Elsevier

Chemosphere

Volume 168, February 2017, Pages 1100-1106
Chemosphere

Review
Fungal endophytes and their interactions with plants in phytoremediation: A review

https://doi.org/10.1016/j.chemosphere.2016.10.097Get rights and content

Highlights

  • Most fungi exhibit better traits for bioremediation.

  • Endophytic fungi showed potentials to enhance phytoremediation.

  • The interaction of endophytic fungi with plants were reviewed.

Abstract

Endophytic microorganisms (including bacteria and fungi) are likely to interact closely with their hosts and are more protected from adverse changes in the environment. The microbiota contribute to plant growth, productivity, carbon sequestration, and phytoremediation. Elevated levels of contaminants (i.e. metals) are toxic to most plants, the plant's metabolism and growth were impaired and their potential for metal phytoextraction is highly restricted. Exploiting endophytic microorganisms to reduce metal toxicity to plants have been investigated to improve phytoremediation efficiencies. Fungi play an important role in organic and inorganic transformation, element cycling, rock and mineral transformations, bioweathering, mycogenic mineral formation, fungal-clay interactions, and metal-fungal interactions. Endophytic fungi also showed potentials to enhance phytoremediation. Compared to bacteria, most fungi exhibit a filamentous growth habit, which provides the ability to adopt both explorative or exploitative growth strategies and form linear organs of aggregated hyphae to protect fungal translocation. However, the information regarding the role of endophytic fungi in phytoremediation are incomplete, this review highlights the taxa, physiological properties, and interaction of endophytic fungi with plants in phytoremediation.

Introduction

The collective communities of plant-associated microorganisms are referred to as the plant microbiome or as the plants’ other genome. In this context, plants can be viewed as superorganisms that rely in part on their microbiome for specific functions and traits (Mendes et al., 2013). The microbiota colonizing the rhizosphere and the endophytic compartment contribute to plant growth, productivity, carbon sequestration and phytoremediation. Endophytic microorganisms can be defined as microorganisms that colonize the internal tissue of the plant without causing visible external sign of infection or a negative effect of the host (Weyens et al., 2009). Root rhizosphere and endophytic compartment microbiota of plants grown under controlled conditions in natural soils are sufficiently dependent on the host to remain consistent across different soil types, developmental stages and host genotype (Lundberg et al., 2012). Since endophytic microorganisms (including bacteria and fungi) can proliferate within the plant tissue, they are likely to interact closely with their host and therefore face less competition for nutrients and are more protected from adverse changes in the rhizosphere and phyllosphere environments. The microbiome within plant roots can differ significantly from that whithin the rhizosphere (Gaiero et al., 2013, Kristin and Miranda, 2013). Endophyte community structure (species diversity, richness and relative abundances) within the plant is dynamic and is influenced by abiotic and biotic factors such as soil conditions, biogeography, plant species, microbe-microbe and plant-microbe interactions. Endophytic microbiota may show more potential in phytoremediation than rhizosphere microbes.

Phytoremediation is based on the natural ability of plants to extract chemicals from water, soil, and air, which is much more cost effective than the traditional remediation technologies (Khan and Doty, 2011). It has been used to treat a wide variety of chemicals including metals, organics, excess nutrients, and radionuclides. Phytoremediation of metals and other inorganic compounds may take one of several forms: phytoextraction, rhizofiltration, phytostabilization and phytovolatilization (Glick, 2003). The major constraints of phytoremediation are the phytotoxicity, small plant size, slow degradation, limited contaminant uptake and evotranspiration of volatile contaminants. The success of phytoremediation is strongly determined by the amount of plant biomass present and the concentration of heavy metals in plant tissues. The high uptake and efficient root-to-shoot transport system endowed with enhanced metal tolerance provide hyperaccumulators with a high potential detoxification potential. However, most hyperaccumulators are not suitable for phytoremediation applications in the field owing to their small biomass and slow growth rate (Rajkumar et al., 2009). Since elevated levels of metals are toxic to most plants, which leads to impaired metabolism, reduced plant growth, and restricted metal phytoextraction. It is necessary to develop other phytoremediation strategies for heavy metal contaminated soils.

