Novi ftsZ genotip Wolbachia endosimbionta cikade Hyalesthes obsoletus (Hemiptera: Fulgoromorpha: Cixiidae) vektora ‘Candidatus Phytoplasma solani’ asocirane sa Convolvulus arvensis
Sažetak
Hyalesthes obsoletus (Hemiptera: Fulgoromorpha: Cixiidae) je polifagna cikada poznata kao značajan vektor fitopatogene bakterije ‘Candidatus Phytoplasma solani’ (stolbur fitoplazma) koja nanosi štetu u proizvodnji brojnih poljoprivrednih kultura. U okviru odabrane populacije H. obsoletus asocirane sa biljkom Convolvulus arvensis u Srbiji, istraženi su prisustvo i genetička raznovrsnost endosimbiontske bakterije Wolbachia, poznate kao perspektivnog agensa u biološkoj kontroli. U ispitivanoj populaciji H. obsoletus pronađena su oba mikroorganizma, ‘Ca. P. solani’ i Wolbachia. Stopa ‘Ca. P. solani’ infekcije H. obsoletus populacije je bila 50%, dok je u slučaju Wolbachia iznosila 80%. Prisustvo Wolbachia nije bilo uslovljeno infekcijom fitoplazmom i pokazalo je minimalne varijacije između polova insekta. Genotipizacijom
identifikovanih sojeva ‘Ca. P. solani’ otkrivena su četiri prethodno opisana stamp genotipa (Rqg50/St1, Rqg31/St2, STOL/St4 i M5/St28). Novi Wolbachia ftsZ genotip, označen kao WHo1, je identifikovan u populaciji H. obsoletus, što pruža novi uvid u genetičku raznovrsnost Wolbachia endosimbionta insekata iz familije Cixiidae. Filogenetska analiza je pokazala složene odnose između WHo1 i Wolbachia sojeva iz domaćina različitih Hemiptera podredova. Iako strategije biološke kontrole zasnovane na Wolbachia imaju potencijal u kontroli vektora fitoplazmi, potrebna su dalja istraživanja kako bi se objasnile interakcije ovog endosimbionta sa ‘Ca. P. solani’ kao i uticaj Wolbachia na reprodukciju i fitnes vektora.
Reference
Aleksić, Ž., Šutić, D., & Aleksić, D. (1967). Ispitivanje intenziteta prenošenja stolbur virusa cikadom Hyalesthes obsoletus Sign. na neke biljke domaćine (Transmission intensity of stolbur virus by means of Hyalesthes obsoletus Sign. on some host plants). Zaštita bilja / Plant Protection, 93-95, 67-73.
Alma, A., Lessio, F., & Nickel, H. (2019). Insects as phytoplasma vectors: ecological and epidemiological aspects. In: A. Bertaccini, P.G. Weintraub, G.P. Rao, N. Mori (eds.), Phytoplasmas: Plant pathogenic bacteria-II: Transmission and management of Phytoplasma-associated diseases (pp 1-25). Singapore: Springer.
