Evaluation of new fermentation and formulation strategies for a high endophytic establishment of Beauveria bassiana in oilseed rape plants

Biological Control - Tập 88 - Trang 26-36 - 2015
Rieke Lohse1, Desiree Jakobs-Schönwandt1, Stefan Vidal2, Anant V. Patel1
1University of Applied Sciences, Department of Engineering and Mathematics, Wilhelm-Bertelsmann-Str. 10, D-33602 Bielefeld, Germany
2Georg-August-University Goettingen, Department of Crop Sciences, Grisebachstr. 6, D-37077 Goettingen, Germany

Tài liệu tham khảo

Akello, 2008, Endophytic Beauveria bassiana in banana (Musa spp.) reduces banana weevil (Cosmopolites sordidus) fitness and damage, Crop Prot., 27, 1437, 10.1016/j.cropro.2008.07.003 Akello, 2012, Systemic acropedal influence of endophyte seed treatment on Acyrthosiphon pisum and Aphis fabae offspring development and reproductive fitness, Biol. Control, 61, 215, 10.1016/j.biocontrol.2012.02.007 Amnuaykanjanasin, 2013, Infection and colonization of tissues of the aphid Myzus persicae and cassava mealybug Phenacoccus manihoti by the fungus Beauveria bassiana, Biocontrol, 58, 379, 10.1007/s10526-012-9499-2 Bextine, 2002, Monitoring Solenopsis invicta (Hymenoptera: Formicidae) foraging with peanut oil-baited, UV-reflective Beauveria bassiana alginate pellets, Southwestern Entomol., 27, 31 Bextine, 2002, Field applications of bait-formulated Beauveria bassiana alginate pellets for biological control of the red imported fire ant (Hymenoptera: Formicidae), Environ. Entomol., 31, 746, 10.1603/0046-225X-31.4.746 Bextine, 2004, Novel Beauveria bassiana delivery system for biological control of the red imported fire ant, Southwestern Entomol., 29, 47 Bing, 1991, Suppression of Ostrinia nubilalis (Hubner) (Lepidoptera: Pyralidae) by endophytic Beauveria bassiana (Balsamo) Vuillemin, Environ. Entomol., 20, 1207, 10.1093/ee/20.4.1207 Biswas, 2012, Establishment of the fungal entomopathogen Beauveria bassiana as a season long endophyte in jute (Corchorus olitorius) and its rapid detection using SCAR marker, Biocontrol, 57, 565, 10.1007/s10526-011-9424-0 Biswas, 2013, Endophytic colonization of white jute (Corchorus capsularis) plants by different Beauveria bassiana strains for managing stem weevil (Apion corchori), Phytoparasitica, 41, 17, 10.1007/s12600-012-0257-x Blum, 2012, The cellulose synthase 3 (CesA3) gene of oomycetes: structure, phylogeny and influence on sensitivity to carboxylic acid amide (CAA) fungicides, Fungal Biol., 116, 529, 10.1016/j.funbio.2012.02.003 Brownbridge, 2012, Persistence of Beauveria bassiana (Ascomycota: Hypocreales) as an endophyte following inoculation of radiata pine seed and seedlings, Biol. Control, 61, 194, 10.1016/j.biocontrol.2012.01.002 Bruck, 2010, Fungal entomopathogens in the rhizosphere, Biocontrol, 55, 103, 10.1007/s10526-009-9236-7 Burges, 1998 Chase, 1986, Selective isolation of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae from an artificial potting medium, Fla. Entomol., 69, 285, 10.2307/3494930 Chuankun, 2004, Soil volatile fungistasis and volatile fungistatic compounds, Soil Biol. Biochem., 36, 1997, 10.1016/j.soilbio.2004.07.020 Cohen, 2009, Photostabilization of Beauveria bassiana conidia using anionic dyes, Appl. Clay Sci., 42, 569, 10.1016/j.clay.2008.03.013 Ehsanfar, 2005, Crop protection by seed coating, Appl. Biol. Sci., 70, 225 Feng, 1994, Production, formulation and application of the entomopathogenic fungus Beauveria bassiana for insect control: current status, Biocontrol Sci. Technol., 4, 3, 10.1080/09583159409355309 Galbraith, 1969, Sporulation of Aspergillus niger in submerged liquid culture, J. Gen. Microbiol., 59, 31, 10.1099/00221287-59-1-31 Gerding-González, 2007, Use of chitin to improve a Beauveria bassiana alginate-pellet formulation, Biocontrol Sci. Technol., 17, 105, 10.1080/09583150600937717 Glare, 2012, Have biopesticides come of age?, Trends Biotechnol., 30, 250, 10.1016/j.tibtech.2012.01.003 Güerri-Agulló, 2010, Infection of the red palm