Skip to main content
SpringerLink
Log in

Biochemical and ecophysiological responses to manganese stress by ectomycorrhizal fungus Pisolithus tinctorius and in association with Eucalyptus grandis

  • Original Article
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

At relatively low concentrations, the element manganese (Mn) is essential for plant metabolism, especially for photosynthesis and as an enzyme antioxidant cofactor. However, industrial and agricultural activities have greatly increased Mn concentrations, and thereby contamination, in soils. We tested whether and how growth of Pisolithus tinctorius is influenced by Mn and glucose and compare the activities of oxidative stress enzymes as biochemical markers of Mn stress. We also compared nutrient accumulation, ecophysiology, and biochemical responses in Eucalyptus grandis which had been colonized by the ectomycorrhizal Pisolithus tinctorius with those which had not, when both were exposed to increasing Mn concentrations. In vitro experiments comprised six concentrations of Mn in three concentrations of glucose. In vivo experiments used plants colonized by Pisolithus tinctorius, or not colonized, grown with three concentrations of Mn (0, 200, and 1000 μM). We found that fungal growth and glucose concentration were correlated, but these were not influenced by Mn levels in the medium. The anti-oxidative enzymes catalase and glutathione S-transferase were both activated when the fungus was exposed to Mn. Also, mycorrhizal plants grew more and faster than non-mycorrhizal plants, whatever Mn exposure. Photosynthesis rate, intrinsic water use efficiency, and carboxylation efficiency were all inversely correlated with Mn concentration. Thus, we originally show that the ectomycorrhizal fungus provides protection for its host plants against varying and potentially toxic concentrations of Mn.

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

Abbreviations

Mn:

Manganese

CAT:

Catalase

GST:

Glutathione S-transferase

gs :

Stomatal conductance

A :

Net carbon assimilation

A/Ci:

Carboxylation efficiency

iWUE:

Intrinsic water use efficiency

References

  • Adeleke RA, Cloete TE, Bertrand A, Khasa DP (2012) Iron ore weathering potentials of ectomycorrhizal plants. Mycorrhiza 22:535–544

    Article  CAS  PubMed  Google Scholar 

  • Adriaensen K, Lelie D, van der Laere AV, Vangronsveld J, Colpaert JV (2003) A zinc-adapted fungus protects pines from zinc stress. New Phytol 161:549–555

    Article  Google Scholar 

  • Angelova MB, Pashova SB, Slokoska LS (2000) Comparison of antioxidant enzyme biosynthesis by free and immobilized Aspergillus nidulans cells. Enzyme Microb Technol 26:544–549

    Article  CAS  PubMed  Google Scholar 

  • Arya SK, Roy BK (2011) Manganese induced changes in growth, chlorophyll content and antioxidants activity in seedlings of broad bean. J Environ Biol 32:707–711

    CAS  PubMed  Google Scholar 

  • Avilez IM, Hori TSF, Almeida LC, Hackbarth A, Bastos Neto JC, Bastos VLFC, Moraes G (2008) Effects of phenol in antioxidant metabolism in matrinxã, Brycon amazonicus (Teleostei; Characidae). Comp Biochem Physiol C 148:136–142

    Google Scholar 

  • Baptista P, Martins A, Pai MS, Tavares RM, Lino-Neto T (2007) Involvement of reactive oxygen species during early stages of ectomycorrhiza establishment between Castanea sativa and Pisolithus tinctorius. Mycorrhiza 17:185–193

    Article  CAS  PubMed  Google Scholar 

  • Bellion M, Courbot M, Jacob C, Blaudez D, Chalot M (2006) Extracellular and cellular mechanisms sustaining metal tolerance in ectomycorrhizal fungi. FEMS Microbiol Lett 254:173–181

    Article  CAS  PubMed  Google Scholar 

  • Bethlenfalvay GJ, Franson RL (1989) Manganese toxicity alleviated by mycorrhizae in soybean. J Plant Nutr 12:953–970

