Fungal Diversity

, Volume 54, Issue 1, pp 11–18 | Cite as

Endophytes and their role in phytoremediation

Review

Abstract

Many endophytes have been found to be resistant to heavy metals and/or capable of degrading organic contaminants, and endophyte-assisted phytoremediation has been documented as a promising technology for in situ remediation of contaminated soils. During the phytoremediation of heavy metals, the heavy-metal-resistant endophytes can enhance plant growth, decrease metal phytotoxicity, and affect metal translocation and accumulation in plants. For the phytoremediation of organic contaminants, endophytes can produce various enzymes to degrade organic contaminants and reduce both the phytotoxicity and evapotranspiration of volatile contaminants. This paper reviews the diversity of contaminant-resistant/degrading endophytes and their role in phytoremediation and discusses some issues that have been raised surrounding this area of research.

Keywords

Endophyte Remediation Toxic metals Organic chemicals Phytohormones Metals mobilization 

Notes

Acknowledgments

H.-Y. Li thanks the Natural Science Foundation of Yunnan Province (KKS0201126013) and the Science Foundation of Yunnan Educational Committee (KKJA201126033) for financial supports.

References

  1. Andria V, Reichenauer TG, Sessitsch A (2009) Expression of alkane monooxygenase (alkB) genes by plant-associated bacteria in the rhizosphere and endosphere of Italian ryegrass (Lolium multiflorum L.) grown in diesel contaminated soil. Environ Pollut 157:3347–3350PubMedCrossRefGoogle Scholar
  2. Balestrazzi A, Bonadei M, Quattrini E, Carbonera D (2009) Occurrence of multiple metal-resistance in bacterial isolates associated with transgenic white poplars (Populus alba L.). Ann Microbiol 59:17–23CrossRefGoogle Scholar
  3. Barzanti R, Ozino F, Bazzicalupo M, Gabbrielli R, Galardi F, Gonnelli C, Mengoni A (2007) Isolation and characterization of endophytic bacteria from the nickel hyperaccumulator Plant Alyssum bertolonii. Microb Ecol 53:306–316PubMedCrossRefGoogle Scholar
  4. Chen L, Luo S, Xiao X, Guo H, Chen J, WanY Li B, Xu T, Xi Q, Rao C, Liu C, Zeng G (2010) Application of plant growth-promoting endophytes (PGPE) isolated from Solanum nigrum L. for phytoextraction of Cd-polluted soils. Appl Soil Ecol 46:383–389CrossRefGoogle Scholar
  5. Chen Y, Peng Y, Dai C, Ju Q (2011) Biodegradation of 4-hydroxybenzoic acid by Phomopsis liquidambari. Appl Soil Ecol 51:102–110CrossRefGoogle Scholar
  6. Clay K, Holah J (1999) Fungal endophyte symbiosis and plant diversity in successional fields. Science 285:1742–1744PubMedCrossRefGoogle Scholar
  7. Davies PJ (2004) Plant hormones: biosynthesis, signal transduction, action! Kluwer Academic Publishers, DordrechtGoogle Scholar
  8. Deng Z, Cao L, Huang H, Jiang X, Wang W, Shi Y, Zhang R (2011) Characterization of Cd- and Pb-resistant fungal endophyte Mucor sp. CBRF59 isolated from rapes (Brassica chinensis) in a metal-contaminated soil. J Hazard Mater 185:717–724PubMedCrossRefGoogle Scholar
  9. Dory SL, Oakley B, Xin G, Kang JW, Singleton G, Khan Z, Vajzovic A, Staley JT (2009) Diazotrophic endophytes of native black cottonwood and willow. Symbiosis 47:23–33CrossRefGoogle Scholar
  10. Feng Y, Shen D, Song W (2006) Rice endophyte Pantoea agglomerans YS19 promotes host plant growth and affects allocations of host photosynthates. J Appl Microbiol 100:938–945PubMedCrossRefGoogle Scholar
  11. Gazis R, Rehner S, Chaverri P (2011) Species delimitation in fungal endophyte diversity studies and its implications in ecological and biogeographic inferences. Mol Ecol. doi: 10.1111/j.1365-294X.2011.05110.x
  12. Gerhardt KE, Huang XD, Glick BR, Greenberg BM (2009) Phytoremediation and rhizoremediation of organic soil contaminants: potential and challenges. Plant Sci 176:20–30CrossRefGoogle Scholar
