{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,13]],"date-time":"2026-10-13T14:07:34Z","timestamp":1791900454130,"version":"4.3.4"},"reference-count":92,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,3,22]],"date-time":"2023-03-22T00:00:00Z","timestamp":1679443200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004281","name":"Narodowe Centrum Nauki","doi-asserted-by":"publisher","award":["2017\/26\/D\/NZ8\/00799"],"award-info":[{"award-number":["2017\/26\/D\/NZ8\/00799"]}],"id":[{"id":"10.13039\/501100004281","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004281","name":"Narodowe Centrum Nauki","doi-asserted-by":"publisher","award":["2018\/30\/E\/NZ8\/00880"],"award-info":[{"award-number":["2018\/30\/E\/NZ8\/00880"]}],"id":[{"id":"10.13039\/501100004281","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100014434","name":"Narodowa Agencja Wymiany Akademickiej","doi-asserted-by":"publisher","award":["2017\/26\/D\/NZ8\/00799"],"award-info":[{"award-number":["2017\/26\/D\/NZ8\/00799"]}],"id":[{"id":"10.13039\/501100014434","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Physiol."],"abstract":"<jats:p>Sap-feeding hemipteran insects live in associations with diverse heritable symbiotic microorganisms (bacteria and fungi) that provide essential nutrients deficient in their hosts\u2019 diets. These symbionts typically reside in highly specialized organs called bacteriomes (with bacterial symbionts) or mycetomes (with fungal symbionts). The organization of these organs varies between insect clades that are ancestrally associated with different microbes. As these symbioses evolve and additional microorganisms complement or replace the ancient associates, the organization of the symbiont-containing tissue becomes even more variable. Planthoppers (Hemiptera: Fulgoromorpha) are ancestrally associated with bacterial symbionts <jats:italic>Sulcia<\/jats:italic> and <jats:italic>Vidania<\/jats:italic>, but in many of the planthopper lineages, these symbionts are now accompanied or have been replaced by other heritable bacteria (e.g., <jats:italic>Sodalis<\/jats:italic>, <jats:italic>Arsenophonus<\/jats:italic>, <jats:italic>Purcelliella<\/jats:italic>) or fungi. We know the identity of many of these microbes, but the symbiont distribution within the host tissues and the bacteriome organization have not been systematically studied using modern microscopy techniques. Here, we combine light, fluorescence, and transmission electron microscopy with phylogenomic data to compare symbiont tissue distributions and the bacteriome organization across planthoppers representing 15 families. We identify and describe seven primary types of symbiont localization and seven types of the organization of the bacteriome. We show that <jats:italic>Sulcia<\/jats:italic> and <jats:italic>Vidania<\/jats:italic>, when present, usually occupy distinct bacteriomes distributed within the body cavity. The more recently acquired gammaproteobacterial and fungal symbionts generally occupy separate groups of cells organized into distinct bacteriomes or mycetomes, distinct from those with <jats:italic>Sulcia<\/jats:italic> and <jats:italic>Vidania<\/jats:italic>. They can also be localized in the cytoplasm of fat body cells. Alphaproteobacterial symbionts colonize a wider range of host body habitats: <jats:italic>Asaia<\/jats:italic>-like symbionts often colonize the host gut lumen, whereas <jats:italic>Wolbachia<\/jats:italic> and <jats:italic>Rickettsia<\/jats:italic> are usually scattered across insect tissues and cell types, including cells containing other symbionts, bacteriome sheath, fat body cells, gut epithelium, as well as hemolymph. However, there are exceptions, including <jats:italic>Gammaproteobacteria<\/jats:italic> that share bacteriome with <jats:italic>Vidania<\/jats:italic>, or <jats:italic>Alphaproteobacteria<\/jats:italic> that colonize <jats:italic>Sulcia<\/jats:italic> cells. We discuss how planthopper symbiont localization correlates with their acquisition and replacement patterns and the symbionts\u2019 likely functions. We also discuss the evolutionary consequences, constraints, and significance of these findings.