Phylogenetics of Buchnera aphidicola Munson et al., 1991 (Enterobacteriales: Enterobacteriaceae) based on 16S rRNA amplified from seven aphid species

Year 2019, Volume: 43 Issue: 2, 227 - 237, 01.06.2019

Gül Satar

https://doi.org/10.16970/entoted.527118

Cited By: 1

Abstract

The obligate symbiont, Buchnera aphidicola Munson et al., 1991 (Enterobacteriales: Enterobacteriaceae) is important for the physiological processes of aphids. Buchnera aphidicola genes detected in seven aphid species, collected in 2017 from different plants and altitudes in Adana Province, Turkey were analyzed to reveal phylogenetic interactions between Buchnera and aphids. The 16S rRNA gene was amplified and sequenced for this purpose and a phylogenetic tree built up by the neighbor-joining method. A significant correlation between B. aphidicola genes and the aphid species was revealed by this phylogenetic tree and the haplotype network. Specimens collected in Feke from Solanum melongena L. was distinguished from the other B. aphidicola genes on Aphis gossypii Glover, 1877 (Hemiptera: Aphididae) with a high bootstrap value of 99. Buchnera aphidicola in Myzus spp. was differentiated from others, and the difference between Myzus cerasi (Fabricius, 1775) and Myzus persicae (Sulzer, 1776) was clear. Although, B. aphidicola is specific to its host aphid, certain nucleotide differences obtained within the species could enable specification to geographic region or host plant in the future.

Keywords

Aphid, genetic similarity, phylogenetics, symbiotic bacterium

Supporting Institution

This study was supported by Çukurova University, Turkey, Grant Project No: FBA-2017-8202

Project Number

This study was supported by Çukurova University, Turkey, Grant Project No: FBA-2017-8202

Thanks

The financial support of Çukurova University is gratefully acknowledged. The important contribution of Dr. Işıl Özdemir (Directorate of Plant Protection Central Research Institute, Republic of Turkey Ministry of Agriculture and Forestry, Ankara) for morphological identification of aphids is highly appreciated. The anonymous reviewers are thanked for their valuable advice and suggestions which greatly improved communication of the findings of this study.

Farklı yaprak biti türlerinden izole edilen Buchnera aphidicola Munson et al., 1991 (Enterobacteriales: Enterobacteriaceae)’nın 16S rRNA’ya göre filogenetiği

Abstract

Obligat simbiyont, Buchnera aphidicola Munson et al., 1991 (Enterobacteriales: Enterobacteriaceae), yaprak bitlerinin fizyolojik olaylarının sürdürülmesinde önemli bir rol oynar. Adana (Türkiye)’ dan 2017 yılında farklı bitki ve yüksekliklerden toplanan yedi yaprak biti türünde saptanan B. aphidicola genleri ile yaprakbiti türleri arasındaki filogenetik etkileşimi ortaya çıkarmak için analiz edilmiştir. Bu amaçla, 16S rRNA’nın gen bölgeleri kullanılmış ve filogenetik ağaç, neighbor-joining ile oluşturulmuştur. Buchrena aphidicola genleri ve aphid türleri arasında filogenetik ağaç ve haploid networke göre anlamlı bir korelasyon tespit edilmiştir. Solanum melongena L. toplanan Feke örneği, diğer Aphis gossypii Glover, 1877 (Hemiptera: Aphididae)’lerdeki B. aphidicola genlerinden çok yüksek bir boostrap değeri (99) ile ayrılmıştır. Myzus cinsindeki B. aphidicola genleri diğer cinslerden ayrı dallanmış ve Myzus cerasi (Fabricus, 1775) ve Myzus persicae Sulzer, 1776 arasındaki ayrım belirgindir. Buchera aphidicola konukçu yaprakbiti türüne özelleşmiş olsa da tür içinde elde edilen bazı nükleotid farklılıkları ilerde coğrafik bölgeye ya da bitkiye de özelleşmeye neden olabilir.

