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Evaluation of Interactions Among Aphids, Endosymbionts, and Host Plants: A Foresight for the Future

Yıl 2022, Cilt: 53 Sayı: 2, 133 - 139, 01.05.2022
https://doi.org/10.54614/AUAF.2022.1002421

Öz

Insects, the most common and most successful animals on earth, establish long-term and stable ecological relationships with bacteria. Aphids (Hemiptera: Aphididae) are an insect group of agricultural importance that can feed on many herbaceous, shrubs, and woody plants as hosts and are also in close relationship with endosymbiont bacteria. It is seen that aphid is going to further increase their current pest potential in the near future due to their high adaptability and rapid reproduction ability. In order to be effective and successful in the biological control of aphids, many features of aphids are required to be known and clarified. Therefore, determining the interactions among aphid, host plant, and endosymbiont in this relationship might make biological control of aphids more effective. In this review, what is known about the relationship among aphids, the primary endosymbiotic bacterium Buchnera aphidicola, and the host plant is examined, and the possibilities of using symbiont bacteria in the biological control of aphids are discussed.

Kaynakça

  • Agrawal, A.A., 2000. Mechanisms, ecological consequences and agricultural implications of tri-trophic interactions. Current Opinion in Plant Biology, 3:329–335.
  • Ali, J.G., Agrawal, A.A., 2012. Specialist versus generalist insect herbivores and plant defense. Trends in Plant Science, 17(5):293-302.
  • Awmack, C.S., Leather, S.R., 2002. Host Plant Quality and Fecundity in Herbivorous Insects. Annual Review of Entomology, 47:817-844.
  • Baumann, L., Baumann, P., 1994. Growth kinetics of the endosymbiont, Buchnera aphidicola, in the aphid Schizaphis graminum. Applied and Environmental Microbiology, 60, 3440–3443.
  • van Bel, A.J.E., Will, T., 2016. Functional Evaluation of Proteins in Watery and Gel Saliva of Aphids. Frontiers in Plant Science, 7, 1840.
  • Birch, A.N.E., Geoghegan, I.E., Majerus, M.E.N., McNicol, J.W., Hackett, C.A. et al., 1999. Tri-trophic interactions involving pest aphids, predatory 2-spot ladybirds and transgenic potatoes expressing snowdrop lectin for aphid resistance. Molecular Breeding, 5:75–83.
  • Brinza, L., Vinuelas, J., Cottret, L., Calevro, F., Rahbe, Y. et al., 2009. Systemic analysis of the symbiotic function of Buchnera aphidicola, the primary endosymbiont of the pea aphid Acyrthosiphon pisum. Comptes Rendus Biologies, 332(11):1034-1049.
  • Bultman, T.L., Bell, G.D., 2003. Interaction between fungal endophytes and environmental stressors influences plant resistance to insects. OIKOS, 103:182–190.
  • Burke, G. R., Normark, B. B., Favret, C., Moran, N. A., 2009. Evolution and Diversity of Facultative Symbionts from the Aphid Subfamily Lachninae. Applied and Environmental Microbiology, 75(16):5328-5335.
  • Charles, H., Ishikawa, H., 1999. Physical and Genetic Map of the Genome of Buchnera, Primary Endosymbiont of the Pea Aphid Acyrthosiphon pisum. Journal of Molecular Evolution, 48(2):142-150.
  • Cheynier, V., Comte, G., Davies, K.M., Lattanzio, V., Martens, S., 2013. Plant phenolics: Recent advances on their biosynthesis, genetics, and ecophysiology. Plant Physiology and Biochemistry, 72,1-20.