<\/jats:p>","DOI":"10.3389\/fphys.2023.1135346","type":"journal-article","created":{"date-parts":[[2023,3,22]],"date-time":"2023-03-22T05:50:54Z","timestamp":1679464254000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":40,"title":["Variable organization of symbiont-containing tissue across planthoppers hosting different heritable endosymbionts"],"prefix":"10.3389","volume":"14","author":[{"given":"Anna","family":"Michalik","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Diego Castillo","family":"Franco","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Junchen","family":"Deng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Teresa","family":"Szklarzewicz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adam","family":"Stroi\u0144ski","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Micha\u0142","family":"Kobia\u0142ka","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Piotr","family":"\u0141ukasik","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2023,3,22]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"118","DOI":"10.1186\/s12862-016-0660-x","article-title":"Evidence for common horizontal transmission of Wolbachia among butterflies and moths","volume":"16","author":"Ahmed","year":"2016","journal-title":"BMC Evol. Biol."},{"key":"B2","doi-asserted-by":"publisher","first-page":"310","DOI":"10.1016\/j.jip.2007.09.009","article-title":"Ultrastructural detection of an unusual intranuclear bacterium in Pentastiridius leporinus (Hemiptera: Cixiidae)","volume":"97","author":"Arneodo","year":"2008","journal-title":"J. Invertebr. Pathol."},{"key":"B3","doi-asserted-by":"publisher","first-page":"1236","DOI":"10.1016\/j.jinsphys.2008.06.008","article-title":"Analysis of milk gland structure and function in Glossina morsitans: Milk protein production, symbiont populations and fecundity","volume":"54","author":"Attardo","year":"2008","journal-title":"J. Insect Physiol."},{"key":"B4","doi-asserted-by":"publisher","first-page":"7144","DOI":"10.1038\/s41598-020-64163-5","article-title":"Role of plants in the transmission of Asaia sp., which potentially inhibit the Plasmodium sporogenic cycle in Anopheles mosquitoes","volume":"10","author":"Bassene","year":"2020","journal-title":"Sci. Rep."},{"key":"B5","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1146\/annurev.micro.59.030804.121041","article-title":"Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects","volume":"59","author":"Baumann","year":"2005","journal-title":"Annu. Rev. Microbiol."},{"key":"B6","doi-asserted-by":"publisher","first-page":"4461","DOI":"10.1111\/1462-2920.14367","article-title":"Comparative genomics of a quadripartite symbiosis in a planthopper host reveals the origins and rearranged nutritional responsibilities of anciently diverged bacterial lineages","volume":"20","author":"Bennett","year":"2018","journal-title":"Environ. Microbiol."},{"key":"B7","doi-asserted-by":"publisher","first-page":"1675","DOI":"10.1093\/gbe\/evt118","article-title":"Small, smaller, smallest: The origins and evolution of ancient dual symbioses in a phloem-feeding insect","volume":"5","author":"Bennett","year":"2013","journal-title":"Genome Biol. Evol."},{"key":"B8","volume-title":"FLOW (Fulgoromorpha Lists on The Web): A world knowledge base dedicated to Fulgoromorpha (Insecta: Hemiptera: Fulgoromorpha). Paris. Version 8","author":"Bourgoin","year":"2022"},{"key":"B9","doi-asserted-by":"publisher","first-page":"499","DOI":"10.1111\/1758-2229.12051","article-title":"Localization and morphological variation of three bacteriome-inhabiting symbionts within a planthopper of the genus Oliarus (Hemiptera: Cixiidae)","volume":"5","author":"Bressan","year":"2013","journal-title":"Environ. Microbiol. Rep."