Hostname: page-component-848d4c4894-pftt2 Total loading time: 0 Render date: 2024-05-04T06:42:19.132Z Has data issue: false hasContentIssue false
  • English
  • Français

Fungal endophytes of barley roots

Published online by Cambridge University Press:  13 June 2013

B. R. MURPHY ,
F. M. DOOHAN  and
T. R. HODKINSON
B. R. MURPHY*
Affiliation:
School of Natural Sciences, Trinity College Dublin, College Green, Dublin 2, Ireland
F. M. DOOHAN
Affiliation:
School of Biology and Environmental Science, University College Dublin, Dublin 4, Ireland
T. R. HODKINSON
Affiliation:
School of Natural Sciences, Trinity College Dublin, College Green, Dublin 2, Ireland
*
*To whom all correspondence should be addressed. Email: murphb16@tcd.ie
Get access Rights & Permissions [Opens in a new window]

Summary

Fungal infections of barley have tremendous agricultural significance, and can be detrimental or beneficial. Beneficial root infections often involve endophytic fungi, but endophytic associations do not always confer benefits on their hosts. Endophyte infection can be negative, positive or neutral for the host. Benefits to barley and other plants infected with endophytic root fungi include an increase in seed yield, enhanced resistance to pathogens and improved stress tolerance. Even if an endophyte is never pathogenic, it is not always beneficial. The most important factors that determine the nature of the relationship are the specific combination of partner genotypes and developmental stage, and the ecological and environmental setting. The nutrient status of the plant and the availability of soil nutrients may have little effect on the degree of beneficial endophyte colonization and, unlike mycorrhizae, there is no apparent increase in endophyte-associated phosphorous transfer. There are indications of an association between successful endophyte colonization and high soil pH and clay content. The greatest benefits to the barley plant resulting from the associations seem to be obtained in abiotically stressed environments. Fungal infection may give the plant a greater ability to cope with the stress if the partners are in a balanced relationship. Each new study reveals an increasing diversity of beneficial fungal root endophytes and the full potential of these organisms is still to be determined. Further studies are urgently required to develop specific beneficial root–endophyte associations, or combination of them, that are tailored to individual barley varieties for maximum impact in agriculture.

Type
Crops and Soils Review
Information
The Journal of Agricultural Science , Volume 152 , Issue 4 , August 2014 , pp. 602 - 615
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Achatz, B., von 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 and Soil 333, 59–70.CrossRefGoogle Scholar
Ahmad, P., Azooz, M. M. & Prasad, M. N. V. (2013). Ecophysiology and Responses of Plants under Salt Stress. Berlin: Springer-Verlag.Google Scholar
Akiyama, K., Matsuzaki, K. & Hayashi, H. (2005). Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435, 824–827.Google Scholar
An, Q., Ehlers, K., Kogel, K-H., van Bel, A. J. E. & Hückelhoven, R. (2006). Multivesicular compartments proliferate in susceptible and resistant MLA12-barley leaves in response to infection by the biotrophic powdery mildew fungus. New Phytologist 172, 563–576.Google Scholar
Arnold, A. E. & Lutzoni, F. (2013). Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88, 541–549.Google Scholar
Baltruschat, H., Fodor, J., Harrach, B. D., Niemczyk, E., Barna, B., Gullner, G., Janeczko, A., Kogel, K-H., Schäfer, P., Schwarczinger, I., Zuccaro, A. & Skooczowski, A. (2008). Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. New Phytologist 180, 501–510.Google Scholar
