Wolbachia infection dynamics in a natural population of the pear psyllid Cacopsylla pyri (Hemiptera: Psylloidea) across its seasonal generations

. 2022 Oct 03 ; 12 (1) : 16502. [epub] 20221003

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid36192576
Odkazy

PubMed 36192576
PubMed Central PMC9529970
DOI 10.1038/s41598-022-20968-0
PII: 10.1038/s41598-022-20968-0
Knihovny.cz E-zdroje

Wolbachia is one of the most abundant intracellular symbionts of arthropods and has profound effects on host biology. Wolbachia transmission and host phenotypes often depend on its density within the host, which can be affected by multiple biotic and abiotic factors. However, very few studies measured Wolbachia density in natural host populations. Here, we describe Wolbachia in the pear psyllid Cacopsylla pyri from three populations in the Czech Republic. Using phylogenetic analyses based on wsp and multilocus sequence typing genes, we demonstrate that C. pyri harbours three new Wolbachia strains from supergroup B. A fourth Wolbachia strain from supergroup A was also detected in parasitised immatures of C. pyri, but likely came from a hymenopteran parasitoid. To obtain insights into natural Wolbachia infection dynamics, we quantified Wolbachia in psyllid individuals from the locality with the highest prevalence across an entire year, spanning several seasonal generations of the host. All tested females were infected and Wolbachia density remained stable across the entire period, suggesting a highly efficient vertical transmission and little influence from the environment and different host generations. In contrast, we observed a tendency towards reduced Wolbachia density in males which may suggest sex-related differences in Wolbachia-psyllid interactions.

Zobrazit více v PubMed

Weinert LA, Araujo-Jnr EV, Ahmed MZ, Welch JJ. The incidence of bacterial endosymbionts in terrestrial arthropods. Proc. R. Soc. B. 2015;282(1807):20150249. doi: 10.1098/rspb.2015.0249. PubMed DOI PMC

Lefoulon E, et al. Breakdown of coevolution between symbiotic bacteria Wolbachia and their filarial hosts. PeerJ. 2016;4:e1840. doi: 10.7717/peerj.1840. PubMed DOI PMC

Zug R, Hammerstein P. Still a host of hosts for Wolbachia: Analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS ONE. 2012;7(6):38544. doi: 10.1371/journal.pone.0038544. PubMed DOI PMC

Werren JH, Baldo L, Clark ME. Wolbachia: Master manipulators of invertebrate biology. Nat. Rev. Microbiol. 2008;6:741–751. doi: 10.1038/nrmicro1969. PubMed DOI

Engelstädter J, Hurst GDD. The ecology and evolution of microbes that manipulate host reproduction. Annu. Rev. Ecol. Evol. Syst. 2009;40:127–149. doi: 10.1146/annurev.ecolsys.110308.120206. DOI

Hurst GDD, Frost CL. Reproductive parasitism: Maternally inherited symbionts in a piparental world. Cold Spring Harb. Perspect. Biol. 2015;7(4):a017699. doi: 10.1101/cshperspect.a017699. PubMed DOI PMC

Bailly-Bechet M, et al. How long does Wolbachia remain on board? Molec. Biol. Evol. 2017;34:1183–1193. doi: 10.1093/molbev/msx073. PubMed DOI

Kaur R, et al. Living in the endosymbiotic world of Wolbachia: A centennial review. Cell Host Microbe. 2021;29:879–893. doi: 10.1016/j.chom.2021.03.006. PubMed DOI PMC

Timmermans MJTN, Ellers J. Wolbachia endosymbiont is essential for egg hatching in a parthenogenetic arthropod. Evol. Ecol. 2009;23:931–942. doi: 10.1007/s10682-008-9282-0. DOI

Hosokawa T, et al. Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc. Nation. Acad. Sci. USA. 2010;107:769–774. doi: 10.1073/pnas.0911476107. PubMed DOI PMC

Nikoh N, et al. Evolutionary origin of insect-Wolbachia nutritional mutualism. Proc. Nation. Acad. Sci. USA. 2014;111:10257–10262. doi: 10.1073/pnas.1409284111. PubMed DOI PMC

Balvín O, Roth S, Talbot B, Reinhardt K. Co-speciation in bedbug Wolbachia parallel the pattern in nematode hosts. Sci. Rep. 2018;8(1):1–9. doi: 10.1038/s41598-018-25545-y. PubMed DOI PMC

