Böcek-Bakteri Etkileşimlerinin Tarımsal Ekosistemlere Etkileri
Özet
Gıda üretiminde tarladan tüketiciye ulaşıncaya kadar geçen süreçlerde en sık karşılaşılan problemlerden bir tanesi böceklerdir. Bu zararlılara karşı uzun zamandan beri uygulanan konvansiyonel mücadele yöntemleri günümüzde etkinliğini kaybetmektedir. Yeni pestisitlerin geliştirilmesi zor ve pahalıdır. Bazı bilinen pestisitlerin birlikte kullanımı böceklerin geliştirdiği direnci kırmakta artık zorlanmaktadır. Ek olarak, yanlış pestisit kullanımı sonucunda ekonomik zararlar ortaya çıkmakta, ürünler gıda niteliğini kaybetmektedir. Üreticiler ve tüketiciler açısından bu tarz riskleri minimize etmek biyolojik mücadele yöntemleri ile mümkün gözükmektedir. Bakteriler yeryüzünde yaygın olarak bulunabilen canlı gruplarından birisidir. Diğer canlılar ile simbiyotik, patojenik ve vektörel etkileşim türleri geliştirmişlerdir. Bakteriler ve böcekler, yaklaşık 250 milyon yıldır birlikte evrimleşmektedir. Entomopatojen bakteriler işte tam bu noktada böceklerle mücadelede sahneye çıkmaktadır. İlk olarak 20. yüzyılın başlarında Bacillus thrungiensis’in tanımlanması ve ardından biyolojik mücadele etmeni olarak böceklere karşı kullanımı entomopatojen bakterilerin günümüze kadar gelen yolculuğunun başlangıcı olmuştur. Özelleşmiş konukçu hassasiyeti ile ekosistemdeki diğer canlılara zarar vermeden hedefine ulaşması çevreci yaklaşımların ön plana çıkarıldığı günümüzde tarımsal uygulamalar açısından büyük fark yaratmaktadır. Sürdürülebilir tarımsal üretim ve toprakta yaşayan organizmaların çeşitliliğine katkılarından dolayı entomopatojen bakteri uygulamaları zararlı yönetimi içerisinde ön plana çıkarılmalıdır. Bu çalışmada, elimizdeki en etkili silahlardan birisi olarak tanımlanabilecek bakteri-böcek etkileşimlerinin kısa bir özeti ilgili literatür ışığında ele alınmıştır.
Referanslar
Nesler A, Perazzolli M, Puopolo G, Giovannini O, Elad Y, Pertot I. A complex protein derivative acts as biogenic elicitor of grapevine resistance against powdery mildew under field conditions. Front Plant Sci.; 2015; 6:715. doi: 10.3389/fpls.2015.00715.
Jurat-Fuentes JL, Jackson TA. Bacterial Entomopathogens In: Vega FE, Kaya HK (eds.) Insect Pathology. 2nd ed. Academic Press; 2012. p. 265-349.
Oliver KM, Martinez AJ. How resident microbes modulate ecologicallyimportant traits of insects. Curr Opin Insect Sci. 2014;4:1–7. Doi:10. 1016/j. cois. 2014. 08. 001.
Sanchez-Contreras M, Vlisidou I.. The Diversity of Insect-bacteria Interactions and its Applications for Disease Control. Biotechnology and Genetic Engineering Reviews; 2008; 25: 203-244. doi: 10.5661/bger-25-203
Priest FG, Dewar SJ. Bacteria and Insects. In: Priest, F.G., Goodfellow, M. (eds) Applied Microbial Systematics. Springer, Dordrecht.; 2000. p. 165-202.
de Bary HA. Die Erscheinung der Symbiose. Verlag von Karl J.Trübner, Strassburg; 1879
Moya A, Pereto J, Gil R, Latorre A,. Learning how to live together: genomic insights into prokaryote-animal symbioses. Nature Review Genetics; 2008; 9, 218-229. doi: 10.1038/nrg2319
Dillon RJ, Dillon VM. The gut bacteria of insects: nonpathogenic interactions. Annual Review Entomolgy; 2004; 49; 71-92. doi: 10.1146/annurev.ento.49.061802.123416
Moran NA. Symbiosis. Curr Biol. 2006;16(20),866-871. doi: 10. 1016/j. cub. 2006. 09. 019. PMID: 17055966.