Basiewicz, M., Weiss, M., Kogel, K-H., Langen, G., Zorn, H. & Zuccaro, A. (2012). Molecular and phenotypic characterization of Sebacina vermifera strains associated with orchids, and the description of Piriformospora williamsii sp. nov. Fungal Biology 116, 204–213.CrossRefGoogle ScholarPubMed
Berg, G. & Smalla, K. (2009). Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiology Ecology 68, 1–13.Google Scholar
Black, R. & Tinker, P. B. (1979). Effect of agronomic factors and soil conditions on the development of vesicular-arbuscular mycorrhizal infection in barley and on the endophyte spore density. New Phytologist 83, 401–413.CrossRefGoogle Scholar
Blumwald, E. & Poole, R. J. (1987). Salt tolerance in suspension cultures of sugar beet: induction of na/h antiport activity at the tonoplast by growth in salt. Plant Physiology 83, 884–887.Google Scholar
Cheplick, G. P. & Faeth, S. (2009). Ecology and Evolution of the Grass-Endophyte Symbiosis. New York: Oxford University Press.CrossRefGoogle Scholar
Clay, K. & Schardl, C. (2002). Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. American Naturalist 160(Suppl.), S99–S127.Google Scholar
Clement, S. L., Wilson, A. D., Lester, D. G. & Davitt, C. M. (1997). Fungal endophytes of wild barley and their effects on Diuraphis noxia population development. Entomologia Experimentalis et Applicata 82, 275–281.Google Scholar
Consultative Group On International Agricultural Research (CGIAR) (2012). Barley. Montpellier, France: CGIAR. Available online at: http://www.cgiar.org/our-research/crop-factsheets/barley/ (accessed 9 May 2013).Google Scholar
Criddle, R. S., Hansen, L. D., Breidenbach, R. W., Ward, M. R. & Huffaker, R. C. (1989). Effects of NaCI on metabolic heat evolution rates by barley roots. Plant Physiology 90, 53–58.Google Scholar
Czarnoleski, M., Olejniczak, P., Górzyńska, K., Kozłowski, J. & Lembicz, M. (2012). Altered allocation to roots and shoots in the endophyte-infected seedlings of Puccinellia distans (Poaceae). Plant Biology (Stuttgart, Germany) 15, 264–273.Google Scholar
Deshmukh, S., Hückelhoven, R., Schäfer, P., Imani, J., Sharma, M., Weiss, M., Waller, F. & Kogel, K-H. (2006). The root endophytic fungus Piriformospora indica requires host cell death for proliferation during mutualistic symbiosis with barley. Proceedings of the National Academy of Sciences of the United States of America 103, 18450–18457.Google Scholar
Deshmukh, S. D. & Kogel, K-H. (2007). Piriformospora indica protects barley from root rot caused by Fusarium graminearum. Journal of Plant Diseases and Protection 114, 263–268.Google Scholar
de Souza Leite, T., Cnossen-Fassoni, A., Pereira, O. L., Mizubuti, E. S. G., De Araújo, E. F. & De Queiroz, M. V. (2013). Novel and highly diverse fungal endophytes in soybean revealed by the consortium of two different techniques. Journal of Microbiology (Seoul, Korea) 51, 56–69.Google Scholar
Dixon, R. K., Rao, M. V. & Garg, V. K. (1993). Salt stress affects in vitro growth and in situ symbioses of ectomycorrhizal fungi. Mycorrhiza 3, 63–68.Google Scholar
Dugan, F., Sitton, J., Sullivan, R. & White, J. (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
Eichmann, R., Dechert, C., Kogel, K-H. & Huckelhoven, R. (2006). Transient over-expression of barley BAX Inhibitor-1 weakens oxidative defence and MLA12-mediated resistance to Blumeria graminis f. sp. hordei. Molecular Plant Pathology 7, 543–552.Google Scholar
Fávaro, L. C. d L., Sebastianes, F. L. d S. & Araújo, W. L. (2012). Epicoccum nigrum P16, a sugarcane endophyte, produces antifungal compounds and induces root growth. PLoS ONE 7, e36826. doi:10.1371/journal.pone.0036826.Google Scholar
Felle, H. H., Waller, F., Molitor, A. & Kogel, K-H. (2009). The mycorrhiza fungus Piriformospora indica induces fast root-surface pH signaling and primes systemic alkalinization of the leaf apoplast upon powdery mildew infection. Molecular Plant-Microbe Interactions 22, 1179–1185.Google Scholar