    Article  CAS  Google Scholar 

  • Beutler E (1975) Catalase. In: Beutler E (ed) Red cell metabolism—a manual of biochemistry methods. Grune and Straton, New York, pp 89–90

    Google Scholar 

  • Blaudez D, Jacob C, Turnau K, Colpaert JV, Ahonen-Jonnarth U, Finlay R et al (2000) Differential responses of ectomycorrhizal fungi to heavy metals in vitro. Mycol Res 104:1366–1371

    Article  CAS  Google Scholar 

  • Bolhár-Nordenkampf HR, Long SP, Baker NR, Öquist G, Schreiber U, Lechner EG (1989) Chlorophyll fluorescence as a probe of the photosynthetic competence of leaves in the field: a review of current instrumentation. Funct Ecol 3:497–514

    Article  Google Scholar 

  • Brown MT, Wilkins DA (1985) Zinc tolerance of mycorrhizal Betula. New Phytol 99:101–106

    Article  CAS  Google Scholar 

  • Brundrett M, Bougher NM, Dell B, Grove T, Malajczuck N (1996) Working with mycorrhizas in forestry and agriculture. Pirie Printers, Canberra

    Google Scholar 

  • Campbell LC, Nable RO (1988) Physiological functions of Mn in plants. In: Graham RD, Hannan RJ, Uren NC (eds) Manganese in soils and plants. Kluwer Academic Publishers, Dordrecht, pp 139–154

    Chapter  Google Scholar 

  • Cardoso EJBN (1994) Interaction of mycorrhiza, phosphate and manganese in soybean. In: Azcón-Aguilar C, Barea JM (eds) Mycorrhizas in integrated systems: from genes to plant development. European Commission Report, Luxemburg, pp 304–306

    Google Scholar 

  • Carneiro JP, Varennes A, Amante H (2001) Manganese toxicity in three species of annual medicis. J Plant Nutr 24:1957–1964

    Article  CAS  Google Scholar 

  • Chen Y, Nara K, Wen Z, Shi L, Xia Y, Shen Z, Lian C (2015) Growth and photosynthetic responses of ectomycorrhizal pine seedlings exposed to elevated Cu in soils. Mycorrhiza 25:561–571

    Article  CAS  PubMed  Google Scholar 

  • Clark RB (1975) Characterization of phosphatase of intact maize roots. J Agric Food Chem 23:458–460

    Article  CAS  PubMed  Google Scholar 

  • Colpaert JV, Van Assche JA (1993) The effects of cadmium on ectomycorrhizal Pinus sylvestris L. New Phytol 123:325–333

    Article  CAS  Google Scholar 

  • Fecht-Christoffers MM, Maier P, Horst WJ (2003) Apoplastic peroxidases and ascorbate are involved in Mn toxicity and tolerance of Vigna unguiculata. Physiol Plant 117:237–244

    Article  CAS  Google Scholar 

  • Finlay RD (2008) Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. J Exp Bot 59:1115–1126

    Article  CAS  PubMed  Google Scholar 

  • Fogarty RV, Tobin JM (1996) Fungal melanins and their interactions with metals. Enzyme Microbiol Technol 19:311–317

    Article  CAS  Google Scholar 

  • Fomina M, Hiller S, Charnock JM, Melville K, Alexander LJ, Gadd GM (2005) Role of oxalic acid over secretion in transformation of toxic metal minerals by Beauveria caledonica. Appl Environ Microbiol 71:371–381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foy CD (1984) Physiological effects of hydrogen, aluminium, and manganese toxicities in acid soils. In: Adams F (ed) Soil acidity and liming. American Society of Agronomy, Madison, pp 57–97

    Google Scholar 

  • Gadd GM (1993) Interactions of fungi with toxic metals. New Phytol 124:25–60

    Article  CAS  Google Scholar 

  • Galli U, Schuepp H, Brunold C (1994) Heavy metal binding by mycorrhizal fungi. Physiol Plant 92:364–368