Keywords

Yaprak biti, genetik benzerlik, filogenetik, simbiyotik bakteri

Project Number

This study was supported by Çukurova University, Turkey, Grant Project No: FBA-2017-8202

References

• Akman Gündüz, E. & A. E. Douglas, 2009. Symbiotic bacteria enable insect to use a nutritionally inadequate diet. Proceedings of the Royal Society B: Biological Sciences, 276 (1658): 987-991.
• Anonymous, 2019a. Collection locations of aphid samples. (Web page: http://www.earth.google.com) (Date accessed: February 2019).
• Anonymous, 2019b. PopART (Population Analysis with Reticulate Trees). (Web page: http://www.popart.otago.ac.nz) (Date accessed: February 2019).
• Baldo l., J. C. Dunning Hotopp, K. A. Jolley, S. R. Bordensteîn, S. A. Biber, R. R. Choudhury, C. Hayashi, M. C. Maiden, H. Tet-Telin & J. H. Werren, 2006. Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Applied and Environmental Microbiology, 72: 7098-7110.
• Bandelt H.-J., P. Forster & A. Röhl, 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution; 16: 37-48.
• Baumann, P., L. Baumann, C. Y. Lai, D. Rouhbakhsh, N. A. Moran & M. A. Clark, 1995. Genetics, physiology, and evolutionary relationships of the genus Buchnera: intracellular symbionts of aphids. Annual Review of Microbiology, 49: 55-94.
• Baumann, P., N. A. Moran & L. Baumann, 1997. The evolution and genetics of aphid endosymbionts. Bioscience, 47: 12-20.
• Betsiashvili, M., K. R. Ahern & G. Jander, 2014. Additive effects of two quantitative trait loci that confer Rhopalosiphum maidis (corn leaf aphid) resistance in maize inbred line Mo17. Journal of Experimental Botany, 66 (2): 571-578.
• Blackman, R. L. & V. F. Eastop, 2000. Aphids on the World’s Crops. An Identification and Information Guide. 2nd Ed. JohnWiley & Sons, Chichester, England, 414 pp.
• Blackman, R. L. & V. F. Eastop, 2019. Aphids of the World’s Plants: An Online Identification and Information Guide. (Web page: www.aphidsonworldsplants.info) (Date accessed: 4 April 2019).
• Brady, C. M., & J. A. White, 2013. Cowpea aphid (Aphis craccivora) associated with different host plants has different facultative endosymbionts. Ecological Entomology, 38 (4): 433-437.
• Buchner, P., 1912. Studien an intracellularen Symbioten. 1. Die intracellularen Symbionten der Hemipteren. Archiv für Protistenkunde. 26: 1-116.
• Çalışkan, A., M. R. Ulusoy & I. Özdemir, 2012. New record of invasive aphid: Myzocallis walshii (Monell, 1879) (Hemiptera: Aphidoidea) in Turkey. Türkiye Entomoloji Bülteni, 2 (4): 277-284.
• Chen, C. Y., C. Y. Lai & M. H. Kuo, 2009. Temperature effect on the growth of Buchnera endosymbiont in Aphis craccivora (Hemiptera: Aphididae). Symbiosis, 49: 53-59.
• Chong, R. A. & N. A. Moran, 2016. Intraspecific genetic variation in hosts affects regulation of obligate heritable symbionts. Proceedings of the National Academy of Sciences of the United States of America, 113: 13114-13119.
• Douglas, A. E., 1998. Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annual Review of Entomology, 43: 17-37.
• Douglas, A. E., 2003. The nutritional physiology of aphids. Advances in Insect Physiology, 31: 73-140.
• FinchTV, 2019. FinchTV v1.4.0. (Web page: http://www.geospiza.com/Products/finchtvdlrequest.shtml) (Date accessed: February 2019).