Manoj RRS, Latrofa MS, Epis S, Otranto D. Wolbachia: Endosymbiont of onchocercid nematodes and their vectors. Parasites Vectors. 2021;14(1):1–24. doi: 10.1186/s13071-021-04742-1. PubMed DOI PMC

Gerth M, Gansauge M-T, Weigert A, Bleidorn C. Phylogenomic analyses uncover origin and spread of the Wolbachia pandemic. Nat. Commun. 2014;5(1):1–7. doi: 10.1038/ncomms6117. PubMed DOI

Brown AMV, et al. Genomic evidence for plant-parasitic nematodes as the earliest Wolbachia hosts. Sci. Rep. 2016;6(1):1–14. doi: 10.1038/srep34955. PubMed DOI PMC

Kajtoch Ł, et al. Using host species traits to understand the Wolbachia infection distribution across terrestrial beetles. Sci. Rep. 2019;9(1):1–15. doi: 10.1038/s41598-018-38155-5. PubMed DOI PMC

Zimmermann BL, et al. Supergroup F Wolbachia in terrestrial isopods: Horizontal transmission from termites? Evol. Ecol. 2021;35:165–182. doi: 10.1007/s10682-021-10101-4. PubMed DOI PMC

Heath BD, Butcher RDJ, Whitfield WGF, Hubbard SF. Horizontal transfer of Wolbachia between phylogenetically distant insect species by a naturally occurring mechanism. Curr. Biol. 1999;9:313–316. doi: 10.1016/S0960-9822(99)80139-0. PubMed DOI

Vavre F, Fleury F, Lepetit D, Fouillet P, Bouletreau M. Phylogenetic evidence for horizontal transmission of Wolbachia in host- parasitoid associations. Mol. Biol. and Evol. 1999;16:1711–1723. doi: 10.1093/oxfordjournals.molbev.a026084. PubMed DOI

Jiggins FM, Bentley JK, Majerus MEN, Hurst GDD. Recent changes in phenotype and patterns of host specialization in Wolbachia bacteria. Mol. Ecol. 2002;11:1275–1283. doi: 10.1046/j.1365-294X.2002.01532.x. PubMed DOI

Schuler H, et al. Evidence for a recent horizontal transmission and spatial spread of Wolbachia from endemic Rhagoletis cerasi (Diptera: Tephritidae) to invasive Rhagoletis cingulata in Europe. Mol. Ecol. 2013;22:4101–4111. doi: 10.1111/mec.12362. PubMed DOI

Sanaei E, Charlat S, Engelstädter J. Wolbachia host shifts: Routes, mechanisms, constraints and evolutionary consequences. Biol. Rev. 2021;96:433–453. doi: 10.1111/brv.12663. PubMed DOI

Hoffmann AA, Ross PA, Rašić G. Wolbachia strains for disease control: Ecological and evolutionary considerations. Evol. Appl. 2015;8:751–768. doi: 10.1111/eva.12286. PubMed DOI PMC

Chu C-C, Gill TA, Hoffmann M, Pelz-Stelinski KS. Inter-population variability of endosymbiont densities in the Asian citrus psyllid (Diaphorina citri Kuwayama) Microb. Ecol. 2016;71:999–1007. doi: 10.1007/s00248-016-0733-9. PubMed DOI PMC

Nováková E, et al. Mosquito microbiome dynamics, a background for prevalence and seasonality of west nile virus. Front. Microbiol. 2017;8:526. doi: 10.3389/fmicb.2017.00526. PubMed DOI PMC

Krstić O, et al. Wolbachia infection in natural populations of dictyophara Europaea, an alternative vector of grapevine flavescence dorée phytoplasma: Effects and interactions: Effects of wolbachia on phytoplasma vector. Ann. Appl. Biol. 2018;172:47–64. doi: 10.1111/aab.12400. DOI

Gong J-T, et al. Stable introduction of plant-virus-inhibiting Wolbachia into planthoppers for rice protection. Curr. Biol. 2020;30:4837–4845. doi: 10.1016/j.cub.2020.09.033. PubMed DOI

Johnston KL, et al. Anti-Wolbachia drugs for filariasis. Trends. Parasit. 2021;37(12):1068–1081. doi: 10.1016/j.pt.2021.06.004. PubMed DOI

Brelsfoard CL, Dobson SL. Wolbachia-based strategies to control insect pests and disease vectors. Asia-Pac. J. Mol. Biol. Biotech. 2009;17:55–63.

