Endophytic fungi as biological control agents and their indirect effects on plants

Primož ŽIGON, Franci Aco CELAR

Abstract


The use of entomopathogenic fungi represents one of the most important non-chemical alternatives for pest control in crop production. In addition to their pathogenicity to arthropods, they have many other important effects that favor their use in biological control. They live in plants as endophytes and have an inhibitory effect on plant pathogens. They inhabit the rhizosphere of many plants in natural and agricultural ecosystems and have a stimulatory effect on their growth and development. These recently acquired ecological functions are not yet fully understood, but point to the broader potential of using entomopathogenic endophytic fungi in crop production, not only as biopesticides but also as mycofungicides and growth stimulants (biostimulants). To achieve the full potential of entomopathogenic endophytic fungi in daily agricultural practice, practical application should be considered in the development of commercial products and the application techniques of entomopathogenic endophytic fungi that allow successful colonization of plants should be considered.

Keywords


entomopathogenic fungi; endophyte; beneficial organisms; bioinsecticides; Beauveria; Metarhizium

References


Akello, J., Sikora, R. (2012). Systemic acropedal influence of endophyte seed treatment on Acyrthosiphon pisum and Aphis fabae offspring development and reproductive fitness. Biological Control, 61(3), 215–221. https://doi.org/10.1016/j.biocontrol.2012.02.007

Akutse, K. S., Maniania, N. K., Fiaboe, K. K. M., Van den Berg, J., Ekesi, S. (2013). Endophytic colonization of Vicia faba and Phaseolus vulgaris (Fabaceae) by fungal pathogens and their effects on the life-history parameters of Liriomyza huidobrensis (Diptera: Agromyzidae). Fungal Ecology, 6(4), 293–301. https://doi.org/10.1016/j.funeco.2013.01.003

Arnold, A. E. (2007). Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. In Fungal Biology Reviews (Vol. 21, Issues 2–3, pp. 51–66). Elsevier. https://doi.org/10.1016/j.fbr.2007.05.003

Bacon, C. W. (1993). Abiotic stress tolerances (moisture, nutrients) and photosynthesis in endophyte-infected tall fescue. Agriculture, Ecosystems and Environment, 44(1–4), 123–141. https://doi.org/10.1016/0167-8809(93)90042-N

Bamisile, Bamisope S., Dash, C. K., Akutse, K. S., Keppanan, R., Wang, L. (2018). Fungal endophytes: Beyond herbivore management. In Frontiers in Microbiology (Vol. 9, Issue MAR, p. 544). Frontiers Media S.A. https://doi.org/10.3389/fmicb.2018.00544

Bamisile, Bamisope Steve, Dash, C. K., Akutse, K. S., Keppanan, R., Afolabi, O. G., Hussain, M., Qasim, M., Wang, L. (2018). Prospects of endophytic fungal entomopathogens as biocontrol and plant growth promoting agents: An insight on how artificial inoculation methods affect endophytic colonization of host plants. Microbiological Research, 217, 34–50. https://doi.org/10.1016/j.micres.2018.08.016

Bark, Y. G., Lee, D. G., Kim, Y. H., Kang, S. C. (1996). Antibiotic properties of an entomopathogenic fungus, Beauveria bassiana, on Fusarium oxysporum and Botrytis cinerea. The Plant Pathology Journal, 12(2), 245–250.

Bary, A. de (Anton). (1866). Morphologie und Physiologie der Pilze, Flechten und Myxomyceten . W. Engelmann,. https://www.biodiversitylibrary.org/item/211464. https://doi.org/10.5962/bhl.title.120970

Batta, Y. A. (2013). Efficacy of endophytic and applied Metarhizium anisopliae (Metch.) Sorokin (Ascomycota: Hypocreales) against larvae of Plutella xylostella L. (Yponomeutidae: Lepidoptera) infesting Brassica napus plants. Crop Protection, 44, 128–134. https://doi.org/10.1016/j.cropro.2012.11.001

Behie, S. W., Zelisko, P. M., Bidochka, M. J. (2012). Endophytic insect-parasitic fungi translocate nitrogen directly from insects to plants. Science, 336(6088), 1576–1577. https://doi.org/10.1126/science.1222289

Behie, Scott W., Bidochka, M. J. (2014). Ubiquity of insect-derived nitrogen transfer to plants by endophytic insect-pathogenic fungi: An additional branch of the soil nitrogen cycle. Applied and Environmental Microbiology, 80(5), 1553–1560. https://doi.org/10.1128/AEM.03338-13