  • Clark, E.L., Karley, A.J., Hubbard, S.F., 2010. Insect endosymbionts: manipulators of insect herbivore trophic interactions. Protoplasma, 244, 25–51.
  • Coppola, M., Manco, E., Vitiello, A., Di-Lelio, I., Giorgini, M., et al., 2018. Plant response to feeding aphids promotes aphid dispersal. Entomologia Experimentalis et Applicata, 166(5):386–394.
  • Dale, C., Moran, N.A., 2006. Molecular interactions between bacterial symbionts and their hosts. Cell, 126(3):453–465.
  • Dixon, A.F.G., 1998. Aphid ecology - An optimization approach, Second Edition, Chapman& Hall, London.
  • Douglas, A.E., 1996. Reproductive Failure and the Free Amino Acid Pools in Pea Aphids (Acyrthosiphon pisum) Lacking Symbiotic Bacteria. Journal of Insect Physiology, 42(3):247-255.
  • Douglas, A.E., Prosser, W.A., 1992. Synthesis of the essential amino acid tryptophan in the pea aphid (Acyrthosiphon pisum) symbiosis. Journal of Insect Physiology, 38(8):565–568.
  • Dunbar, H.E., Wilson, A.C.C., Ferguson, N.R., Moran, N.A., 2007. Aphid thermal tolerance is governed by a point mutation in bacterial symbionts. PLOS Biology, 5(5): e96, 1006-1015.
  • Eyres, I., Duvaux, L., Gharbı,K., Tucker, R., Hopkıns, D. et al., 2017. Specıal Issue: The Molecular Mechanısms Of Adaptatıon And Specıatıon: Integratıng Genomıc And Molecular Approaches Targeted Re-Sequencing Confirms The İmportance Of chemosensory genes in aphid host race differentiation. Molecular Ecology, 26:43-58.
  • Frago, E., Dicke, M., Godfray, H.C.J., 2012. Insect symbionts as hidden players in insect–plant interactions. Trends in Ecology and Evolution, 27(12):705-711.
  • Francis, F., Gerkens, P., Harmel, N., De Pauw, E., Haubruge, E., 2006. Proteome variations of the Myzus persicae aphid according to host plant change. Insect Biochemistry and Molecular Physiology 36, 219–227.
  • Francis, F., Guillonneau, F., Leprince, P., De Pauw, E., Haubruge, E. et al., 2010. Tritrophic interactions among Macrosiphum euphorbiae aphids, their host plants and endosymbionts: Investigation by a proteomic approach. Journal of Insect Physiology, 56:575-585.
  • Fukatsu, T., Nikoh, N., Kawai R., Koga, R., 2000. The secondary endosymbiotic bacterium of the pea aphid Acyrthosiphon pisum (Insecta: Homoptera). Applied and Environmental Microbiology, 66(7):2748-2758.
  • Gill, R., Sabater-Munoz, B., Latorre, A., Silva, F. J., Moya, A., 2002. Extreme genome reduction in Buchnera spp.: Toward the minimal genome needed for symbiotic life. Proceedings of the Natural Academy of Sciences, 99(7):4454-4458.
  • Giordanengo, P., Brunissen, L., Rusterucci, C., Vincent, C., Bel, A. et al., 2010. Compatible plant-aphid interactions: How aphids manipulate plant responses. Comptes Rendus Biologies, 333(6–7):516-523.
  • Gosalbes, M.J., Lamelas, A., Moya, A., Latorre, A., 2008. The Striking Case of Tryptophan Provision in the Cedar Aphid Cinara cedri. Journal of Bacteriology, 190(17):6026-6029.
  • Güz, N., Dağeri, A., Aksoy, S., 2015. Endosimbiyotik bakterilerin böcekler üzerine etkisi. Türkiye Entomoloji Bülteni, 5(2):101-113.
  • van Ham, R.C.H.J., Kamerbeek, J., Palacios, C., Rausell, C., Abascal, F. et al., 2003. Reductive genome evolution in Buchnera aphidicola. Proc Natl Acad Sci, 100(2):581–586.
  • Hardie, J., Leckstein, P., 2007. Antibiotics, primary symbionts and wing polyphenism in three aphid species. Insect Biochemistry and Molecular Biology, 37(8):886-890.