The interface between microorganisms and plant roots is considered to greatly influence the growth and survival of plants. The features of rhizosphere microorganisms resistant to heavy metals and/or promoting plant growth may lead to ecologically friendly and cost-effective strategies towards reclamation of heavy metal polluted soils. The exploitation of metal resistant endophytic microorganisms is also important for host plants because they can provide nutrients to plants, and metabolites produced by the microorganisms could enhance metal bioavailability in the rhizosphere of plants (Rajkumar et al., 2010). The resulting increase in trace metal uptake by the plants should enhance the effectiveness of phytoextraction processes of contaminated soil. The various metabolic pathways employed by endophytes make them valuable resources for bioremediation, which can be used for bioremediation of pollutants and biotransformation of organic substances (Stepniewska and Kuzniar, 2013). Nevertheless, microbial activities are constrained by environmental factors, such as regional climate, soil characteristics, and vegetation. Plants can provide shelter for microbes during severe environmental conditions, also assist the microbes in reducing ambient environmental stress (Zhao et al., 2013). Endophytic bacteria and their potential to improve phytoremediation have been studied and reviewed (Barac et al., 2004, Rajkumar et al., 2009, Weyens et al., 2009a, Luo et al., 2011, Li et al., 2012a, Langella et al., 2014). However, the investigations have been mostly focused on endophytic bacteria, while fungi have been largely ignored as constituents of the host microbiota (Moyes and Naglik, 2012). Endophytic fungi possess suitable metal sequestration or chelation systems to increase their tolerance to heavy metals and their higher biomass is also suitable for bioremediation (Aly et al., 2011). Nonetheless, except for arbuscular mycorrhizal fungi, effects of fungi on the phytoextraction of metals have been seldom reported (Pawlowska et al., 2000).

Vascular plants host a great variety of fungi. In addition to being susceptible to soil-borne pathogens, plant roots are also colonized by non-pathogenic or mutualistic fungi, such as arbuscular mycorrhizae (AM), ectomycorrhizae (EM), and dark septate endophytes (DSE). The AM fungi comprise about 150 species of zygomycetous fungi, and EM fungi include about 6000 species that are primarily basidiomycetes along with a few ascomycetes and zygomycetes. The AM fungi are associated with most of herbaceous plants and with various woody plant families, while the EM fungi are mainly associated with a limited number of woody plant families (Mandyam and Jumpponen, 2005). The mycorrhizal fungi absorbed non-mobile nutrients from the soil and translocate them to host plants, sequester potentially harmful heavy metal ions, facilitate interplant transfer of nutrients, and beneficially modify plant water relations (Fomina et al., 2005). Members of the cruciferae, which include major commercial crops such as Chinese cabbage, broccoli, and rapeseed, are known as nonmycorrhizal plants, nethereless, some dark septate endophytes (DSE) have been found as fungal symbionts in these plant species (Usuki and Narisawa, 2007). The dark septate endophytes (DSE) are broadly classified as conidial and sterile septate fungal endophytes, which form melanised structures, such as inter- and intracellular hyphae and microsclerotia, in the plant roots. The DSE fungi have been found worldwide and coexist often with different mycorrhizal fungi (Upson et al., 2009). They have been reported from more than 600 plant species, including plants that are considered non-mycorrhizal (Mandyam and Jumpponen, 2005).

Endophytic fungal communities generally demonstrate single host specificity at the plant species level, which can be further influenced by microhabitat and microclimatic conditions. Many endophytes such as members of the genera Phomopsis, Phoma, Colletotrichum, and Phyllosticta, have a wide host range and colonize several taxonomically unrelated plant hosts. However, endophytic fungi may also exhibit organ and tissue specificity as a result of their adaptation to different physiological conditions in plants. It is fascinating to observe that after 400 million years of evolution there are still plants that require symbiotic associations with fungi for stress tolerance (Aly et al., 2011). Fungi play an important role in organic and inorganic transformation, element cycling, rock and mineral transformations, bioweathering mycogenic mineral formation, fungal-clay interactions, and metal-fungal interactions (Gadd, 2007). Endophytic fungi also show potential to enhance phytoremediation. Most fungi can produce hyphae, which provide the ability to adopt both explorative and exploitative growth strategies and protect fungal translocation (Gadd, 2007). However, the studies of endophytic fungi have been focused on the unknown fungal species and novel bioactive compounds (Rodriguez et al., 2009, Wang and Dai, 2011, Suryanarayanan et al., 2012, Suryanarayanan, 2013). The information regarding the role of endophytic fungi in phytoremediation is incomplete, which will be thoroughly discussed in this review.

Section snippets

Fungal taxa in plant tissue at contaminated sites

Endophytic diversity is expected to be high in tropical forests, while the diversity of endophytic fungi in hyperaccumulatters has not been well studied. Studies on endophytic fungi from dominant plant species in Pb-Zn mine wasteland showed that stems harbour more endophytic fungi than leaves in each plant species. For example, twenty fungal taxa have been identified, in which Phoma, Alternaria, and Peyronellaea are the dominant genera and some of which have a marked adaptation to Pb2+ and Zn 2+

The physiological properties of endophytic fungi

The unique ability of hyperaccumulator plants to accumulate excessive amount of metals or metalloids are related to transport systems of the root tissues. Root exudates are believed to have a major influence on the diversity of microorganisms (Weyens et al., 2009b). More recently, attention has concentrated on the plant-growth promoting capacity of endophytes with a close relationship between microorganisms living in the rhizosphere and those inside the plant roots (endophytes). Plant roots are

Fungal effects on phytoremediation

Root endophytic fungi that facilitate the proliferation of various plants especially under environmentally stressful conditions can reduce the level of growth-inhibiting stress ethylene within the plants and also provide the plants with iron from the soil. The endophytic fungus is a suitable candidate for remediation of long-term cropping soil. With fungal application, seed germination significantly increased to 69.8% and seedling growth was enhanced (Chen et al., 2013). The endophytic fungus

Concluding remarks and future prospects

The recent researches of endophytic fungi on remediation of contaminated soils show a brilliant prospect for the successive studies. However, many key issues in this field need to be further studied, some of which are summarized as follows.