Behie, Scott W, Padilla-Guerrero, I. E., Bidochka, M. J. (2013). Nutrient transfer to plants by phylogenetically diverse fungi suggests convergent evolutionary strategies in rhizospheric symbionts. Communicative Integrative Biology, 6(1), e22321–e22321. https://doi.org/10.4161/cib.22321

Benhamou, N., Brodeur, J. (2001). Pre-inoculation of Ri T-DNA transformed cucumber roots with the mycoparasite, Verticillium lecanii, induces host defense reactions against Pythium ultimum infection. Physiological and Molecular Plant Pathology, 58(3), 133–146. https://doi.org/10.1006/pmpp.2001.0322

Carroll, G. (1988). Fungal endophytes in stems and leaves: From latent pathogen to mutualistic symbiont. Ecology, 69(1), 2–9. https://doi.org/10.2307/1943154

Dara, S. K. (2016). Impact of entomopathogenic fungi and beneficial microbes on strawberry growth , health , and yield. 1–4. https://ucanr.edu/blogs/blogcore/postdetail.cfm?postnum=22709

Dara, S. K. (2019). Non-entomopathogenic roles of entomopathogenic fungi in promoting plant health and growth. In Insects (Vol. 10, Issue 9). MDPI AG. https://doi.org/10.3390/insects10090277

Dara, S. K., Dara, S. S. (2013). Endophytic colonization and pest management potential of Beauveria bassiana in strawberries. Journal of Berry Research, 3(4), 203–211. https://doi.org/10.3233/JBR-130058

Dara, S. K., Dara, S. S. R., Dara, S. S. (2017). Impact of entomopathogenic fungi on the growth, development, and health of cabbage growing under water stress. American Journal of Plant Sciences, 8, 1224–1233. https://doi.org/10.4236/ajps.2017.86081

El-Deeb, H. M., Lashin, S. M., Arab, Y. A. S. (2012). Reaction of some tomato cultivars to tomato leaf curl virus and evaluation of the endophytic colonisation with Beauveria bassiana on the disease incidence and its vector, Bemisia tabaci. Archives of Phytopathology and Plant Protection, 45(13), 1538–1545. https://doi.org/10.1080/03235408.2012.681246

Faria, M. R. d., Wraight, S. P. (2007). Mycoinsecticides and Mycoacaricides: A comprehensive list with worldwide coverage and international classification of formulation types. Biological Control, 43(3), 237–256. https://doi.org/10.1016/j.biocontrol.2007.08.001

Field, K. J., Pressel, S., Duckett, J. G., Rimington, W. R., Bidartondo, M. I. (2015a). Symbiotic options for the conquest of land. Trends in Ecology Evolution, 30(8), 477–486. https://doi.org/10.1016/J.TREE.2015.05.007

Field, K. J., Rimington, W. R., Bidartondo, M. I., Allinson, K. E., Beerling, D. J., Cameron, D. D., Duckett, J. G., Leake, J. R., Pressel, S. (2015b). Functional analysis of liverworts in dual symbiosis with Glomeromycota and Mucoromycotina fungi under a simulated Palaeozoic CO2 decline. The ISME Journal, 10(6), 1514–1526. https://doi.org/10.1038/ismej.2015.204

Flori, P., Roberti, R. (1993). Treatment of onion bulbs with antagonistic fungi for the control of Fusarium oxysporum f.sp. cepae. Difesa Delle Piante, 16(4), 5–12.

https://eurekamag.com/research/002/724/002724654.php

Freeman, E. M., Ward, H. M. (1904). The seed-fungus of Lolium temulentum L., the darnel. Philosophical Transactions of the Royal Society of London. Series B, Containing Papers of a Biological Character, 196(214–224), 1–27. https://doi.org/10.1098/rstb.1904.0001

Garrido-Jurado, I., Resquín-Romero, G., Amarilla, S. P., Ríos-Moreno, A., Carrasco, L., Quesada-Moraga, E. (2017). Transient endophytic colonization of melon plants by entomopathogenic fungi after foliar application for the control of Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae). Journal of Pest Science, 90(1), 319–330. https://doi.org/10.1007/s10340-016-0767-2

Gautam, S., Mohankumar, S., Kennedy, J. S. (2016). Induced host plant resistance in cauliflower by Beauveria bassiana. Journal of Entomology and Zoology Studies, 4(2), 476–482.

