Skip to main content
SpringerLink
Log in

Effects of a dark septate endophyte (DSE) on growth, cadmium content, and physiology in maize under cadmium stress

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

Abstract

Dark septate endophytes (DSE) are widely distributed in plant roots grown in stressful habitats, especially in heavy metal-polluted soils. But little is known about the physiological interactions between DSE and plants under heavy metal stress. In the present study, the growth, Cd content, and physiological response of Zea mays L. to a root-colonized DSE, Exophiala pisciphila, were analyzed under Cd stress (0, 5, 10, 20, and 40 mg/kg) in a sand culture experiment. Under high Cd (10, 20, and 40 mg/kg) stress, the DSE colonization in roots increased the maize growth, kept more Cd in roots, and decreased Cd content in shoots. The DSE colonization improved the photosynthesis and induced notable changes on phytohormones but had no significant effect on the antioxidant capability in the maize leaves. Moreover, there were significant positive correlations between the gibberellic acid (GA) content and transpiration rate, zeatin riboside (ZR) content, and photosynthetic rate in maize leaves. These results indicated that the DSE’s ability to promote plant growth was related to a decrease on Cd content and the regulation on phytohormone balance and photosynthetic activities in maize leaves.

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

Similar content being viewed by others

References

  • Agami RA, Mohamed GF (2013) Exogenous treatment with indole-3-acetic acid and salicylic acid alleviates cadmium toxicity in wheat seedlings. Ecotox Environ Safe 94:164–171

    Article  CAS  Google Scholar 

  • Anjum SA, Tanveer M, Hussain S, Bao M, Wang L, Khan I, Ullah E, Tung SA, Samad RA, Shahzad B (2015) Cadmium toxicity in maize (Zea mays L.): consequences on antioxidative systems, reactive oxygen species and cadmium accumulation. Environ Sci Pollut R 22:17022–17030

    Article  CAS  Google Scholar 

  • Atici Ö, Ağar G, Battal P (2005) Changes in phytohormone contents in chickpea seeds germinating under lead or zinc stress. Biol Plantarum 49:215–222

    Article  CAS  Google Scholar 

  • Baltruschat H, Fodor J, Harrach BD, Niemczyk E, Barna B, Gullner G, Zuccaro A (2008) Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytol 180(2):501–510

    Article  CAS  Google Scholar 

  • Ban Y, Tang M, Chen H, Xu Z, Zhang H, Yang Y (2012) The response of dark septate endophytes (DSE) to heavy metals in pure culture. PLoS One 7:e47968

    Article  CAS  Google Scholar 

  • Barrow JR (2003) Atypical morphology of dark septate fungal root endophytes of Bouteloua in arid southwestern USA rangelands. Mycorrhiza 13:239–247

    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:w144

    Article  Google Scholar 

  • Chaca MP, Vigliocco A, Reinoso H, Molina A, Abdala G, Zirulnik F, Pedranzani H (2014) Effects of cadmium stress on growth, anatomy and hormone contents in Glycine max (L.) Merr. Acta Physiol Plant 36:2815–2826

    Article  Google Scholar 

  • Deram A, Languereau-Leman F, Howsam M, Petit D, Haluwyn CV (2008) Seasonal patterns of cadmium accumulation in Arrhenatherum elatius (Poaceae): influence of mycorrhizal and endophytic fungal colonisation. Soil Biol Biochem 40:845–848

    Article  CAS  Google Scholar 

  • Dias MC, Monteiro C, Moutinho-Pereira J, Correia C, Gonçalves B, Santos C (2013) Cadmium toxicity affects photosynthesis and plant growth at different levels. Acta Physiol Plant 35:1281–1289

    Article  CAS  Google Scholar 

  • Gratão PL, Monteiro CC, Tezotto T, Carvalho RF, Alves LR, Peters LP, Azevedo RA (2015) Cadmium stress antioxidant responses and root-to-shoot communication in grafted tomato plants. Biometals 28:803–816

    Article  Google Scholar 

  • Gray WM (2004) Hormonal regulation of plant growth and development. PLoS Biol 2:e311

    Article  Google Scholar 

  • Hamilton CE, Gundel PE, Helander M, Saikkonen K (2012) Endophytic mediation of reactive oxygen species and antioxidant activity in plants: a review. Fungal Divers 54:1–10

    Article  Google Scholar 

  • Hu YF, Zhou G, Na XF, Yang L, Nan WB, Liu X, Zhang QY, Li JL, Bi YR (2013) Cadmium interferes with maintenance of auxin homeostasis in Arabidopsis seedlings. J Plant Physiol 170:965–975