},{"key":"B10","doi-asserted-by":"publisher","first-page":"218","DOI":"10.1038\/nrmicro2262","article-title":"A complex journey: Transmission of microbial symbionts","volume":"8","author":"Bright","year":"2010","journal-title":"Nat. Rev. Microbiol."},{"key":"B11","doi-asserted-by":"publisher","first-page":"703","DOI":"10.1016\/j.cell.2019.08.054","article-title":"Peptidoglycan production by an insect-bacterial mosaic","volume":"179","author":"Bublitz","year":"2019","journal-title":"Cell"},{"key":"B12","volume-title":"Endosymbiosis of animals with plant microorganisms","author":"Buchner","year":"1965"},{"key":"B13","doi-asserted-by":"publisher","first-page":"9077","DOI":"10.1093\/nar\/gkab688","article-title":"tRNAscan-SE 2.0: improved detection and functional classification of transfer RNA genes","volume":"49","author":"Chan","year":"2021","journal-title":"Nucleic Acids Res."},{"key":"B14","doi-asserted-by":"publisher","first-page":"997","DOI":"10.1093\/sysbio\/syw037","article-title":"Terrace-aware data structure for phylogenomic inference from supermatrices","volume":"65","author":"Chernomor","year":"2016","journal-title":"Syst. Biol."},{"key":"B15","doi-asserted-by":"publisher","first-page":"692024","DOI":"10.3389\/fpls.2021.692024","article-title":"Diversity of plastid types and their interconversions","volume":"12","author":"Choi","year":"2021","journal-title":"Front. Plant Sci."},{"key":"B16","doi-asserted-by":"publisher","first-page":"519479","DOI":"10.1101\/2022.12.07.519479","article-title":"Genome comparison reveals inversions and alternative evolutionary history of nutritional endosymbionts in planthoppers (Hemiptera: Fulgoromorpha)","volume":"2022","author":"Deng","year":"2022","journal-title":"BioRxiv"},{"key":"B17","doi-asserted-by":"publisher","first-page":"731","DOI":"10.1038\/nrmicro.2016.151","article-title":"How multi-partner endosymbioses function","volume":"14","author":"Douglas","year":"2016","journal-title":"Nat. Rev. Microbiol."},{"key":"B18","volume-title":"Insects and their beneficial microbes","author":"Douglas","year":"2022"},{"key":"B19","doi-asserted-by":"publisher","first-page":"10021955","DOI":"10.1371\/journal.pcbi.1002195","article-title":"Accelerated profile HMM searches","volume":"7","author":"Eddy","year":"2011","journal-title":"PLOS Comput. Biol."},{"key":"B96","doi-asserted-by":"publisher","first-page":"2460","DOI":"10.1093\/bioinformatics\/btq461","article-title":"Search and clustering orders of magnitude faster than BLAST","volume":"26","author":"Edgar","year":"2010","journal-title":"Bioinformatics"},{"key":"B97","doi-asserted-by":"publisher","first-page":"2194","DOI":"10.1093\/bioinformatics\/btr381","article-title":"UCHIME improves sensitivity and speed of chimera detection","volume":"27","author":"Edgar","year":"2011","journal-title":"Bioinformatics"},{"key":"B21","doi-asserted-by":"publisher","first-page":"629","DOI":"10.1016\/j.chom.2017.04.003","article-title":"Quorum sensing attenuates virulence in Sodalis praecaptivus","volume":"21","author":"Enomoto","year":"2017","journal-title":"Cell Host Microbe"},{"key":"B22","doi-asserted-by":"publisher","first-page":"2623","DOI":"10.1093\/gbe\/evv169","article-title":"Genomic analysis of an Ascomycete fungus from the rice planthopper reveals how it adapts to an endosymbiotic lifestyle","volume":"7","author":"Fan","year":"2015","journal-title":"Genome Biol. Evol."},{"key":"B23","doi-asserted-by":"publisher","first-page":"9047","DOI":"10.1073\/pnas.0610451104","article-title":"Bacteria of the genus Asaia stably associate with Anopheles stephensi, an Asian malarial mosquito vector","volume":"104","author":"Favia","year":"2007","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B24","doi-asserted-by":"publisher","first-page":"533","DOI":"10.1111\/j.1365-2311.2011.01318.x","article-title":"Bacterial symbionts as mediators of ecologically important traits of insect hosts","volume":"36","author":"Feldhaar","year":"2011","journal-title":"Ecol. Entomol."