Arora AK, Douglas AE. Hype or opportunity? Using microbial symbionts in novel strategies for insect pest control. J. Insect Phys. 2017;103:10–17. doi: 10.1016/j.jinsphys.2017.09.011. PubMed DOI

Landmann F. The Wolbachia Endosymbionts. Microbiol. Spectr. 2019;7(2):72. doi: 10.1128/microbiolspec.BAI-0018-2019. PubMed DOI PMC

McMeniman CJ, et al. Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science. 2009;323:141–144. doi: 10.1126/science.1165326. PubMed DOI

Bourtzis K, et al. Harnessing mosquito-Wolbachia symbiosis for vector and disease control. Acta Trop. 2014;132S:S150–S163. doi: 10.1016/j.actatropica.2013.11.004. PubMed DOI

Schmidt TL, et al. Local introduction and heterogeneous spatial spread of dengue-suppressing Wolbachia through an urban population of Aedes aegypti. PLoS Biol. 2017;15(5):2001894. doi: 10.1371/journal.pbio.2001894. PubMed DOI PMC

Fagen J, et al. Characterization of the relative abundance of the citrus pathogen Ca. Liberibacter Asiaticus in the microbiome of its insect vector, Diaphorina citri, using high throughput 16S rRNA sequencing. Open Microbiol. J. 2012;6:29–33. doi: 10.2174/1874285801206010029. PubMed DOI PMC

Kolora LD, Powell CM, Hunter W, Bextine B, Lauzon CR. Internal extracellular bacteria of diaphorina citri Kuwayama (hemiptera: Psyllidae), the Asian citrus psyllid. Curr. Microbiol. 2015;70:710–715. doi: 10.1007/s00284-015-0774-1. PubMed DOI

Hosseinzadeh S, et al. Distribution and variation of bacterial endosymbiont and “Candidatus Liberibacter asiaticus” titer in the huanglongbing insect vector Diaphorina citri Kuwayama. Microb. Ecol. 2019;78:206–222. doi: 10.1007/s00248-018-1290-1. PubMed DOI

Moussa A, et al. Bacterial microbiota associated with insect vectors of grapevine Bois noir disease in relation to phytoplasma infection. FEMS Microbiol. Ecol. 2020;96(11):fiaa203. doi: 10.1093/femsec/fiaa203. PubMed DOI

Bordenstein SR, O’Hara FP, Werren JH. Wolbachia-induced incompatibility precedes other hybrid incompatibilities in Nasonia. Nature. 2001;409:707–710. doi: 10.1038/35055543. PubMed DOI

Johnson K. The impact of Wolbachia on virus infection in mosquitoes. Viruses. 2015;7:5705–5717. doi: 10.3390/v7112903. PubMed DOI PMC

López-Madrigal S, Duarte EH. Titer regulation in arthropod-Wolbachia symbioses. FEMS Microbiol. Let. 2019;366(23):fnz232. doi: 10.1093/femsle/fnz232. PubMed DOI

Min K-T, Benzer S. Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc. Nation. Acad. Sci. 1997;94:10792–10796. doi: 10.1073/pnas.94.20.10792. PubMed DOI PMC

Chrostek E, et al. Wolbachia variants induce differential protection to viruses in Drosophila melanogaster: A phenotypic and phylogenomic analysis. PLoS Genet. 2013;9(12):e1003896. doi: 10.1371/journal.pgen.1003896. PubMed DOI PMC

Stacey DA, et al. Genotype and temperature influence pea aphid resistance to a fungal entomopathogen. Physiol. Entomol. 2003;28:75–81. doi: 10.1046/j.1365-3032.2003.00309.x. DOI

Thomas MB, Blanford S. Thermal biology in insect-parasite interactions. Trends in Ecol. Evol. 2003;18:344–350. doi: 10.1016/S0169-5347(03)00069-7. DOI

Jaenike J. Coupled population dynamics of endosymbionts within and between hosts. Oikos. 2009;118:353–362. doi: 10.1111/j.1600-0706.2008.17110.x. DOI

Versace E, Nolte V, Pandey RV, Tobler R, Schlötterer C. Experimental evolution reveals habitat-specific fitness dynamics among Wolbachia clades in Drosophila melanogaster. Mol. Ecol. 2014;23:802–814. doi: 10.1111/mec.12643. PubMed DOI PMC

