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Article | Open Access

Profundae diversitas: the uncharted genetic diversity in a newly studied group of fungal root endophytes

Brian R. Murphya,( ), Lucia Martin Nietob, Fiona M. Doohanc, Trevor R. Hodkinsona
School of Natural Sciences & Trinity Centre for Biodiversity Research, Trinity College Dublin, College Green, Dublin 2, Ireland
Agricultural and Environmental Sciences Faculty, Salamanca University, 37007 Salamanca, Spain
UCD Earth Institute and School of Biology & Environmental Science, University College Dublin, Dublin 4, Ireland

This research was carried out at Botany Department, School of Natural Sciences & Trinity Centre for Biodiversity Research, Trinity College Dublin, College Green, Dublin 2, Ireland.

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Abstract

Endophytes associated with crops have potential as beneficial inoculants in agriculture, but little is known about their genetic diversity and phylogenetic relationships. We carried out the first ever ecological and phylogenetic survey of the culturable fungal root endophytes of a wild barley species. Fungal root endophytes were isolated from 10 populations of wall barley (Hordeum murinum), and 112 taxa of fungi were identified based on internal transcribed spacer sequence similarity. We found representatives from 8 orders, 12 families and 18 genera. Within this group, only 34 isolates (30% of the total) could be confidently assigned to a species, and 23 of the isolates (21% of the total) had no significant match to anything deposited in GenBank (based on <85% sequence similarity). These results suggest a high proportion of novel fungi, with 28% not assigned to a known fungal order. This includes three endophytes that have been shown to significantly improve agronomic traits in cultivated barley. This study has, therefore, revealed a profound diversity of fungal root endophytes in a single wild relative of barley. Extrapolating from this, the study highlights the largely unknown, hugely diverse and potentially useful resource of crop wild relative endophytes.

Keywords

genetic diversitybiocontrolHordeum murinumfungal root endophytesbiofertilisation

References

 

Achatz B, Rüden S, Andrade D, Neumann E, Pons-Kühnemann J, Kogel K-H, Franken P, Waller F. 2010. Root colonization by Piriformospora indica enhances grain yield in barley under diverse nutrient regimes by accelerating plant development. Plant Soil. 333:59–70.
Crossref Google Scholar
 

Allen TR, Millar T, Berch SM, Berbee ML. 2003. Culturing and direct DNA extraction find different fungi from the same ericoid mycorrhizal roots. New Phytol. 160:255–272.
Crossref Google Scholar
 

Altschul S, Madden T, Schaffer A, Zhang J, Zhang Z, Miller W, Dj L. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389–3402.
Crossref Google Scholar
 

Anderson IC, Cairney JWG. 2004. Diversity and ecology of soil fungal communities: increased understanding through the application of molecular techniques. Environ Microbiol. 6:769–779.
Crossref Google Scholar
 

Andrade-Linares DR, Grosch R, Franken P, Rexer K-H, Kost G, Restrepo S, de Garcia MCC, Maximova E. 2011. Colonization of roots of cultivated Solanum lycopersicum by dark septate and other ascomycetous endophytes. Mycologia. 103:710–721.
Crossref Google Scholar
 

Arnold AE, Lutzoni F. 2007. Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology. 88:541–549.
Crossref Google Scholar
 

Blattner FR. 2009. Progress in phylogenetic analysis and a new infrageneric classification of the barley genus Hordeum (Poaceae: Triticeae). Breed Sci. 59:471–480.
Crossref Google Scholar
 

Booth TA, Richards AJ. 1976. Studies in the Hordeum murinum aggregate: 1. Morphology. Bot J Linnean Soc. 72:149–159.
Crossref Google Scholar
 

Booth TA, Richards AJ. 1978. Studies in the Hordeum murinum L. aggregate: disc electrophoresis of seed proteins. Bot J Linnean Soc. 76:115–125.
Crossref Google Scholar
 