Gómez-Vidal, S., Lopez-Llorca, L. V., Jansson, H. B., Salinas, J. (2006). Endophytic colonization of date palm (Phoenix dactylifera L.) leaves by entomopathogenic fungi. Micron, 37(7), 624–632. https://doi.org/10.1016/j.micron.2006.02.003

Gurulingappa, P., McGee, P. A., Sword, G. (2011). Endophytic Lecanicillium lecanii and Beauveria bassiana reduce the survival and fecundity of Aphis gossypii following contact with conidia and secondary metabolites. Crop Protection, 30(3), 349–353. https://doi.org/10.1016/j.cropro.2010.11.017

Hackman, R. H. (1953). Chemistry of insect cuticle. I. The water-soluble proteins. The Biochemical Journal, 54(3), 362–367. https://doi.org/10.1042/bj0540362

Hajek, A. (1997). Ecology of terrestrial fungal entomopathogens. Advances in Microbial Ecology, 15, 193–249. https://doi.org/10.1007/978-1-4757-9074-0_5

Hardoim, P. R., van Overbeek, L. S., Berg, G., Pirttilä, A. M., Compant, S., Campisano, A., Döring, M., Sessitsch, A. (2015). The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiology and Molecular Biology Reviews : MMBR, 79(3), 293–320. https://doi.org/10.1128/MMBR.00050-14

Humber, R. A. (2008). Evolution of entomopathogenicity in fungi. Journal of Invertebrate Pathology, 98(3), 262–266. https://doi.org/10.1016/j.jip.2008.02.017

Jaber, L. R. (2015). Grapevine leaf tissue colonization by the fungal entomopathogen Beauveria bassiana s.l. and its effect against downy mildew. BioControl, 60(1), 103–112. https://doi.org/10.1007/s10526-014-9618-3

Jaber, L. R., Araj, S. E. (2018). Interactions among endophytic fungal entomopathogens (Ascomycota: Hypocreales), the green peach aphid Myzus persicae Sulzer (Homoptera: Aphididae), and the aphid endoparasitoid Aphidius colemani Viereck (Hymenoptera: Braconidae). Biological Control, 116, 53–61. https://doi.org/10.1016/j.biocontrol.2017.04.005

Jaber, L. R., Enkerli, J. (2017). Fungal entomopathogens as endophytes: can they promote plant growth? Biocontrol Science and Technology, 27(1), 28–41. https://doi.org/10.1080/09583157.2016.1243227

Jaber, L. R., Ownley, B. H. (2018). Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens? In Biological Control (Vol. 116, pp. 36–45). Academic Press Inc. https://doi.org/10.1016/j.biocontrol.2017.01.018

Jaber, L. R., Salem, N. M. (2014). Endophytic colonisation of squash by the fungal entomopathogen Beauveria bassiana (Ascomycota: Hypocreales) for managing Zucchini yellow mosaic virus in cucurbits. Biocontrol Science and Technology, 24(10), 1096–1109. https://doi.org/10.1080/09583157.2014.923379

Jallow, M. F. A., Dugassa-Gobena, D., Vidal, S. (2008). Influence of an endophytic fungus on host plant selection by a polyphagous moth via volatile spectrum changes. Arthropod-Plant Interactions, 2(1), 53–62. https://doi.org/10.1007/s11829-008-9033-8

Kabaluk, J. T., Ericsson, J. D. (2007). Metarhizium anisopliae seed treatment increases yield of field corn when applied for wireworm control. Agronomy Journal, 99(5), 1377–1381. https://doi.org/10.2134/agronj2007.0017N

Kaur, T., Singh, B., Kaur, A., Kaur, S. (2015). Endophyte-mediated interactions between cauliflower, the herbivore Spodoptera litura, and the ectoparasitoid Bracon hebetor. Oecologia, 179(2), 487–494. https://doi.org/10.1007/s00442-015-3358-7

Kim, J. J., Goettel, M. S., Gillespie, D. R. (2008). Evaluation of Lecanicillium longisporum, Vertalec® for simultaneous suppression of cotton aphid, Aphis gossypii, and cucumber powdery mildew, Sphaerotheca fuliginea, on potted cucumbers. Biological Control, 45(3), 404–409. https://doi.org/10.1016/j.biocontrol.2008.02.003