  • Hendry T.A., Clark, K.J., Baltrus, D.A., 2016. A highly infective plant-associated bacterium influences reproductive rates in pea aphids. R. Soc. Open Sci.3: 150478.
  • Heyworth, E.R., Ferrari, J., 2015. A facultative endosymbiont in aphids can provide diverse ecological benefits. Journal of Evolutionary Biology, 28(10):1753-1760.
  • Humphreys, N.J., Douglas, A.E.,1997. Partitioning of Symbiotic Bacteria between Generations of an Insect: a Quantitative Study of a Buchnera sp. in the Pea Aphid Acyrthosiphon pisum) Reared at Different Temperatures. Applied and Environmental Microbiology, 63(8):3294-3296.
  • Jaouannet, M., Rodriguez P.A., Thorpe, P., Lenoir, C.J.G., MacLeod, R. et al., 2014. Plant immunity in plant–aphid interactions. Front Plant Sci, 5:663.
  • Jousselin, E., Clamens, A.L., Galan, M., Bernard M., Maman, S. et al., 2016. Assessment of a 16S rRNA amplicon Illumina sequencing procedure for studying the microbiome of a symbiont-rich aphid genus. Molecular Ecology Resources, 16(3):628-640.
  • Karban, R., Yang, L.H., Edwards K.F., 2014. Volatile communication between plants that affects herbivory: a meta-analysis. Ecology Letters, 17:44–52.
  • Koç, E., Üstün, A.S, 2008. Patojenlere Karşı Bitkilerde Savunma ve Antioksidanlar. Erciyes Üniv Fen Bil. Ens. Derg., 24(1-2):82-100.
  • Koga, R., Tsuchida, T., Fukatsu, T., 2003. Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid. Proceedings of The Royal Society, 270(1533):2543-2550.
  • Luan, J-B., Chen, W., Hasegawa, D.K., Simmons, A.M., Wintermantel, W.M. et al., 2015. Metabolic coevolution in the bacterial symbiosis of whiteflies and related plant Sap-feeding insects. Genome Biology and Evolution, 7:2635-2647.
  • Machado-Assefh, C.R., Lopez-Isasmendi, G., Tjallingii, W.F., Jander, G., Alvarez, A.E., 2015. Distrupting Buchnera aphidicola, the Endosymbiotic bacteria of Myzus persicae, delays host plant acceptance. Arthropod-Plant Interactions, 9(5):529-541.
  • Martinez-Torres, D., Buades, C., Latorre A., Moya, A., 2001. Molecular Systematics of Aphids and Their Primary Endosymbionts. Molecular Phylogenetics and Evolution, 20(3):437-449.
  • Mattson, W.J., 1980. Herbivory in relation to plant nitrogen content. Ann. Rev. Ecol. Syst, 11:119-161.
  • McLean, A.H.C., van Asch, M., Ferrari, J., Godfray, H.C.J., 2010. Effects of bacterial secondary symbionts on host plant use in pea aphids. Proceedings of the Royal Society B, 278(1706):760-766.
  • Moran, N.A., Degnan, P.H., Santos, S.R., Dunbar, H.E., Ochman, H. et al., 2005. The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genes. Proceedings of the National Academy of Sciences of the USA, 102(47):16919–16926.
  • Morgan, D., Walters K.F.A., Aegerter, J.N., 2001. Effect of temperature and cultivar on pea aphid, Acyrthosiphon pisum (Hemiptera: Aphididae) life history. Bulletin of Entomological Research, 91(1):47-52.
  • Montllor, C.B., Maxmen, A., Purcell, A.H., 2002. Facultative Bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecological Entimology, 27(2):189-195.
  • Mugford, S.T., Barclay, E., Drurey, C., Findlay, K.C., Hogenhout, S.A., 2016. An immuno-suppressive aphid saliva protein is delivered into the cytosol of plant mesophyll cells during feding. Molecular Plant-Microbe Interactions, 29(11):854–861.
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Afitler, Endosimbiyontlar ve Konukçu Bitkiler Arasındaki İlişkilerin Değerlendirilmesi: Gelecek için Bir Öngörü