Jing TZ, Qi FH, Wang ZY. Most dominant roles of insect gut bacteria: digestion, detoxification, or essential nutrient provision?. Microbiome; 2020; 8; 38. doi: 10.1186/s40168-020-00823-y
Bucher C. (1981). Identification of bacteria found in insects. In: Burges HD (ed), Microbial Control of Pests and Plant Diseases1970-1980. London: Academic Press; 1981. p. 7-33.
Davidson EW. Biochemistry and mode of action of the Bacillus sphaericus toxins. Memorias do Instituto Oswaldo Cruz; 1995; 90: 81-86. doi: 10.1590/s0074-02761995000100018
Gill SS. Biochemistry and mode of action of Bacillus thuringiensis toxins. Memorias do Instituto Oswaldo Cruz; 1995; 90: 69-74. doi: 10.1590/s0074-02761995000100016.
Charles JF. Nielsen Leroux, C. Delecluse A. Bacillus sphaericus toxins: molecular biology andmode of action. Annual Review of Entomology; 1996; 41: 451-472. doi: 10.1146/annurev.en.41.010196.002315
Kumar PA, Sharma RP, Malik VS.. The insecticidal proteins of Bacillus thuringiensis. Advancesin Applied Microbiology; 1996; 42: 1-43. doi: 10.1016/S0065-2164(08)70371
Hurlburt, R.E. Investigations into the pathogenic mechanisms of the bacterium-nematode complex: the search for virulence determinants of Xenorhabdus nematophilus ATCC 19061 could lead to agriculturally useful products. ASM News; 1994; 60:473-478.
Forst S, Nealson K. Molecular biology of the symbiotic pathogenic bacteria Xenorhabdus spp. and Photorhabdus spp. Microbiological Reviews; 1996; 60: 21-43. doi: 10.1128/mr.60.1.21-43.1996
Gordon RE. Haynes WC, Pang CHN. The genus Bacillus. Agriculture Handbook.Washington DC; 1973.
Ash C, Farrow JA, Wallbanks S, Collins MD. Phylogenetic heterogeneity of the genus Bacillus revealed by comparative analysis of small subunit ribosomal RNA sequences. Letters in AppliedMicrobiology; 1991; 13: 202-206. doi: 10.1111/j.1472-765X.1991.tb00608.x
Rainey FA, Fritze D, Stackebrandt E. The phylogenetic diversity of thermophilic members ofthe genus Bacillus as revealed by 16S rDNA analysis. FEMS Microbiology Letters; 1994; 115; 205-212. doi: 10.1111/j.1574-6968.1994.tb06639.x.
Nielsen P, Rainey FA, Outtrup H, Priest FG, Fritze D. Comparative 16S rDNA sequence analysis of some alkaliphilic bacilli and the establishment of a sixth rRNA group within Bacillus.FEMS Microbiology Letters; 1994; 117: 61-66. doi: 10.1016/0378-1097(94)90171-6
Ash C, Priest KG, Collins MD. Molecular identification of rRNA group 3 bacilli (Ash. Farrow.Wall banks and Collins) using a PCR probe test. Antonie van Leeuwenhoek; 1993; 64: 253-260. doi: 10.1007/BF00873085
Shida O, Takagi H, Kadowaki K, Komagata K.. Proposal for two new genera, Brevibacillus gen. nov. and Aneurinibacillus gen. nov. International Journal of Systematic Bacteriology; 1996; 46: 939-946. doi:10.1099/00207713-46-4-939
Favret ME, Yousten AA. Insecticidal activity of Bacillus laterosporus. Journal of Invertebrate Pathology; 1985; 45: 195-203. doi: 10.1128/aem.64.7.2723-2725.1998
Singer S. The utility of strains of morphological group II Bacillus. Advances in Applied Microbiology; 1996; 42: 219-261. doi:10.1016/S0065-2164(08)70374-5
Falkow S. What is a pathogen? ASM News; 1997; 63: 359-365.
Buchner P. Endosymbiosis of Animals with Plant Microorganisms. New York: Interscience; 1965.