  13. Germaine KJ, Liu X, Cabellos GG, Hogan JP, Ryan D, Dowling DN (2006) Bacterial endophyte-enhanced phytoremediation of the organochlorine herbicide 2,4-dichlorophenoxyacetic acid. FEMS Microbiol Ecol 57:302–310PubMedCrossRefGoogle Scholar
  14. Germaine KJ, Keogh E, Ryan D, Dowling D (2009) Bacterial endophyte-mediated naphthalene phytoprotection and phytoremediation. FEMS Microbiol Lett 296:226–234PubMedCrossRefGoogle Scholar
  15. Ghimire SR, Charlton ND, Bell JD, Krishnamurthy YL, Craven KD (2011) Biodiversity of fungal endophyte communities inhabiting switchgrass (Panicum virgatum L.) growing in the native tallgrass prairie of northern Oklahoma. Fungal Divers 47:19–27CrossRefGoogle Scholar
  16. Gonzalez V, Tello ML (2011) The endophytic mycota associated with Vitis vinifera in central Spain. Fungal Divers 47:29–42CrossRefGoogle Scholar
  17. Guo B, Wang Y, Sun X, Tang K (2008) Bioactive natural products from endophytes: a review. Appl Biochem Microbiol 44:136–142CrossRefGoogle Scholar
  18. Guo H, Luo S, Chen L, Xiao X, Xi Q, Wei W, Zeng G, Liu C, Wan Y, Chen J, He Y (2010) Bioremediation of heavy metals by growing hyperaccumulaor endophytic bacterium Bacillus sp. L14. Bioresour Technol 101:8599–8605PubMedCrossRefGoogle Scholar
  19. Hamayun M, Sumera AK, Iqbal I, Ahmad B, Lee I (2010) Isolation of a gibberellin-producing fungus (Penicillium sp. MH7) and growth promotion of crown daisy (Chrysanthemum coronarium). J Microbiol Biotechnol 20:202–207PubMedGoogle Scholar
  20. Hamilton CE, Bauerle TL (2012) A new currency for mutualism? fungal endophytes alter antioxidant activity in hosts responding to drought. Fungal Divers. doi: 10.1007/s13225-012-0156-y
  21. Hamilton CE, Gundel PE, Helander M, Saikkonen K (2012) Endophytic mediation of reactive oxygen species and antioxidant activity in plants: a review. Fungal Divers. doi: 10.1007/s13225-012-0158-9
  22. Hardoim PR, Overbeek LS, Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:467–471CrossRefGoogle Scholar
  23. Ho YN, Shih CH, Hsiao SC, Huang CC (2009) A novel endophytic bacterium, Achromobacter xylosoxidans, helps plants against pollutant stress and improves phytoremediation. Abstracts/J Biosci Bioeng 108:S75–S95Google Scholar
  24. Huo W, Zhuang C, Cao Y, Pu M, Yao H, Lou L, Cai Q (2012) Paclobutrazol and plant-growth promoting bacterial endophyte Pantoea sp. enhance copper tolerance of guinea grass (Panicum maximum) in hydroponic culture. Acta Physiol Plant 34:139–150CrossRefGoogle Scholar
  25. Hurek T, Reinhold-Hurek B (2003) Azoarcus sp. strain BH72 as a model for nitrogen-fixing grass endophytes. J Biotechnol 106:169–178PubMedCrossRefGoogle Scholar
  26. Hyde KD, Soytong K (2008) The fungal endophyte dilemma. Fungal Divers 33:163–173Google Scholar
  27. Idris R, Trifonova R, Puschenreiter M, Welzel WW, Seissitsch A (2004) Bacterial communities associated with flowering plants of the Ni hyperaccumulator Thlaspi goesingense. Appl Environ Microbiol 70:2667–2677PubMedCrossRefGoogle Scholar
  28. Kobayashi DY, Palumbo JD (2000) Bacterial endophytes and their effects on plants and uses in agriculture. In: Bacon CW, White JF (eds) Microbial endophytes. Marcel Dekker, New York, pp 199–236Google Scholar
  29. Kuffner M, Maria SD, Puschenreiter M, Fallmann K, Wieshammer G, Gorfer M, Strauss J, Rivelli AR, Sessitsch A (2010) Culturable bacteria from Zn- and Cd-accumulating Salix caprea with differential effects on plant growth and heavy metal availability. J Appl Microbiol 108:1471–1484PubMedCrossRefGoogle Scholar
  30. Kuklinsky-Sobral J, Araujo WL, Mendes R, Geraldi IO, Pizzirani-Kleine AA, Azevedo JL (2004) Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ Microbiol 6:1244–1251PubMedCrossRefGoogle Scholar