Yıl 2022, Cilt: 53 Sayı: 2, 133 - 139, 01.05.2022
https://doi.org/10.54614/AUAF.2022.1002421

Öz

Yeryüzündeki en yaygın ve en başarılı hayvanlar olan böcekler, bakterilerle uzun vadeli ve istikrarlı ekolojik ilişkiler kurarlar. Afitler (Yaprak bitleri), konak olarak birçok otsu bitki, çalı ve odunsu bitki ile beslenen, aynı zamanda endosimbiyont bakterilerle de yakın ilişki içinde olan, tarımsal öneme sahip bir böcek grubudur. Yaprak bitlerinin yüksek adaptasyon ve hızlı üreme yetenekleri nedeniyle yakın gelecekte mevcut zararlı potansiyellerini daha da artıracağı görülmektedir. Yaprak bitlerinin biyolojik mücadelesinde etkili ve başarılı olabilmek için yaprak bitlerinin birçok özelliğinin bilinmesi ve netleştirilmesi gerekmektedir. Bu nedenle, bu ilişkide yaprak biti, konak bitki ve endosimbiyont arasındaki etkileşimlerin belirlenmesi, yaprak bitleri ile biyolojik mücadeleyi daha etkin kılabilir. Bu derlemede, yaprak biti, birincil endosimbiyotik bakteri Buchnera aphidicola ve konak bitki arasındaki ilişki hakkında bilinenler incelenmekte ve yaprak bitlerinin bisyolojik kontrolünde simbiyotik bakterilerin kullanım olanakları tartışılmaktadır.

