Details

Title

Endophytic colonization by Beauveria bassiana and Metarhizium anisopliae induces growth promotion effect and increases the resistance of cucumber plants against Aphis gossypii

Journal title

Journal of Plant Protection Research

Yearbook

2021

Volume

vol. 61

Issue

No 4

Affiliation

Shaalan, Roshan S. : Department of Plant Protection, University of Forestry, Sofia, Bulgaria ; Shaalan, Roshan S. : Department of Plant Protection, Lebanese University, Beirut, Lebanon ; Gerges, Elvis : Department of Plant Protection, Lebanese Agricultural Research Institute, Lebanon ; Habib, Wassim : Department of Plant Protection, Lebanese Agricultural Research Institute, Lebanon ; Ibrahim, Ludmilla : Department of Plant Protection, Lebanese University, Beirut, Lebanon

Authors

Keywords

aphid biocontrol ; entomopathogenic fungi as endophytes ; growth promoters ; phenolic compounds

Divisions of PAS

Nauki Biologiczne i Rolnicze

Coverage

358-370

Publisher

Committee of Plant Protection PAS ; Institute of Plant Protection – National Research Institute

Bibliography


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
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
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.funeco.2013.01.003
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.
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.micres.2018.08.016
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.
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/10.1016/0098-8472(92)90034-Y
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
Blackman R.L. 2010. Aphids − Aphidinae (Macrosiphini). Handbook for the Identification of British Insects 2 (7): 1−413.
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.
Braniša J., Jenisova Z., Porubska M., Jomova 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.
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/91.1.324
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
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
Clay K. 1996. Interactions among fungal endophytes, grasses and herbivores. Researches on Population Ecology 38 (2): 191–201. DOI: https://doi.org/10.1007/BF02515727
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/10.2307/1939935
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/journal.pone.0194815
Daayf F., Ongena M., Boulanger R., El Hadrami I., Belanger 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:1005578510954
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
Dugassa-Gobena D., Raps A., Vidal S. 1996. Einfluß von Acremonium strictum auf den Sterolhaushalt von Pflanzen: Ein möglicher Faktor zum veränderten Verhalten von Herbivoren. Mitteilungen aus der Biologischen Bundesanstalt fur Land- und Forstwirtschaft 321: 299.
Furstenberg-Hagg J., Zagrobelny M., Bak S. 2013. Plant defense against insect herbivores. International Journal of Molecular Sciences 14 (5): 10242–10297. DOI: 10.3390/ijms140510242
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.15859
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
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
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
Gonzalez-Mas N., Sanchez-Ortiz A., Valverde-Garcia 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
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
Gurulingappa P., McGee P.A., Sword G. 2011. Endophytic Lecanicillium 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
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. Bio- Control 55 (1): 34–41. DOI: https://doi.org/10.1016/j.biocontrol.2010.06.011
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/10.1603/0022-0493-94.2.439
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/B978-012432555-5/50011-7
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
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
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.2001.1461
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.biocontrol.2016.09.008
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/10.1080/09583157.2016.1243227
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.1365-2311.2009.01152.x
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 Beauveria bassiana. PLoS ONE 14 (10): 1−13, e0223616. DOI: https://doi.org/10.1371/journal.pone.0223616
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
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.
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/B978-0-12-803527- 6.00001-9
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/10.4148/1941-4765.1531
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/journal.pone.0087044
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
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/10.1016/0022-2011(81)90122-1
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
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/S0261-2194(02)00221-1
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.12037
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.
Omkar P.A. 2004. Predaceous coccinellids in India: predatorprey catalogue. Oriental Insects 38 (1): 27–61. DOI: 10.1080/00305316.2004.10417373
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.
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.
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
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/s13197-018-3269-9
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.1993.1028
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/S0007-1536-(86)80109-7
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.tplants.2010.05.007
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/10.18474/0749-8004-44.4.391
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/s41938-020-00344-8
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
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 persicae (Hemiptera: Aphididae). Florida Entomologist 95 (3): 674−682. DOI: 10.1653/024.095.0318
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.1469-8137.2009.02773.x
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 bassiana (Ascomycota, Hypocreales). Biocontrol Science and Technology 25 (4): 475−480. DOI: 10.1080/09583157.2014.982511
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/s00248-010-9749-8
Saikkonen K., Lehtonen P., Helander M., Koricgeva J., Faeth S.H. 2006. Model systems in ecology: dissecting the endophyte grass literature. Trends in Plant Science 11 (9): 428−433. DOI: 10.1016/j.tplants.2006.07.001
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.scienta.2015.09.029
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
Schulz B., Boyle C. 2005. Fungal endophyte continuum. Mycological Research 109 (6): 661–686. DOI: https://doi.org/10.1017/S095375620500273X
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.
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 gossypii (Glover). Journal of Food, Agriculture and Environment 10 (2): 1227−1230.
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/B978-0-12-398529-3.00011-7
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
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
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
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
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. DOI: 10.1399/JfK.2017.09.02
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.
Vandre W. 2013. Cucumber production in greenhouses. University of Alaska Fairbanks Cooperative Extension Service. Available on: www.uaf.edu/ces
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/10.1080/00275514.2017.1418578
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. et al. 2009. Fungal entomopathogens: New insights on their ecology. Fungal Ecology 2 (4): 149–159. DOI: https://doi.org/10.1016/j.funeco.2009.05.001
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
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.biocontrol.2008.01.008
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. 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
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
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/B978-0-12-372180-8.50042-1
Wilson D. 1995. Endophyte – the evolution of a term, and clarification of its use and definition. Oikos 73: 274−276. DOI: https://doi.org/10.2307/3545919
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.
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.

Date

2021.12.30

Type

Article

Identifier

DOI: 10.24425/jppr.2021.139244
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