Corbin C, Heyworth ER, Ferrari J, Hurst GDD. Heritable symbionts in a world of varying temperature. Heredity. 2017;118:10–20. doi: 10.1038/hdy.2016.71. PubMed DOI PMC

Berticat C, Rousset F, Raymond M, Berthomieu A, Weill M. High Wolbachia density in insecticide–resistant mosquitoes. Proc. R. Soc. Lond. B. 2002;269:1413–1416. doi: 10.1098/rspb.2002.2022. PubMed DOI PMC

Mouton L, Henri H, Bouletreau M, Vavre F. Strain-specific regulation of intracellular Wolbachia density in multiply infected insects. Mol. Ecol. 2003;12:3459–3465. doi: 10.1046/j.1365-294X.2003.02015.x. PubMed DOI

Mouton L, Henri H, Charif D, Boulétreau M, Vavre F. Interaction between host genotype and environmental conditions affects bacterial density in Wolbachia symbiosis. Biol. Lett. 2007;3:210–213. doi: 10.1098/rsbl.2006.0590. PubMed DOI PMC

Kondo N, Shimada M, Fukatsu T. Infection density of Wolbachia endosymbiont affected by co-infection and host genotype. Biol. Lett. 2005;1:488–491. doi: 10.1098/rsbl.2005.0340. PubMed DOI PMC

Duron O, et al. High Wolbachia density correlates with cost of infection for insecticide resistant Culex pipiens mosquitoe. Evol. 2006;60:303–314. doi: 10.1111/j.0014-3820.2006.tb01108.x. PubMed DOI

Dittmer J, et al. Host tissues as microhabitats for Wolbachia and quantitative insights into the bacterial community in terrestrial isopods. Mol. Ecol. 2014;23:2619–2635. doi: 10.1111/mec.12760. PubMed DOI

Mouton L, et al. Virulence, multiple Infections and regulation of symbiotic population in the Wolbachia-Asobara tabida symbiosis. Genetics. 2004;168:181–189. doi: 10.1534/genetics.104.026716. PubMed DOI PMC

Goto S, Anbutsu H, Fukatsu T. Asymmetrical interactions between Wolbachia and Spiroplasma endosymbionts coexisting in the same insect host. Appl. Environ. Microbiol. 2006;72:4805–4810. doi: 10.1128/AEM.00416-06. PubMed DOI PMC

Mousson L, et al. Wolbachia modulates Chikungunya replication in Aedes albopictus. Mol. Ecol. 2010;19:1953–1964. doi: 10.1111/j.1365-294X.2010.04606.x. PubMed DOI

Unckless RL, Boelio LM, Herren JK, Jaenike J. Wolbachia as populations within individual insects: Causes and consequences of density variation in natural populations. Proc. R. Soc. B. 2009;276:2805–2811. doi: 10.1098/rspb.2009.0287. PubMed DOI PMC

Tortosa P, et al. Wolbachia age-sex-specific density in Aedes albopictus: A host evolutionary response to cytoplasmic incompatibility? PLoS ONE. 2010;5:e9700. doi: 10.1371/journal.pone.0009700. PubMed DOI PMC

Moretti R, et al. Increased biting rate and decreased Wolbachia density in irradiated Aedes mosquitoes. Paras. Vectors. 2022;15(1):1–16. PubMed PMC

Duron O, Fort P, Weill M. Influence of aging on cytoplasmic incompatibility, sperm modification and Wolbachia density in Culex pipiens mosquitoes. Heredity. 2007;98:368–374. doi: 10.1038/sj.hdy.6800948. PubMed DOI

Shropshire JD, Hamant E, Cooper BS. Male age and Wolbachia dynamics: investigating how fast and why bacterial densities and cytoplasmic incompatibility strengths vary. MBio. 2021;12(6):e02998. doi: 10.1128/mbio.02998-21. PubMed DOI PMC

Zhao D-X, Zhang X-F, Chen D-S, Zhang Y-K, Hong X-Y. Wolbachia-host interactions: host mating patterns affect Wolbachia density dynamics. PLoS ONE. 2013;8(6):e66373. doi: 10.1371/journal.pone.0066373. PubMed DOI PMC

Mouton L, Henri H, Bouletreau M, Vavre F. Effect of temperature on Wolbachia density and impact on cytoplasmic incompatibility. Parasitology. 2006;132:49–56. doi: 10.1017/S0031182005008723. PubMed DOI