Kaynakça

  • Agrawal, A.A., 2000. Mechanisms, ecological consequences and agricultural implications of tri-trophic interactions. Current Opinion in Plant Biology, 3:329–335.
  • Ali, J.G., Agrawal, A.A., 2012. Specialist versus generalist insect herbivores and plant defense. Trends in Plant Science, 17(5):293-302.
  • Awmack, C.S., Leather, S.R., 2002. Host Plant Quality and Fecundity in Herbivorous Insects. Annual Review of Entomology, 47:817-844.
  • Baumann, L., Baumann, P., 1994. Growth kinetics of the endosymbiont, Buchnera aphidicola, in the aphid Schizaphis graminum. Applied and Environmental Microbiology, 60, 3440–3443.
  • van Bel, A.J.E., Will, T., 2016. Functional Evaluation of Proteins in Watery and Gel Saliva of Aphids. Frontiers in Plant Science, 7, 1840.
  • Birch, A.N.E., Geoghegan, I.E., Majerus, M.E.N., McNicol, J.W., Hackett, C.A. et al., 1999. Tri-trophic interactions involving pest aphids, predatory 2-spot ladybirds and transgenic potatoes expressing snowdrop lectin for aphid resistance. Molecular Breeding, 5:75–83.
  • Brinza, L., Vinuelas, J., Cottret, L., Calevro, F., Rahbe, Y. et al., 2009. Systemic analysis of the symbiotic function of Buchnera aphidicola, the primary endosymbiont of the pea aphid Acyrthosiphon pisum. Comptes Rendus Biologies, 332(11):1034-1049.
  • Bultman, T.L., Bell, G.D., 2003. Interaction between fungal endophytes and environmental stressors influences plant resistance to insects. OIKOS, 103:182–190.
  • Burke, G. R., Normark, B. B., Favret, C., Moran, N. A., 2009. Evolution and Diversity of Facultative Symbionts from the Aphid Subfamily Lachninae. Applied and Environmental Microbiology, 75(16):5328-5335.
  • Charles, H., Ishikawa, H., 1999. Physical and Genetic Map of the Genome of Buchnera, Primary Endosymbiont of the Pea Aphid Acyrthosiphon pisum. Journal of Molecular Evolution, 48(2):142-150.
  • Cheynier, V., Comte, G., Davies, K.M., Lattanzio, V., Martens, S., 2013. Plant phenolics: Recent advances on their biosynthesis, genetics, and ecophysiology. Plant Physiology and Biochemistry, 72,1-20.
  • Clark, E.L., Karley, A.J., Hubbard, S.F., 2010. Insect endosymbionts: manipulators of insect herbivore trophic interactions. Protoplasma, 244, 25–51.
  • Coppola, M., Manco, E., Vitiello, A., Di-Lelio, I., Giorgini, M., et al., 2018. Plant response to feeding aphids promotes aphid dispersal. Entomologia Experimentalis et Applicata, 166(5):386–394.
  • Dale, C., Moran, N.A., 2006. Molecular interactions between bacterial symbionts and their hosts. Cell, 126(3):453–465.
  • Dixon, A.F.G., 1998. Aphid ecology - An optimization approach, Second Edition, Chapman& Hall, London.
  • Douglas, A.E., 1996. Reproductive Failure and the Free Amino Acid Pools in Pea Aphids (Acyrthosiphon pisum) Lacking Symbiotic Bacteria. Journal of Insect Physiology, 42(3):247-255.
  • Douglas, A.E., Prosser, W.A., 1992. Synthesis of the essential amino acid tryptophan in the pea aphid (Acyrthosiphon pisum) symbiosis. Journal of Insect Physiology, 38(8):565–568.
  • Dunbar, H.E., Wilson, A.C.C., Ferguson, N.R., Moran, N.A., 2007. Aphid thermal tolerance is governed by a point mutation in bacterial symbionts. PLOS Biology, 5(5): e96, 1006-1015.
  • Eyres, I., Duvaux, L., Gharbı,K., Tucker, R., Hopkıns, D. et al., 2017. Specıal Issue: The Molecular Mechanısms Of Adaptatıon And Specıatıon: Integratıng Genomıc And Molecular Approaches Targeted Re-Sequencing Confirms The İmportance Of chemosensory genes in aphid host race differentiation. Molecular Ecology, 26:43-58.
  • Frago, E., Dicke, M., Godfray, H.C.J., 2012. Insect symbionts as hidden players in insect–plant interactions. Trends in Ecology and Evolution, 27(12):705-711.
  • Francis, F., Gerkens, P., Harmel, N., De Pauw, E., Haubruge, E., 2006. Proteome variations of the Myzus persicae aphid according to host plant change. Insect Biochemistry and Molecular Physiology 36, 219–227.
  • Francis, F., Guillonneau, F., Leprince, P., De Pauw, E., Haubruge, E. et al., 2010. Tritrophic interactions among Macrosiphum euphorbiae aphids, their host plants and endosymbionts: Investigation by a proteomic approach. Journal of Insect Physiology, 56:575-585.