  31. Lebeau T, Braud A, Jézéquel K (2008) Performance of bioaugmentation-assisted phytoextraction applied to metal contaminated soils: a review. Environ Pollut 153:497–522PubMedCrossRefGoogle Scholar
  32. Li HY, Zhao CA, Liu CJ, Xu XF (2010) Endophytic fungi diversity of aquatic/riparian plants and their antifungal activity in vitro. J Microbiol 48:1–6PubMedCrossRefGoogle Scholar
  33. Li HY, Li DW, He CM, Zhou ZP, Mei T, Xu HM (2011) Diversity and heavy metal tolerance of endophytic fungi from six dominant plant species in a Pb-Zn mine wasteland in China. Fungal Ecol. doi: 10.1016/j.funeco.2011.06.002
  34. Lodewyckx C, Taghavi S, Mergeay M, Vangronsveld J, Clijsters H, van der Lelie D (2001) The effect of recombinant heavy metal resistant endophytic bacteria in heavy metal uptake by their host plant. Int J Phytoremediation 3:173–187CrossRefGoogle Scholar
  35. Lodewyckx C, Vangronsveld J, Porteous F, Moore ERB, Taghavi S, van der Lelie D (2002) Endophytic bacteria and their potential applications. Crit Rev Plant Sci 21:583–606CrossRefGoogle Scholar
  36. Luo S, Chen L, Chen J, Xiao X, Xu T, Wan Y, Rao C, Liu C, Liu Y, Lai C, Zeng G (2011) Analysis and characterization of cultivable heavy metal-resistant bacterial endophytes isolated from Cd-hyperaccumulator Solanum nigrum L. and their potential use for phytoremediation. Chemosphere 85:1130–1138PubMedCrossRefGoogle Scholar
  37. Ma Y, Rajkumar M, Luo Y, Freitas H (2011a) Inoculation of endophytic bacteria on host and non-host plants—effects on plant growth and Ni uptake. J Hazard Mater 195:230–237PubMedCrossRefGoogle Scholar
  38. Ma Y, Prasad MNV, Rajkumar M, Freitas H (2011b) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29:248–258PubMedCrossRefGoogle Scholar
  39. Madhaiyan M, Poonguzhali S, Sa T (2007) Metal tolerating methylotrophic bacteria reduces nickel and cadmium toxicity and promotes plant growth of tomato (Lycopersicon esculentum L.). Chemosphere 69:220–228PubMedCrossRefGoogle Scholar
  40. Mastretta C, Taghavi S, van der Lelie D, Mengoni A, Galardi F, Gonnelli C, Barac T, Boulet J, Weyens N, Vangronsveld J (2009) Endophytic bacteria from seeds of Nicotiana tabacum can reduce cadmium phytotoxicity. Int J Phytoremediation 11:251–267CrossRefGoogle Scholar
  41. Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42:565–572PubMedCrossRefGoogle Scholar
  42. Meagher RB (2000) Phytoremediation of toxic elemental and organic pollutants. Curr Opin Plant Biol 3:153–162PubMedCrossRefGoogle Scholar
  43. Miethke M, Marahiel MA (2007) Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 71:413–451PubMedCrossRefGoogle Scholar
  44. Moore FP, Barac T, Borremans B, Oeyen L, Vangronsveld J, Lelie D, Campbell CD, Moore ER (2006) Endophytic bacterial diversity in poplar trees growing on a BTEX-contaminated site: the characterisation of isolates with potential to enhance phytoremediation. Syst Appl Microbiol 29:539–556PubMedCrossRefGoogle Scholar
  45. Mouhamadou B, Molitor C, Baptist F, Sage L, Clément J, Lavorel S, Monier A, Geremia RA (2011) Differences in fungal communities associated to Festuca paniculata roots in subalpine grasslands. Fungal Divers 47:55–63CrossRefGoogle Scholar
  46. Muthukumarasamy R, Revathi G, Seshadri S, Lakshminarasimhan C (2002) Gluconacetobacter diazotrophicus (syn. Acetobacter diazotrophicus), a promising diazotrophic endophyte in tropics. Curr Sci 83:137–145Google Scholar
  47. Oelmüller R, Sherameti I, Tripathi S, Varma A (2009) Piriformospora indica, a cultivable root endophyte with multiple biotechnological applications. Symbiosis 49:1–17CrossRefGoogle Scholar
  48. Omacini M, Chaneton EJ, Ghersa CM, Müller CB (2001) Symbiotic fungal endophytes control insect host-parasite interaction webs. Nature 409:78–81PubMedCrossRefGoogle Scholar