},{"key":"B25","doi-asserted-by":"publisher","first-page":"904","DOI":"10.1039\/C5NP00010F","article-title":"Defensive symbioses of animals with prokaryotic and eukaryotic microorganisms","volume":"32","author":"Fl\u00f3rez","year":"2015","journal-title":"Nat. Prod. Rep."},{"key":"B26","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1016\/bs.aiip.2020.04.002","article-title":"Microbial symbionts of herbivorous species across the insect tree","volume-title":"Mechanisms underlying microbial symbiosis","author":"Frago","year":"2020"},{"key":"B27","doi-asserted-by":"publisher","first-page":"765","DOI":"10.1016\/0022-1910(92)90029-D","article-title":"A novel eukaryotic extracellular symbiont in an aphid, Astegopteryx styraci (Homoptera, Aphididae, Hormaphidinae)","volume":"38","author":"Fukatsu","year":"1992","journal-title":"J. Insect. Physiol."},{"key":"B28","doi-asserted-by":"publisher","first-page":"evab123","DOI":"10.1093\/gbe\/evab123","article-title":"The evolution of interdependence in a four-way mealybug symbiosis","volume":"13","author":"Garber","year":"2021","journal-title":"Genome Biol. Evol."},{"key":"B29","doi-asserted-by":"publisher","first-page":"2591","DOI":"10.1096\/fj.07-101162","article-title":"Inherited intracellular ecosystem: Symbiotic bacteria share bacteriocytes in whiteflies","volume":"22","author":"Gottlieb","year":"2008","journal-title":"FASEB J."},{"key":"B30","doi-asserted-by":"publisher","first-page":"e00920","DOI":"10.1128\/mSystems.00920-20","article-title":"phyloFlash: Rapid small-subunit rRNA profiling and targeted assembly from metagenomes","volume":"5","author":"Gruber-Vodicka","year":"2020","journal-title":"mSystems"},{"key":"B33","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1007\/s13199-010-0065-3","article-title":"Bacterial symbionts in insects: Balancing life and death","volume":"51","author":"Harris","year":"2010","journal-title":"Symbiosis"},{"key":"B34","doi-asserted-by":"publisher","first-page":"313","DOI":"10.1016\/S0960-9822(99)80139-0","article-title":"Horizontal transfer of Wolbachia between phylogenetically distant insect species by a naturally occurring mechanism","volume":"9","author":"Heath","year":"1999","journal-title":"Curr. Biol."},{"key":"B35","doi-asserted-by":"publisher","first-page":"6814","DOI":"10.1073\/pnas.96.12.6814","article-title":"Four intracellular genomes direct weevil biology: Nuclear, mitochondrial, principal endosymbiont, and Wolbachia","volume":"96","author":"Heddi","year":"1999","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B36","doi-asserted-by":"publisher","first-page":"588841","DOI":"10.3389\/fmicb.2020.588841","article-title":"Bacteriome-associated endosymbiotic bacteria of Nosodendron tree sap beetles (Coleoptera: Nosodendridae)","volume":"11","author":"Hirota","year":"2020","journal-title":"Front. Microbiol."},{"key":"B37","doi-asserted-by":"publisher","first-page":"769","DOI":"10.1073\/pnas.0911476107","article-title":"Wolbachia as a bacteriocyte-associated nutritional mutualist","volume":"107","author":"Hosokawa","year":"2010","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B38","doi-asserted-by":"publisher","first-page":"119","DOI":"10.2307\/3496671","article-title":"The larval habitat of Cedusa inflata (Hemiptera: Auchenorrhyncha: Derbidae) and its relationship with adult distribution on palms","volume":"84","author":"Howard","year":"2001","journal-title":"Fla. Entomol."},{"key":"B39","doi-asserted-by":"publisher","first-page":"029577","DOI":"10.1128\/AEM.02957-19","article-title":"Transovarial transmission of bacteriome-associated symbionts in the cicada Pycna repanda (Hemiptera: Cicadidae)","volume":"86","author":"Huang","year":"2020","journal-title":"Appl. Environ. Microbiol."