  • Fukatsu, T., Nikoh, N., Kawai R., Koga, R., 2000. The secondary endosymbiotic bacterium of the pea aphid Acyrthosiphon pisum (Insecta: Homoptera). Applied and Environmental Microbiology, 66(7):2748-2758.
  • Gill, R., Sabater-Munoz, B., Latorre, A., Silva, F. J., Moya, A., 2002. Extreme genome reduction in Buchnera spp.: Toward the minimal genome needed for symbiotic life. Proceedings of the Natural Academy of Sciences, 99(7):4454-4458.
  • Giordanengo, P., Brunissen, L., Rusterucci, C., Vincent, C., Bel, A. et al., 2010. Compatible plant-aphid interactions: How aphids manipulate plant responses. Comptes Rendus Biologies, 333(6–7):516-523.
  • Gosalbes, M.J., Lamelas, A., Moya, A., Latorre, A., 2008. The Striking Case of Tryptophan Provision in the Cedar Aphid Cinara cedri. Journal of Bacteriology, 190(17):6026-6029.
  • Güz, N., Dağeri, A., Aksoy, S., 2015. Endosimbiyotik bakterilerin böcekler üzerine etkisi. Türkiye Entomoloji Bülteni, 5(2):101-113.
  • van Ham, R.C.H.J., Kamerbeek, J., Palacios, C., Rausell, C., Abascal, F. et al., 2003. Reductive genome evolution in Buchnera aphidicola. Proc Natl Acad Sci, 100(2):581–586.
  • Hardie, J., Leckstein, P., 2007. Antibiotics, primary symbionts and wing polyphenism in three aphid species. Insect Biochemistry and Molecular Biology, 37(8):886-890.
  • Hendry T.A., Clark, K.J., Baltrus, D.A., 2016. A highly infective plant-associated bacterium influences reproductive rates in pea aphids. R. Soc. Open Sci.3: 150478.
  • Heyworth, E.R., Ferrari, J., 2015. A facultative endosymbiont in aphids can provide diverse ecological benefits. Journal of Evolutionary Biology, 28(10):1753-1760.
  • Humphreys, N.J., Douglas, A.E.,1997. Partitioning of Symbiotic Bacteria between Generations of an Insect: a Quantitative Study of a Buchnera sp. in the Pea Aphid Acyrthosiphon pisum) Reared at Different Temperatures. Applied and Environmental Microbiology, 63(8):3294-3296.
  • Jaouannet, M., Rodriguez P.A., Thorpe, P., Lenoir, C.J.G., MacLeod, R. et al., 2014. Plant immunity in plant–aphid interactions. Front Plant Sci, 5:663.
  • Jousselin, E., Clamens, A.L., Galan, M., Bernard M., Maman, S. et al., 2016. Assessment of a 16S rRNA amplicon Illumina sequencing procedure for studying the microbiome of a symbiont-rich aphid genus. Molecular Ecology Resources, 16(3):628-640.
  • Karban, R., Yang, L.H., Edwards K.F., 2014. Volatile communication between plants that affects herbivory: a meta-analysis. Ecology Letters, 17:44–52.
  • Koç, E., Üstün, A.S, 2008. Patojenlere Karşı Bitkilerde Savunma ve Antioksidanlar. Erciyes Üniv Fen Bil. Ens. Derg., 24(1-2):82-100.
  • Koga, R., Tsuchida, T., Fukatsu, T., 2003. Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid. Proceedings of The Royal Society, 270(1533):2543-2550.
  • Luan, J-B., Chen, W., Hasegawa, D.K., Simmons, A.M., Wintermantel, W.M. et al., 2015. Metabolic coevolution in the bacterial symbiosis of whiteflies and related plant Sap-feeding insects. Genome Biology and Evolution, 7:2635-2647.
  • Machado-Assefh, C.R., Lopez-Isasmendi, G., Tjallingii, W.F., Jander, G., Alvarez, A.E., 2015. Distrupting Buchnera aphidicola, the Endosymbiotic bacteria of Myzus persicae, delays host plant acceptance. Arthropod-Plant Interactions, 9(5):529-541.
  • Martinez-Torres, D., Buades, C., Latorre A., Moya, A., 2001. Molecular Systematics of Aphids and Their Primary Endosymbionts. Molecular Phylogenetics and Evolution, 20(3):437-449.
  • Mattson, W.J., 1980. Herbivory in relation to plant nitrogen content. Ann. Rev. Ecol. Syst, 11:119-161.
  • McLean, A.H.C., van Asch, M., Ferrari, J., Godfray, H.C.J., 2010. Effects of bacterial secondary symbionts on host plant use in pea aphids. Proceedings of the Royal Society B, 278(1706):760-766.
  • Moran, N.A., Degnan, P.H., Santos, S.R., Dunbar, H.E., Ochman, H. et al., 2005. The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genes. Proceedings of the National Academy of Sciences of the USA, 102(47):16919–16926.
  • Morgan, D., Walters K.F.A., Aegerter, J.N., 2001. Effect of temperature and cultivar on pea aphid, Acyrthosiphon pisum (Hemiptera: Aphididae) life history. Bulletin of Entomological Research, 91(1):47-52.