    Article  CAS  Google Scholar 

  • Giovannetti M, Mosse B (1980) An evaluation of techniques to measure vesicular-arbuscular mycorrhizal infection in roots. New Phytol 84:484–500

    Article  Google Scholar 

  • Grant CM, Perrone G, Dawes IW (1998) Glutathione and catalase provide overlapping defenses for protection against hydrogen peroxide in the yeast Saccharomyces cerevisiae. Biochem Bioph Res Commun 253:893–898

    Article  CAS  Google Scholar 

  • Guehl JM, Garbaye J (1990) The effect of ectomycorrhizal status on carbon dioxide assimilation capacity, water-use efficiency and response to transplanting in seedlings of Pseudotsuga menziesii (Mirb.) Franco. Ann For Sci 21:551–563

    Article  Google Scholar 

  • Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases the first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139

    CAS  PubMed  Google Scholar 

  • Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11

    Article  CAS  PubMed  Google Scholar 

  • Horst WJ (1988) The physiology of manganese toxicity. In: Graham RD, Hannam RJ, Uren NC (eds) Manganese in soil and plants. Kluwer Academic, Boston, pp 175–188

    Chapter  Google Scholar 

  • Jackson ML (1965) Soil chemical analysis. Prentice Hall, New Jersey

    Google Scholar 

  • Joner EJ, Briones R, Leyval C (2000) Metal-binding capacity of arbuscular mycorrhizal mycelium. Plant Soil 226:227–234

    Article  CAS  Google Scholar 

  • Jones MD, Hutchinson TC (1986) The effect of mycorrhizal infection on the response of Betula papyrifera to nickel and copper. New Phytol 102:429–442

    Article  CAS  Google Scholar 

  • Jourand P, Hannibal L, Majorel C, Mengant S, Ducousso M, Lebrun M (2014) Ectomycorrhizal Pisolithus albus inoculation of Acacia spirorbis and Eucalyptus globulus grown in ultramafic topsoil enhances plant growth and mineral nutrition while limits metal uptake. J Plant Physiol 171:164–172

    Article  CAS  PubMed  Google Scholar 

  • Kalra YP (1997) Handbook of reference methods for plant analysis. CRC Press, Florida

    Book  Google Scholar 

  • Karki P, Lee E, Aschner M (2013) Manganese neurotoxicity: a focus on glutamate transporters. Ann Occup Environ Med 25:4

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim CG, Power SA, Bell JNB (2003) Effects of cadmium on growth and glucose utilization of ectomycorrhizal fungi in vitro. Mycorrhiza 13:223–226

    Article  CAS  PubMed  Google Scholar 

  • Kitao M, Lei TT, Koike T (1997) Comparison of photosynthetic responses to manganese toxicity of deciduous broad-leaved trees in northern Japan. Environ Pollut 97:113–118

    Article  CAS  PubMed  Google Scholar 

  • Kottke I, Qian XM, Pritsch K, Haug I, Oberwinkler F (1998) Xerocomus badius–Picea abies, an ectomycorrhiza of high activity and element storage capacity in acidic soil. Mycorrhiza 7:267–275

    Article  CAS  PubMed  Google Scholar 

  • Lehto T (1992) Mycorrhizas and drought resistance of Picea sitchensis (Bong.) Carr. I. In conditions of nutrient deficiency. New Phytol 122:661–668

    Article  CAS  Google Scholar 

  • Lei Y, Korpelainen H, Li C (2007) Physiological and biochemical responses to high manganese concentrations in two contrasting Populus cathayana populations. Chemosphere 68:686–694

    Article  CAS  PubMed  Google Scholar 

  • Li Q, Chen LS, Jiang HX, Tang N, Yang LT, Lin ZH et al (2010) Effects of Mn-excess on CO2 assimilation, ribulose-1,5-bisphosphate carboxylase/oxygenase, carbohydrates and photosynthetic electron transport of leaves, and antioxidant systems of leaves and roots in Citrus grandis seedlings. BMC Plant Biol 10:1–16