Genre, A., Chabaud, M., Timmers, T., Bonfante, P. & Barker, D. G. (2005). Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17, 3489–3499.Google Scholar
Ghahfarokhi, R. M. & Goltapeh, M. E. (2010). Potential of the root endophytic fungus Piriformospora indica, Sebacina vermifera and Trichoderma species in biocontrol of take-all disease of wheat Gaeumannomyces graminis var. tritici in vitro. Journal of Agricultural Technology 6, 11–18.Google Scholar
Gorischek, A. M., Afkhami, M. E., Seifert, E. K. & Rudgers, J. A. (2013). Fungal symbionts as manipulators of plant reproductive biology. American Naturalist 181, 562–570.Google Scholar
Harrach, B. D., Baltruschat, H., Barna, B., Fodor, J. & Kogel, K-H. (2013). The mutualistic fungus Piriformospora indica protects barley roots from a loss of antioxidant capacity caused by the necrotrophic pathogen Fusarium culmorum. Molecular Plant-Microbe Interactions 26, 599–605.Google Scholar
Hashem, M. & Ali, E. (2004). Epicoccum nigrum as biocontrol agent of Pythium damping-off and root-rot of cotton seedlings. Archives of Phytopathology and Plant Protection 37, 283–297.Google Scholar
Hilbert, M., Voll, L. M., Ding, Y., Hofmann, J., Sharma, M. & Zuccaro, A. (2012). Indole derivative production by the root endophyte Piriformospora indica is not required for growth promotion but for biotrophic colonization of barley roots. New Phytologist 196, 520–534.Google Scholar
Horie, T. & Schroeder, J. I. (2004). Sodium transporters in plants. Diverse genes and physiological functions. Plant Physiology 136, 2457–2462.Google Scholar
Imani, J., Li, L., Schäfer, P. & Kogel, K-H. (2011). STARTS – a stable root transformation system for rapid functional analyses of proteins of the monocot model plant barley. Plant Journal 67, 726–35.Google Scholar
Istifadah, N. & McGee, P. A. (2006). Endophytic Chaetomium globosum reduces development of tan spot in wheat caused by Pyrenophora tritici-repentis. Australasian Plant Pathology 35, 411–418.Google Scholar
Joseph, B. & Priya, R. M. (2011). Bioactive compounds from endophytes and their potential in pharmeceutical effect: a review. American Journal of Biochemistry and Molecular Biology 1, 291–309.Google Scholar
Kaldorf, M., Koch, B., Rexer, K.-H., Kost, G. & Varma, A. (2005). Patterns of interaction between Populus Esch5 and Piriformospora indica: a transition from mutualism to antagonism. Plant Biology 7, 210–218.Google Scholar
Khaosaad, T., García-Garrido, J. M., Steinkellner, S. & Vierheilig, H. (2007). Take-all disease is systemically reduced in roots of mycorrhizal barley plants. Soil Biology and Biochemistry 39, 727–734.Google Scholar
Khatabi, B., Molitor, A., Lindermayr, C., Pfiffi, S., Durner, J., Von Wettstein, D., Kogel, K-H. & Schäfer, P. (2012). Ethylene supports colonization of plant roots by the mutualistic fungus Piriformospora indica. PLoS ONE 7, e35502. doi:10.1371/journal.pone.0035502.Google Scholar
Knupfer, H., Maggioni, L., Jalli, M., Kolodinsla, A., Fasoula, D. & Lipman, E. (2011). Report of a Working Group on Barley. Seventh Meeting, 11–12 May 2011, Nicosia, Cyprus. Nicosia, Cyprus: ECPGR.Google Scholar
Kogel, K-H., Franken, P. & Hückelhoven, R. (2006). Endophyte or parasite – what decides? Current Opinion in Plant Biology 9, 358–363.Google Scholar
Kumar, D. S. S. & Hyde, K. D. (2004). Biodiversity and tissue-recurrence of endophytic fungi in Tripterygium wilfordii. Fungal Diversity 17, 69–90.Google Scholar
Lahrmann, U. & Zuccaro, A. (2012). Opprimo ergo sum – evasion and suppression in the root endophytic fungus Piriformospora indica. Molecular Plant-Microbe Interactions 25, 727–737.Google Scholar