  • Montllor, C.B., Maxmen, A., Purcell, A.H., 2002. Facultative Bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecological Entimology, 27(2):189-195.
  • Mugford, S.T., Barclay, E., Drurey, C., Findlay, K.C., Hogenhout, S.A., 2016. An immuno-suppressive aphid saliva protein is delivered into the cytosol of plant mesophyll cells during feding. Molecular Plant-Microbe Interactions, 29(11):854–861.
  • Nakabachi, A., Ishikawa, H., 1999. Provision of riboflavin to the host aphid, Acyrthosiphon pisum, by endosymbiotic bacteria, Buchnera. Journal of Insect Physiology, 45(1):1-6.
  • Oliver, K.M., Degnan, P.H., Burke, G.R., Moran, N.A., 2010. Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annual Review of Entomology, 55:247–266.
  • Parker, B.J., Spragg, C.J., Altincicek, B., Gerardo, N.M., 2013. Symbiont-mediated protection against fungal pathogens in pea aphids: a role for pathogen specificity. Appl Environ Microbiol, 79(7):2455-2458.
  • Pérez-Brocal, V., Gil, R., Ramos, S., Lamelas, A., Postigo, M. et al., 2006. A Small Microbial Genome: The End of a Long Symbiotic Relationship. Science, 314(5797):312-313.
  • Pontes, M.H., Dale, C., 2006. Culture and manipulation of insect facultative symbionts. Trends in Microbiology, 14(9):406–412.
  • Sasaki, T., Ishikawa, H., 1995. Production of Essential Amino Acids from Glutamate by Mycetocyte Symbionts of the Pea Aphid, Acyrthosiphon pisum. Journal of Insect Physiology, 41(1):41-46.
  • Scarborough, C.L., Ferrari, J., Godfray, H.C.J., 2005. Aphid Protected from Pathogen by Endosymbiont. Science, 310(5755):1781-81.
  • Sharma, G., Malthankar, P.A., Mathur, V., 2021. Insect–Plant Interactions: A Multilayered Relationship. Annals of the Entomological Society of America, 114(1):1-16.
  • Shigenobu, S., Watanabe, H., Hattori, M., Sakaki, Y., Ishikawa, H., 2000. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature, 407(6800):81–86.
  • Skaljac, M., 2016. Biology and Ecology of Aphids, Editör Andreas Vilcinskas, CRC Press, Germany.
  • Smith, C.M., Chuang, W.P., 2014. Plant resistance to aphid feeding: behavioral, physiological, genetic and molecular cues regulate aphid host selection and feeding. Pest Management Science, 70(4):528-540.
  • Thomas, F., Adamo, S., Moore, J., 2005. Parasitic manipulation: where are we and where should we go. Behav. Processes, 68:185-199.
  • Thorpe, P., Cock, P.J.A., Bos, J.,2016. Comparative transcriptomics and proteomics of three different aphid species identifies core and diverse effector sets. BMC Genomics, 17(172):1-18.
  • Tsuchida, T., Koga, R., Meng, X.Y., Matsumoto, T., Fukatsu, T., 2005. Characterization of a facultative endosymbiotic bacterium of the pea aphid Acyrthosiphon pisum. Microbial Ecology, 49(1):126-133.
  • Tsuchida, T., Koga, R., Matsumoto, S., Fukatsu, T., 2011. Interspecifi c symbiont transfection confers a novel ecological trait to the recipient insect. Biology Letters, 7(2):245-248.
  • Wang, J., Chung, S.H., Peiffer, M., Rosa, C., Hoover, K. et al., 2016. Herbivore oral secreted bacteria trigger distinct defense responses in preferred and non-preferred host plants. Journal of Chemical Ecology, 42(6):463–474.
  • Wilkinson, T.L., Douglas, A.E., 1995. Aphid Feeding, as Influenced by Disruption of the Symbiotic Bacteria: an Analysis of the Pea Aphid (Acyrthosiphon pisum). Journal of Insect Physiology, 41(8):635-640.
  • Wittstock, U., Gershenzon, J., 2002. Constitutive plant toxins and their role in defense against herbivores and pathogens. Current Opinion in Plant Biology, 5(4):300-307.
  • Yao, I., 2019. Seasonal changes in the density of the symbionts Buchnera and Wolbachia of the aphid Tuberculatus macrotuberculatus on Quercus dentata. Entomologia Experimentalis et Applicata, 167(3):261-268.
  • Zepeda-Paulo, F., Lavandero, B.,2021. Effect of the Genotypic Variation of an Aphid Host on the Endosymbiont Associations in Natural Host Populations. Insects,12(3):217.
  • Zhang, F., Li, X., Zhang, Y., Coates, B., Zhou, X.J. et al., 2015. Bacterial symbionts, Buchnera, and starvation on wing dimorphism in English grain aphid, Sitobion avenae (F.) (Homoptera:Aphididae). Frontiers in Physiology, 6(155):1-9.
Toplam 67 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Bölüm ARAŞTIRMALAR
Yazarlar