    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  Google Scholar 

  • Janero DR (1990) Malondialdehyde and thiobarbituric acid-reactivity as diagnostic indices of lipid peroxidation and peroxidative tissue injury. Free Radical Bio Med 9:515–540

    Article  CAS  Google Scholar 

  • Johnson JM, Alex T, Oelmüller R (2014) Piriformospora indica: the versatile and multifunctional root endophytic fungus for enhanced yield and tolerance to biotic and abiotic stress in crop plants. J Trop Agr 52(2):103–122

    Google Scholar 

  • Jumpponen A (2001) Dark septate endophytes—are they mycorrhizal? Mycorrhiza 11:207–211

    Article  Google Scholar 

  • Jumpponen A, Trappe JM (1998) Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi. New Phytol 140:295–310

    Article  Google Scholar 

  • Khan AL, Lee IJ (2013) Endophytic Penicillium funiculosum LHL06 secretes gibberellin that reprograms Glycine max L. growth during copper stress. BMC Plant Biol 13:86

    Article  CAS  Google Scholar 

  • Khan AL, Hamayun M, Kang SM, Kim YH, Jung HY, Lee JH, Lee IJ (2012) Endophytic fungal association via gibberellins and indole acetic acid can improve plant growth under abiotic stress: an example of Paecilomyces formosus LHL10. BMC Microbiol 12:3

    Article  CAS  Google Scholar 

  • Khan AL, Waqas M, Hussain J, Al-Harrasi A, Lee IJ (2014) Fungal endophyte Penicillium janthinellum LK5 can reduce cadmium toxicity in Solanum lycopersicum (Sitiens and Rhe). Biol Fert Soils 50:75–85

    Article  CAS  Google Scholar 

  • Khan AL, Hussain J, Al-Harrasi A, Al-Rawahi A, Lee IJ (2015) Endophytic fungi: resource for gibberellins and crop abiotic stress resistance. Crit Rev Biotechnol 35:62–74

    Article  CAS  Google Scholar 

  • Li X, Zhang L (2015) Endophytic infection alleviates Pb2+ stress effects on photosystem II functioning of Oryza sativa leaves. J Hazard Mater 295:79–85

    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 X, Bu N, Li Y, Ma L, Xin S, Zhang L (2012) Growth, photosynthesis and antioxidant responses of endophyte infected and non-infected rice under lead stress conditions. J Hazard Mater 213:55–61

    Article  Google Scholar 

  • Li Z, Ma Z, van der Kuijp TJ, Yuan Z, Huang L (2014) A review of soil heavy metal pollution from mines in China: pollution and health risk assessment. Sci Total Environ 468:843–853

    Article  Google Scholar 

  • Likar M, Regvar M (2013) Isolates of dark septate endophytes reduce metal uptake and improve physiology of Salix caprea L. Plant Soil 370:593–604

    Article  CAS  Google Scholar 

  • López-Climent MF, Arbona V, Pérez-Clemente RM, Gómez-Cadenas A (2011) Effects of cadmium on gas exchange and phytohormone contents in citrus. Biol Plantarum 55:187–190

    Article  Google Scholar 

  • Mandyam KG, Jumpponen A (2015) Mutualism–parasitism paradigm synthesized from results of root-endophyte models. Front Microbiol 5:776

    Article  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 

  • Newsham KK (2011) A meta-analysis of plant responses to dark septate root endophytes. New Phytol 190(3):783–793

    Article  CAS  Google Scholar 

  • Newsham KK, Upson R, Read DJ (2009) Mycorrhizas and dark septate root endophytes in polar regions. Fungal Ecol 2:10–20

    Article  Google Scholar 

  • Piotrowska-Niczyporuk A, Bajguz A, Zambrzycka E, Godlewska-Żyłkiewicz B (2012) Phytohormones as regulators of heavy metal biosorption and toxicity in green alga Chlorella vulgaris (Chlorophyceae). Plant Physiol Bioch 52:52–65

    Article  CAS  Google Scholar 

  • Ruotsalainen AL, Markkola A, Kozlov MV (2007) Root fungal colonisation in Deschampsia flexuosa: effects of pollution and neighbouring trees. Environ Pollut 147:723–728

    Article  CAS  Google Scholar 

  • San-oh Y, Sugiyama T, Yoshita D, Ookawa T, Hirasawa T (2006) The effect of planting pattern on the rate of photosynthesis and related processes during ripening in rice plants. Field Crop Res 96(1):113–124

