ORIGINAL ARTICLE
Endophytic colonization by Beauveria bassiana and Metarhizium anisopliae induces growth promotion effect and increases the resistance of cucumber plants against Aphis gossypii
1
Department of Plant Protection, University of Forestry, Sofia, Bulgaria
2
Department of Plant Protection, Lebanese Agricultural Research Institute, Lebanon
3
Department of Plant Protection, Lebanese University, Beirut, Lebanon
A - Research concept and design; B - Collection and/or assembly of data; C - Data analysis and interpretation; D - Writing the article; E - Critical revision of the article; F - Final approval of article
Submission date: 2021-02-02
Acceptance date: 2021-05-27
Online publication date: 2021-12-20
Corresponding author
Journal of Plant Protection Research 2021;61(4):358-370
KEYWORDS
TOPICS
ABSTRACT
The entomopathogenic fungi (EPF) are characterized as fungi with various functions and
numerous mechanisms of action. The ability to establish themselves as beneficial endo-
phytes provides a sound ground for their exploitation in crop production and protection.
The purpose of this study was to evaluate the entomopathogenic strains of Beauveria bas
siana and Mertarhizium anisopliae for their potential to colonize cucumber plants under
natural environmental conditions in non-sterile substrate. Seed submersion in conidial
suspension resulted in systemic colonization of cucumber plants 28 days post-inoculation.
Scanning electron microscope micrographs demonstrated that conidia of both fungal gen-
era have adhered, germinated and directly penetrated seed epidermal cells 24 hr post-sub-
mersion. Treated with EPF cucumber seeds resulted seedlings tissues of which contained
a significantly higher amount of total phenolic compounds and unchanged amounts of
chlorophylls. There was a significant negative effect of endophytic colonization on the Aphis
gossypii population size after 5 days of exposure as well as a positive effect on cucumber
growth and development 7 weeks post-inoculation. We suggest that reduction of A. gossypii
population on mature Cucumis sativus plants is caused via an endophyte-triggered improve-
ment of plant’s physiological parameters such as enhanced plant growth with subsequent
increase in plant resistance through augmented production of phenolic compounds.
ACKNOWLEDGEMENTS
The authors wish to thank the National Council for
Scientific Research (CNRS) and the Lebanese Univer-
sity for funding this study. We also appreciate the as-
sistance of the plant protection team at the Lebanese
Agricultural Institute (LARI), including Eng. C. Saab
and Z. Moussa. We also wish to thank Dr. R. Habchi
(Research Platform for Nanoscience and Nanotech-
nology, Fanar Campus 90656, Lebanese University) for
helping with SEM work.
RESPONSIBLE EDITOR
Natasza Borodynko-Filas
CONFLICT OF INTEREST
The authors have declared that no conflict of interests exist.
REFERENCES (89)
1.
Ainsworth E.A., Gillespie K.M. 2007. Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin-Ciocalteu reagent. Nature Protocols 2: 875−877. DOI: 10.1038/nprot.2007.102.
2.
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: 215−221. DOI: 10.1016/J.BIOCONTROL.2012.02.007.
3.
Akutse K., Maniania N., Fiaboe K., 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: 293−301. DOI: https://doi.org/10.1016/j.fune....
4.
Bajan C., Tyrawska D., Popowska-Nowak E., Bienkowski P. 1998. Biological response of Beauveria bassiana strains to heavy metal pollution and their accumulative ability. Ecological Chemistry and Engineering 5 (8−9): 676−685.
5.
Bamisile B.S., 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. DOI: https://doi.org/10.1016/j.micr....
6.
Barelli L., Moreira C.C., Bidochka M.J. 2018. Initial stages of endophytic colonization by Metarhizium involves rhizoplane colonization. Microbiology 164: 1531–1540. DOI: 10.1099/mic.0.000729.
7.
Barnes J.D., Balaguer L., Manrique E., Elvira S., Davison A.W. 1992. A reappraisal of the use of DMSO for the extraction and determination of chlorophylls a and b in lichens and higher plants. Environment 32: 83–100. DOI: http://dx.doi.org/10.1016/0098....