Douglas AE. Prosser WA. Synthesis of the essential amino acid tryptophan in the pea aphid (Acyrthosiphon pisumi) symbiosis. Journal of Insect Physiology; 1992; 38: 565-568. doi: 10.1016/0022-1910(92)90107-O
Schröder D, Deppisch H, Obermayer M, Krohne G, Stackebrandt E, Hölldober B, Goebel W, Gross R. Intracellular endosymbiotic bacteria of Camponotus species (carpenter ants): systematics, evolution and ultrastructural characterization. Molecular Microbiology; 1996; 21: 479-489. doi: 10.1111/j.1365-2958.1996.tb02557.x
Aksoy S. Wigglesworthia gen. nov. and Wigglesworthia glossinidia sp. nov., taxa consisting of the mycetocyte-associated, primary endosymbionts of tsetse flies. International Journal of Systematic Bacteriology; 1995; 45: 848-851. doi: 10.1099/00207713-45-4-848
Hertig M. The rickettsia, Wolbachia pipientis (gen. nov. et sp. nov.) and associated inclusions ofthe mosquito Culex pipiens. Parasitology; 1936; 28: 453-486.
Yen JH, Barr AR. New hypothesis on the cause of cytoplasmic incompatibility in Culex pipiens. Nature; 1971; 232 (5313): 657-658. doi: 10.1038/232657a0
Hart S. When Wolbachia invades, insect sex lives get into a spin. BioScience; 1995; 45 (1): 4-6. doi: 10.2307/1312527
Rigaud T, Rousset F. What generates the diversity of Wolbachia - arthropod interactions?Biodiversity and Conservation; 1996; 5: 999-1013. doi: 10.1007/BF00054417
Whitfield AE, Falk BW, Rotenberg D. Insect vector-mediated transmission of plant viruses. Virology; 2015; 479–480: 278–289. doi:10.1016/j.virol.2015.03.026
Perilla-Henao L, Casteel C. Vector-borne bacterial plant pathogens: interactions with hemipteran insects and plants. Front Plant Sci.; 2016; 7: 1163. doi:10.3389/fpls.2016.01163
Huang W, Reyes-Caldas P, Mann M, Seifbarghi S, Kahn A, Almeida RPP, Béven L, Heck M, Hogenhout SA, Coaker G. Bacterial Vector-Borne Plant Diseases: Unanswered Questions and Future Directions. Molecular Plant; 2020; 13(10): 1379-1393. doi: 10.1016/j.molp.2020.08.010.
Eigenbrode SD, Bosque-Pérez NA, Davis TS. Insect-borne plant pathogens and their vectors: ecology, evolution, and complex interactions. Annual Reviews Entomolgy; 2018; 63: 169–191. doi:10.1146/annurev-ento-020117-043119
Ng JCK, Perry KL. Transmission of plant viruses by aphid vectors. Molecular Plant Patholgy; 2004; 5: 505–511. doi:10.1111/j.1364-3703.2004.00240.x
Nault LR. Arthropod transmission of plant viruses: a new synthesis. Annals of the Entomolgical Society of America; 1997; 90: 521–541. doi:10.1093/aesa/90.5.521
Eigenbrode SD, Ding H, Shiel P, Berger PH. 2002 Volatiles from potato plants infected with potato leafroll virus attract and arrest the virus vector, Myzus persicae (Homoptera: Aphididae). Proc. R. Soc. Lond. B 269, 455–460. doi:10.1098/rspb. 2001.1909
Luan JB, Yao DM, Zhang T, Walling LL, Yang M, Wang YJ, Liu SS. Suppression of terpenoid synthesis in plants by a virus promotes its mutualism with vectors. Ecology Letterrs; 2013; 16: 390–398. doi:10.1111/ele.12055
Santiago MFM, King KC, Drew GC. Interactions between insect vectors and plant pathogens span the parasitism–mutualism continuum. Biology Letters; 2023; 19: 20220453. doi: 10.1098/rsbl.2022.0453
Ruiu L. Insect Pathogenic Bacteria in Integrated Pest Management. Insects; 2015; 6: 352-367; doi:10.3390/insects6020352
Morris, O.N. Susceptibility of some forest insects to mixtures of commercial Bacillus thuringiensis and chemical insecticides, and sensitivity of the pathogen to the insecticides. Can. Entomol.; 1972; 104: 1419–1425.