Lu W-N, Chiu M-C, Kuo M-H. Host life stage- and temperature-dependent density of the symbiont Buchnera aphidicola in a subtropical pea aphid (Acyrthosiphon pisum) population. J. Asia-Pac. Entomol. 2014;17:537–541. doi: 10.1016/j.aspen.2014.03.012. DOI

Perrot-Minnot M-J, Guo LR, Werren JH. Single and double infections with Wolbachia in the parasitic wasp Nasonia vitripennis effects on compatibility. Genetics. 1996;143:961–972. doi: 10.1093/genetics/143.2.961. PubMed DOI PMC

Van Opijnen T, Breeuwer JAJ. High temperatures eliminate Wolbachia, a cytoplasmic incompatibility inducing endosymbiont, from the two-spotted spider mite. Experim. Appl. Acarol. 1999;23:871–881. doi: 10.1023/A:1006363604916. PubMed DOI

Bordenstein SR, Bordenstein SR. Temperature affects the tripartite interactions between bacteriophage WO, Wolbachia, and cytoplasmic incompatibility. PLoS ONE. 2011;6(12):e29106. doi: 10.1371/journal.pone.0029106. PubMed DOI PMC

Jiang R-X, et al. The Influence of temperature and host gender on bacterial communities in the Asian citrus psyllid. Insects. 2021;12(12):1054. doi: 10.3390/insects12121054. PubMed DOI PMC

Hurst GDD, Jiggins FM, Robinson SJ. What causes ineffcient transmission of male-killing Wolbachia in Drosophila? Heredity. 2001;87:220–226. doi: 10.1046/j.1365-2540.2001.00917.x. PubMed DOI

Hague MTJ, et al. Temperature effects on cellular host-microbe interactions explain continent-wide endosymbiont prevalence. Curr. Biol. 2021;32(4):878–88. doi: 10.1016/j.cub.2021.11.065. PubMed DOI PMC

Sumi T, Miura K, Miyatake T. No seasonal trend in infection of the pale grass blue butterfly, Zizeeria maha (Lepidoptera: Lycaenidae), by Wolbachia. Appl. Entomol. Zool. 2013;48:35–38. doi: 10.1007/s13355-012-0152-4. DOI

Sumi T, Miura K, Miyatake T. Wolbachia density changes seasonally amongst populations of the pale grass blue butterfly, Zizeeria maha (Lepidoptera: Lycaenidae) PLoS ONE. 2017;12(4):e0175373. doi: 10.1371/journal.pone.0175373. PubMed DOI PMC

Cohen C, Toh E, Munro D, Dong Q, Hawlena H. Similarities and seasonal variations in bacterial communities from the blood of rodents and from their flea vectors. ISME J. 2015;9:1662–1676. doi: 10.1038/ismej.2014.255. PubMed DOI PMC

Kriesner P, Conner WR, Weeks AR, Turelli M, Hoffmann AA. Persistence of a Wolbachia infection frequency cline in Drosophila melanogaster and the possible role of reproductive dormancy. Evolution. 2016;70:979–997. doi: 10.1111/evo.12923. PubMed DOI PMC

Overholt WA, Diaz R, Rosskopf E, Green SJ, Overholt WA. Deep characterization of the microbiomes of Calophya spp. (Hemiptera: Calophyidae) gall-inducing psyllids reveals the absence of plant pathogenic bacteria and three dominant endosymbionts. PLoS ONE. 2015;10(7):e0132248. doi: 10.1371/journal.pone.0132248. PubMed DOI PMC

Morrow JL, Hall AAG, Riegler M. Symbionts in waiting: The dynamics of incipient endosymbiont complementation and replacement in minimal bacterial communities of psyllids. Microbiome. 2017;5(1):1–23. doi: 10.1186/s40168-017-0276-4. PubMed DOI PMC

Morrow JL, et al. Characterization of the bacterial communities of psyllids associated with Rutaceae in Bhutan by high throughput sequencing. BMC Microbiol. 2020;20(1):1–6. doi: 10.1186/s12866-020-01895-4. PubMed DOI PMC