},{"key":"B40","doi-asserted-by":"publisher","first-page":"2434","DOI":"10.3390\/ijms24032434","article-title":"A study on symbiotic systems of cicadas provides new insights into distribution of microbial symbionts and improves fluorescence in situ hybridization technique","volume":"24","author":"Huang","year":"2023","journal-title":"Int. J. Mol. Sci."},{"key":"B41","doi-asserted-by":"publisher","first-page":"E5416","DOI":"10.1073\/pnas.1603910113","article-title":"Repeated replacement of an intrabacterial symbiont in the tripartite nested mealybug symbiosis","volume":"113","author":"Husnik","year":"2016","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B43","doi-asserted-by":"publisher","first-page":"587","DOI":"10.1038\/nmeth.4285","article-title":"ModelFinder: Fast model selection for accurate phylogenetic estimates","volume":"14","author":"Kalyaanamoorthy","year":"2017","journal-title":"Nat. Methods"},{"key":"B44","doi-asserted-by":"publisher","first-page":"268","DOI":"10.1016\/j.asd.2018.03.005","article-title":"Diversity of symbiotic microbiota in Deltocephalinae leafhoppers (Insecta, Hemiptera, Cicadellidae)","volume":"47","author":"Kobia\u0142ka","year":"2018","journal-title":"Arthropod Struct. Dev."},{"key":"B45","doi-asserted-by":"publisher","first-page":"903","DOI":"10.1007\/s00709-015-0854-x","article-title":"Sulcia symbiont of the leafhopper Macrosteles laevis (Ribaut, 1927) (Insecta, Hemiptera, Cicadellidae: Deltocephalinae) harbors Arsenophonus bacteria","volume":"253","author":"Kobia\u0142ka","year":"2016","journal-title":"Protoplasma"},{"key":"B46","doi-asserted-by":"publisher","first-page":"2073","DOI":"10.1111\/1462-2920.12121","article-title":"Evolutionary replacement of obligate symbionts in an ancient and diverse insect lineage","volume":"15","author":"Koga","year":"2013","journal-title":"Environ. Microbiol."},{"key":"B47","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1007\/978-3-642-30197-1_396","article-title":"The family Acetobacteraceae","volume-title":"The Prokaryotes: Alphaproteobacteria and Betaproteobacteria","author":"Komagata","year":"2014"},{"key":"B48","doi-asserted-by":"publisher","first-page":"290","DOI":"10.3390\/life12020290","article-title":"Of cockroaches and symbionts: Recent advances in the characterization of the relationship between Blattella germanica and its dual symbiotic system","volume":"12","author":"Latorre","year":"2022","journal-title":"Life"},{"key":"B49","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1016\/j.ymeth.2016.02.020","article-title":"Megahit v1.0: A fast and scalable metagenome assembler driven by advanced methodologies and community practices","volume":"102","author":"Li","year":"2016","journal-title":"Methods"},{"key":"B50","doi-asserted-by":"publisher","first-page":"247","DOI":"10.1093\/jhered\/esy068","article-title":"One hundred mitochondrial genomes of cicadas","volume":"110","author":"\u0141ukasik","year":"2019","journal-title":"J. Hered."},{"key":"B51","doi-asserted-by":"publisher","first-page":"E226","DOI":"10.1073\/pnas.1712321115","article-title":"Multiple origins of interdependent endosymbiotic complexes in a genus of cicadas","volume":"115","author":"\u0141ukasik","year":"2018","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B52","doi-asserted-by":"publisher","first-page":"E11691","DOI":"10.1073\/pnas.1811932115","article-title":"Evolution of host support for two ancient bacterial symbionts with differentially degraded genomes in a leafhopper host","volume":"115","author":"Mao","year":"2018","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B53","doi-asserted-by":"publisher","first-page":"819","DOI":"10.1186\/s12864-015-2048-5","article-title":"Weevil endosymbiont dynamics is associated with a clamping of immunity","volume":"16","author":"Masson","year":"2015","journal-title":"BMC Genomics"},{"key":"B54","doi-asserted-by":"publisher","first-page":"E5970","DOI":"10.1073\/pnas.1803245115","article-title":"Recurrent symbiont recruitment from fungal parasites in cicadas","volume":"115","author":"Matsuura","year":"2018","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B55","doi-asserted-by":"publisher","first-page":"R485","DOI":"10.1016\/j.cub.2019.03.032","article-title":"The life of an insect endosymbiont from the cradle to the grave","volume":"29","author":"McCutcheon","year":"2019","journal-title":"Curr. Biol."