    Article  CAS  Google Scholar 

  • Lowry OH, Rosembrough NJ, Farr AL (1951) Protein measurement with pholin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • Ma Y, He J, Ma C, Luo J, Li H, Liu T, Polle A, Peng C, Luo Z-B (2013) Ectomycorrhizas with Paxillus involutus enhance cadmium uptake and tolerance in Populus x canascens. Plant Cell Environ 37:627–642

    Article  PubMed  Google Scholar 

  • Malcová R, Gryndler M, Vosátka M (2002) Magnesium ions alleviate the negative effect of manganese on Glomus claroideum BEG23. Mycorrhiza 12:125–129

    Article  PubMed  Google Scholar 

  • Mannazzu I, Guerra E, Ferretti R, Pediconi D, Fatichenti F (2000) Vanadate and copper induce overlapping oxidative stress responses in the vanadate-tolerant yeast Hansenula polymorpha. Biochim Biophys Acta 1475:151–156

    Article  CAS  PubMed  Google Scholar 

  • Marschner P (2012) Marschner’s mineral nutrition of higher plants. Academic Press, London

    Google Scholar 

  • Marx DH (1969) The influence of ectotrophic mycorrhizal fungi on the resistance of pine roots to pathogenic infections. I Antagonism of mycorrhizal fungi to root pathogenic fungi and soil bacteria. Phytopathology 59:153–163

    Google Scholar 

  • Millaleo R, Reyes-Diaz M, Ivanov AG, Mora ML, Alberdi M (2010) Manganese as essential and toxic element for plants: transport, accumulation and resistance mechanisms. J Soil Sci Plant Nutr 10:470–481

    Article  Google Scholar 

  • Nogueira MA, Cardoso EJBN (2003) Mycorrhizal effectiveness and Mn toxicity in soybean as affected by soil type and endophyte. Sci Agric 60:329–335

    Article  CAS  Google Scholar 

  • Nogueira MA, Magalhães GC, Cardoso EJBN (2004) Manganese toxicity in mycorrhizal and phosphorus-fertilized soybean plants. J Plant Nutr 27:141–156

    Article  CAS  Google Scholar 

  • Ott T, Fritz E, Polle A, Schützendübel A (2002) Characterization of antioxidative systems in the ectomycorrhiza-building basidiomycete Paxillus involutus (Bartsch) Fr. and its reaction to cadmium. FEMS Microbiol Ecol 42:359–366

    Article  CAS  PubMed  Google Scholar 

  • Pacovsky RS, Bethlenfalvay GJ, Paul EA (1986) Comparison between P-fertilized and mycorrhizal plants. Crop Sci 26:151–156

    Article  Google Scholar 

  • Page V, Feller U (2005) Selective transport of zinc, manganese, nickel, cobalt and cadmium in the root system and transfer to the leaves in young wheat plants. Ann Bot 96:425–434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Page V, Weisskopf L, Feller U (2006) Heavy metals in white lupin: uptake, root-to-shoot transfer and redistribution within the plant. New Phytol 171:329–341

    Article  CAS  PubMed  Google Scholar 

  • Parker DR, Chaney RL, Norvell WA (1995) Chemical equilibrium models: applications to plant nutrition research. In: Loeppert RH, Schwab AP, Goldberg S (eds) Chemical equilibrium and reaction models. Soil Science Society of America, Inc, Madison, pp 163–200, 253-269

    Google Scholar 

  • Peters JB (2005) Wisconsin procedures for soil testing, plant analysis and feed & forage analysis: plant analysis. Department of Soil Science, College of Agriculture and Life Sciences, University of Wisconsin-Extension, Madison