    Article  Google Scholar 

  • Shi Y, 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 

  • Sukumar P, Legue V, Vayssieres A, Martin F, Tuskan GA, Kalluri UC (2013) Involvement of auxin pathways in modulating root architecture during beneficial plant–microorganism interactions. Plant Cell Environ 36:909–919

    Article  CAS  Google Scholar 

  • Veselov D, Kudoyarova G, Symonyan M, Veselov S (2003) Effect of cadmium on ion uptake, transpiration and cytokinin content in wheat seedlings. Bulg J Plant Physiol 29:353–359

    Google Scholar 

  • Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Hückelhoven 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 

  • Wang YP, Huang J, Gao YZ (2012) Arbuscular mycorrhizal colonization alters subcellular distribution and chemical forms of cadmium in Medicago sativa L. and resists cadmium toxicity. PLoS One 7:e48669

    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

    Article  CAS  Google Scholar 

  • Waqas M, Khan AL, Kamran M, Hamayun M, Kang SM, Kim YH, Lee IJ (2012) Endophytic fungi produce gibberellins and indoleacetic acid and promotes host-plant growth during stress. Molecules 17:10754–10773

    Article  CAS  Google Scholar 

  • Weiler EW, Jourdan PS, Conrad W (1981) Levels of indole-3-acetic acid in intact and decapitated coleoptiles as determined by a specific and highly sensitive solid-phase enzyme immunoassay. Planta 153:561–571

    Article  CAS  Google Scholar 

  • Xu RB, Li T, Cui HL, Wang JL, Yu X, Ding YH, Wang CJ, Yang ZL, Zhao ZW (2015) Diversity and characterization of cd-tolerant dark septate endophytes (DSEs) associated with the roots of Nepal alder (Alnus nepalensis) in a metal mine tailing of southwest China. Appl Soil Ecol 93:11–18

    Article  Google Scholar 

  • Zhan FD, He YM, Li T, Yang YY, Toor GS, Zhao ZW (2015) Tolerance and antioxidant response of a dark septate endophyte (DSE), Exophiala pisciphila, to cadmium stress. B Environ Contam Tox 94:96–102

    Article  CAS  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: An Int J 22:532–545

    Article  CAS  Google Scholar 

  • Zhao J, Li G, Yi GX, Wang BM, Deng AX, Nan TG, Li ZH, Li QX (2006) Comparison between conventional indirect competitive enzyme-linked immunosorbent assay (icELISA) and simplified icELISA for small molecules. Anal Chim Acta 571:79–85

    Article  CAS  Google Scholar 

  • Zhao D, Li T, Shen M, Wang JL, Zhao ZW (2015) Diverse strategies conferring extreme cadmium (Cd) tolerance in the dark septate endophyte (DSE), Exophiala pisciphila: evidence from RNA-seq data. Microbiol Res 170:27–35

    Article  CAS  Google Scholar 

  • Zhu XF, Jiang T, Wang ZW, Lei GJ, Shi YZ, Li GX, Zheng SJ (2012) Gibberellic acid alleviates cadmium toxicity by reducing nitric oxide accumulation and expression of IRT1 in Arabidopsis thaliana. J Hazard Mater 239:302–307

    Article  Google Scholar 

Download references

Acknowledgements

The National Natural Science Foundation of China (Nos. 41461093, 41661056, and U1202236) and the Natural Science Foundation of Yunnan Province (No. 2016FB032) provided financial support for this work.

Author information

Authors and Affiliations

  1. College of Resources and Environment, Yunnan Agricultural University, Kunming, 650201, People’s Republic of China

    Yongmei He, Zhixin Yang, Mingrui Li, Ming Jiang, Fangdong Zhan & Yanqun Zu

  2. Laboratory for Conservation and Utilization of Bio-Resources, and Key Laboratory for Microbial Resources of the Ministry of Education, Yunnan University, Kunming, 650091, People’s Republic of China

    Tao Li & Zhiwei Zhao

Authors
  1. Yongmei He
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhixin Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mingrui Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ming Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fangdong Zhan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yanqun Zu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tao Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Zhiwei Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fangdong Zhan.

Additional information

Responsible editor: Elena Maestri

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

He, Y., Yang, Z., Li, M. et al. Effects of a dark septate endophyte (DSE) on growth, cadmium content, and physiology in maize under cadmium stress. Environ Sci Pollut Res 24, 18494–18504 (2017). https://doi.org/10.1007/s11356-017-9459-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-017-9459-6

Keywords

Search

Navigation