Shapoval NA, Nokkala S, Nokkala C, Kuftina GN, Kuznetsova VG. The incidence of Wolbachia bacterial endosymbiont in bisexual and parthenogenetic populations of the psyllid genus Cacopsylla (Hemiptera, Psylloidea) Insects. 2021;12:853. doi: 10.3390/insects12100853. PubMed DOI PMC

Nakabachi A, Inoue H, Hirose Y. Microbiome analyses of 12 psyllid species of the family Psyllidae identified various bacteria including Fukatsuia and Serratia symbiotica, known as secondary symbionts of aphids. BMC Microbiol. 2022;22(1):1–21. doi: 10.1186/s12866-021-02429-2. PubMed DOI PMC

Kruse A, et al. Combining ’omics and microscopy to visualize interactions between the Asian citrus psyllid vector and the Huanglongbing pathogen Candidatus Liberibacter asiaticus in the insect gut. PLoS ONE. 2017;12(6):e0179531. doi: 10.1371/journal.pone.0179531. PubMed DOI PMC

Song X, et al. Composition and change in the microbiome of Diaphorina citri infected with Candidatus Liberibacter asiaticus in China. Int. J. Trop. Insect. Sci. 2019;39:283–290. doi: 10.1007/s42690-019-00036-3. DOI

Nachappa P, Levy J, Pierson E, Tamborindeguy C. Diversity of endosymbionts in the potato psyllid, Bactericera cockerelli (Hemiptera: Triozidae), vector of zebra chip disease of potato. Curr. Microbiol. 2011;62:1510–1520. doi: 10.1007/s00284-011-9885-5. PubMed DOI

Hail D, Dowd SE, Bextine B. Identification and location of symbionts associated with potato psyllid (Bactericera cockerelli) lifestages. Environ. Entomol. 2012;41:98–107. doi: 10.1603/EN11198. PubMed DOI

Cooper WR, et al. Wolbachia infection differs among divergent mitochondrial haplotypes of Bactericera cockerelli (Hemiptera: Triozidae) Ann. Entomol. Soc. Amer. 2015;108:137–145. doi: 10.1093/aesa/sau048. DOI

Fu Z, et al. Host plants and Wolbachia shape the population genetics of sympatric herbivore populations. Evol. Appl. 2020;13:2740–2753. doi: 10.1111/eva.13079. PubMed DOI PMC

Štarhová Serbina L, et al. Microbiome of pear psyllids: a tale about closely-related species sharing their endosymbionts. Environ. Microbiol. 2022 doi: 10.1111/1462-2920.16180. PubMed DOI PMC

Jarausch, B., Tedeschi, R., Sauvion, N., Gross, J. & Jarausch, W. Psyllid Vectors. In: Phytoplasmas: Plant Pathogenic Bacteria - II (eds. Bertaccini, A., Weintraub, P. G., Rao, G. P. & Mori, N.) 53–78 (Springer Singapore, 2019).

Lauterer P. Results of the investigations on Hemiptera in Moravia, made by the Moravian museum (Psylloidea 2) Acta Musei. Morav. Sci. biol. 1999;84:71–151.

Hodkinson ID. Life cycle variation and adaptation in jumping plant lice (Insecta: Hemiptera: Psylloidea): A global synthesis. J. Natur. Hist. 2009;43:65–179. doi: 10.1080/00222930802354167. DOI

Hague MTJ, Mavengere H, Matute DR, Cooper BS. Environmental and genetic contributions to imperfect wMel-like Wolbachia transmission and frequency variation. Genetics. 2020;215:1117–1132. doi: 10.1534/genetics.120.303330. PubMed DOI PMC

Brinker P, Fontaine MC, Beukeboom LW, Falcao Salles J. Host, symbionts, and the microbiome: the missing tripartite interaction. Trends Microbiol. 2019;27:480–488. doi: 10.1016/j.tim.2019.02.002. PubMed DOI

Sinkins SP, et al. Wolbachia variability and host effects on crossing type in Culex mosquitoes. Nature. 2005;436:257–260. doi: 10.1038/nature03629. PubMed DOI

Ant TH, Herd C, Louis F, Failloux AB, Sinkins SP. Wolbachia transinfections in Culex quinquefasciatus generate cytoplasmic incompatibility. Insect Mol. Biol. 2020;29:1–8. doi: 10.1111/imb.12604. PubMed DOI PMC

James AC, Ballard JWO. Expression of cytoplasmic incompatibility in Drosophila simulans and its impact on infection frequencies and distribution of Wolbachia pipientis. Evol. 2000;54:1661–1672. doi: 10.1111/j.0014-3820.2000.tb00710.x. PubMed DOI

