Skip to main content
Log in

The continuing relevance of “older” mycorrhiza literature: insights from the work of John Laker Harley (1911–1990)

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

Abstract

To new generations of scientists beginning their careers in research, we strongly recommend the practice of reading older literature. To illustrate the value of doing so, we highlight six insights of one of the most influential mycorrhiza researchers of the twentieth century, Jack Harley. These insights concerning mycotrophy, the new niche, the sheath, C cycling, N cycling, and mutualism were published prior to 1975 and so may have escaped the notice of many, but they laid the groundwork for some of the most important research of today.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Notes

  1. In the 1960s and 1970s, it was common to refer to arbuscular, orchid, and ericaceous mycorrhizal fungi as endophytes. This is no longer done, possibly because mycorrhizal fungi exist only partially and not wholly within plant tissues.

References

  • Abuzinadah R, Read D (1986) The role of proteins in the nitrogen nutrition of ectomycorrhizal plants II. Utilization of protein by mycorrhizal plants of Pinus contorta. New Phytol 103:495–506

    Article  CAS  Google Scholar 

  • Beiler KJ, Durall DM, Simard SW, Maxwell SA, Kretzer AM (2010) Architecture of the wood-wide web: Rhizopogon spp. genets link multiple Douglas-fir cohorts. New Phytol 185:543–553

    Article  CAS  Google Scholar 

  • Chen W, Koide RT, Adams TS, Deforest JL, Cheng L, Eissenstat D (2016) Root morphology and mycorrhizal symbioses together shape nutrient foraging strategies of temperate trees. PNAS 113(31):8741–8746

    Article  CAS  Google Scholar 

  • Chen W, Eissenstat DM, Koide RT (2018) Root diameter predicts the extramatrical hyphal exploration distance of the ectomycorrhizal fungal community. Ecosphere 9. https://doi.org/10.1002/ecs2.2202

    Article  Google Scholar 

  • Cheng L, Chen W, Adams TS, Wei X, Li L, McCormack ML, DeForest JL, Koide RT, Eissenstat DM (2016) Mycorrhizal fungi and roots are complementary in foraging within nutrient patches. Ecology 97:2815–2823. https://doi.org/10.1002/ecy.1514

    Article  PubMed  Google Scholar 

  • Clemmensen KE, Bahr A, Ovaskainen O, Dahlberg A, Ekblad A, Wallander H, Stenlid J, Finlay RD, Wardle DA, Lindahl BD (2013) Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339(6127):1615–1618

    Article  CAS  Google Scholar 

  • Cotrufo MF, Wallenstein MD, Boot CM, Denef K, Paul E (2013) The microbial efficiency-matrix stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Glob Chang Biol 19:988–995. https://doi.org/10.1111/gcb.12113

    Article  PubMed  Google Scholar 

  • Delaye L, García-Guzmán G, Heil M (2013) Endophytes versus biotrophic and necrotrophic pathogens-are fungal lifestyles evolutionarily stable traits? Fungal Divers 60:125–135. https://doi.org/10.1007/s13225-013-0240-y

    Article  Google Scholar 

  • Ekblad A, Wallander H, Godbold DL, Cruz C, Johnson D, Baldrian P, Björk RG, Epron D, Kieliszewska-Rokicka B, Kjøller R, Kraigher H, Matzner E, Neumann J, Plassard C (2013) The production and turnover of extramatrical mycelium of ectomycorrhizal fungi in forest soils: role in carbon cycling. Plant Soil 366(1–2):1–27

    Article  CAS  Google Scholar 

  • Fernandez CW, Kennedy PG (2015) Revisiting the “Gadgil effect”: do interguild fungal interactions control carbon cycling in forest soils? New Phytol 209:1382–1394

    Article  Google Scholar 

  • Fernandez CW, Kennedy PG (2018) Melanization of mycorrhizal fungal necromass structures microbial decomposer communities. J Ecol 106:468–479

    Article  CAS  Google Scholar 

  • Fernandez CW, Koide RT (2012) The role of chitin in the decomposition of ectomycorrhizal fungal litter. Ecology 93(1):24–28

    Article  Google Scholar 

  • Fernandez CW, Koide RT (2014) Initial melanin and nitrogen concentrations control the decomposition of ectomycorrhizal fungal litter. Soil Biol Biochem 77:150–157

    Article  CAS  Google Scholar 

  • Fitter AH, Graves JD, Watkins NK, Robinson D, Scrimgeour C (1998) Carbon transfer between plants and its control in networks of arbuscular mycorrhizas. Funct Ecol 12(3):406–412. https://doi.org/10.1046/j.1365-2435.1998.00206.x

    Article  Google Scholar 

  • Gadgil RL, Gadgil PD (1971) Mycorrhiza and litter decomposition. Nature 233:133