  49. Phillips LA, Germida JJ, Farrell RE, Greer CW (2008) Hydrocarbon degradation potential and activity of endophytic bacteria associated with prairie plants. Soil Biol Biochem 40:3054–3064CrossRefGoogle Scholar
  50. Ping L, Boland W (2004) Signals from the underground: bacterial volatiles promote growth in Arabidopsis. Trends Plant Sci 9:263–266PubMedCrossRefGoogle Scholar
  51. Plackett ARG, Thomas SG, Wilson ZA, Hedden P (2011) Gibberellin control of stamen development: a fertile field. Trends Plant Sci 16:568–578PubMedCrossRefGoogle Scholar
  52. Puente ME, Li CY, Bashan Y (2009) Endophytic bacteria in cacti seeds can improve the development of cactus seedlings. Environ Exp Bot 66:402–408CrossRefGoogle Scholar
  53. Pulford ID, Watson C (2003) Phytoremediation of heavy metal-contaminated land by trees—a review. Environ Int 29:529–540PubMedCrossRefGoogle Scholar
  54. Purahong W, Hyde KD (2011) Effects of fungal endophytes on grass and non-grass litter decomposition rates. Fungal Divers 47:1–7CrossRefGoogle Scholar
  55. Raghukumar C (2008) Marine fungal biotechnology: an ecological perspective. Fungal Divers 31:5–19Google Scholar
  56. Rajkumar M, Ae N, Freitas H (2009) Endophytic bacteria and their potential to enhance heavy metal phytoextraction. Chemosphere 77:153–160PubMedCrossRefGoogle Scholar
  57. Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotech 28:142–149CrossRefGoogle Scholar
  58. Rivera-Orduña F, Suarez-Sanchez R, Flores-Bustamante Z, Gracida-Rodriguez J, Flores-Cotera L (2011) Diversity of endophytic fungi of Taxus globosa (Mexican yew). Fungal Divers 47:65–74CrossRefGoogle Scholar
  59. Robinson BH, Lombi E, Zhao FJ, McGrath SP (2003) Uptake and distribution of nickel and other metals in the hyperaccumulator Berkheya coddii. New Phytol 158:279–285CrossRefGoogle Scholar
  60. Rodriguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339PubMedCrossRefGoogle Scholar
  61. Rosa G, Peralta-Videa JR, Montes M, Parsons JG, Cano-Aguilera I, Gardea-Torresdey JL (2004) Cadmium uptake and translocation in tumbleweed (Salsola kali), a potential Cd-hyperaccumulator desert plant species: ICP/OES and XAS studies. Chemosphere 55:1159–1168PubMedCrossRefGoogle Scholar
  62. Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1–9PubMedCrossRefGoogle Scholar
  63. Saikkonen K, Saari S, Helander M (2010) Defensive mutualism between plants and endophytic fungi? Fungal Divers 41:101–113CrossRefGoogle Scholar
  64. Saravanan VS, Madhaiyan M, Thangaraju M (2007) Solubilization of zinc compounds by the diazotrophic, plant growth promoting bacterium Gluconacetobacter diazotrophicus. Chemosphere 66:1794–1798PubMedCrossRefGoogle Scholar
  65. Sheng X, Chen X, He L (2008a) Characteristics of an endophytic pyrene-degrading bacterium of Enterobacter sp. 12J1 from Allium macrostemon Bunge. Int Biodeterior Biodegrad 62:88–95CrossRefGoogle Scholar
  66. Sheng X, Xia J, Jiang C, He L, Qian M (2008b) 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 156:1164–1170PubMedCrossRefGoogle Scholar
  67. Shi Y, Lou K, Li C (2011) Growth promotion effects of the endophyte Acinetobacter johnsonii strain 3–1 on sugar beet. Symbiosis 54:159–166CrossRefGoogle Scholar
  68. Shin M, Shim J, You Y, Myung H, Bang K, Cho M, Kamala-Kannan S, Oh B (2011) Characterization of lead resistant endophytic Bacillus sp. MN3-4 and its potential for promoting lead accumulation in metal hyperaccumulator Alnus firma. J Hazard Mater. doi: 10.1016/j.jhazmat.2011.11.010
  69. Soleimani M, Afyuni M, Hajabbasi MA, Nourbakhsh F, Sabzalian MR, Christensen JH (2010) Phytoremediation ofan aged petroleum contaminated soil using endophyt infected and non-infected grasses. Chemosphere 81:1084–1090PubMedCrossRefGoogle Scholar
  70. Stone JK, Bacon CW, White JF (2000) An overview of endophytic microbes: endophytism defined. In: Bacon CW, White JF (eds) Microbial endophytes. Marcel Dekker, New York, pp 3–29Google Scholar