Cannon PF, Kirk PM, editors. 2007. Fungal families of the world. London: CABI.
Crossref
 

Chen K-H, Miadlikowska J, Molnar K, Arnold AE, U’Ren JM, Gaya E, Gueidan C, Lutzoni F. 2015. Phylogenetic analyses of eurotiomycetous endophytes reveal their close affinities to Chaetothyriales, Eurotiales, and a new order – Phaeomoniellales. Mol Phylogenet Evol. 85:117–130.
Crossref Google Scholar
 

Cheplick GP, Faeth S. 2009. Ecology and evolution of the grass-endophyte symbiosis. New York (NY): Oxford University Press.
Crossref
 

Clement SL, Wilson AD, Lester DG, Davitt CM. 1997. Fungal endophytes of wild barley and their effects on Diuraphis noxia population development. Entomol Exp Appl. 82:275–281.
Crossref Google Scholar
 
Consultative Group on International Agricultural Research (CGIAR). 2012. Barley. Montpellier (France): CGIAR; [cited 2014 Mar 17]. Available from: http://www.cgiar.org/our-research/crop-factsheets/barley/
 
Cope T, Gray A. 2009. Grasses of the British Isles. B.S.B.I. Handbook No. 13. London: Botanical Society of the British Isles; 612 pp.
 

de Souza Leite T, Cnossen-Fassoni A, Pereira OL, Mizubuti ESG, de Araújo EF, de Queiroz MV. 2013. Novel and highly diverse fungal endophytes in soybean revealed by the consortium of two different techniques. J Microbiol. 51:56–69.
Crossref Google Scholar
 

Dugan S, Sullivan W. 2002. The Neotyphodium endophyte of wild barley (Hordeum brevisubulatum subsp. violaceum) grows and sporulates on leaf surfaces of the host. Symbiosis. 32:147–159.
Google Scholar
 

Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792–1797.
Crossref Google Scholar
 

Ek-Ramos MJ, Zhou W, Valencia CU, Antwi JB, Kalns LL, Morgan GD, Kerns DL, Sword GA. 2013. Spatial and temporal variation in fungal endophyte communities isolated from cultivated cotton (Gossypium hirsutum). Plos One. 8:e66049.
Crossref Google Scholar
 

El-Mougith AA. 1993. The effect of salinity on some halophilic soil fungi. In: Lieth H, Al Masoom AA, editors. Tasks for vegetation science. Towards the rational use of high salinity tolerant plants: tasks for vegetation science. Dordrecht (Netherlands): Springer; p. 473–477.
Crossref Google Scholar
 

Etherington GJ, Dicks J, Roberts IN. 2005. Recombination Analysis Tool (RAT): a program for the high-throughput detection of recombination. Bioinformatics. 21:278–281.
Crossref Google Scholar
 
Fernandes EG, Pereira OL, da Silva CC, Bento CBP, de Queiroz MV. 2015. Diversity of endophytic fungi in Glycine max. Microbiol Res. doi: 10.1016/j.micres.2015.05.010
Crossref
 

Garthwaite AJ, von Bothmer R, Colmer TD. 2005. Salt tolerance in wild Hordeum species is associated with restricted entry of Na+ and Cl- into the shoots. J Exp Bot. 56:2365–2378.
Crossref Google Scholar
 

Giles BE, Lefkovitch LP. 1986. A taxonomic investigation of the Hordeum murinum complex (Poaceae). Plant Syst Evol. 153:181–197.
Crossref Google Scholar
 

Jakob SS, Blattner FR. 2010. Molecular phylogenetics and evolution two extinct diploid progenitors were involved in allopolyploid formation in the Hordeum murinum (Poaceae: Triticeae) taxon complex. Mol Phylogenet Evol. 55:650–659.
Crossref Google Scholar
 