},{"key":"B56","doi-asserted-by":"publisher","first-page":"15394","DOI":"10.1073\/pnas.0906424106","article-title":"Convergent evolution of metabolic roles in bacterial co-symbionts of insects","volume":"106","author":"McCutcheon","year":"2009","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B57","doi-asserted-by":"publisher","first-page":"708","DOI":"10.1093\/gbe\/evq055","article-title":"Functional convergence in reduced genomes of bacterial symbionts spanning 200 My of evolution","volume":"2","author":"McCutcheon","year":"2010","journal-title":"Genome Biol. Evol."},{"key":"B58","doi-asserted-by":"publisher","first-page":"951","DOI":"10.1046\/j.1529-8817.2001.01126.x","article-title":"Primary and secondary endosymbiosis and the origin of plastids","volume":"37","author":"McFadden","year":"2001","journal-title":"J. Phycol."},{"key":"B59","doi-asserted-by":"publisher","first-page":"e0122821","DOI":"10.1128\/mBio.01228-21","article-title":"Alternative transmission patterns in independently acquired nutritional co-symbionts of Dictyopharidae planthoppers","volume":"12","author":"Michalik","year":"2021","journal-title":"mBio"},{"key":"B60","doi-asserted-by":"publisher","first-page":"579","DOI":"10.1016\/j.asd.2014.07.005","article-title":"Symbiosis in the green leafhopper, Cicadella viridis (Hemiptera, Cicadellidae). Association in statu nascendi?","volume":"43","author":"Michalik","year":"","journal-title":"Arthropod Struct. Dev."},{"key":"B61","doi-asserted-by":"publisher","first-page":"131","DOI":"10.3409\/fb57_3-4.131-137","article-title":"Ultrastructure and transovarial transmission of endosymbiotic microorganisms in Conomelus anceps and Metcalfa pruinosa (Insecta, Hemiptera, Fulgoromorpha)","volume":"57","author":"Michalik","year":"2009","journal-title":"Folia Biol. Krak\u00f3w"},{"key":"B62","doi-asserted-by":"publisher","first-page":"1597","DOI":"10.1007\/s00709-019-01405-y","article-title":"Molecular characterization, ultrastructure and transovarial transmission of Tremblaya phenacola in six mealybugs of the Phenacoccinae subfamily (Insecta, Hemiptera, Coccomorpha)","volume":"256","author":"Michalik","year":"2019","journal-title":"Protoplasma"},{"key":"B63","doi-asserted-by":"publisher","first-page":"1148","DOI":"10.1111\/1462-2920.14057","article-title":"Coexistence of novel gammaproteobacterial and Arsenophonus symbionts in the scale insect Greenisca brachypodii (Hemiptera, Coccomorpha: Eriococcidae)","volume":"20","author":"Michalik","year":"","journal-title":"Environ. Microbiol."},{"key":"B64","doi-asserted-by":"publisher","first-page":"91","DOI":"10.14411\/eje.2014.011","article-title":"Endosymbiotic microorganisms of aphids (Hemiptera: Sternorrhyncha: Aphidoidea): Ultrastructure, distribution and transovarial transmission","volume":"111","author":"Michalik","year":"","journal-title":"Eur. J. Entomol."},{"key":"B65","doi-asserted-by":"publisher","first-page":"1317","DOI":"10.1007\/s00709-018-1234-0","article-title":"Symbiotic cornucopia of the monophagous planthopper Ommatidiotus dissimilis (fall\u00e9n, 1806) (Hemiptera: Fulgoromorpha: Caliscelidae)","volume":"255","author":"Michalik","year":"","journal-title":"Protoplasma"},{"key":"B66","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1109\/GCE.2010.5676129","article-title":"Creating the CIPRES Science Gateway for inference of large phylogenetic trees","volume":"2010","author":"Miller","year":"2010","journal-title":"Gatew. Comput. Environ. Workshop GCE"},{"key":"B67","doi-asserted-by":"publisher","first-page":"1530","DOI":"10.1093\/molbev\/msaa015","article-title":"IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era","volume":"37","author":"Minh","year":"2020","journal-title":"Mol. Biol. Evol."