8.
Behie S.W., Jones S.J., Bidochka M.J. 2015. Plant tissue localization of the endophytic insect pathogenic fungi Metarhizium and Beauveria. Fungal Ecology 13: 112–119. DOI: 10.1016/J.FUNECO.2014.08.001.
9.
Blackman R.L. 2010. Aphids − Aphidinae (Macrosiphini). Handbook for the Identification of British Insects 2 (7): 1−413.
10.
Blackman R.L., Eastop V.F. 2000. Aphids on the world’s crops: An identification and information guide. John Wiley and Sons, Chichester, UK. XF2006251066.
11.
Braniša J., Jenisová Z., Porubská M., Jomová K., Valko M. 2014. Spectrophotometric determination of chlorophylls and carotenoids. An effect of sonication and sample processing. Journal of Microbiology, Biotechnology and Food Sciences 3 (2): 61−64.
12.
Carriere Y., Bouchard A., Bourassa S., Brodeur J. 1998. Effect of endophyte incidence in perennial ryegrass on distribution, host choice, and performance of the hairy chinch bug (Hemiptera: Lygaeidae). Economic Entomology 91: 324–328. DOI: https://doi.org/10.1093/jee/91....
13.
Castillo-Lopez D., Zhu-Salzman K., Ek-Ramos M.J., Sword G.A. 2014.The entomopathogenic fungal endophytes Purpureocillium lilacinum (formerly Paecilomyces lilacinus) and Beauveria bassiana negatively affect cotton aphid reproduction under both greenhouse and field conditions. PLoS ONE 9 (8): e103891. DOI: 10.1371/journal.pone.0103891.
14.
Chung I.M., Park Chun J.C., Yun S.J. 2003. Resveratrol accumulation and resveratrol synthase gene expression in response to abiotic stresses and hormones in peanut plants. Plant Science 164: 103–109. DOI: 10.1016/S0168-9452(02)00341-2.
15.
Clay K. 1996. Interactions among fungal endophytes, grasses and herbivores. Researches on Population Ecology 38 (2): 191–201. DOI: https://doi.org/10.1007/BF0251....
16.
Clay K., Marks S., Cheplick G.P. 1993. Effects of insect herbivory and fungal endophyte infection on competitive interactions among grasses. Ecology 74 (6): 1767–1777. DOI: https://doi.org/10.2307/193993....
17.
Clifton E.H., Jaronski S.T., Coates B.S., Hodgson E.W., Gassmann A.J. 2018. Effects of endophytic entomopathogenic fungi on soybean aphid and identification of Metarhizium isolates from agricultural fields. PLoS ONE 13 (3): e0194815. DOI: https://doi.org/10.1371/journa...
18.
Daayf F., Ongena M., Boulanger R., El Hadrami I., Bélanger R.R. 2000. Induction of phenolic compounds in two cultivars of cucumber by treatment of healthy and powdery mildew infected plants with extracts of Reynoutria sachalinensis. Journal of Chemical Ecology 26 (7): 1579−1593. DOI: https://doi.org/10.1023/A:1005....
19.
Diaz Napal G.N., Defago M., Valladares G., Palacios S. 2010. Response of Epilachna paenulata to two flavonoids, pinocembrin and quercetin, in a comparative study. Journal of Chemical Ecology 36 (8): 898–904. DOI: 10.1007/s10886-010-9823-1.
20.
Dugassa-Gobena D., Raps A., Vidal S. 1996. Einuu von Acremo nium strictum auf den Sterolhaushalt von Panzen: ein moE `glicher Faktor zum veraE` nderten Verhalten von Herbivoren. Mitteilungen aus der Biologischen Bundesanstalt für Land-und Forstwirtschaft 321: 299.
21.
Fürstenberg-Hägg J., Zagrobelny M., Bak S. 2013. Plant defense against insect herbivores. International Journal of Molecular Sciences 14 (5): 10242–10297. DOI: 10.3390/ijms140510242.