Liang, H., Xing, Y., Chen, J., Zhang, D., Guo, S. & Wang, C. (2012). Antimicrobial activities of endophytic fungi isolated from Ophiopogon japonicus (Liliaceae). BMC Complementary and Alternative Medicine 12, 238. doi:10.1186/1472-6882-12-238.Google Scholar
Maciá-Vicente, J. G., Jansson, H-B., Mendgen, K. & Lopez-Llorca, L. V. (2008 a). Colonization of barley roots by endophytic fungi and their reduction of take-all caused by Gaeumannomyces graminis var. tritici. Canadian Journal of Microbiology 54, 600–609.Google Scholar
Maciá-Vicente, J. G., Jansson, H-B., Abdullah, S. K., Descals, E., Salinas, J. & Lopez-Llorca, L. V. (2008 b). Fungal root endophytes from natural vegetation in Mediterranean environments with special reference to Fusarium spp. FEMS Microbiology Ecology 64, 90–105.CrossRefGoogle ScholarPubMed
Maciá-Vicente, J. G., Jansson, H-B., Talbot, N. J. & Lopez-Llorca, L. V. (2009). Real-time PCR quantification and live-cell imaging of endophytic colonisation of barley (Hordeum vulgare) roots by Fusarium equiseti and Pochonia chlamydosporia. New Phytologist 182, 213–228.Google Scholar
Martín, J. A., Witzell, J., Blumenstein, K., Rozpedowska, E., Helander, M., Sieber, T. N. & Gil, L. (2013). Resistance to Dutch elm disease reduces presence of xylem endophytic fungi in elms (Ulmus spp.). PLoS ONE 8: e56987. doi:10.1371/journal.pone.0056987.Google Scholar
Mathre, D. E. (1997). Compendium of Barley Diseases. New York: American Phytopathological Society.Google Scholar
Mayerhofer, M. S., Kernaghan, G. & Harper, K. A. (2012). The effects of fungal root endophytes on plant growth: a meta-analysis. Mycorrhiza 23, 119–128.Google Scholar
Mohammad, M. J., Malkawi, H. I. & Shibli, R. (2011). Effects of arbuscular mycorrhizal fungi and phosphorus fertilization on growth and nutrient uptake of barley grown on soils with different levels of salts. Journal of Plant Nutrition 26, 125–137.Google Scholar
Molitor, A. & Kogel, K. (2009). Induced resistance triggered by Piriformospora indica. Plant Signaling and Behavior 4, 215–216.Google Scholar
Mousa, W. K. & Raizada, M. N. (2013). The diversity of anti-microbial secondary metabolites produced by fungal endophytes: an interdisciplinary perspective. Frontiers in Microbiology 4, 65. doi: 10.3389/fmicb.2013.00065.Google Scholar
Nukina, M., Sassa, T., Oyama, H. & Ikeda, M. (1979). Structures and biological activities of fungal macrolides, pyrenolide and resorcylide. Tennen Yuki Kagobutsu Toronkai Koen Yoshishu 36, 2–9 (in Japanese).Google Scholar
Oberwinkler, F., Riess, K., Bauer, R., Selosse, M-A., Weiß, M., Garnica, S. & Zuccaro, A. (2013). Enigmatic Sebacinales. Mycological Progress 12, 1–27.Google Scholar
Oelmüller, R., Sherameti, I., Tripathi, S. & Varma, A. (2009). Piriformospora indica, a cultivable root endophyte with multiple biotechnological applications. Symbiosis 49, 1–17.Google Scholar
Opalski, K. S., Schultheiss, H., Kogel, K-H. & Hückelhoven, R. (2005). The receptor-like MLO protein and the RAC/ROP family G-protein RACB modulate actin reorganization in barley attacked by the biotrophic powdery mildew fungus Blumeria graminis f.sp. hordei. Plant Journal 41, 291–303.Google Scholar
Peskan-Berghofer, T., Shahollari, B., Giong, P. H., Hehl, S., Markert, C., Blanke, V., Kost, G., Varma, A. & Oelmuller, R. (2004). Association of Piriformospora indica with Arabidopsis thaliana roots represents a novel system to study beneficial plant–microbe interactions and involves early plant protein modifications in the endoplasmic reticulum and at the plasma membrane. Physiologia Plantarum 122, 465–477.CrossRefGoogle Scholar
Poling, S. M., Wicklow, D. T., Rogers, K. D. & Gloer, J. B. (2008). Acremonium zeae, a protective endophyte of maize, produces dihydroresorcylide and 7-hydroxydihydroresorcylides. Journal of Agricultural and Food Chemistry 56, 3006–3009.Google Scholar
