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The effects of dark septate endophyte (DSE) inoculation on tomato seedlings under Zn and Cd stress

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Abstract

Dark septate endophytes (DSEs) are a heterogeneous group of endophytic fungi that frequently colonize the roots of plants growing in trace metal element-contaminated soils. However, the functional role of DSEs in host plants growing in metal-stressed environments remains to be elucidated. In this study, two DSE strains of Phialophora mustea Neerg. (K36 and Z48) were separately inoculated in tomato (Lycopersicon esculentum Miller) seedlings under metal stress conditions (0, 5, 10 mg kg−1 Cd or 0, 300, 600 mg kg−1 Zn) to evaluate the effects of DSE inoculation on tomato seedlings in pot cultures. The results showed that DSE colonization increased tomato seedling biomass whether or not there was metal addition. DSE-inoculated tomatoes had a lower Cd and Zn accumulation in both the shoots and roots compared with their respective non-inoculated controls. Under metal stress conditions, DSE inoculation significantly enhanced the activities of antioxidant enzymes, such as superoxide dismutase (SOD) and peroxidase (POD), thus relieving the membrane lipid peroxidation damage caused by metal stress, and reduced the leaf malondialdehyde (MDA) concentrations more than that of the non-inoculated treatments. The results revealed that DSE enhanced metal tolerance and improved tomato plant growth, both by the reduced metal uptake into root and shoot accumulation and by the enhanced activities of antioxidant enzymes to eliminate reactive oxygen species (ROS) stress induced by excessive metals.

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References

  • Anderson MD, Prasad TK, Stewart CR (1995) Changes in isozyme profiles of catalase, peroxidase, and glutathione reductase during acclimation to chilling in mesocotyls of maize seedlings. Plant Physiol 109:1247–1257

    Article  CAS  Google Scholar 

  • Berch SM, Kendrick B (1982) Vesicular-arbuscular mycorrhizae of southern Ontario ferns and fern-allies. Mycologia 74:769–776

    Article  Google Scholar 

  • Berthelot C, Leyval C, Foulon J, Chalot M, Blaudez D (2016) Plant growth promotion, metabolite production and metal tolerance of dark septate endophytes isolated from metal-polluted poplar phytomanagement sites. FEMS Microbiol Ecol 92:fiw144

    Article  Google Scholar 

  • Cao GH, Li T, Li XB, Zhan FD, Shen M, Zhao ZW (2016) Heavy metal pollution and accumulation in maize grown in arable soils located near a lead and zinc slag heap in Yunnan, Southwest China. Int J Environ Pollut 59:97–115

    Article  CAS  Google Scholar 

  • Chen H, Teng Y, Lu S, Wang Y, Wang J (2015) Contamination features and health risk of soil heavy metals in China. Sci Total Environ 512-513:143–153

    Article  CAS  Google Scholar 

  • Demiral T, Türkan I (2005) Comparative lipid peroxidation, antioxidant defense systems and proline content in roots of two rice cultivars differing in salt tolerance. Environ Exp Bot 53:247–257

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Göhre V, Paszkowski U (2006) Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation. Planta 223:1115–1122

    Article  Google Scholar 

  • Gonzalez EM, de Ancos B, Cano MP (1999) Partial characterization of polyphenol oxidase activity in raspberry fruits. J Agric Food Chem 47:4068–4072

    Article  CAS  Google Scholar 

  • Hui F, Liu J, Gao Q, Lou B (2015) Piriformospora indica confers cadmium tolerance in Nicotiana tabacum. J Environ Sci 37:184–191

    Article  CAS  Google Scholar 

  • Khan AR, Ullah I, Khan AL, Park GS, Waqas M, Hong SJ, Jung BK, Kwak Y, Lee IJ, Shin JH (2015) Improvement in phytoremediation potential of Solanum nigrum under cadmium contamination through endophytic-assisted Serratia sp. RSC-14 inoculation. Environ Sci Pollut Res Int 22:14032–14042

    Article  CAS  Google Scholar 

  • Li T, Liu MJ, Zhang XT, Zhang HB, Sha T, Zhao ZW (2011) Improved tolerance of maize (Zea mays L.) to heavy metals by colonization of a dark septate endophyte (DSE) Exophiala pisciphila. Sci Total Environ 409:1069–1074

    Article  CAS  Google Scholar 

  • Li KL, Wang YT, Han XX, Jiang J (2013) Changes in reactive oxygen species and antioxidative defense mechanism in tomato leaves under low potassium stress (in Chinese). Acta Botan Boreali-Occiden Sin 33:66–73

    Google Scholar 

  • Li H, Luo N, Zhang LJ, Zhao HM, Li YW, Cai QY, Wong MH, Mo CH (2016) Do arbuscular mycorrhizal fungi affect cadmium uptake kinetics, subcellular distribution and chemical forms in rice? Sci Total Environ 571:1183–1190

    Article  CAS  Google Scholar 

  • Liu H, Li T, Ding Y, Yang Y, Zhao Z (2017) Dark septate endophytes colonizing the roots of ‘non-mycorrhizal’ plants in a mine tailing pond and in a relatively undisturbed environment, Southwest China. J Plant Interact 12:264–271

    Article  CAS  Google Scholar 

  • Luck H (1963) Peroxidase. In: Bergmeyer HU (ed) Methods of enzymic analysis. Academic Press Inc., New York, pp 895–897

    Google Scholar 

  • Ma Y, Raijkumar M, Zhang C, Freitas H (2016) Beneficial role of bacterial endophytes in heavy metal phytoremediation. J Environ Manag 174:14–25