22.
Gange A.C., Koricheva J., Currie A.F., Jaber L.R., Vidal S. 2019. Meta-analysis of the role of entomopathogenic and unspecialized fungal endophytes as plant bodyguards. New Pathologist 223 (4): 2002–2010. DOI: https://doi.org/10.1111/nph.15....
23.
Gawel N.J., Jarret R.L. 1991. A modified CTAB DNA extraction procedure for musa and ipomoea. Plant Molecular Biology Reporter 9 (3): 262−266. DOI: 10.1007/BF02672076.
24.
Gissella M.V., David B.O., James R.B. 2006. Efficacy assessment of Aphidius colemani (Hymenoptera: Braconidae) for suppression of Aphis gossypii (Homoptera: Aphididae) in greenhouse-grown chrysanthemum. Economic Entomology 99 (4): 1104–1111. DOI: 10.1603/0022-0493-99.4.1104.
25.
Godfrey L.D., Rosenheim J.A., Goodell P.B. 2000. Cotton aphid emerges as major pest in SVJ cotton. California Agriculture 54 (6): 32–34. DOI: 10.3733/ca.v054n06p26.
26.
González-Mas N., Sánchez-Ortiz A., Valverde-García P., Quesada-Moraga E. 2019. Effects of endophytic entomopathogenic ascomycetes on the life-history traits of Aphis gossypii Glover and its interactions with melon plants. Insects 10 (6): 165. DOI: 10.3390/insects10060165.
27.
Grace S.C., Logan B.A. 2000. Energy dissipation and radical scavenging by the plant phenylpropanoid pathway. Philosophical Transactions: Biological Sciences 355 (1402): 1499−1510. DOI: 10.1098/rstb.2000.0710.
28.
Gurulingappa P., McGee P.A., Sword G. 2011. Endophytic Le canicillium lecnii and Beauveria bassiana reduce the survival and fecundity of Aphis gossypii following contact with conidia and secondary metabolites. Crop Protection 30 (3): 349−353. DOI: 10.1016/J.CROPRO.2010.11.017.
29.
Gurulingappa P., Sword G.A., Murdoch G., McGee P.A. 2010. Colonization of crop plants by fungal entomopathogens and their effects on two insect pests when in planta. BioControl 55 (1): 34–41. DOI: https://doi.org/10.1016/j.bioc....
30.
Hermoso de Mendoza A., Belliure B., Carbonell E.A., Real V. 2001. Economic thresholds for Aphis gossypii (Hemiptera: Aphididae) on Citrus clementina. Journal of Economic Entomology 94 (2): 439–444. DOI: https://doi.org/10.1603/0022-0....
31.
Humber R.A. 1997. Fungi: identification. p. 153–185. In: “Manual of Techniques in Insect Pathology” (L.A. Lacey, ed.). Academic Press, London. DOI: https://doi.org/10.1016/B978-0....
32.
Ibrahim L., Hamieh A., Ghanem H., Ibrahim S. 2011. Pathogenicity of entomopathogenic fungi from Lebanese soils against aphids, whitefly and non-target beneficial insects. International Journal of Agriculture Sciences 3 (3): 156−164. DOI: 10.9735/0975-3710.3.3.156-164.
33.
Ibrahim L., Laham L., Tomma A., Ibrahim S. 2015. Mass production, yield, quality, formulation and efficacy of entomopathogenic Metarhizium anisopliae conidia. British Journal of Applied Sciences and Technology 9 (5): 427−440. DOI: 10.9734/bjast/2015/17882.
34.
Ibrahim L., Spackman V.M.T., Cobb A.H. 2001. An investigation of wound healing in sugar beet roots using light and fluorescence microscopy. Annals of Botany 88 (2): 313−320. DOI: https://doi.org/10.1006/anbo.2....
35.