Gülay Olcabey Ergin 0000-0002-2521-2312

Ayten Öztürk 0000-0002-1860-8394

Gazi Görür 0000-0001-5713-418X

Yayımlanma Tarihi 1 Mayıs 2022
Yayımlandığı Sayı Yıl 2022 Cilt: 53 Sayı: 2

Kaynak Göster

APA Olcabey Ergin, G., Öztürk, A., & Görür, G. (2022). Evaluation of Interactions Among Aphids, Endosymbionts, and Host Plants: A Foresight for the Future. Atatürk Üniversitesi Ziraat Fakültesi Dergisi, 53(2), 133-139. https://doi.org/10.54614/AUAF.2022.1002421
AMA Olcabey Ergin G, Öztürk A, Görür G. Evaluation of Interactions Among Aphids, Endosymbionts, and Host Plants: A Foresight for the Future. Atatürk Üniversitesi Ziraat Fakültesi Dergisi. Mayıs 2022;53(2):133-139. doi:10.54614/AUAF.2022.1002421
Chicago Olcabey Ergin, Gülay, Ayten Öztürk, ve Gazi Görür. “Evaluation of Interactions Among Aphids, Endosymbionts, and Host Plants: A Foresight for the Future”. Atatürk Üniversitesi Ziraat Fakültesi Dergisi 53, sy. 2 (Mayıs 2022): 133-39. https://doi.org/10.54614/AUAF.2022.1002421.
EndNote Olcabey Ergin G, Öztürk A, Görür G (01 Mayıs 2022) Evaluation of Interactions Among Aphids, Endosymbionts, and Host Plants: A Foresight for the Future. Atatürk Üniversitesi Ziraat Fakültesi Dergisi 53 2 133–139.
IEEE G. Olcabey Ergin, A. Öztürk, ve G. Görür, “Evaluation of Interactions Among Aphids, Endosymbionts, and Host Plants: A Foresight for the Future”, Atatürk Üniversitesi Ziraat Fakültesi Dergisi, c. 53, sy. 2, ss. 133–139, 2022, doi: 10.54614/AUAF.2022.1002421.
ISNAD Olcabey Ergin, Gülay vd. “Evaluation of Interactions Among Aphids, Endosymbionts, and Host Plants: A Foresight for the Future”. Atatürk Üniversitesi Ziraat Fakültesi Dergisi 53/2 (Mayıs 2022), 133-139. https://doi.org/10.54614/AUAF.2022.1002421.
JAMA Olcabey Ergin G, Öztürk A, Görür G. Evaluation of Interactions Among Aphids, Endosymbionts, and Host Plants: A Foresight for the Future. Atatürk Üniversitesi Ziraat Fakültesi Dergisi. 2022;53:133–139.
MLA Olcabey Ergin, Gülay vd. “Evaluation of Interactions Among Aphids, Endosymbionts, and Host Plants: A Foresight for the Future”. Atatürk Üniversitesi Ziraat Fakültesi Dergisi, c. 53, sy. 2, 2022, ss. 133-9, doi:10.54614/AUAF.2022.1002421.
Vancouver Olcabey Ergin G, Öztürk A, Görür G. Evaluation of Interactions Among Aphids, Endosymbionts, and Host Plants: A Foresight for the Future. Atatürk Üniversitesi Ziraat Fakültesi Dergisi. 2022;53(2):133-9.

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