Koehncke A, Telschow A, Werren JH, Hammerstein P. Life and death of an influential passenger: Wolbachia and the evolution of CI-modifiers by their hosts. PLoS ONE. 2009;4(2):e4425. doi: 10.1371/journal.pone.0004425. PubMed DOI PMC

Schuler H, et al. Diversity and distribution of Wolbachia in relation to geography, host plant affiliation and life cycle of a heterogonic gall wasp. BMC Evol. Biol. 2018;18(1):1–5. doi: 10.1186/s12862-018-1151-z. PubMed DOI PMC

Bakovic V, Schebeck M, Telschow A, Stauffer C, Schuler H. Spatial spread of Wolbachia in Rhagoletis cerasi populations. Biol. Lett. 2018;14(5):20180161. doi: 10.1098/rsbl.2018.0161. PubMed DOI PMC

Kriesner P, Hoffmann AA, Lee SF, Turelli M, Weeks AR. Rapid sequential spread of two Wolbachia variants in Drosophila simulans. PLoS Pathog. 2013;9(9):e1003607. doi: 10.1371/journal.ppat.1003607. PubMed DOI PMC

Wolfe TM, et al. Comparative genome sequencing reveals insights into the dynamics of Wolbachia in native and invasive cherry fruit flies. Mol. Ecol. 2021;30:6259–6272. doi: 10.1111/mec.15923. PubMed DOI PMC

Jerinić-Prodanović D, Mihajlović L, Stojanović A. Parasitoids of jumping plant-lice (Psylloidea, Hemiptera) from the family Encyrtidae (Hymenoptera, Chalcidoidea) in Serbia. Zootaxa. 2019;4577:29–50. doi: 10.11646/zootaxa.4577.1.2. PubMed DOI

Meyer JM, Hoy MA. Molecular survey of endosymbionts in Florida populations of Diaphorina citri (Hemiptera: Psyllidae) and its parasitoids Tamarixia radiata (Hymenoptera: Eulophidae) and Diaphorencyrtus aligarhensis (Hymenoptera: Encyrtidae) Flor. Entomol. 2008;91:294–304. doi: 10.1653/0015-4040(2008)91[294:MSOEIF]2.0.CO;2. DOI

Ashraf HJ, et al. Comparative microbiome analysis of Diaphorina citri and its associated parasitoids Tamarixia radiata and Diaphorencyrtus aligarhensis reveals Wolbachia as a dominant endosymbiont. Environ. Microbiol. 2022;24(3):1638–1652. doi: 10.1111/1462-2920.15948. PubMed DOI

Le Goff GJ, et al. Effect of the instar of the pear psyllid Cacopsylla pyri (Hemiptera: Psyllidae) on the behaviour and fitness of the parasitoid Trechnites insidiosus (Hymenoptera: Encyrtidae) Eur. J. Entomol. 2021;118:279–287. doi: 10.14411/eje.2021.028. DOI

Tougeron K, et al. Ecology and biology of the parasitoid Trechnites insidiosus and its potential for biological control of pear psyllids. Pest Manag. Sci. 2021;77(11):4836–47. doi: 10.1002/ps.6517. PubMed DOI

Dedeine F, Ahrens M, Calcaterra L, Shoemaker DD. Social parasitism in fire ants (Solenopsis spp.): A potential mechanism for interspecies transfer of Wolbachia. Mol. Ecol. 2005;14:1543–1548. doi: 10.1111/j.1365-294X.2005.02499.x. PubMed DOI

Gehrer L, Vorburger C. Parasitoids as vectors of facultative bacterial endosymbionts in aphids. Biol. Lett. 2012;8:613–615. doi: 10.1098/rsbl.2012.0144. PubMed DOI PMC

Mascarenhas RO, Prezotto LF, Perondini ALP, Marino CL, Selivon D. Wolbachia in guilds of Anastrepha fruit flies (Tephritidae) and parasitoid wasps (Braconidae) Genet. Mol. Biol. 2016;39:600–610. doi: 10.1590/1678-4685-gmb-2016-0075. PubMed DOI PMC

Ossiannilsson, F. The Psylloidea (Homoptera) of Fennoscandia and Denmark. (Brill, E.J., 1992).