    Article  CAS  Google Scholar 

  • McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–501

    Article  Google Scholar 

  • Nalli Y, Mirza DN, Wani ZA, Wadhwa B, Mallik FA, Raina C, chaubey A, Riyaz-Ul-Hassan S, Ali A (2015) Phialomustin A-D, new antimicrobial and cytotoxic metabolites from an endophytic fungus, Phialophora mustea. RSC Adv 5:95307–95312

    Article  CAS  Google Scholar 

  • Newsham KK (2011) A meta-analysis of plant responses to dark septate root endophytes. New Phytol 190:783–793

    Article  CAS  Google Scholar 

  • Ouziad F, Hildebrandt U, Schmelzer E, Bothe H (2005) Differential gene expressions in arbuscular mycorrhizal-colonized tomato grown under heavy metal stress. J Plant Physiol 162:634–649

    Article  CAS  Google Scholar 

  • Regvar M, Matevž L, Piltaver A, Kugonič N, Smith JE (2010) Fungal community structure under goat willows (Salix caprea L.) growing at metal polluted site: the potential of screening in a model phytostabilisation study. Plant Soil 330:345–356

    Article  CAS  Google Scholar 

  • Shahabivand S, Maivan HZ, Mahmoudi E, Soltani BM, Sharifi M, Aliloo AA (2016) Antioxidant activity and gene expression associated with cadmium toxicity in wheat affected by mycorrhizal fungus. Zemdirbyste 103:53–60

    Article  Google Scholar 

  • Shi Y, Xie H, Cao L, Zhang R, Xu Z, Wang Z, Deng Z (2017) Effects of Cd- and Pb-resistant endophytic fungi on growth and phytoextraction of Brassica napus in metal-contaminated soils. Environ Sci Pollut Res Int 24:417–426

    Article  CAS  Google Scholar 

  • Tosi L, Zazzerini A (1996) Phialophora mustea, a new lily pathogen. Petria 6:209–214

    Google Scholar 

  • Usuki F, Narisawa K (2007) A mutualistic symbiosis between a dark septate endophytic fungus, Heteroconium chaetospira, and a nonmycorrhizal plant, Chinese cabbage. Mycologia 99:175–184

    Article  CAS  Google Scholar 

  • Vamerali T, Bandiera M, Mosca G (2010) Field crops for phytoremediation of metal-contaminated land. A review. Environ Chem Lett 8:1–17

    Article  CAS  Google Scholar 

  • Wang JL, Li T, Liu GY, Smith JM, Zhao ZW (2016) Unraveling the role of dark septate endophyte (DSE) colonizing maize (Zea mays) under cadmium stress: physiological, cytological and genic aspects. Sci Rep 6:22028

  • Wani ZA, Mirza DN, Arora P, Hassan SR (2016) Molecular phylogeny, diversity, community structure, and plant growth promoting properties of fungal endophytes associated with the corms of saffron plant: an insight into the microbiome of Crocus sativus Linn. Fungal Biol 120:1509–1524

    Article  Google Scholar 

  • Wehner J, Powell JR, Muller LAH, Caruso T, Veresoglou SD, Hempel S, Rillig MC (2014) Determinants of root-associated fungal communities within Asteraceae in a semi-arid grassland. J Ecol 102:425–436

    Article  Google Scholar 

  • Zhang YJ, Zhang Y, Liu MJ, Shi XD, Zhao ZW (2008) Dark septate endophyte (DSE) fungi isolated from metal polluted soils: their taxonomic position, tolerance, and accumulation of heavy metals in vitro. J Microbiol 46:624–632

    Article  Google Scholar 

  • Zhang Y, Li T, Zhao ZW (2013) Colonization characteristics and composition of dark septate endophytes (DSE) in a lead and zinc slag heap in Southwest China. Soil Sediment Contam 22:532–545

    Article  CAS  Google Scholar 

  • Zheng YK, Miao CP, Chen HH, Huang FF, Xia YM, Chen YW, Zhao LX (2017) Endophytic fungi harbored in Panax notoginseng: diversity and potential as biological control agents against host plant pathogens of root-rot disease. J Ginseng Res 41:353–360

    Article  Google Scholar 

Download references

Acknowledgements

The authors gratefully acknowledge Dr. Fangdong Zhan (College of Resources and Environment, Yunnan Agricultural University, PR China) for his help in metal analysis. This work was financially supported by the National Science Foundation of China (41461073, 31460114, and 41761106) and Yunnan University’s Research Innovation Fund for Graduate Students (YNUY201697).

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  1. Lingling Zhu and Tao Li contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Conservation and Utilization for Bioresources in Yunnan, Yunnan University, Kunming, 650091, Yunnan, People’s Republic of China

    Lingling Zhu, Tao Li, Chaojun Wang, Xiaorong Zhang, Lujuan Xu, Runbing Xu & Zhiwei Zhao

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  1. Lingling Zhu
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  2. Tao Li
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  3. Chaojun Wang
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  4. Xiaorong Zhang
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  5. Lujuan Xu
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  7. Zhiwei Zhao
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Correspondence to Zhiwei Zhao.

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Zhu, L., Li, T., Wang, C. et al. The effects of dark septate endophyte (DSE) inoculation on tomato seedlings under Zn and Cd stress. Environ Sci Pollut Res 25, 35232–35241 (2018). https://doi.org/10.1007/s11356-018-3456-2

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  • DOI: https://doi.org/10.1007/s11356-018-3456-2

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