Seleena P, Lee HL, Chiang YF. Compatibility of Bacillus thuringiensis serovar israelensis and chemical insecticides for the control of Aedes mosquitoes. J. Vector Ecol.; 1999; 24: 216–223.
Musser FR, Nyrop JP, Shelton AM. Integrating biological and chemical controls in decision making: European corn borer (Lepidoptera: Crambidae) control in sweet corn as an example. J. Econ. Entomol.; 2006; 99: 1538–1549. doi: 10.1603/0022-0493-99.5.1538
Karabörklü S, Azizoglu U, Azizoglu ZB. Recombinant entomopathogenic agents: a review of biotechnological approaches to pest insect control. World Journal of Microbiology and Biotechnology; 2018; 34: 14. doi:10.1007/s11274-017-2397-0
Van der Putten WH, Vet LEM, Harvey JA, Wackers FL. Linking above- and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists. Trends in Ecology & Evolution; 2001; 16: 547–554. doi:10.1016/S0169-5347(01)02265-0
Ohgushi T. Indirect interaction webs: herbivore-induced effects through trait change in plants. Annual Review of Ecology, Evolution, and Systematics; 2005; 36, 81–105. doi: 10.1146/annurev.ecolsys.36.091704.175523
Ohgushi T. Herbivore-induced indirect interaction webs on terrestrial plants: the importance of non-trophic, indirect, and facilitative interactions. Entomologia Experimentalis et Applicata; 2008; 128: 217–229. doi: 10.1111/j.1570-7458.2008.00705.x
Van Zandt PA, Agrawal AA. Community-wide impacts of herbivore-induced plant responses in milkweed (Asclepias syriaca). Ecology; 2004; 85: 2616–2629. doi: 10.1890/03-0622
Poelman EH, Broekgaarden C, Van Loon, JJA, Dicke M. Early season herbivore differentially affects plant defence responses to subsequently colonizing herbivores and their abundance in the field. Molecular Ecology; 2008; 17: 3352–3365. doi: 10.1111/j.1365-294X.2008.03838.x.
Utsumi S. Eco-evolutionary dynamics in herbivorous insect communities mediated by induced plant responses. Population Ecology; 2011; 53: 23–34. Doi:10.1007/s10144-010-0253-2
Kluth S, Kruess A, Tscharntke T. Interactions between the rust fungus Puccinia punctiformis and ectophagous and endophagous insects on creeping thistle. Journal of Applied Ecology; 2001; 38: 548–556. doi: 10.1046/j.1365-2664.2001.00612.x
Omacini M, Chaneton EJ, Ghersa CM, Muller CB. Symbiotic fungal endophytes control insect host-parasite interaction webs. Nature; 2001; 409: 78–81. doi: 10.1038/35051070
Katayama N, Zhang ZQ, Ohgushi T. Community-wide effects of below-ground rhizobia on above-ground arthropods. Ecological Entomology; 2011; 36: 43–51. doi: 10.1111/j.1365-2311.2010.01242.x
Tack AJM, Gripenberg S, Roslin T. Cross-kingdom interactions matter: fungal-mediated interactions structure an insect community on oak. Ecology Letters; 2012; 15: 177–185. doi: 10.1111/j.1461-0248.2011.01724.x.
Referanslar
Nesler A, Perazzolli M, Puopolo G, Giovannini O, Elad Y, Pertot I. A complex protein derivative acts as biogenic elicitor of grapevine resistance against powdery mildew under field conditions. Front Plant Sci.; 2015; 6:715. doi: 10.3389/fpls.2015.00715.
Jurat-Fuentes JL, Jackson TA. Bacterial Entomopathogens In: Vega FE, Kaya HK (eds.) Insect Pathology. 2nd ed. Academic Press; 2012. p. 265-349.
Oliver KM, Martinez AJ. How resident microbes modulate ecologicallyimportant traits of insects. Curr Opin Insect Sci. 2014;4:1–7. Doi:10. 1016/j. cois. 2014. 08. 001.