Powell, K. A. & Jutsum, A. R. (1993). Technical and commercial aspects of biocontrol products. Pesticide Science 37, 315–321.Google Scholar
Qiang, X., Weiss, M., Kogel, K-H. & Schäfer, P. (2011). Piriformospora indica – a mutualistic basidiomycete with an exceptionally large plant host range. Molecular Plant Pathology 13, 508–518.Google Scholar
Qiang, X., Zechmann, B., Reitz, M. U., Kogel, K-H. & Schäfer, P. (2012). The mutualistic fungus Piriformospora indica colonizes arabidopsis roots by inducing an endoplasmic reticulum stress-triggered caspase-dependent cell death. Plant Cell 24, 794–809.Google Scholar
Rahnamaeian, M., Langen, G., Imani, J., Khalifa, W., Altincicek, B., von Wettstein, D., Kogel, K-H. & Vilcinskas, A. (2009). Insect peptide metchnikowin confers on barley a selective capacity for resistance to fungal ascomycetes pathogens. Journal of Experimental Botany 60, 4105–4114.Google Scholar
Redman, R. S., Kim, Y. O., Woodward, C. J. D. A., Greer, C., Espino, L., Doty, S. L. & Rodriguez, R. J. (2011). Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: a strategy for mitigating impacts of climate change. PLoS ONE 6, e14823. doi:10.1371/journal.pone.0014823.Google Scholar
Reininger, V., Grünig, C. R. & Sieber, T. N. (2012). Host species and strain combination determine growth reduction of spruce and birch seedlings colonized by root-associated dark septate endophytes. Environmental Microbiology 14, 1064–1076.CrossRefGoogle ScholarPubMed
Rodriguez, R. J., Henson, J., Van Volkenburgh, E., Hoy, M., Wright, L., Beckwith, F., Kim, Y-O. & Redman, R. S. (2008). Stress tolerance in plants via habitat-adapted symbiosis. ISME Journal 2, 404–416.Google Scholar
Rodriguez, R. J., White, J. F., Arnold, A. E. & Redman, R. S. (2009). Fungal endophytes: diversity and functional roles. New Phytologist 182, 314–330.Google Scholar
Sánchez Márquez, S., Bills, G. F., Domínguez Acuña, L. & Zabalgogeazcoa, I. (2010). Endophytic mycobiota of leaves and roots of the grass Holcus lanatus. Fungal Diversity 41, 115–123.Google Scholar
Schafer, P. & Kogel, K-H. (2009). The sebacinoid fungus Piriformospora indica, an orchid mycorrhiza which may increase host plant reproduction and fitness. In Plant Relationships (Ed. Deising, H.), pp. 99–112. Berlin: Springer-Verlag.Google Scholar
Schäfer, P., Pfiffi, S., Voll, L. M., Zajic, D., Chandler, P. M., Waller, F., Scholz, U., Pons-Kühnemann, J., Sonnewald, S., Sonnewald, U. & Kogel, K-H. (2009). Manipulation of plant innate immunity and gibberellin as factor of compatibility in the mutualistic association of barley roots with Piriformospora indica. Plant Journal 59, 461–474.Google Scholar
Schulz, B. & Boyle, C. (2006). What are endophytes? In Microbial Root Endophytes (Eds Schulz, B. J. E., Boyle, C. J. C. & Sieber, Th. N.), pp. 1–13. Berlin: Springer-Verlag.Google Scholar
Schulz, B., Rommert, A-K., Dammann, U., Aust, H-J. & Strack, D. (1999). The endophyte–host interaction: a balanced antagonism? Mycological Research 103, 1275–1283.Google Scholar
Sharma, M., Schmid, M., Rothballer, M., Hause, G., Zuccaro, A., Imani, J., Kämpfer, P., Domann, E., Schäfer, P., Hartmann, A. & Kogel, K-H. (2008). Detection and identification of bacteria intimately associated with fungi of the order Sebacinales. Cellular Microbiology 10, 2235–2246.Google Scholar
Singh, A., Singh, A., Kumari, M., Rai, M. K. & Varma, A. (2003). Biotechnological importance of Piriformospora indica Verma et al. – a novel symbiotic mycorrhiza-like fungus: an overview. Indian Journal of Biotechnology 2, 65–75.Google Scholar
Singh, L. P., Gill, S. S. & Tuteja, N. (2011). Unraveling the role of fungal symbionts in plant abiotic stress tolerance. Plant Signaling and Behavior 6, 175–191.Google Scholar