Jorgensen RB, Jensen CJ, Andersen B, Von Bothmer R. 1986. High capacity of plant regeneration from callus of interspecific hybrids with cultivated barley (Hordeum vulgare L.). Plant Cell Tissue Organ Cult. 6:199–207.
Crossref Google Scholar
 

Ko Ko TW, Stephenson SL, Bahkali AH, Hyde KD. 2011. From morphology to molecular biology: can we use sequence data to identify fungal endophytes? Fungal Divers. 50:113–120.
Crossref Google Scholar
 
Murphy BR. 2013. Fungal infection in barley roots – friend and foe. In: Schneider C, Leifert C, Feldman F, editors. Endophytes for plant protection: the state of the art. Braunschweig: Deutsche Phytomedizinische Gesellschaft; p. 102–116.
 

Murphy BR, Doohan FM, Hodkinson TR. 2013. Mechanisms of beneficial colonisation of barley by fungal root endophytes. Asp Appl Biol. 120:35–44.
Google Scholar
 

Murphy BR, Doohan FM, Hodkinson TR. 2014a. Fungal endophytes of barley roots. J Agric Sci. 152:602–615.
Crossref Google Scholar
 

Murphy BR, Doohan FM, Hodkinson TR. 2014b. Yield increase induced by the fungal root endophyte Piriformospora indica in barley grown at low temperature is nutrient limited. Symbiosis. 62:29–39.
Crossref Google Scholar
 

Murphy BR, Doohan FM, Hodkinson TR. 2015a. Persistent fungal root endophytes isolated from a wild barley species suppress seed-borne infections in a barley cultivar. Biocontrol. 60:281–292.
Crossref Google Scholar
 

Murphy BR, Doohan FM, Hodkinson TR. 2015b. Fungal root endophytes of a wild barley species increase yield in a nutrient-stressed barley cultivar. Symbiosis. 65:1–7.
Crossref Google Scholar
 

Nilsson RH, Ryberg M, Kristiansson E, Abarenkov K, Larsson KH, Koljalg U. 2006. Taxonomic reliability of DNA sequences in public sequence databases: a fungal perspective. PLoS One. 1:e59.
Crossref Google Scholar
 

Parnell J, Curtis T. 2012. Webb’s: an Irish flora. Cork: Cork University Press.
Crossref
 
Poland J, Clement E. 2009. The vegetative key to the British flora. Southampton: John Poland.
 

Porras-alfaro A, Bayman P. 2011. Hidden fungi, emergent properties: endophytes and microbiomes. Annu Rev Phytopathol. 49:291–315.
Crossref Google Scholar
 

Porter MS, Beiko RG. 2013. SPANNER: taxonomic assignment of sequences using pyramid matching of similarity profiles. Bioinformatics. 29:1858–1864.
Crossref Google Scholar
 

Quaedvlieg W, Verkley GJM, Shin H-D, Barreto RW, Alfenas AC, Swart WJ, Groenewald JZ, Crous PW. 2013. Sizing up Septoria. Stud Mycol. 75:307–390.
Crossref Google Scholar
 
Rambaut A. 2012. FigTree. Tree figure drawing tool version 1.4.0. Institute of Evolutionary Biology, University of Edinburgh. Available from: http://tree.bio.ed.ac.uk
 

Richards AJ, Booth TA. 1977. Karyological indications of evolution in Hordeum murinum sensu lato. In: Jones K, Brandham PE, editors. Current chromosome research. Amsterdam: North-Holland; p. 167–174.
Google Scholar
 

Riess K, Oberwinkler F, Bauer R, Garnica S. 2014. Communities of endophytic Sebacinales associated with roots of herbaceous plants in agricultural and grassland ecosystems are dominated by Serendipita herbamans sp. nov. Plos One. 9:e94676.
Crossref Google Scholar
 

Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim Y-O, Redman RS. 2008. Stress tolerance in plants via habitat-adapted symbiosis. ISME J. 2:404–416.
Crossref Google Scholar
 