},{"key":"B69","doi-asserted-by":"publisher","first-page":"167","DOI":"10.1098\/rspb.1993.0098","article-title":"A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts","volume":"253","author":"Moran","year":"1993","journal-title":"Proc. R. Soc. Lond. B Biol. Sci."},{"key":"B70","doi-asserted-by":"publisher","first-page":"8802","DOI":"10.1128\/AEM.71.12.8802-8810.2005","article-title":"Symbiosis and insect diversification: An ancient symbiont of sap-feeding insects from the bacterial phylum Bacteroidetes","volume":"71","author":"Moran","year":"2005","journal-title":"Appl. Environ. Microbiol."},{"key":"B71","first-page":"1","article-title":"Die Symbiose der Fulgoroiden (Homoptera-Cicadina)","volume":"98","author":"M\u00fcller","year":"","journal-title":"Zoologica"},{"key":"B72","first-page":"111","article-title":"Die Symbiose der Fulgoroiden (Homoptera-Cicadina)","volume":"98","author":"M\u00fcller","year":"","journal-title":"Zoologica"},{"key":"B73","first-page":"343","article-title":"Zur Systematik und Phylogenie der Zikadenendosymbiose","volume":"1949","author":"M\u00fcller","year":"1949","journal-title":"Biol. Zb."},{"key":"B74","doi-asserted-by":"publisher","first-page":"1478","DOI":"10.1016\/j.cub.2013.06.027","article-title":"Defensive bacteriome symbiont with a drastically reduced genome","volume":"23","author":"Nakabachi","year":"2013","journal-title":"Curr. Biol."},{"key":"B75","doi-asserted-by":"publisher","first-page":"962252","DOI":"10.3389\/fmicb.2022.962252","article-title":"Endosymbiotic bacteria of the boar louse Haematopinus apri (insecta: Phthiraptera: Anoplura)","volume":"13","author":"Nishide","year":"2022","journal-title":"Front. Microbiol."},{"key":"B76","doi-asserted-by":"publisher","first-page":"465","DOI":"10.1007\/s13355-016-0422-7","article-title":"Fungal and bacterial endosymbionts of eared leafhoppers of the subfamily Ledrinae (Hemiptera: Cicadellidae)","volume":"51","author":"Nishino","year":"2016","journal-title":"Appl. Entomol. Zool."},{"key":"B77","doi-asserted-by":"publisher","first-page":"639","DOI":"10.1016\/0965-1748(94)00107-S","article-title":"Phylogenetic position of yeast-like symbiotes of rice planthoppers based on partial 18S rDNA sequences","volume":"25","author":"Noda","year":"1995","journal-title":"Insect Biochem. Mol. Biol."},{"key":"B78","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1038\/s41576-021-00395-z","article-title":"Genetic innovations in animal\u2013microbe symbioses","volume":"23","author":"Perreau","year":"2021","journal-title":"Nat. Rev. Genet."},{"key":"B79","doi-asserted-by":"publisher","first-page":"923","DOI":"10.1002\/mbo3.390","article-title":"The rich somatic life of Wolbachia","volume":"5","author":"Pietri","year":"2016","journal-title":"Wolbachia Microbiol. Open"},{"key":"B80","doi-asserted-by":"publisher","first-page":"a015990","DOI":"10.1101\/cshperspect.a015990","article-title":"Eukaryotic Origins: How and when was the mitochondrion acquired?","volume":"6","author":"Poole","year":"2014","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"B81","doi-asserted-by":"publisher","first-page":"002400","DOI":"10.1128\/mBio.00240-11","article-title":"Insight into the transmission biology and species-specific functional capabilities of tsetse (Diptera: Glossinidae) obligate symbiont Wigglesworthia","volume":"3","author":"Rio","year":"2012","journal-title":"mBio"},{"key":"B98","doi-asserted-by":"publisher","first-page":"e2584","DOI":"10.7717\/peerj.2584","article-title":"VSEARCH: a versatile open source tool for metagenomics","volume":"4","author":"Rognes","year":"2016","journal-title":"PeerJ"},{"key":"B95","doi-asserted-by":"publisher","first-page":"R1177","DOI":"10.1016\/j.cub.2017.09.015","article-title":"The origin and diversification of mitochondria","volume":"27","author":"Roger","year":"2017","journal-title":"Curr. Biol."