• Fukatsu, T., 2001. Secondary intracellular symbiotic bacteria in Aphids of the genus Yamatocallis (Homoptera: Aphididae: Drepanosiphinae). Applied Environmental Microbiology, 67: 5315-5320.
• Funk, D. J., L. Helbling, J. J. Wernegreen & N. A. Moran, 2000. Intraspecific phylogenetic congruence among multiple symbiont genomes. Proceedings of the Royal Society B: Biological Sciences, 267: 2517-2521.
• Görür, G., O. Senol, G. Geizici, H. Akyıldırım Begen & D. Parmaksız, 2017. New aphid (Hemiptera: Aphidoidea) records from south eastern parts of Turkey. Journal of Insect Biodiversity and Systematics, 3 (3): 257-264.
• Güz, N., A. Dağeri & S. Aksoy, 2015. The impacts of endosymbiotic bacteria on insects. Türkiye Entomoloji Bülteni, 5: 101-113.
• Holman, J., 2009. Host plant catalog of aphids. Springer, 1206: 53-141.
• Jousselin, E., Y. Desdevises & A. Coeur d’acier, 2009. Fine-scale cospeciation between Brachycaudus and Buchnera aphidicola: bacterial genome helps define species and evolutionary relationships in aphids. Proceedings of the Royal Society B: Biological Sciences, 276: 187-196.
• Kimura, M., 1980. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16: 111-120.
• Kök, Ş., İ. Kasap, & I. Özdemir, 2016. Aphid (Hemiptera: Aphididae) species determined in Çanakkale Province with a new record for the aphid fauna of Turkey. Turkish Journal of Entomology, 40 (4): 397-412.
• Kozo-Polyansky, B. P. & V. Fet, 2010. Symbiogenesis: A New Principle of Evolution. Harvard University Press, Cambridge, MA, USA, 198 pp.
• Lagos, D. M., D. J. Voegtlin, A. Coeur d’acier & R. Giordano, 2014. Aphis (Hemiptera: Aphididae) species groups found in the Midwestern United States and their contribution to the phylogenetic knowledge of the genus. Insect Science, 21: 374-391.
• Librado, P. & J. Rozas, 2009. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25: 1451-1452.
• Liu, L., X. Huang, Y. Wang, & G. Qiao, 2014. Revisiting the first case of insect-bacteria cospeciation: phylogenetic incongruence between aphids and their obligate endosymbiont at subfamily level. PeerJ PrePrints, 2: e346v1.
• Liu, L., X. Huang, R. Zhang, L. Jiang & G. Qiao, 2013. Phylogenetic congruence between Mollitrichosiphum (Aphididae: Greenideinae) and Buchnera indicates insect-bacteria parallel evolution. Systematic Entomology, 38: 81-92.
• Martine, A. J., S. R. Weldon & K. M. Oliver, 2013. Effects of parasitism on aphid nutritional and protective symbioses. Molecular Ecology, 23 (6): 1594-1607.
• Mereschkowsky, C., 1909.The theory of the two plasms as the foundation of symbiogenesis. A new concept of the origin of organisms. Proceedings Studies of the Imperial Kazan University, 12: 1-102.
• Moran, N. A., J. A. Russell, R. Koga & T. Fukatsu, 2005. Evolutionary relationships of three new species of Enterobacteriaceae living as symbionts of aphids and other insects. Applied Environmental Microbiology, 2005 (71): 3302-3310.
• Munson, M. A., P. Baumann, M. A. Clark, L. Baumann, N. A. Moran, D. J. Voegtlin & B. C. Campbell, 1991. Aphid-eubacterial endosymbiosis: evidence for its establishment in an ancestor of four aphid families. Journal of Bacteriology, 173: 6321-6324.
• Nei, M. & S. Kumar, 2000. Molecular Evolution and Phylogenetics. Oxford University Press, New York, NY, USA. 348 pp.