weevil (Rhynchophorus ferrugineus) by the entomopathogenic fungus Beauveria bassiana: a SEM study, Microsc. Res. Tech., 73, 714 Guesmi-Jouini, 2014, Establishment of fungal entomopathogens Beauveria bassiana and Bionectria ochroleuca (Ascomycota: Hypocreales) as endophytes on artichoke Cynara scolymus, J. Invertebr. Pathol., 119, 1, 10.1016/j.jip.2014.03.004 Gurulingappa, 2010, Colonization of crop plants by fungal entomopathogens and their effects on two insect pests when in planta, Biol. Control, 55, 34, 10.1016/j.biocontrol.2010.06.011 Hegedus, 1992, A comparison of the virulence, stability and cell-wall-surface characteristics of three spore types produced by the entomopathogenic fungus Beauveria bassiana, Appl. Microbiol. Biotechnol., 36, 785, 10.1007/BF00172195 Hegedus, 1990, Beauveria bassiana submerged conidia production in a defined medium containing chitin, two hexosamines or glucose, Appl. Microbiol. Biotechnol., 33, 641, 10.1007/BF00604930 Humphreys, 1990, Comparison of sporulation of Paecilomyces farinosus and Beauveria bassiana in batch and fed-batch culture, Mycol. Res., 94, 1046, 10.1016/S0953-7562(09)81331-2 Humphreys, 1989, Effects of water activity on morphology, growth and blastospore production of Metarhizium anisopliae, Beauveria bassiana and Paecilomyces farinosus in batch and fed-batch culture, Mycol. Res., 92, 257, 10.1016/S0953-7562(89)80063-2 Kassa, 2004, Production and processing of Metarhizium anisopliae var. acridum submerged conidia for locust and grasshopper control, Mycol. Res., 108, 93, 10.1017/S0953756203008827 Khachatourians, 1986, Production and use of biological pest control agents, Trends Biotechnol., 4, 120, 10.1016/0167-7799(86)90144-7 Knudsen, 1991, Method to enhance growth and sporulation of pelletized biocontrol fungi, Appl. Environ. Microbiol., 57, 2864, 10.1128/aem.57.10.2864-2867.1991 Knudsen, 1990, Alginate pellet formulation of a Beauveria bassiana (Fungi: Hyphomycetes) isolate pathogenic to cereal aphids, J. Econ. Entomol., 83, 2225, 10.1093/jee/83.6.2225 Landa, 2013, In-planta detection and monitorization of endophytic colonization by a Beauveria bassiana strain using a new-developed nested and quantitative PCR-based assay and confocal laser scanning microscopy, J. Invertebr. Pathol., 114, 128, 10.1016/j.jip.2013.06.007 Lane, 1991, Endogenous reserves and survival of blastospores of Beauveria bassiana harvested from carbon- and nitrogen-limited batch cultures, Mycol. Res., 95, 821, 10.1016/S0953-7562(09)80045-2 Leroux, 2002, Mechanisms of resistance to fungicides in field strains of Botrytis cinerea, Pest Manag. Sci., 58, 876, 10.1002/ps.566 Lohse, 2014, Screening of liquid media and fermentation of an endophytic Beauveria bassiana strain in a bioreactor, AMB Express, 4, 47, 10.1186/s13568-014-0047-6 Majchrowicz, 1990, Effects of entomopathogenic and opportunistic fungi on Delia antiqua (Diptera: Anthomyiidae) at low relative humidity, Environ. Entomol., 19, 1163, 10.1093/ee/19.4.1163 Marques, 1999, Effects of the temperature and storage on formulations with mycelia of Beauveria bassiana (Bals.) Vuill and Metarhizium anisopliae (Metschn.) Sorok, Braz. Arch. Biol. Technol., 42, 153, 10.1590/S1516-89131999000200004 Mert, 1977, The effect of osmotic pressure and salinity of the medium on the growth and sporulation of Aspergillus niger and Paecilomyces lilacinum species, Mycopathologia, 61, 125, 10.1007/BF00443842 Mert, 1987, The effect of salinity and osmotic pressure of the medium on the growth, sporulation and changes in the total organic acid content of Aspergillus flavus and Penicillium chrysogenum, Mycopathologia, 100, 85, 10.1007/BF00467099 Odds, 1991, Sabouraud(‘s) agar, J. Med. Vet. Mycol., 29, 355, 10.1080/02681219180000581 Ownley, 2008, Beauveria bassiana: endophytic colonization and plant disease control, J. Invertebr. Pathol., 98, 267, 10.1016/j.jip.2008.01.010 Patel, 2011, Fermentation and microencapsulation of the nematophagous fungus Hirsutella rhossiliensis