    Google Scholar 

  • Philips JM, Hayman DS (1970) Improved procedure for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. T Brit Mycol Soc 55:158–161

    Article  Google Scholar 

  • Porter G, Bajita-Locke J, Hue N, Strand S (2004) Manganese solubility and phytotoxicity affected by soil moisture, oxygen levels, and green manure additions. Commun Soil Sci Plant Anal 35:99–116

    Article  CAS  Google Scholar 

  • Posta K, Marschner H, Römheld V (1994) Manganese reduction in the rhizosphere of mycorrhizal and nonmycorrhizal maize. Mycorrhiza 5:119–124

    Article  CAS  Google Scholar 

  • Ramos AC, Lima PT, Dias PN, Kasuya MCM, Feijó JA (2009) A pH signaling mechanism involved in the spatial distribution of calcium and anion fluxes in ectomycorrhizal roots. New Phytol 181:448–462

    Article  CAS  PubMed  Google Scholar 

  • Rékási M, Filep T (2015) Factors determining Cd, Co, Cr, Cu, Ni, Mn, Pb and Zn mobility in uncontaminated arable and forest surface soils in Hungary. Environ Earth Sci 74:6805–6817

    Article  Google Scholar 

  • Rezai K, Farboodnia T (2008) Manganese toxicity effects on chlorophyll content and antioxidant enzymes in pea plant (Pisum sativum L. c.v qazvin). Agric J 3:454–45

    CAS  Google Scholar 

  • Rodaki A, Bohovych IM, Enjalbert B, Young T, Odds FC, Gow NA, Brown AJ (2009) Glucose promotes stress resistance in the fungal pathogen Candida albicans. Mol Biol Cell 20:4845–4855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sato I, Shimizu M, Hoshino T, Takaya N (2009) The glutathione system of Aspergillus nidulans involve a fungus specific glutathione-S-transferase. J Biol Chem 284:8042–8053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sheng H, Zeng J, Yan F, Wang X, Wang Y, Kang H, Fan X, Sha L, Zhang H, Zhou Y (2015) Effect of exogenous salicylic acid on manganese toxicity, mineral nutrients translocation and antioxidative system in polish wheat (Triticum polonicum L.). Acta Physiol Plant 37:32

    Article  Google Scholar 

  • Strasser BJ, Strasser RJ (1995) Measuring fast fluorescence transients to address environmental questions: the JIP-test. In: Proceedings of Xth International Photosynthesis Congress. Netherlands, Dordrecht, pp 977–980

    Google Scholar 

  • Strasser R, Tsimilli-Michael M (2001) Stress in plants, from daily rhythm to global changes, detected and quantified by the JIP-test. Chim Nouv 75:3321–3326

    Google Scholar 

  • Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing photosynthesis: mechanism, regulation and adaptation. Taylor and Francis, London, pp 443–480

    Google Scholar 

  • Strasser RJ, Srivastava A, Tsimilli-Michael M (2004) Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou G, Govindjee (eds) Advances in photosynthesis and respiration. Vol. 19: chlorophyll fluorescence: a signature of photosynthesis. Kluwer Academic Publishers, Netherlands, pp 321–362

    Google Scholar 

  • Tam PCF (1995) Heavy metal tolerance by ectomycorrhizal fungi and metal amelioration by Pisolithus tinctorius. Mycorrhiza 5:181–187

    Article  CAS  Google Scholar 

  • Thach LB, Shapcott A, Schmidt S, Critchley C (2007) The OJIP fast fluorescence rise characterizes Graptophyllum species and their stress responses. Photosynth Res 94:423–436

    Article  CAS  Google Scholar 

  • Thompson GW, Medve RJ (1984) Effects of aluminium and Mn on the growth of ectomycorrhizal fungi. Appl Environ Biol 48:556–560

    CAS  Google Scholar 

  • Van Tichelen KK, Colpaert JV, Vangronsveld J (2001) Ectomycorrhizal protection of Pinus sylvestris against copper toxicity. New Phytol 150:203–213