Jaber L.R., Enkerli J. 2016. Effect of seed treatment duration on growth and colonization of Vicia faba by endophytic Beauveria bassiana and Metarhizium brunneum. Biological Control 103: 187–195. DOI: https://doi.org/10.1016/j.bioc....
36.
Jaber L.R., Enkerli J. 2017. Fungal entomopathogens as endophytes: can they promote plant growth? Biocontrol Science and Technology 27 (1): 28–41. DOI: https://doi.org/10.1080/095831....
37.
Jaber L.R., Vidal S. 2010. Fungal endophyte negative effects on herbivory are enhanced on intact plants and maintained in a subsequent generation. Ecological Entomology 35 (1): 25–36. DOI: https://doi.org/10.1111/j.1365....
38.
Jensen R.E., Enkegaard A., Steenberg T. 2019. Increased fecundity of Aphis fabae on Vicia faba plants following seed or leaf inoculation with the entomopathogenic fungus Beau veria bassiana. PLoS ONE 14 (10): 1−13, e0223616. DOI: https://doi.org/10.1371/journa....
39.
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. DOI: 10.2134/agronj2007.0017N.
40.
Kumar P.K.R., Hemanth G., Niharika P.S., Kolli S.K. 2015. Isolation and identification of soil mycoflora in agricultural fields at Tekkali Mandal in Srikakulam District. International Journal of Advances in Pharmacy, Biology and Chemistry 4 (2): 484−490.
41.
Lacey L.A. 2016. Entomopathogens used as microbial control agents. p. 3−12. In: “Microbial Control of Insect and Mite Pests” (L.A. Lacey, ed.). Amsterdam: Elsevier/Academic Press. DOI: https://doi.org/10.1016/B978-0....
42.
Lee S.B., Milgroom M.G., Taylor J.W. 1988. A rapid, high yield mini-prep method for isolation of total genomic DNA from fungi. Fungal Genetics Newsletter 35: 23–24. DOI: https://doi.org/10.4148/1941-4...
43.
Liao J., Li X., Wong T.Y., Wang J.J., Khor C.C., Tai ES., Aung T., Teo Y.Y., Cheng C.Y. 2014. Impact of measurement error on testing genetic association with quantitative traits. PloS ONE 9 (1): e87044. DOI: https://doi.org/10.1371/journa....
44.
Liao X., Lovett B., Fang W., St. Leger R.J. 2017. Metarhizium robertsii produces indole-3-acetic acid, which promotes root growth in Arabidopsis and enhances virulence to insects. Microbiology 163 (7): 980–991. DOI: 10.1099/mic.0.000494.
45.
Lingg A.J., Donaldson M.D. 1981. Biotic and abiotic factors affecting stability of Beauveria bassiana conidia in soil. Journal of Invertebrate Pathology 38 (2): 191−200. DOI: https://doi.org/10.1016/0022-2....
46.
Lopez D.C., Zhu-Salzman K., Ek-Ramos M.J., Sword G.A. 2014. The entomopathogenic fungal endophytes Purpureocillium lilacinum (formerly Paecilomyces lilacinus) and Beauveria bassiana negatively affect cotton aphid reproduction under both greenhouse and field conditions. PLoS One 9: e103891. DOI: 10.1371/journal.pone.0104342.
47.
Maniania N.K., Sithanantham S., Ekesi S., Ampong-Nyarko K., Baumgärtner J., Löhr B., Matoka C.M. 2003. A field trial of the entomogenous fungus Metarhizium anisopliae for control of onion thrips, Thrips tabaci. Crop Protection 22 (3): 553–559. DOI: https://doi.org/10.1016/S0261-....
48.
Matallanas B., Lantero E., M’Saad M., Callejas C., Ochando M.D. 2013. Genetic polymorphism at the cytochrome oxidase I gene in mediterranean populations of Batrocera oleae (Diptera: Tephritidae). Applied Entomology 137 (8): 624–630. DOI: https://doi.org/10.1111/jen.12....
49.