Klieber, J., Reineke, A. (2016). The entomopathogen Beauveria bassiana has epiphytic and endophytic activity against the tomato leaf miner Tuta absoluta. Journal of Applied Entomology, 140(8), 580–589. https://doi.org/10.1111/jen.12287

Kogel, K. H., Franken, P., Hückelhoven, R. (2006). Endophyte or parasite - what decides? In Current Opinion in Plant Biology (Vol. 9, Issue 4, pp. 358–363). Elsevier Current Trends. https://doi.org/10.1016/j.pbi.2006.05.001

Krell, V., Unger, S., Jakobs-Schoenwandt, D., Patel, A. V. (2018). Endophytic Metarhizium brunneum mitigates nutrient deficits in potato and improves plant productivity and vitality. Fungal Ecology, 34, 43–49. https://doi.org/10.1016/j.funeco.2018.04.002

Lacey, L. A., Grzywacz, D., Shapiro-Ilan, D. I., Frutos, R., Brownbridge, M., Goettel, M. S. (2015). Insect pathogens as biological control agents: Back to the future. Journal of Invertebrate Pathology, 132, 1–41. https://doi.org/10.1016/j.jip.2015.07.009

Lewis, L. C., Bing, L. A. (1991). Bacillus thuringiensis Berliner and Beauveria bassiana (Balsamo) Vuillimen for european corn borer control: Program for immediate and season-long suppression 1. The Canadian Entomologist, 123(2), 387–393. https://doi.org/10.4039/Ent123387-2

Lopez, D. C., Sword, G. A. (2015). The endophytic fungal entomopathogens Beauveria bassiana and Purpureocillium lilacinum enhance the growth of cultivated cotton (Gossypium hirsutum) and negatively affect survival of the cotton bollworm (Helicoverpa zea). Biological Control, 89, 53–60. https://doi.org/10.1016/j.biocontrol.2015.03.010

Mantzoukas, S., Chondrogiannis, C., Grammatikopoulos, G. (2015). Effects of three endophytic entomopathogens on sweet sorghum and on the larvae of the stalk borer Sesamia nonagrioides. Entomologia Experimentalis et Applicata, 154(1), 78–87. https://doi.org/10.1111/eea.12262

Mantzoukas, S., Eliopoulos, P. A. (2020). Endophytic entomopathogenic fungi: A valuable biological control tool against plant pests. In Applied Sciences (Switzerland) (Vol. 10, Issue 1, p. 360). MDPI AG. https://doi.org/10.3390/app10010360

Mantzoukas, S., Lagogiannis, I. (2019). Endophytic colonization of pepper (Capsicum annum) controls aphids (Myzus persicae Sulzer). Applied Sciences (Switzerland), 9(11), 2239. https://doi.org/10.3390/app9112239

Mutune, B., Ekesi, S., Niassy, S., Matiru, V., Bii, C., Maniania, N. K. (2016). Fungal endophytes as promising tools for the management of bean stem maggot Ophiomyia phaseoli on beans Phaseolus vulgaris. Journal of Pest Science, 89(4), 993–1001. https://doi.org/10.1007/s10340-015-0725-4

Muvea, A. M., Meyhöfer, R., Subramanian, S., Poehling, H. M., Ekesi, S., Maniania, N. K. (2014). Colonization of onions by endophytic fungi and their impacts on the biology of Thrips tabaci. PLoS ONE, 9(9), 108242. https://doi.org/10.1371/journal.pone.0108242

Ownley, B. H., Griffin, M. R., Klingeman, W. E., Gwinn, K. D., Moulton, J. K., Pereira, R. M. (2008). Beauveria bassiana: Endophytic colonization and plant disease control. Journal of Invertebrate Pathology, 98(3), 267–270. https://doi.org/10.1016/j.jip.2008.01.010

Ownley, B. H., Gwinn, K. D., Vega, F. E. (2010). Endophytic fungal entomopathogens with activity against plant pathogens: Ecology and evolution. BioControl, 55(1), 113–128. https://doi.org/10.1007/s10526-009-9241-x

Parsa, S., Ortiz, V., Vega, F. E. (2013). Establishing fungal entomopathogens as endophytes: towards endophytic biological control. Journal of Visualized Experiments : JoVE, 74, 50360. https://doi.org/10.3791/50360