Burckhardt, D. Psyllid-key of Cacopsylla on Rosaceae. https://www.dlr.rlp.de/Psylliden-english (2010).

Braig HR, Zhou W, Dobson SL, O’Neill SL. Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. J. Bacteriol. 1998;180:2373–2378. doi: 10.1128/JB.180.9.2373-2378.1998. PubMed DOI PMC

Baldo L, et al. Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Appl. Environ. Microbiol. 2006;72:7098–7110. doi: 10.1128/AEM.00731-06. PubMed DOI PMC

Zhou W, Rousset F, O’Neill S. Phylogeny and PCR–based classification of Wolbachia strains using wsp gene sequences. Proc. R. Soc. Lond. B. 1998;265:509–515. doi: 10.1098/rspb.1998.0324. PubMed DOI PMC

Jeffries CL, et al. Diverse novel resident Wolbachia strains in Culicine mosquitoes from Madagascar. Sci. Rep. 2018;8(1):1–5. doi: 10.1038/s41598-018-35658-z. PubMed DOI PMC

Zimmermann, B. L., Bouchon, D., Almerão, M. P. & Araujo, P. B. Wolbachia in Neotropical terrestrial isopods. FEMS Microbiol. Ecol.91, (2015). PubMed

Kawasaki Y, Schuler H, Stauffer C, Lakatos F, Kajimura H. Wolbachia endosymbionts in haplodiploid and diploid scolytine beetles (Coleoptera: Curculionidae: Scolytinae): Wolbachia infection in scolytine beetles. Environ. Microbiol. Rep. 2016;8:680–688. doi: 10.1111/1758-2229.12425. PubMed DOI

Schuler H, et al. Wolbachia in parasitoids attacking native European and introduced Eastern cherry fruit flies in Europe. Environ. Entomoll. 2016;45:1424–1431. doi: 10.1093/ee/nvw137. PubMed DOI

Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molec. Biol. and Evol. 2018;35:1547–1549. doi: 10.1093/molbev/msy096. PubMed DOI PMC

Jolley KA, Bray JE, Maiden MCJ. Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res. 2018;3:124. doi: 10.12688/wellcomeopenres.14826.1. PubMed DOI PMC

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J. Molec. Biol. 1990;215:403–410. doi: 10.1016/S0022-2836(05)80360-2. PubMed DOI

Katoh K, Rozewicki J, Yamada KD. MAFFT online service: Multiple sequence alignment, interactive sequence choice and visualization. Brief. Bioinform. 2019;20:1160–1166. doi: 10.1093/bib/bbx108. PubMed DOI PMC

Trifinopoulos J, Nguyen L-T, von Haeseler A, Minh BQ. W-IQ-TREE: A fast online phylogenetic tool for maximum likelihood analysis. Nucl. Acids Res. 2016;44:W232–W235. doi: 10.1093/nar/gkw256. PubMed DOI PMC

Ronquist F, et al. MrBayes 3.2: Efficient bayesian phylogenetic inference and model choice across a large model space. Syste. Biol. 2012;61:539–542. doi: 10.1093/sysbio/sys029. PubMed DOI PMC

Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: More models, new heuristics and parallel computing. Nat. Methods. 2012;9:772–772. doi: 10.1038/nmeth.2109. PubMed DOI PMC

Miller, M. A., Pfeiffer, W. & Schwartz, T. Creating the CIPRES science gateway for inference of large phylogenetic trees. In: 2010 Gateway Computing Environments Workshop (GCE) 1–8 (IEEE, 2010).

Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: An online tool for phylogenetic tree display and annotation. Nucl. Acids Res. 2021;49:293–296. doi: 10.1093/nar/gkab301. PubMed DOI PMC

Le Clec’h W, et al. High virulence of Wolbachia after host switching: when autophagy hurts. PLoS Pathog. 2012;8(8):e1002844. doi: 10.1371/journal.ppat.1002844. PubMed DOI PMC

Fox J, Weisberg S. An R companion to applied regression. 3. Sage; 2019.

de Mendiburu, F. & Yaseen, M. Agricolae: statistical procedures for agricultural research. R package version 1.4.0. (2020).

R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing (2021).

Wickham H. ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag; 2016.

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Seasonal wild dance of dual endosymbionts in the pear psyllid Cacopsylla pyricola (Hemiptera: Psylloidea)

. 2023 Sep 25 ; 13 (1) : 16038. [epub] 20230925

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...