McKinnon A.C., Saari S., Moran-Diez M.E., Meyling N.V., Raad M., Glare T.R. 2017. Beauveria bassiana as an endophyte: a critical review on associated methodology and biocontrol potential. BioControl 62: 1–17. DOI: 10.1007/s10526-016-9769-5.
50.
Omkar P.A. 2004. Predaceous coccinellids in India: predatorprey catalogue. Oriental Insects 38 (1): 27–61. DOI: 10.1080/00305316.2004.10417373.
51.
Ownley B.H., Dee M.M., Gwinn K. 2008. Effect of conidial seed treatment rate of entomopathogenic Beauveria bassiana 11-98 on endophytic colonization of tomato seedlings and control of Rhizoctonia disease. Phytopathology 98 (6): S118−S118.
52.
Pańka D., Piesik D., Jeske M., Musiał N., Koczwara K. 2013. Production of phenolic compounds by perennial ryegrass (Lolium perenne L.)/Neotyphodium lolii association as a defense reaction towards infection by Fusarium poae and Rhizoctonia solani. p. 124−125. In: “Endophytes for Plant Protection: the State of the Art” (C. Schneider, C. Leifert, F. Feldmann, eds.). Deutsche Phytomedizinische Gesellschaft, Braunschweig.
53.
Pathan A.K., Bond J., Gaskin R.E. 2010. Sample preparation for SEM of plant surfaces. Materials Today 12 (1): 32−43. DOI: 10.1016/S1369-7021(10)70143-7.
54.
Perea-Domínguez X.P., Hernández-Gastelum L.Z., Olivas-Olguin H.R., Espinosa-Alonso L.G., Valdez-Morale M., Medina-Godoy S. 2018. Phenolic composition of tomato varieties and an industrial tomato by-product: free, conjugated and bound phenolics and antioxidant activity. Journal of Food Science and Technology 55 (9): 3453–3461. DOI: https://doi.org/10.1007/s13197....
55.
Pereira R.M., Stimac J.L., Alves S.B. 1993. Soil antagonism affecting the dose − response of workers of the red imported fire ant, Solenopsis invicta, to Beauveria bassiana conidia. Journal of Invertebrate Pathology 61 (2): 156−161. DOI: https://doi.org/10.1006/jipa.1....
56.
Petrini O., Fisher P.J. 1987. Fungal endophytes in Salicornia perennis. Transactions of the British Mycological Society 87 (4): 647−651. DOI: https://doi.org/10.1016/S0007-...
57.
Pineda A., Zheng S.-J., van Loon J.J.A., Pieterse C.M.J., Dicke M. 2010. Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends in Plant Science 15 (9): 507–514. DOI: https://doi.org/10.1016/j.tpla....
58.
Powell W.A., Klingeman W.E., Ownley B.H., Gwinn K.D. 2009. Evidence of endophytic Beauveria bassiana in seed-treated tomato plants acting as a systemic entomopathogen to larval Helicoverpa zea (Lepidoptera: Noctuidae). Journal of Entomological Science 44 (4): 391−396. DOI: https://doi.org/10.18474/0749-....
59.
Rajab L., Ahmad M., Gazal I. 2020. Endophytic establishment of the fungal entomopathogen, Beauveria bassiana (Bals.) Vuil., in cucumber plants. Egyptian Journal of Biological Pest Control 30: 143. DOI: https://doi.org/10.1186/s41938....
60.
Raps A., Vidal S. 1998. Indirect effects of an unspecialized endophytic fungus on specialized plant-herbivorous insect interactions. Oecologia 114 (4): 541–547. DOI: 10.1007/s004420050478.
61.
Rebijith K.B., Asoka R., Krishna V., Krishna Kumar N.K., Ramamurth V.V. 2012. Development of species-specific markers and molecular differences in mitochondrial and nuclear DNA sequences of Aphis gossypii and Myzus per sicae (Hemiptera: Aphididae). Florida Entomologist 95 (3): 674−682. DOI: 10.1653/024.095.0318.
62.