in a novel type of hollow beads, Appl. Microbiol. Biotechnol., 89, 1751, 10.1007/s00253-010-3046-9 Patel, 1994, Entrapment of biological control agents applied to entomopathogenic nematodes, Biotechnol. Tech., 8, 569, 10.1007/BF00152148 Pekrul, 1979, Mode of infection of the corn earworm (Heliothis zea) by Beauveria bassiana as revealed by scanning electron microscopy, J. Invertebr. Pathol., 34, 238, 10.1016/0022-2011(79)90069-7 Pereira, 1991, Alginate and cornstarch mycelial formulations of entomopathogenic fungi, Beauveria bassiana and Metarhizium anisopliae, J. Econ. Entomol., 84, 1657, 10.1093/jee/84.6.1657 Pereira, 1993, Soil antagonism affecting the dose response of workers of the red imported fire ant, Solenopsis invicta, to Beauveria bassiana conidia, J. Invertebr. Pathol., 61, 156, 10.1006/jipa.1993.1028 Posada, 2007, Inoculation of coffee plants with the fungal entomopathogen Beauveria bassiana (Ascomycota: Hypocreales), Mycol. Res., 11, 748, 10.1016/j.mycres.2007.03.006 Posada, 2005, Establishment of the fungal entomopathogen Beauveria bassiana (Ascomycota: Hypocreales) as an endophyte in cocoa seedlings (Theobroma cacao), Mycologia, 97, 1195, 10.1080/15572536.2006.11832729 Powell, 2009, Evidence of endophytic Beauveria bassiana in seedtreated tomato plants acting as a systemic entomopathogen to larval Helicoverpa zea (Lepidoptera: Noctuidae), J. Entomol. Sci., 44, 391, 10.18474/0749-8004-44.4.391 Quesada-Moraga, 2006, Endophytic colonisation of opium poppy, Papaver somniferum, by an entomopathogenic Beauveria bassiana strain, Mycopathologia, 161, 323, 10.1007/s11046-006-0014-0 Quesada-Moraga, 2009, Systemic protection of Papaver somniferum L. against Iraella luteipes (Hymenoptera: Cynipidae) by an endophytic strain of Beauveria bassiana (Ascomycota: Hypocreales), Environ. Entomol., 38, 723, 10.1603/022.038.0324 Rangel, 2010, Susceptibility of Metarhizium spp. and other entomopathogenic fungi to dodine-based selective media, Biocontrol Sci. Technol., 20, 375, 10.1080/09583150903518370 Ravensberg, 2011 Rombach, 1989, Production of Beauveria bassiana [Deuteromycotina. Hyphomycetes] sympoduloconidia in submerged culture, Biocontrol, 34, 45 Rombach, 1988, Production of Beauveria bassiana [Deuteromycotina: Hyphomycetes] in different liquid media and subsequent conidiation of dry mycelium, Biocontrol, 33, 315 Saha, 1988, A rapid staining method for detection of endophytic fungi in turf and forage grasses, Phytopathology, 78, 237, 10.1094/Phyto-78-237 Schulz, 2005, The endophytic continuum, Mycol. Res., 109, 661, 10.1017/S095375620500273X Shields, 1981, Identification of a Penicillium urticae metabolite which inhibits Beauveria bassiana, J. Invertebr. Pathol., 38, 374, 10.1016/0022-2011(81)90104-X Smith, 1981, Microcycle conidiation, 627 Tefera, 2009, Effect of inoculation method and plant growth medium on endophytic colonization of sorghum by the entomopathogenic fungus Beauveria bassiana, Biocontrol, 54, 663, 10.1007/s10526-009-9216-y Thomas, 1987, Production and properties of Beauveria bassiana conidia cultivated in submerged culture, Can. J. Microbiol., 33, 12, 10.1139/m87-003 Thorvilson, 2002, Development of Beauveria bassiana formulations and genetically marked strains as a potential biopesticide for imported fire ant control, Southwestern Entomol., 19 Vega, 2008, Insect pathology and fungal endophytes, J. Invertebr. Pathol., 98, 277, 10.1016/j.jip.2008.01.008 Vemmer, 2013, Review of encapsulation methods suitable for microbial biological control agents, Biol. Control, 67, 380, 10.1016/j.biocontrol.2013.09.003 Wucherpfennig, 2011, Morphology engineering – osmolality and its effect on Aspergillus niger morphology and productivity, Microb. Cell Fact., 10, 10.1186/1475-2859-10-58 Xiong, 2013, Morphological and ultrastructural characterization of Carposina sasakii larvae (Lepidoptera: Carposinidae) infected by Beauveria bassiana (Ascomycota: Hypocreales: Clavicipitaceae), Micron, 44, 303, 10.1016/j.micron.2012.08.002