• Nikoh, N., J. P. McCutcheon, T. Kudo, S. Y. Miyagishima, N. A. Moran, & A. Nakabachi. 2010. Bacterial genes in the aphid genome: Absence of functional gene transfer from Buchnera to its host. PLoS Genetics, 6: 18-21.
• Nováková, E., V. Hypša, J. Klein, R. G. Foottit, C. D., von Dohlen, & N. A. Moran, 2013. Reconstructing the phylogeny of aphids (Hemiptera: Aphididae) using DNA of the obligate symbiont Buchnera aphidicola. Molecular Phylogenetics and Evolution, 68 (1): 42-54.
• Pan, H. P., D. Chu, B. M Liu, W. Xie, S. L. Wang, Q. J. Wu, B. Y. Xu & Y. J. Zhang, 2013. Relative amount of symbionts in insect hosts changes with host-plant adaptation and insecticide resistance. Environmental Entomology, 42 (1): 74-78.
• Peccoud, J., J. Bonhomme, F. Mahéo, M. de la Huerta, O. Cosson & J. C. Simon, 2014. Inheritance patterns of secondary symbionts during sexual reproduction of pea aphid biotypes. Insect Science, 21 (3): 291-300.
• Qi, J., S. ul Malook, G. Shen, L. Gao, C. Zhang, J. Li, J. Zhang, L. Wang & J. Wu, 2018. Current understanding of maize and rice defense against insect herbivores. Plant diversity, 40: 189-195.
• Russell, J. A. & N. A. Moran, 2006. Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proceedings of the Royal Society Biological Science, 273: 603-10.
• Satar, S., U. Kersting & R. Yokomi, 2013. Presence of two host races of Aphis gossypii Glover (Hemiptera: Aphididae) collected in Turkey. Annals of Applied Biology, 162 (1): 41-49.
• Schobert, C., L. Baker, J. Szederkényi, P. Großmann, E. Komor, H. Hayashi, M. Chino & W. J. Lucas, 1998. Identification of immunologically related proteins in sieve-tube exudate collected from monocotyledonous and dicotyledonous plants. Planta, 206 (2): 245-252.
• Shigenobu, S., H. Watanabe, M. Hattori, Y. Sakaki & H. Ishikawa. 2000. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature. 407: 81-86.
• Simon, J.-C., S. Boutin, T. Tsuchida, R. Koga, J.-F Le Gallic, A. Frantz & T. Fukatsu, 2011. Facultative symbiont infections affect aphid reproduction. PloS One, 6 (7): 1-10.
• Tamura, K., G. Stecher, D. Peterson, A. Filipski & S. Kumar, 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution, 30: 2725-2729.
• Telesnicki, M. C., C. M. Ghersa, M. A., Martínez-Ghersa & J. D. Arneodo, 2012. Molecular identification of the secondary endosymbiont Hamiltonella defensa in the rose-grain aphid Metopolophium dirhodum. Revista Argentina de Microbiología, 44 (4): 255-258.
• Tsuchida, T., R. Koga, M. Horikawa, T. Tsunoda, T. Maoka, S. Matsumoto, J. C. Simon & T. Fukatsu, 2010. Symbiotic bacterium modifies aphid body color. Science, 330 (6007): 1102-1104.
• Uygun N., S. Toros, R. Ulusoy, S. Satar & I. Özdemir, 2001. Doğu Akdeniz Bölgesi Aphidoidea (Homoptera) Türleri ile Bunların Parazitoit ve Predatörlerinin Saptanması. Türkiye Bilimsel ve Teknik Araştırma Kurumu, Tarım ve Orman Araştırma Grubu Proje No: TÜBİTAK- TOGTAG 1720, 214s.
• van Ham, R. J., A. Moya, & A. Latorre, 1997. Putative evolutionary origin of plasmids carrying the genes involved in leucine bio-synthesis in Buchnera aphidicola (endosymbiont of aphids). Journal of Bacteriology, 179: 4768-4777.
• Vorburger, C., L. Gehrer & P. A. Rodriguez, 2010. A strain of the bacterial symbiont Regiella insecticola protects aphids against parasitoids. Biology Letters, 6 (1): 109-111.