Rodriguez RJ, White, Jr. JF, Arnold AE, Redman RS. 2009. Fungal endophytes: diversity and functional roles. New Phytologist. 182:314–330.
Crossref Google Scholar
 

Sánchez Márquez S, Bills GF, Herrero N, Zabalgogeazcoa Í. 2012. Non-systemic fungal endophytes of grasses. Fungal Ecol. 5:289–297.
Crossref Google Scholar
 

Saunders M, Glenn AE, Kohn LM. 2010. Exploring the evolutionary ecology of fungal endophytes in agricultural systems: using functional traits to reveal mechanisms in community processes. Evol Appl. 3:525–537.
Crossref Google Scholar
 
Scannell MJP, Synnott DM. 1987. Census catalogue of the flora of Ireland. Dublin: The Stationery Office.
 

Schulz B, Boyle C. 2006. What are endophytes? In: Schulz BJE, Boyle CJC, Sieber TN, editors. Microbial root endophytes. Berlin: Springer-Verlag; p. 1–14.
Crossref Google Scholar
 

Stace C. 2010. New flora of the British Isles. Cambridge: Cambridge University Press.
 
Streeter D, Hart-Davies C, Hardcastle A, Cole F, Harper L. 2009. Collins flower guide. London: HarperCollins Publishers.
 

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 30:2725–2729.
Crossref Google Scholar
 

Torres MS, White JF, Zhang X, Hinton DM, Bacon CW. 2012. Endophyte-mediated adjustments in host morphology and physiology and effects on host fitness traits in grasses. Fungal Ecol. 5:322–330.
Crossref Google Scholar
 

Verma VC, Gond SK, Kumar A, Kharwar RN, Boulanger L-A, Strobel GA. 2011. Endophytic fungal flora from roots and fruits of an Indian neem plant Azadirachta indica A. Juss., and impact of culture media on their isolation. Indian J Microbiol. 51:469–476.
Crossref Google Scholar
 
Von Bothmer R, Jacobsen N, Baden C, Jorgensen R, Linde-Laursen I. 1995. An ecogeographical study of the genus Hordeum. Rome: International Plant Genetic Resources Institute.
 

Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Hückelhoven R, Neumann C, von Wettstein D, et al. 2005. The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci USA. 102:13386–13391.
Crossref Google Scholar
 

Wang Z, Johnston PR, Yang ZL, Townsend JP. 2009. Evolution of reproductive morphology in leaf endophytes. Plos One. 4:e4246.
Crossref Google Scholar
 

Weiss M, Selosse M-A, Rexer K-H, Urban A, Oberwinkler F. 2004. Sebacinales: a hitherto overlooked cosm of heterobasidiomycetes with a broad mycorrhizal potential. Mycol Res. 108:1003–1010.
Crossref Google Scholar
 

Weiss M, Sýkorová Z, Garnica S, Riess K, Martos F, Krause C, Oberwinkler F, Bauer R, Redecker D. 2011. Sebacinales everywhere: previously overlooked ubiquitous fungal endophytes. Plos One. 6:e16793.
Crossref Google Scholar
 

White TJ, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics, PCR protocols: a guide to methods and applications. San Diego (CA): Academic Press; p. 315–322.
Crossref
 

Zadoks JC, Chang TT, Konzak CF. 1974. A decimal code for the growth stages of cereals. Weed Res. 14:415–421.
Crossref Google Scholar
Mycology
Volume 6 Issue 3-4,
December 2015
Pages 139-150
DOI: 10.1080/21501203.2015.1070213
Cite this article:
Murphy BR, Nieto LM, Doohan FM, et al. Profundae diversitas: the uncharted genetic diversity in a newly studied group of fungal root endophytes. Mycology, 2015, 6(3-4): 139-150. https://doi.org/10.1080/21501203.2015.1070213

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Received: 22 March 2015
Accepted: 02 July 2015
Published: 24 July 2015
© 2015 The Author(s).

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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