Sanchez-Contreras M, Vlisidou I.. The Diversity of Insect-bacteria Interactions and its Applications for Disease Control. Biotechnology and Genetic Engineering Reviews; 2008; 25: 203-244. doi: 10.5661/bger-25-203
Priest FG, Dewar SJ. Bacteria and Insects. In: Priest, F.G., Goodfellow, M. (eds) Applied Microbial Systematics. Springer, Dordrecht.; 2000. p. 165-202.
de Bary HA. Die Erscheinung der Symbiose. Verlag von Karl J.Trübner, Strassburg; 1879
Moya A, Pereto J, Gil R, Latorre A,. Learning how to live together: genomic insights into prokaryote-animal symbioses. Nature Review Genetics; 2008; 9, 218-229. doi: 10.1038/nrg2319
Dillon RJ, Dillon VM. The gut bacteria of insects: nonpathogenic interactions. Annual Review Entomolgy; 2004; 49; 71-92. doi: 10.1146/annurev.ento.49.061802.123416
Moran NA. Symbiosis. Curr Biol. 2006;16(20),866-871. doi: 10. 1016/j. cub. 2006. 09. 019. PMID: 17055966.
Jing TZ, Qi FH, Wang ZY. Most dominant roles of insect gut bacteria: digestion, detoxification, or essential nutrient provision?. Microbiome; 2020; 8; 38. doi: 10.1186/s40168-020-00823-y
Bucher C. (1981). Identification of bacteria found in insects. In: Burges HD (ed), Microbial Control of Pests and Plant Diseases1970-1980. London: Academic Press; 1981. p. 7-33.
Davidson EW. Biochemistry and mode of action of the Bacillus sphaericus toxins. Memorias do Instituto Oswaldo Cruz; 1995; 90: 81-86. doi: 10.1590/s0074-02761995000100018
Gill SS. Biochemistry and mode of action of Bacillus thuringiensis toxins. Memorias do Instituto Oswaldo Cruz; 1995; 90: 69-74. doi: 10.1590/s0074-02761995000100016.
Charles JF. Nielsen Leroux, C. Delecluse A. Bacillus sphaericus toxins: molecular biology andmode of action. Annual Review of Entomology; 1996; 41: 451-472. doi: 10.1146/annurev.en.41.010196.002315
Kumar PA, Sharma RP, Malik VS.. The insecticidal proteins of Bacillus thuringiensis. Advancesin Applied Microbiology; 1996; 42: 1-43. doi: 10.1016/S0065-2164(08)70371
Hurlburt, R.E. Investigations into the pathogenic mechanisms of the bacterium-nematode complex: the search for virulence determinants of Xenorhabdus nematophilus ATCC 19061 could lead to agriculturally useful products. ASM News; 1994; 60:473-478.
Forst S, Nealson K. Molecular biology of the symbiotic pathogenic bacteria Xenorhabdus spp. and Photorhabdus spp. Microbiological Reviews; 1996; 60: 21-43. doi: 10.1128/mr.60.1.21-43.1996
Gordon RE. Haynes WC, Pang CHN. The genus Bacillus. Agriculture Handbook.Washington DC; 1973.
Ash C, Farrow JA, Wallbanks S, Collins MD. Phylogenetic heterogeneity of the genus Bacillus revealed by comparative analysis of small subunit ribosomal RNA sequences. Letters in AppliedMicrobiology; 1991; 13: 202-206. doi: 10.1111/j.1472-765X.1991.tb00608.x
Rainey FA, Fritze D, Stackebrandt E. The phylogenetic diversity of thermophilic members ofthe genus Bacillus as revealed by 16S rDNA analysis. FEMS Microbiology Letters; 1994; 115; 205-212. doi: 10.1111/j.1574-6968.1994.tb06639.x.