Rodriguez R.J., White Jr. J.F., Arnold A.E., Redman R.S. 2009. Fungal endophytes: Diversity and functional roles. New Phytologist 182 (2): 314–330. DOI: http://dx.doi.org/10.1111/j.14....
63.
Russo M.L., Pelizza S.A., Cabello M.N., Stenglein S.A., Scorsetti A.C. 2015. Endophytic colonisation of tobacco, corn, wheat and soybeans by the fungal entomopathogen Beauveria bassi ana (Ascomycota, Hypocreales). Biocontrol Science and Technology 25 (4): 475−480. DOI: 10.1080/09583157.2014.982511.
64.
Saari S., Helander M., Faeth S.H. 2010. The effects of endophytes on seed production and seed predation of tall fescue and meadow fescue. Microbial Ecology 60: 928–934. DOI: https://doi.org/10.1007/s00248....
65.
Saikkonen K., Lehtonen P., Helander M., Koricgeva J., Faeth S.H. 2006. Model systems in ecology: dissecting the endophytegrass literature. Trends in Plant Science 11 (9): 428−433. DOI: 10.1016/j.tplants.2006.07.001.
66.
Sánchez-Rodríguez A.R., Del Campillo M.C., Quesada-Moraga E. 2015. Beauveria bassiana: An entomopathogenic fungus alleviates Fe chlorosis symptoms in plants grown on calcareous substrates. Scientia Horticulturae 197: 193–202. DOI: https://doi.org/10.1016/j.scie....
67.
Sasan R.K., Bidochka M.J. 2012. The insect-pathogenic fungus Metarhezium robertsii (Clavicipitaceae) is also an endophyte that stimulates plant root development. American Journal of Botany 99 (1): 101−107. DOI: 10.3732/ajb.1100136.
68.
Schulz B., Boyle C. 2005. Fungal endophyte continuum. Mycological Research 109 (6): 661–686. DOI: https://doi.org/10.1017/S09537....
69.
Shaalan R., Ibrahim L. 2019. Entomopathogenic fungal endophytes: can they colonize cucumber plants? p. 853−860. In: “Book of Proceedings of the IX International Scientific Agriculture Symposium AGROSYM 2018”. 04−07 October 2018, Bosnia and Herzegovina.
70.
Shi X.G., Zhu Y.K., Xia X.M., Qiao K., Wang HY., Wang KY. 2012. The mutation in nicotinic acetylcholine receptor β1 subunit may confer resistance to imidacloprid in Aphis gos sypii (Glover). Journal of Food, Agriculture and Environment 10 (2): 1227−1230.
71.
Skinner M., Parker B.L., Kim J.S. 2014. Role of entomopathogenic fungi in integrated pest management. p. 169–191. In: “Integrated Pest Management: Current Concepts and Ecological Perspectives” (D.P. Abrol, ed.). Academic Press, San Diego. DOI: https://doi.org/10.1016/B978-0....
72.
Song H., Chen J., Staub J., Simon P. 2010. QTL analyses of orange color and carotenoid content and mapping of carotenoid biosynthesis genes in cucumber (Cucumis sativus L.). Acta Horticulturae 871: 607−614. DOI: 10.17660/ACTAHORTIC.2010.871.83.
73.
Stoetzel M.B., Miller G.L., O’Brien P.J., Graves J.B. 1996. Aphids (Homoptera: Aphididae) colonizing cotton in the United States. Florida Entomologist 79 (2): 193−205. DOI: 10.2307/3495817.
74.
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: 663−669. DOI: 10.1007/s10526-009-9216-y.
75.
Tucker S.L., Talbot N.J. 2001. Surface attachment and pre-penetration stage development by plant pathogenic fungi. Annual Review of Phytopathology 39: 385–417. DOI: 10.1146/annurev.phyto.39.1.385.
76.
Ullrich C.I., Koch E., Matecki C., Schäfer J., Burkl T., Rabenstein F., Kleespies R.G. 2017. Detection and growth of endophytic entomopathogenic fungi in dicot crop plants. Journal für Kulturpflanzen 69 (9): 291–302.