    Article  CAS  Google Scholar 

  • Garrett SD (1950) Ecology of root-inhabiting fungi. Biol Rev 25:220–254

    Article  CAS  Google Scholar 

  • Gray TRG, Williams ST (1971) Microbial productivity in the soil. In: Hughes AH, Rose AA (eds) Microbes and biological productivity. Cambridge University Press, pp. 255–286

  • Harley JL (1949) Mycorrhiza. Nature 164:1041–1042

    Article  Google Scholar 

  • Harley JL (1952) Associations between microorganisms and higher plants (mycorrhiza). Annu Rev Microbiol 6:367–386

    Article  CAS  Google Scholar 

  • Harley JL (1969) The Biology of mycorrhiza, second edition. Plant science monographs, Ed. N. Polunin. Leonard Hill, London

    Google Scholar 

  • Harley JL (1975) Problems of mycotrophy. In: endomycorrhizas. Proceedings of a symposium held at University of Leeds, 22–25 July 1974. Academic Press, London

  • Harley JL (1989) Concluding address. Agric Ecosyst Environ 29:457–461

    Article  Google Scholar 

  • Hasselquist NJ, Metcalfe DB, Inselsbacher E, Stangl Z, Oren R, Näsholm T, Högberg P (2016) Greater carbon allocation to mycorrhizal fungi reduces tree nitrogen uptake in a boreal forest. Ecology 97:1012–1022. https://doi.org/10.1890/15-1222.1

    Article  PubMed  Google Scholar 

  • Hibbett DS, Gilbert LB, Donoghue MJ (2000) Evolutionary instability of ectomycorrhizal symbioses in basidiomycetes. Nature 407:506–508. https://doi.org/10.1038/35035065

    Article  CAS  PubMed  Google Scholar 

  • Högberg MN, Högberg P (2002) Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil. New Phytol 154(3):791–795

    Article  Google Scholar 

  • Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol 135(4):575–585

    Article  Google Scholar 

  • Jones MD, Smith SE (2004) Exploring functional definitions of mycorrhizas: are mycorrhizas always mutualisms? Can J Bot 82:1089–1109. https://doi.org/10.1139/b04-110

    Article  Google Scholar 

  • Karst J, Marczak L, Jones MD, Turkington R (2008) The mutualism-parasitism continuum in ectomycorrhizas: a quantitative assessment using meta-analysis. Ecology 89(4):1032–1042

    Article  Google Scholar 

  • Koide R, Kabir Z (2001) Nutrient economy of red pine is affected by interactions between Pisolithus tinctorius and other forest-floor microbes. New Phytol 150(1):179–188

    Article  Google Scholar 

  • Koide RT, Wu T (2003) Ectomycorrhizas and retarded decomposition in a Pinus resinosa plantation. New Phytol 158:401–407. https://doi.org/10.1046/j.1469-8137.2003.00732.x

    Article  Google Scholar 

  • Koide RT, Sharda JN, Herr JR, Malcolm GM (2008) Ectomycorrhizal fungi and the biotrophy–saprotrophy continuum. New Phytol 178:230–233

    Article  Google Scholar 

  • Koide RT, Fernandez CW, Peoples MS (2011) Can ectomycorrhizal colonization of Pinus resinosa roots affect their decomposition? New Phytol 191(2):508–514

    Article  Google Scholar 

  • Kuzyakov Y, Friedel JK, Stahr K (2000) Review of mechanisms and quantification of priming effects. Soil Biol Biochem 32:1485–1498. https://doi.org/10.1016/S0038-0717(00)00084-5

    Article  CAS  Google Scholar 

  • Kyaschenko J, Clemmensen KE, Karltun E, Lindahl BD (2017) Below-ground organic matter accumulation along a boreal forest fertility gradient relates to guild interaction within fungal communities. Ecol Lett 20:1546–1555. https://doi.org/10.1111/ele.12862

    Article  Google Scholar 

  • Lenaers M, Reyns W, Czech J, Carleer R, Basak I, Deferme W, Krupinska P, Yildiz T, Saro S, Remans T, Vangronsveld J, de Laender F, Rineau F (2018) Links between heathland fungal biomass mineralization, melanization, and hydrophobicity. Microb Ecol. https://doi.org/10.1007/s00248-018-1167-3

    Article  CAS  Google Scholar 

  • Lewis DH (1975) Comparative aspects of the carbon nutrition of mycorrhizas. In: Endomycorrhizas. Proceedings of a symposium held at University of Leeds, 22–25 July 1974. Academic Press, London

  • Lindahl BD, Tunlid A (2014) Ectomycorrhizal fungi—potential organic matter decomposers, yet not saprotrophs. New Phytol 205(205):1443–1447

    PubMed  Google Scholar 

  • Manzoni S, Taylor P, Richter A, Porporato A, Ågren GI (2012) Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytol 196:79–91. https://doi.org/10.1111/j.1469-8137.2012.04225.x