  • (1)

    Fungi and bacteria colonize in the hyperaccumulating plants simultaneously. However, recent investigations have been mostly focused on bacteria, with fungi largely being ignored as constituents of the host plant. Indeed, the idiom ‘microbiome’ has become

Acknowledgements

The authors gratefully acknowledge support from the grants of the Chinese National Natural Science Foundation (No 31400111).

References (67)

  • B.R. Glick

    Phytoremediation: synergistic use of plants and bacteria to clean up the environment

    Biotechnol. Adv.

    (2003)
  • B.R. Glick

    Using soil bacteria to facilitate phytoremediation

    Biotechnol. Adv.

    (2010)
  • P. Kidd et al.

    Trace element behaviour at the root-soil interface: implications in phytoremediation

    Environ. Exp. Bot.

    (2009)
  • P. Kotrba et al.

    Genetically modified plants in phytoremediation of heavy metal and metalloid soil and sediment pollution

    Biotechnol. Adv.

    (2009)
  • T. Li et al.

    Improved tolerance of maize (Zea mays L.) to heavy metals by colonization of a dark septate endophyte (DSE) Exophiala pisciphila

    Sci. Total Environ.

    (2011)
  • H. Li et al.

    Diversity and heavy metal tolerance of endophytic fungi from six dominant plant species in a Pb-Zn mine wasteland in China

    Fungal Ecol.

    (2012)
  • S. Luo et al.

    Analysis and characterization of cultivable heavy metal-resistant bacterial endophytes isolated from Cd-hyperaccumulator Solanum nigrum L. and their potentail use for phytoremediation

    Chemosphere

    (2011)
  • K. Mandyam et al.

    Seeking the elusive function of the root-colonising dark septate endophytic fungi

    Stud. Mycol.

    (2005)
  • L. Marchiol et al.

    Phytoextraction of heavy metals by canola (Brassica napus) and radish (Raphanus sativus) grown on multicontamianted soil

    Environ. Poll.

    (2004)
  • D.L. Moyes et al.

    The mycobiome: influencing IBD severity

    Cell Host Microb.

    (2012)
  • M.P. Ortega-Larrocea et al.

    Plant and fungal biodiversity from metal mine wastes under remediation at Zimapan, Hidalgo, Mexico

    Environ. Poll.

    (2010)
  • Z. Qiu et al.

    Enhanced phytoremediation of toxic metals by inoculating endophytic Enterobacter sp. CBSB1 expressing bifunctional glutathione synthase

    J. Hazard. Mat.

    (2014)
  • M. Rajkumar et al.

    Endophytic bacteria and their potential to enhance heavy metal phytoextraction

    Chemosphere

    (2009)
  • B. Schulz et al.

    The endophyte-host interaction: a balanced antagonism?

    Mycol. Res.

    (1999)
  • M. Shen et al.

    The effect of endophytic Peyronellaea from heavy metal-contaminated and uncontaminated sites on maize growth, heavy metal absorption and accumulation

    Fungal Ecol.

    (2013)
  • M. Soleimani et al.

    Phytoremediation of an aged petroleum contaminated soil using endophyte infected and non-infected grasses

    Chemosphere

    (2010)
  • T.S. Suryanarayanan

    Endophyte research: going beyond isolation and metabolite documentation

    Fungal Ecol.

    (2013)
  • R. Upson et al.

    Taxonomic affinities of dark septate root endophytes of Colobanthus quitensis and Deschampsia antarctica, the two native Antarctic vascular plant species

    Fungal Ecol.

    (2009)
  • J.W. Wang et al.

    Laccase production by Monotospora sp., an endophytic fungus in Cynodon dactylon

    Bioresourc. Technol.

    (2006)
  • N. Weyens et al.

    Exploiting plant-microbe partnerships to improve biomass production and remediation

    Trend. Biotechnol.

    (2009)
  • X. Xiao et al.

    Biosorption of cadmium by endophytic fungus (EF) Microsphaeropsis sp. LSE10 isolated from cadmium hyperaccumulator Solanum nigrum L.

    Bioresourc. Technol.

    (2010)
  • G. Xin et al.

    Characterization of three endophytic, indole-3-acetic acid-producing yeasts occurring in Populus trees

    Mycol. Res.

    (2009)
  • Z. Zhang et al.

    Remediation of petroleum contaminated soils by joint action of Pharbitis nil L. and its microbial community

    Sci. Total Environ.

    (2010)
  • Cited by (204)

    View all citing articles on Scopus
    View full text