Nielsen P, Rainey FA, Outtrup H, Priest FG, Fritze D. Comparative 16S rDNA sequence analysis of some alkaliphilic bacilli and the establishment of a sixth rRNA group within Bacillus.FEMS Microbiology Letters; 1994; 117: 61-66. doi: 10.1016/0378-1097(94)90171-6
Ash C, Priest KG, Collins MD. Molecular identification of rRNA group 3 bacilli (Ash. Farrow.Wall banks and Collins) using a PCR probe test. Antonie van Leeuwenhoek; 1993; 64: 253-260. doi: 10.1007/BF00873085
Shida O, Takagi H, Kadowaki K, Komagata K.. Proposal for two new genera, Brevibacillus gen. nov. and Aneurinibacillus gen. nov. International Journal of Systematic Bacteriology; 1996; 46: 939-946. doi:10.1099/00207713-46-4-939
Favret ME, Yousten AA. Insecticidal activity of Bacillus laterosporus. Journal of Invertebrate Pathology; 1985; 45: 195-203. doi: 10.1128/aem.64.7.2723-2725.1998
Singer S. The utility of strains of morphological group II Bacillus. Advances in Applied Microbiology; 1996; 42: 219-261. doi:10.1016/S0065-2164(08)70374-5
Falkow S. What is a pathogen? ASM News; 1997; 63: 359-365.
Buchner P. Endosymbiosis of Animals with Plant Microorganisms. New York: Interscience; 1965.
Douglas AE. Prosser WA. Synthesis of the essential amino acid tryptophan in the pea aphid (Acyrthosiphon pisumi) symbiosis. Journal of Insect Physiology; 1992; 38: 565-568. doi: 10.1016/0022-1910(92)90107-O
Schröder D, Deppisch H, Obermayer M, Krohne G, Stackebrandt E, Hölldober B, Goebel W, Gross R. Intracellular endosymbiotic bacteria of Camponotus species (carpenter ants): systematics, evolution and ultrastructural characterization. Molecular Microbiology; 1996; 21: 479-489. doi: 10.1111/j.1365-2958.1996.tb02557.x
Aksoy S. Wigglesworthia gen. nov. and Wigglesworthia glossinidia sp. nov., taxa consisting of the mycetocyte-associated, primary endosymbionts of tsetse flies. International Journal of Systematic Bacteriology; 1995; 45: 848-851. doi: 10.1099/00207713-45-4-848
Hertig M. The rickettsia, Wolbachia pipientis (gen. nov. et sp. nov.) and associated inclusions ofthe mosquito Culex pipiens. Parasitology; 1936; 28: 453-486.
Yen JH, Barr AR. New hypothesis on the cause of cytoplasmic incompatibility in Culex pipiens. Nature; 1971; 232 (5313): 657-658. doi: 10.1038/232657a0
Hart S. When Wolbachia invades, insect sex lives get into a spin. BioScience; 1995; 45 (1): 4-6. doi: 10.2307/1312527
Rigaud T, Rousset F. What generates the diversity of Wolbachia - arthropod interactions?Biodiversity and Conservation; 1996; 5: 999-1013. doi: 10.1007/BF00054417
Whitfield AE, Falk BW, Rotenberg D. Insect vector-mediated transmission of plant viruses. Virology; 2015; 479–480: 278–289. doi:10.1016/j.virol.2015.03.026
Perilla-Henao L, Casteel C. Vector-borne bacterial plant pathogens: interactions with hemipteran insects and plants. Front Plant Sci.; 2016; 7: 1163. doi:10.3389/fpls.2016.01163
Huang W, Reyes-Caldas P, Mann M, Seifbarghi S, Kahn A, Almeida RPP, Béven L, Heck M, Hogenhout SA, Coaker G. Bacterial Vector-Borne Plant Diseases: Unanswered Questions and Future Directions. Molecular Plant; 2020; 13(10): 1379-1393. doi: 10.1016/j.molp.2020.08.010.