Pedrini, N., Crespo, R., Juárez, M. P. (2007). Biochemistry of insect epicuticle degradation by entomopathogenic fungi. In Comparative Biochemistry and Physiology - C Toxicology and Pharmacology (Vol. 146, Issues 1-2 SPEC. ISS., pp. 124–137). Elsevier Inc. https://doi.org/10.1016/j.cbpc.2006.08.003

Petrini, O. (1991). Microbial ecology of leaves. Spring-Verlag, New York, 179–197. https://doi.org/10.1007/978-1-4612-3168-4_9

Philippot, L., Raaijmakers, J. M., Lemanceau, P., van der Putten, W. H. (2013). Going back to the roots: the microbial ecology of the rhizosphere. Nature Reviews. Microbiology, 11(11), 789–799. https://doi.org/10.1038/nrmicro3109

Qayyum, M. A., Wakil, W., Arif, M. J., Sahi, S. T., Dunlap, C. A. (2015). Infection of Helicoverpa armigera by endophytic Beauveria bassiana colonizing tomato plants. Biological Control, 90, 200–207. https://doi.org/10.1016/j.biocontrol.2015.04.005

Raad, M., Glare, T. R., Brochero, H. L., Müller, C., Rostás, M. (2019). Transcriptional reprogramming of Arabidopsis thaliana defence pathways by the entomopathogen Beauveria bassiana correlates with resistance against a fungal pathogen but not against insects. Frontiers in Microbiology, 10(MAR), 615. https://doi.org/10.3389/fmicb.2019.00615

Ramirez-Rodriguez, D., Sánchez-Peña, S. R. (2016). Endophytic Beauveria bassiana in Zea mays: Pathogenicity against larvae of fall armyworm, Spodoptera frugiperda. Southwestern Entomologist, 41(3), 875–878. https://doi.org/10.3958/059.041.0330

Rana, K. L., Kour, D., Sheikh, I., Dhiman, A., Yadav, N., Yadav, A. N., Rastegari, A. A., Singh, K., Saxena, A. K. (2019). Endophytic Fungi: Biodiversity, Ecological Significance, and Potential Industrial Applications (pp. 1–62). Springer International Publishing. https://doi.org/10.1007/978-3-030-10480-1_1

Razinger, J., Lutz, M., Schroers, H. J., Palmisano, M., Wohler, C., Urek, G., Grunder, J. (2014). Direct plantlet inoculation with soil or insect-associated fungi may control cabbage root fly maggots. Journal of Invertebrate Pathology, 120, 59–66. https://doi.org/10.1016/j.jip.2014.05.006

Reddy, G. V. P., Tangtrakulwanich, K., Wu, S., Miller, J. H., Ophus, V. L., Prewett, J., Jaronski, S. T. (2014). Evaluation of the effectiveness of entomopathogens for the management of wireworms (Coleoptera: Elateridae) on spring wheat. Journal of Invertebrate Pathology, 120, 43–49. https://doi.org/10.1016/j.jip.2014.05.005

Reddy, G. V. P., Zhao, Z., Humber, R. A. (2014). Laboratory and field efficacy of entomopathogenic fungi for the management of the sweetpotato weevil, Cylas formicarius (Coleoptera: Brentidae). Journal of Invertebrate Pathology, 122, 10–15. https://doi.org/10.1016/j.jip.2014.07.009

Renwick., A., Campbell, R., Coe, S. (1991). Assessment of in vivo screening systems for potential biocontrol agents of Gaeumannomyces graminis. Plant Pathology, 40(4), 524–532. https://doi.org/10.1111/j.1365-3059.1991.tb02415.x

Rho, H., Hsieh, M., Kandel, S. L., Cantillo, J., Doty, S. L., Kim, S.-H. (2018). Do endophytes promote growth of host plants under stress? A meta-analysis on plant stress mitigation by endophytes. Microbial Ecology, 75(2), 407–418. https://doi.org/10.1007/s00248-017-1054-3

Robert-Seilaniantz, A., Grant, M., Jones, J. D. G. (2011). Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annual Review of Phytopathology, 49, 317–343. https://doi.org/10.1146/annurev-phyto-073009-114447

Rodriguez, R. J., White, J. F., Arnold, A. E., Redman, R. S. (2009). Fungal endophytes: Diversity and functional roles: Tansley review. In New Phytologist (Vol. 182, Issue 2, pp. 314–330). John Wiley Sons, Ltd. https://doi.org/10.1111/j.1469-8137.2009.02773.x