Soytong, K. & Ratanacherdchai, K. (2005). Application of mycofungicide to control late blight of potato. Journal of Agricultural Technology 1, 19–32.Google Scholar
Soytong, K., Kanokmedhakul, S., Kukongviriyapa, V. & Isobe, M. (2001). Application of Chaetomium species (Ketomium) as a new broad spectrum biological fungicide for plant disease control: A review article. Fungal Diversity 7, 1–15.Google Scholar
Statkevičiūtė, G. & Leistrumaitė, A. (2010). Modern varieties of spring barley as a genetic resource for disease resistance breeding. Agronomy Research 8, 721–728.Google Scholar
Stein, E., Molitor, A., Kogel, K-H. & Waller, F. (2008). Systemic resistance in Arabidopsis conferred by the mycorrhizal fungus Piriformospora indica requires jasmonic acid signaling and the cytoplasmic function of NPR1. Plant and Cell Physiology 49, 1747–1751.Google Scholar
Stone, J. K., Polishook, J. D. & White, J. F. Jr. (2004). Endophytic fungi. In Biodiversity of Fungi: Inventory and Monitoring Methods (Eds Mueller, G. M., Bills, G. F. & Foster, M. S.), pp. 241–270. Amsterdam: Elsevier Inc.Google Scholar
Stracke, S., Kistner, C., Yoshida, S., Mulder, L., Sato, S., Kaneko, T., Tabata, S., Sandal, N., Stougaard, J., Szczyglowski, K. & Parniske, M. (2002). A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417, 959–962.Google Scholar
Sun, C., Liu, Y. L. & Zhang, W. H. (2002). Mechanism of the effect of polyamines on the activity of tonoplast of barley roots under salt stress. Acta Botanica Sinica 44, 1167–1172.Google Scholar
Tellenbach, C., Grünig, C. R. & Sieber, T. N. (2011). Negative effects on survival and performance of Norway spruce seedlings colonized by dark septate root endophytes are primarily isolate-dependent. Environmental Microbiology 13, 2508–2517.CrossRefGoogle ScholarPubMed
Toyoda, K., Collins, N. C., Takahashi, A. & Shirasu, K. (2002). Resistance and susceptibility of plants to fungal pathogens. Transgenic Research 11, 567–582.Google Scholar
Underwood, A. K. (2000). Adjuvant trends for the new millennium. Weed Technology 14, 765–772.Google Scholar
Verma, S., Varma, A., Rexer, K-H., Hassel, A., Kost, G., Sarbhoy, A., Bisen, P., Bütehorn, B. & Franken, P. (1998). Piriformospora indica, gen. et sp. nov., a new root-colonizing fungus. Mycologia 90, 896–903.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, K-H. (2005). The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proceedings of the National Academy of Sciences of the United States of America 102, 13386–13391.CrossRefGoogle ScholarPubMed
Waller, F., Mukherjee, K., Deshmukh, S. D., Achatz, B., Sharma, M., Schäfer, P. & Kogel, K-H. (2008). Systemic and local modulation of plant responses by Piriformospora indica and related Sebacinales species. Journal of Plant Physiology 165, 60–70.Google Scholar
Wang, Z., Johnston, P. R., Yang, Z. L. & Townsend, J. P. (2009). Evolution of reproductive morphology in leaf endophytes. PLoS ONE 4, e4246. doi:10.1371/journal.pone.0004246.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. doi:10.1371/journal.pone.0016793.Google Scholar
Willcox, G. (2005). The distribution, natural habitats and availability of wild cereals in relation to their domestication in the Near East, multiple events, multiple centres. Vegetation History and Archaeobotany 14, 534–541.Google Scholar
Wilson, D. (1995). Endophyte: the evolution of a term, and clarification of its use and definition. Oikos 73, 274–276.Google Scholar
Zelicourt, A., De Al-Yousif, M. & Hirt, H. (2013). Rhizosphere microbes as essential partners for plant stress tolerance. Molecular Plant 6, 242–245.Google Scholar
Zhao, F. & Qin, P. (2005). Protective effects of exogenous fatty acids on root tonoplast function against salt stress in barley seedlings. Environmental and Experimental Botany 53, 215–223.Google Scholar