Eigenbrode SD, Bosque-Pérez NA, Davis TS. Insect-borne plant pathogens and their vectors: ecology, evolution, and complex interactions. Annual Reviews Entomolgy; 2018; 63: 169–191. doi:10.1146/annurev-ento-020117-043119
Ng JCK, Perry KL. Transmission of plant viruses by aphid vectors. Molecular Plant Patholgy; 2004; 5: 505–511. doi:10.1111/j.1364-3703.2004.00240.x
Nault LR. Arthropod transmission of plant viruses: a new synthesis. Annals of the Entomolgical Society of America; 1997; 90: 521–541. doi:10.1093/aesa/90.5.521
Eigenbrode SD, Ding H, Shiel P, Berger PH. 2002 Volatiles from potato plants infected with potato leafroll virus attract and arrest the virus vector, Myzus persicae (Homoptera: Aphididae). Proc. R. Soc. Lond. B 269, 455–460. doi:10.1098/rspb. 2001.1909
Luan JB, Yao DM, Zhang T, Walling LL, Yang M, Wang YJ, Liu SS. Suppression of terpenoid synthesis in plants by a virus promotes its mutualism with vectors. Ecology Letterrs; 2013; 16: 390–398. doi:10.1111/ele.12055
Santiago MFM, King KC, Drew GC. Interactions between insect vectors and plant pathogens span the parasitism–mutualism continuum. Biology Letters; 2023; 19: 20220453. doi: 10.1098/rsbl.2022.0453
Ruiu L. Insect Pathogenic Bacteria in Integrated Pest Management. Insects; 2015; 6: 352-367; doi:10.3390/insects6020352
Morris, O.N. Susceptibility of some forest insects to mixtures of commercial Bacillus thuringiensis and chemical insecticides, and sensitivity of the pathogen to the insecticides. Can. Entomol.; 1972; 104: 1419–1425.
Seleena P, Lee HL, Chiang YF. Compatibility of Bacillus thuringiensis serovar israelensis and chemical insecticides for the control of Aedes mosquitoes. J. Vector Ecol.; 1999; 24: 216–223.
Musser FR, Nyrop JP, Shelton AM. Integrating biological and chemical controls in decision making: European corn borer (Lepidoptera: Crambidae) control in sweet corn as an example. J. Econ. Entomol.; 2006; 99: 1538–1549. doi: 10.1603/0022-0493-99.5.1538
Karabörklü S, Azizoglu U, Azizoglu ZB. Recombinant entomopathogenic agents: a review of biotechnological approaches to pest insect control. World Journal of Microbiology and Biotechnology; 2018; 34: 14. doi:10.1007/s11274-017-2397-0
Van der Putten WH, Vet LEM, Harvey JA, Wackers FL. Linking above- and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists. Trends in Ecology & Evolution; 2001; 16: 547–554. doi:10.1016/S0169-5347(01)02265-0
Ohgushi T. Indirect interaction webs: herbivore-induced effects through trait change in plants. Annual Review of Ecology, Evolution, and Systematics; 2005; 36, 81–105. doi: 10.1146/annurev.ecolsys.36.091704.175523
Ohgushi T. Herbivore-induced indirect interaction webs on terrestrial plants: the importance of non-trophic, indirect, and facilitative interactions. Entomologia Experimentalis et Applicata; 2008; 128: 217–229. doi: 10.1111/j.1570-7458.2008.00705.x
Van Zandt PA, Agrawal AA. Community-wide impacts of herbivore-induced plant responses in milkweed (Asclepias syriaca). Ecology; 2004; 85: 2616–2629. doi: 10.1890/03-0622
Poelman EH, Broekgaarden C, Van Loon, JJA, Dicke M. Early season herbivore differentially affects plant defence responses to subsequently colonizing herbivores and their abundance in the field. Molecular Ecology; 2008; 17: 3352–3365. doi: 10.1111/j.1365-294X.2008.03838.x.
Utsumi S. Eco-evolutionary dynamics in herbivorous insect communities mediated by induced plant responses. Population Ecology; 2011; 53: 23–34. Doi:10.1007/s10144-010-0253-2
Kluth S, Kruess A, Tscharntke T. Interactions between the rust fungus Puccinia punctiformis and ectophagous and endophagous insects on creeping thistle. Journal of Applied Ecology; 2001; 38: 548–556. doi: 10.1046/j.1365-2664.2001.00612.x
Omacini M, Chaneton EJ, Ghersa CM, Muller CB. Symbiotic fungal endophytes control insect host-parasite interaction webs. Nature; 2001; 409: 78–81. doi: 10.1038/35051070
Katayama N, Zhang ZQ, Ohgushi T. Community-wide effects of below-ground rhizobia on above-ground arthropods. Ecological Entomology; 2011; 36: 43–51. doi: 10.1111/j.1365-2311.2010.01242.x
Tack AJM, Gripenberg S, Roslin T. Cross-kingdom interactions matter: fungal-mediated interactions structure an insect community on oak. Ecology Letters; 2012; 15: 177–185. doi: 10.1111/j.1461-0248.2011.01724.x.
