). Biol Control 56:43–49

    Article  Google Scholar 

  • Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol Plant 118:10–15

    Article  CAS  Google Scholar 

  • Porra RJ (2002) The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosynth Res 73:149–156

    Article  CAS  Google Scholar 

  • Prasad MNV (2003) Phytoremediation of metal-polluted ecosystems: hype for commercialization. Russ J Plant Physiol 50:686–700

    Article  CAS  Google Scholar 

  • Saravanan VS, Madhaiyan M, Thangaraju M (2007) Solubilization of zinc compounds by the diazotrophic, plant growth promoting bacterium Gluconacetobacter diazotrophicus. Chemosphere 66:1794–1798

    Article  CAS  Google Scholar 

  • Sarwar M, Kremer RJ (1995) Enhanced suppression of plant-growth through production of l-tryptophan-derived compounds by deleterious rhizobacteria. Plant Soil 172:261–269

    Article  CAS  Google Scholar 

  • Sessitsch A, Kuffner M, Kidd P, Vangronsveld J, Wenzel WW, Fallmann K, Puschenreiter M (2013) The role of plant-associated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils. Soil Biol Biochem 60:182–194

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Sheng X, Sun L, Huang Z, He L, Zhang W, Chen Z (2012) Promotion of growth and Cu accumulation of bio-energy crop (Zea mays) by bacteria: implications for energy plant biomass production and phytoremediation. J Environ Manag 103:58–64

    Article  CAS  Google Scholar 

  • Sheng XF, Xia JJ, Jiang CY, He LY, Qian M (2008a) 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

    Article  CAS  Google Scholar 

  • Sheng X, He L, Wang Q, Ye H, Jiang C (2008b) Effects of inoculation of biosurfactant-producing Bacillus sp. J119 on plant growth and cadmium uptake in a cadmium-amended soil. J Hazard Mater 155:17–22

  • Sherameti I, Tripathi SV, Ajit, Oelmueller R (2008) The root-colonizing endophyte Pirifomosporaindica confers drought tolerance in Arabidopsis by stimulating the expression of drought stress-related genes in leaves. Am Phytopathol Soc 21:799–807

    CAS  Google Scholar 

  • Shi YW, Lou K, Li C (2010) Growth and photosynthetic efficiency promotion of sugar beet (Beta vulgaris L.) by endophytic bacteria. Photosynth Res 105:5–13

    Article  CAS  Google Scholar 

  • Taghavi S, Garafola C, Monchy S, Newman L, Hoffman A, Weyens N, Barac T, Vangronsveld J, van der Lelie D (2009) Genome survey and characterization of endophytic bacteria exhibiting a beneficial effect on growth and development of poplar trees. Appl Environ Microbiol 75:748–757

    Article  CAS  Google Scholar 

  • Tang B, Zhang L, Hu JX, Li P, Zhang H, Zhao YX (2004) Indirect determination of superoxide anion radical in the plant of red sage based on vanillin-8-aminoquinoline with fluorescence. Anal Chim Acta 502:125–131

    Article  CAS  Google Scholar 

  • Tao Q, Hou DD, Yang XE, Li TQ (2016) Oxalate secretion from the root apex of Sedum alfredii contributes to hyperaccumulation of Cd. Plant Soil 398:139–152

    Article  CAS  Google Scholar 

  • Tian SK, Lu LL, Labavitch J, Yang XE, He ZL, Hu HN, Sarangi R, Newville M, Commisso J, Brown P (2011) Cellular sequestration of cadmium in the hyperaccumulator plant species Sedum alfredii. Plant Physiol 157:1914–1925

    Article  CAS  Google Scholar 

  • Tsavkelova EA, Cherdyntseva TA, Klimova SY, Shestakov AI, Botina SG, Netrusov AI (2007) Orchid-associated bacteria produce indole-3-acetic acid, promote seed germination, and increase their microbial yield in response to exogenous auxin. Arch Microbiol 188:655–664