77.
Umboh S.D., Salaki C.L., Tulung M., Mandey L.C., Maramis R.T.D. 2016. The isolation and identification of fungi from the soil in gardens of cabbage were contaminated with pesticide residues in subdistrict Modoinding. International Journal of Research in Engineering and Science 4 (7): 25−32.
78.
Vandre W. 2013. Cucumber production in greenhouses. University of Alaska Fairbanks Cooperative Extension Service. Available on: www.uaf.edu/ces.
79.
Vega F.E. 2018. The use of fungal entomopathogens as endophytes in biological control: a review. Mycologia 110 (1): 4–30. DOI: https://doi.org/10.1080/002755....
80.
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. et al. 2009. Fungal entomopathogens: New insights on their ecology. Fungal Ecology 2 (4): 149–159. DOI: https://doi.org/10.1016/j.fune....
81.
Vega F.E., Meyling N.V., Luangsa-Ard J.J., Blackwell M. 2012. Fungal entomopathogens. p. 171–220. In: “Insect Pathology” 2nd ed. (F.E. Vega, H.K. Kaya, eds.). Academic Press, San Diego. DOI: 10.1016/B978-0-12-384984-7.00006-3.
82.
Vega F.E., Posada F., Aime M.C., Pava-Ripolli M., Infante F., Rehner S.A. 2008. Entomopathogenic fungal endophytes. Biological Control 46 (1): 72–82. DOI: https://doi.org/10.1016/j.bioc....
83.
Vidal S., Jaber L. 2015. Entomopathogenic fungi as endophytes: plant–endophyte–herbivore interactions and prospects for use in biological control. Current Science 109 (1): 46−54.
84.
Vincent C., Goettel M.S., Lazarovits G. (eds.) 2007. Biological Control: A Global Perspective. CAB International/AAFC, Wallingford, United Kingdom. DOI: 10.1079/9781845932657.0000.
85.
Wagner B.L., Lewis L.C. 2000. Colonization of corn, Zea mays, by the entomopathogenic fungus Beauveria bassiana. Applied and Environmental Microbiology 66 (8): 3468−3473. DOI: 10.1128/aem.66.8.3468-3473.2000.
86.
White T.J., Bruns T.D., Lee S.B., Taylor J.W. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. p. 315–322. In: “PCR Protocols: A Guide to Methods and Applications” (M.A. Innis, D.H. Gelfand, J.J. Sninsky, T.J. White, eds.). Academic Press, San Diego. DOI: http://dx.doi.org/10.1016/B978....
87.
Wilson D. 1995. Endophyte – the evolution of a term, and clarification of its use and definition. Oikos 73: 274−276. DOI: https://doi.org/10.2307/354591....
88.
Wraight S.P., Inglis G.D., Goettel M.S. 2007. Fungi. p. 223−248. In: “Field Manual of Techniques in Invertebrate Pathology: application and Evaluation of Pathogens for Control of Insects and other Invertebrate Pest”. 2nd ed. (L.A. Lacey, H.K. Kaya, eds.). Springer, Dordrecht, the Netherlands.
89.
Wu Z.H., Wang T.H., Huang W., Qu Y.B. 2001. A simplified method for chromosome DNA preparation from filamentous fungi. Mycosystema 20 (4): 575–577.
Share
RELATED ARTICLE
| eISSN: | 1899-007X |
| ISSN: | 1427-4345 |
We process personal data collected when visiting the website. The function of obtaining information about users and their behavior is carried out by voluntarily entered information in forms and saving cookies in end devices. Data, including cookies, are used to provide services, improve the user experience and to analyze the traffic in accordance with the Privacy policy. Data are also collected and processed by Google Analytics tool (more).
You can change cookies settings in your browser. Restricted use of cookies in the browser configuration may affect some functionalities of the website.
You can change cookies settings in your browser. Restricted use of cookies in the browser configuration may affect some functionalities of the website.