Rodriguez, R., Redman, R. (2008). More than 400 million years of evolution and some plants still can’t make it on their own: plant stress tolerance via fungal symbiosis. Journal of Experimental Botany, 59(5), 1109–1114. https://doi.org/10.1093/jxb/erm342

Rondot, Y., Reineke, A. (2018). Endophytic Beauveria bassiana in grapevine Vitis vinifera (L.) reduces infestation with piercing-sucking insects. Biological Control, 116, 82–89. https://doi.org/10.1016/j.biocontrol.2016.10.006

Saikkonen, K., Wäli, P., Helander, M., Faeth, S. H. (2004). Evolution of endophyteplant symbioses. Trends in Plant Science, 9(6), 275–280. https://doi.org/10.1016/j.tplants.2004.04.005

Sandhu, S. S., Sharma, A. K., Beniwal, V., Goel, G., Batra, P., Kumar, A., Jaglan, S., Sharma, A. K., Malhotra, S. (2012). Myco-biocontrol of insect pests: Factors involved, mechanism, and regulation. Journal of Pathogens, 2012, 1–10. https://doi.org/10.1155/2012/126819

Sang Myeong, L., Woon Hong, Y., Hyeong Jin, J., Sang Chul, S., Yil Seong, M. (1999). Effect of entomopathogenic fungi on growth of cucumber and Rhizoctonia solani. FRI Journal of Forest Science Seoul, 62, 118–125. https://eurekamag.com/research/003/417/003417068.php

Sasan, R. K., Bidochka, M. J. (2013). Antagonism of the endophytic insect pathogenic fungus Metarhizium robertsii against the bean plant pathogen Fusarium solani f. sp. phaseoli. Canadian Journal of Plant Pathology, 35(3), 288–293. https://doi.org/10.1080/07060661.2013.823114

Tefera, T., Vidal, S. (2009). Effect of inoculation method and plant growth medium on endophytic colonization of sorghum by the entomopathogenic fungus Beauveria bassiana. BioControl, 54(5), 663–669. https://doi.org/10.1007/s10526-009-9216-y

Van Wees, S. C., Van der Ent, S., Pieterse, C. M. (2008). Plant immune responses triggered by beneficial microbes. In Current Opinion in Plant Biology (Vol. 11, Issue 4, pp. 443–448). Elsevier Current Trends. https://doi.org/10.1016/j.pbi.2008.05.005

Vega, F. E. (2008). Insect pathology and fungal endophytes. Journal of Invertebrate Pathology, 98(3), 277–279. https://doi.org/10.1016/j.jip.2008.01.008

Vega, F. E. (2018). The use of fungal entomopathogens as endophytes in biological control: a review. In Mycologia (Vol. 110, Issue 1, pp. 4–30). NLM (Medline). https://doi.org/10.1080/00275514.2017.1418578

Vega, F. E., Goettel, M. S., Blackwell, M., Chandler, D., Jackson, M. A., Keller, S., Koike, M., Maniania, N. K., Monzón, A., Ownley, B. H., Pell, J. K., Rangel, D. E. N., Roy, H. E. (2009). Fungal entomopathogens: new insights on their ecology. In Fungal Ecology (Vol. 2, Issue 4, pp. 149–159). Elsevier. https://doi.org/10.1016/j.funeco.2009.05.001

Vidal, S., Jaber, L. R. (2015). Entomopathogenic fungi as endophytes: plantendophyteherbivore interactions and prospects for use in biological control. Current Science, 109(1), 46–54. http://www.jstor.org/stable/24905690

Wilson, D. (1995). Endophyte: The evolution of a term, and clarification of its use and definition. Oikos, 73(2), 274–276. https://doi.org/10.2307/3545919

Zamioudis, C., Pieterse, C. M. J. (2012). Modulation of host immunity by beneficial microbes. Molecular Plant-Microbe Interactions : MPMI, 25(2), 139–150. https://doi.org/10.1094/MPMI-06-11-0179




DOI: http://dx.doi.org/10.14720/aas.2021.117.4.2241

Refbacks

  • There are currently no refbacks.


Copyright (c) 2021 Primož Žigon, Franci Aco Celar

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

 

Acta agriculturae Slovenica is an Open Access journal published under the terms of the Creative Commons CC BY License.

                           


eISSN 1854-1941