},{"key":"B82","doi-asserted-by":"publisher","first-page":"20142957","DOI":"10.1098\/rspb.2014.2957","article-title":"An out-of-body experience: The extracellular dimension for the transmission of mutualistic bacteria in insects","volume":"282","author":"Salem","year":"2015","journal-title":"Proc. R. Soc. B"},{"key":"B83","doi-asserted-by":"publisher","first-page":"201","DOI":"10.1146\/annurev-ento-061421-063433","article-title":"Beetle\u2013bacterial symbioses: Endless forms most functional","volume":"67","author":"Salem","year":"2022","journal-title":"Annu. Rev. Entomol."},{"key":"B84","doi-asserted-by":"publisher","first-page":"479","DOI":"10.1111\/j.1365-2958.1996.tb02557.x","article-title":"Intracellular endosymbiotic bacteria of Camponotus species (carpenter ants): Systematics, evolution and ultrastructural characterization","volume":"21","author":"Schr\u00f6der","year":"1996","journal-title":"Mol. Microbiol."},{"key":"B85","doi-asserted-by":"publisher","first-page":"2113","DOI":"10.1073\/pnas.1916748117","article-title":"Coordination of host and symbiont gene expression reveals a metabolic tug-of-war between aphids and Buchnera","volume":"117","author":"Smith","year":"2020","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B87","doi-asserted-by":"publisher","first-page":"3925","DOI":"10.1016\/j.cub.2022.07.036","article-title":"Rational engineering of a synthetic insect-bacterial mutualism","volume":"32","author":"Su","year":"2022","journal-title":"Curr. Biol."},{"key":"B88","doi-asserted-by":"publisher","first-page":"375","DOI":"10.1016\/j.tim.2017.02.014","article-title":"Symbiont acquisition and replacement as a source of ecological innovation","volume":"25","author":"Sudakaran","year":"2017","journal-title":"Trends Microbiol."},{"key":"B89","doi-asserted-by":"publisher","first-page":"1922","DOI":"10.3390\/cells10081922","article-title":"Fungal associates of soft scale insects (Coccomorpha: Coccidae)","volume":"10","author":"Szklarzewicz","year":"2021","journal-title":"Cells"},{"key":"B90","doi-asserted-by":"publisher","first-page":"876","DOI":"10.1111\/een.12861","article-title":"Conservatism and stability of the symbiotic system of the invasive alien treehopper Stictocephala bisonia (Hemiptera, Cicadomorpha, Membracidae)","volume":"45","author":"Szklarzewicz","year":"2020","journal-title":"Ecol. Entomol."},{"key":"B91","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1186\/1471-2148-12-87","article-title":"Two ancient bacterial endosymbionts have coevolved with the planthoppers (Insecta: Hemiptera: Fulgoroidea)","volume":"12","author":"Urban","year":"2012","journal-title":"BMC Evol. Biol."},{"key":"B92","doi-asserted-by":"publisher","first-page":"2487","DOI":"10.1093\/bioinformatics\/btt403","article-title":"nhmmer: DNA homology search with profile HMMs","volume":"29","author":"Wheeler","year":"2013","journal-title":"Bioinformatics"},{"key":"B93","doi-asserted-by":"publisher","first-page":"180","DOI":"10.1002\/wics.147","article-title":"ggplot2","volume":"3","author":"Wickham","year":"2011","journal-title":"WIREs Comput. Stat."},{"key":"B94","article-title":"Survey of planthopper pests of economically important plants (Homoptera: Fulgoroidea)","volume-title":"Proceedings of 2nd international workshop on leafhoppers and planthoppers of economic importance","author":"Wilson","year":"1987"}],"container-title":["Frontiers in Physiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fphys.2023.1135346\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,3,22]],"date-time":"2023-03-22T05:51:03Z","timestamp":1679464263000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fphys.2023.1135346\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,3,22]]},"references-count":92,"alternative-id":["10.3389\/fphys.2023.1135346"],"URL":"https:\/\/doi.org\/10.3389\/fphys.2023.1135346","relation":{},"ISSN":["1664-042X"],"issn-type":[{"value":"1664-042X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,3,22]]},"article-number":"1135346"}}