    Article  CAS  Google Scholar 

  • Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Huckelhoven R, Neumann C, von Wettstein D, Franken P, Kogel KH (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci U S A 102:13386–13391

    Article  CAS  Google Scholar 

  • Wei S, Li Y, Zhou Q, Srivastava M, Chiu S, Zhan J, Wu Z, Sun T (2010) Effect of fertilizer amendments on phytoremediation of Cd-contaminated soil by a newly discovered hyperaccumulator Solanum nigrum L. J Hazard Mater 176:269–273

    Article  CAS  Google Scholar 

  • Wood JL, Tang C, Franks AF (2016) Microbial associated plant growth and heavy metal accumulation to improve phytoextraction of contaminated soils. Soil Biol Biochem 103:131–137

    Article  CAS  Google Scholar 

  • Yang XE, Long XX, Ye HB, He ZL, Calvert DV, Stoffella PJ (2004a) Cadmium tolerance and hyperaccumulation in a new Zn-hyperaccumulating plant species (Sedum alfredii Hance). Plant Soil 259:181–189

    Article  CAS  Google Scholar 

  • Yang XE, Ye HB, Long XX, He B, He ZL, Stoffella PJ, Calvert DV (2004b) Uptake and accumulation of cadmium and zinc by Sedum alfredii Hance at different Cd/Zn supply levels. J Plant Nutr 27:1963–1977

  • Zhang X, Lin L, Zhu Z, Yang X, Wang Y, An Q (2013) Colonization and modulation of host growth and metal uptake by endophytic bacteria of Sedum alfredii. Int J Phytoremediation 15:51–64

    Article  CAS  Google Scholar 

  • Zhang XX, Li CJ, Nan ZB (2010) Effects of cadmium stress on growth and anti-oxidative systems in Achnatherum inebrians symbiotic with Neotyphodium gansuense. J Hazard Mater 175:703–709

    Article  CAS  Google Scholar 

  • Zhao FJ, Hamon RE, McLaughlin MJ (2001) Root exudates of the hyperaccumulator Thlaspi caerulescens do not enhance metal mobilization. New Phytol 151:613–620

    Article  CAS  Google Scholar 

  • Zhou W, Qiu B (2005) Effects of cadmium hyperaccumulation on physiological characteristics of Sedum alfredii Hance (Crassulaceae). Plant Sci 169:737–745

    Article  CAS  Google Scholar 

  • Zhu E, Liu D, Li JG, Li TQ, Yang XE, He ZL, Stoffella PJ (2010) Effect of nitrogen fertilizer on growth and cadmium accumulation in Sedum alfredii Hance. J Plant Nutr 34:115–126

    Article  CAS  Google Scholar 

  • Zhu L-J, Guan D-X, Luo J, Rathinasabapathi B, Ma LQ (2014) Characterization of arsenic-resistant endophytic bacteria from hyperaccumulators Pteris vittata and Pteris multifida. Chemosphere 113:9–16

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Prof. Caixian Tang (La Trobe University, Australia), Dr. Ejazul Islam (National Institute for Biotechnology and Genetic Engineering, Pakistan), and Dr. Jiale Xu (University of California Davis, CA, USA) for their constructive comments and manuscript revision.

Funding

This research was supported by the National Natural Science Foundation of China (21477104, 41671315) and National Key Research and Development Projects of China (2016YFD0800802).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tingqiang Li.

Additional information

Responsible editor: Yi-ping Chen

Electronic supplementary material

Table S1

(DOCX 22 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wu, K., Luo, J., Li, J. et al. Endophytic bacterium Buttiauxella sp. SaSR13 improves plant growth and cadmium accumulation of hyperaccumulator Sedum alfredii. Environ Sci Pollut Res 25, 21844–21854 (2018). https://doi.org/10.1007/s11356-018-2322-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-018-2322-6

Keywords

Navigation