    Article  Google Scholar 

  • Ward JT, Lahner B, Yakubova E, Salt DE, Raghothama KG (2008) The effect of iron on the primary root elongation of Arabidopsis during phosphate deficiency. Plant Physiol 147:1181–1191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao-Xiao M, Jiang YL, He YX, Bao R, Chen Y, Zhou CZ (2009) Structures of yeast glutathione-S-transferase Gtt2 reveal a new catalytic type of GST family. EMBO Rep 10:1320–13

    Article  Google Scholar 

Download references

Acknowledgments

We would like to acknowledge Dr Anderson Peçanha and Alena Torres-Neto for the contribution to the photosynthetic analysis. The authors would like to acknowledge Dr. Erwan Michard (University of Maryland, EUA) and Steve Houghton for revision of the manuscript and helpful suggestions. This work was supported by Fundação de Amparo à Pesquisa e Inovação do Espírito Santo (FAPES) PhD fellowship awarded to GCC and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) to AAB. ACR’s laboratory is supported by grants from FAPES (#546879852011), Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) (#E-26/110.0821/2014; #E-26/111.428/2014), and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (#475436/2010-5; #312399/2013-8). NS is funded by Welcome Trust grant number 091924 and the Fundação para a Ciência e Tecnologia through the project Pest-OE/MAT/UI0006/2011.

Author information

Authors and Affiliations

  1. Environmental Microbiology and Biotechnology Lab, Universidade Vila Velha (UVV), Boa Vista, Vila Velha, ES, 29102-770, Brazil

    Gabriela C. Canton & Ary Gomes da Silva

  2. Plant Physiology Lab, Universidade Estadual do Norte Fluminense (UENF), Campos dos Goytacazes, RJ, 28013-602, Brazil

    Amanda A. Bertolazi, Sávio Bastos de Souza, Eliemar Campostrini & Arnoldo R. Façanha

  3. Laboratory of Biochemistry and Physiology of Microorganisms, Universidade Estadual do Norte Fluminense (UENF), Campos dos Goytacazes, RJ, 28013-602, Brazil

    Antônio J. D. Cogo, Frederico Jacob Eutrópio, Juliana Melo, Cesar A. Krohling & Alessandro C. Ramos

  4. Cell Tissue and Biology Lab, Universidade Estadual do Norte Fluminense (UENF), Campos dos Goytacazes, RJ, 28013-602, Brazil

    Arnoldo R. Façanha

  5. London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, Faculty of Sciences, United Kingdom & Center of Statistics and Applications of University of Lisbon, Campo Grande, 1749-016, Lisbon, Portugal

    Nuno Sepúlveda

  6. Center for Ecology, Evolution and Environmental Changes (Ce3C), Faculty of Sciences, Universidade de Lisboa, Campo Grande, 1749-016, Lisbon, Portugal

    Cristina Cruz

Authors
  1. Gabriela C. Canton
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amanda A. Bertolazi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Antônio J. D. Cogo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Frederico Jacob Eutrópio
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Juliana Melo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sávio Bastos de Souza
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Cesar A. Krohling
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Eliemar Campostrini
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Ary Gomes da Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Arnoldo R. Façanha
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Nuno Sepúlveda
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Cristina Cruz
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Alessandro C. Ramos
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alessandro C. Ramos.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1

(DOC 32 kb)

Table S2

(DOC 31 kb)

Table S3

(DOC 31 kb)

Table S4

(DOC 34 kb)

Table S5

(DOC 40 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Canton, G.C., Bertolazi, A.A., Cogo, A.J.D. et al. Biochemical and ecophysiological responses to manganese stress by ectomycorrhizal fungus Pisolithus tinctorius and in association with Eucalyptus grandis . Mycorrhiza 26, 475–487 (2016). https://doi.org/10.1007/s00572-016-0686-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-016-0686-3

Keywords

Search

Navigation