  71. Su YY, Guo LD, Hyde KD (2010) Response of endophytic fungi of Stipa grandis to experimental plant function group removal in Inner Mongolia steppe, China. Fungal Divers 43:93–101CrossRefGoogle Scholar
  72. Sun L, Zhang Y, He L, Chen Z, Wang Q, Qian M, Sheng X (2010) Genetic diversity and characterization of heavy metal-resistant-endophytic bacteria from two copper-tolerant plant species on copper mine wasteland. Bioresour Technol 101:501–509PubMedCrossRefGoogle Scholar
  73. Sun X, Guo LD, Hyde KD (2011) Community composition of endophytic fungi in Acer truncatum and their role in decomposition. Fungal Divers 47:85–95CrossRefGoogle Scholar
  74. Verma SC, Ladha JK, Tripathi AK (2001) Evaluation of plant growth promoting and colonization ability of endophytic diazotrophs from deep water rice. J Biotechnol 91:127–141PubMedCrossRefGoogle Scholar
  75. Wang Y, Li H, Zhao W, He X, Chen J, Geng X, Xiao M (2010) Induction of toluene degradation and growth promotion in corn and wheat by horizontal gene transfer within endophytic bacteria. Soil Biol Biochem 42:1051–1057CrossRefGoogle Scholar
  76. Werner T, Schmuülling T (2009) Cytokinin action in plant development. Curr Opin Plant Biol 12:527–538PubMedCrossRefGoogle Scholar
  77. Weyens N, Lelie D, Taghavi S, Newman L, Vangronsveld J (2009a) Exploiting plant–microbe partnerships to improve biomass production and remediation. Trends Biotechnol 27:591–598PubMedCrossRefGoogle Scholar
  78. Weyens N, van der Lelie D, Taghavi S, Vangronsveld J (2009b) Phytoremediation: plant–endophyte partnerships take the challenge. Curr Opin Biotechnol 20:248–254PubMedCrossRefGoogle Scholar
  79. Weyens N, Truyens S, Dupae J, Newman L, Taghavi S, Lelie D, Carleer R, Vangronsveld J (2010) Potential of the TCE-degrading endophyte Pseudomonas putida W619-TCE to improve plant growth and reduce TCE phytotoxicity and evapotranspiration in poplar cuttings. Environ Pollut 158:2915–2919PubMedCrossRefGoogle Scholar
  80. Weyens N, Truyens S, Saenen E, Boulet J, Dupae J, Taghavi S, Lelie D, Carleer R, Vangronsveld J (2011) Endophytes and their potential to deal with co-contamination of organic contaminants (toluene) and toxic metals (nickel) during phytoremediation. Int J Phytoremediation 13:244–255PubMedCrossRefGoogle Scholar
  81. Xiao X, Luo S, Zeng G, Wei W, Wan Y, Chen L, Guo H, Cao Z, Yang L, Chen J, Xi Q (2010) Biosorption of cadmium by endophytic fungus (EF) Microsphaeropsis sp. LSE10 isolated from cadmium hyperaccumulator Solanum nigrum L. Bioresour Technol 101:1668–1674PubMedCrossRefGoogle Scholar
  82. Yousaf S, Andria V, Reichenauer TG, Smalla K, Sessitsch A (2010) Phylogenetic and functional diversity of alkane degrading bacteria associate with Italian ryegrass (Lolium multiflorum) and Birdsfoot trefoil (Lotus corniculatus) in a petroleum oil-contaminated environment. J Hazard Mater 184:523–532PubMedCrossRefGoogle Scholar
  83. Yuan ZL, Rao LB, Chen YC, Zhang CL, Wu YG (2011) From pattern to process: species and functional diversity in fungal endophytes of Abies beshanzuensis. Fungal Biol 115:197–213PubMedCrossRefGoogle Scholar
  84. Zhang Y, He L, Chen Z, Zhang W, Wang Q, Qian M, Sheng X (2011) Characterization of lead-resistant and ACC deaminase-producing endophytic bacteria and their potential in promoting lead accumulation of rape. J Hazard Mater 186:1720–1725PubMedCrossRefGoogle Scholar

Copyright information

© The Mushroom Research Foundation 2012

Authors and Affiliations

  • Hai-Yan Li
    • 1
  • Da-Qiao Wei
    • 1
  • Mi Shen
    • 1
  • Zuo-Ping Zhou
    • 1
  1. 1.Faculty of Life Science and TechnologyKunming University of Science and TechnologyKunmingChina

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