    Article  CAS  Google Scholar 

  • Näsholm T, Högberg P, Franklin O, Metcalfe D, Keel SG, Campbell C, Hurry V, Linder S, Högberg MN (2013) Are ectomycorrhizal fungi alleviating or aggravating nitrogen limitation of tree growth in boreal forests? New Phytol 198:214–221. https://doi.org/10.1111/nph.12139

    Article  CAS  PubMed  Google Scholar 

  • Orwin KH, Kirschbaum MUF, St John MG, Dickie IA (2011) Organic nutrient uptake by mycorrhizal fungi enhances ecosystem carbon storage: a model-based assessment. Ecol Lett 14:493–502. https://doi.org/10.1111/j.1461-0248.2011.01611.x

    Article  Google Scholar 

  • Reid CPP, Kidd FA, Ekwebelam SA (1983) Nitrogen nutrition, photosynthesis and carbon allocation in ectomycorrhizal pine. Plant Soil 71(1–3):415–443

    Article  CAS  Google Scholar 

  • Rineau F, Shah F, Smits MM, Persson P, Johansson T, Carleer R, Troein C, Tunlid A (2013) Carbon availability triggers the decomposition of plant litter and assimilation of nitrogen by an ectomycorrhizal fungus. ISME J 7(10):2010–2022

    Article  CAS  Google Scholar 

  • Rygiewicz PT, Andersen CP (1994) Mycorrhizae alter quality and quantity of carbon allocated below ground. Nature 369(6475):58–60

    Article  Google Scholar 

  • Sanders FE, Tinker PB (1973) Phosphate flow in mycorrhizal roots. Pestic Sci 4:388–395

    Article  Google Scholar 

  • Schwartz MW, Hoeksema JD (1998) Specialization and resource trade: biological markets as a model of mutualisms. Ecology 79:1029–1038. https://doi.org/10.1890/0012-9658(1998)079[1029:SARTBM]2.0.CO;2

    Article  Google Scholar 

  • Siletti CE, Zeiner CA, Bhatnagar JM (2017) Distributions of fungal melanin across species and soils. Soil Biol Biochem 113:285–293. https://doi.org/10.1016/j.soilbio.2017.05.030

    Article  CAS  Google Scholar 

  • Smith D, Lewis D (1994) John Laker Harley. 17 November 1911 - 13 December 1990. Biogr Mem Fellows R Soc 39:158–175

    Article  Google Scholar 

  • Smith GR, Finlay RD, Stenlid J, Vasaitis R, Menkis A (2017) Growing evidence for facultative biotrophy in saprotrophic fungi: data from microcosm tests with 201 species of wood-decay basidiomycetes. New Phytol 215:747–755. https://doi.org/10.1111/nph.14551

    Article  CAS  PubMed  Google Scholar 

  • Song YY, Simard SW, Carroll A, Mohn WW, Zeng RS (2015) Defoliation of interior Douglas-fir elicits carbon transfer and stress signalling to ponderosa pine neighbors through ectomycorrhizal networks. Sci Rep 5:1–9. https://doi.org/10.1038/srep08495

    Article  CAS  Google Scholar 

  • Vasiliauskas R, Menkis A, Finlay RD, Stenlid J (2007) Wood-decay fungi in fine living roots of conifer seedlings. New Phytol 174(2):441–446

    Article  CAS  Google Scholar 

  • Wang T, Tian Z, Bengtson P, Tunlid A, Persson P (2017) Mineral surface-reactive metabolites secreted during fungal decomposition contribute to the formation of soil organic matter. Environ Microbiol 19:5117–5129. https://doi.org/10.1111/1462-2920.13990

    Article  CAS  PubMed  Google Scholar 

  • Wiemken V, Boller T (2002) Ectomycorrhiza: gene expression, metabolism and the wood-wide web. Curr Opin Plant Biol 5(4):355–361. https://doi.org/10.1016/S1369-5266(02)00269-8

    Article  CAS  PubMed  Google Scholar 

  • Wu B (2014) Visualization of nutrient translocation in ectomycorrhizal symbioses. Botany 133:129–133. https://doi.org/10.1139/cjb-2013-0093

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank the planning committee of the 9th International Conference on Mycorrhiza and, particularly, Jan Jansa for inviting us to present this paper. We also thank two anonymous reviewers for their valuable comments. Roger Koide received funding from Brigham Young University.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Roger T. Koide.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Koide, R.T., Fernandez, C.W. The continuing relevance of “older” mycorrhiza literature: insights from the work of John Laker Harley (1911–1990). Mycorrhiza 28, 577–586 (2018). https://doi.org/10.1007/s00572-018-0854-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-018-0854-8

Keywords

Navigation