Aryan, A., Brader, G., Mortel, J., Pastar, M., & Riedle-Bauer, M. (2014). An abundant ‘Candidatus Phytoplasma solani’ tuf b strain is associated with grapevine, stinging nettle and Hyalesthes obsoletus. European Journal of Plant Pathology, 140, 213-227. https://doi.org/10.1007/s10658-014-0455-0
Baldo, L., Dunning Hotopp, J.C., Jolley, K.A., Bordenstein, S.R., Biber, S.A., Choudhury, R.R. ... & Werren, J.H. (2006). Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Applied and Environmental Microbiology, 72(11), 7098-7110. https://doi.org/10.1128/AEM.00731-06
Bandelt, H.J., Forster, P., & Rohl, A. (1999). A. medianjoining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16(1), 37-48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
Bressan, A., Semetey, O., Nusillard, B., Clair, D. & Boudon-Padieu, E. (2008). Insect vectors (Hemiptera: Cixiidae) and pathogens associated with the disease syndrome “basses richesses” of sugar beet in France. Plant Disease, 92, 113-119. https://doi.org/10.1094/PDIS-92-1-0113
Bressan, A., Arneodo, J., Simonato, M., Haines, W.P., & Boudon-Padieu, E. (2009). Characterization and evolution of two bacteriome-inhabiting symbionts in cixiid planthoppers (Hemiptera: Fulgoromorpha: Pentastirini). Environmental Microbiology, 11(12), 3265-3279. https://doi.org/10.1111/j.1462-2920.2009.02055.x
Chuche, J., Danet, J.L., Theil, S., Foissac, X., Thiery, D., & Arricau-Bouvery, N. (2016). Microbiomes of the “Candidatus Phytoplasma solani” vectors Hyalesthes obsoletus signoret isolated from different host plants. Mitteilungen Klosterneuburg, 66, 22-39.
Ćurčić, Ž., Stepanović, J., Zubert, C., Taški-Ajduković, K., Kosovac, A., Rekanović, E. … & Duduk, B. (2021). Rubbery taproot disease of sugar beet in Serbia associated with ‘Candidatus Phytoplasma solani’. Plant Disease, 105(2), 255-263. https://doi.org/10.1094/PDIS-07-20-1602-RE
Duan, X.Z., Sun, J.T., Wang, L.T., Shu, X.H., Guo, Y., Keiichiro, M. … & Hong, X.Y. (2020). Recent infection by Wolbachia alters microbial communities in wild Laodelphax striatellus populations. Microbiome, 8, 1-15. https://doi.org/10.1186/s40168-020-00878-x
Fabre, A., Danet, J.L., & Foissac, X. (2011). The stolbur phytoplasma antigenic membrane protein gene stamp is submitted to diversifying positive selection. Gene, 472(1-2), 37-41. https://doi.org/10.1016/j.gene.2010.10.012
Gonella, E., Negri, I., Marzorati, M., Mandrioli, M., Sacchi, L., Pajoro, M. … & Bandi, C. (2011). Bacterial endosymbiont localization in Hyalesthes obsoletus, the insect vector of Bois noir in Vitis vinifera. Applied and Environmental Microbiology, 77(4), 1423-1435. https://doi.org/10.1128/AEM.02121-10
Gong, J.T., Li, Y., Li, T.P., Liang, Y., Hu, L., Zhang, D. … & Xi, Z. (2020). Stable introduction of plant-virus-inhibiting Wolbachia into planthoppers for rice protection. Current Biology, 30(24), 4837-4845.
Gong, J.T., Li, T.P., Wang, M.K., & Hong, X.Y. (2023). Wolbachia-based strategies for control of agricultural pests. Current Opinion in Insect Science, 101039. https://doi.org/10.1016/j.cois.2023.101039
Hilgenboecker, K., Hammerstein, P., Schlattmann, P., Telschow, A., & Werren, J. H. (2008). How many species are infected with Wolbachia?–a statistical analysis of current data. FEMS Microbiology Letters, 281(2), 215-220. https://doi.org/10.1111/j.1574-6968.2008.01110.x
Hoch, H., & Remane R. (1985). Evolution und Speziation der Zikaden-Gattung Hyalesthes SIGNORET, 1865 (Homoptera Auchenorrhyncha Fulgoroidea Cixiidae). Marburger Entomologische Publikationen (Vol. 2). Germany: Goecke & Evers.
Holzinger, W.E., Kammerlander, I., & Nickel, H. (2003). The Auchenorrhyncha of Central Europe: Die Zikaden Mitteleuropas (Vol. 1). Leiden, The Netherlands: Brill.
Hosokawa, T., Koga, R., Kikuchi, Y., Meng, X.Y., & Fukatsu, T. (2010). Wolbachia as a bacteriocyte-associated nutritional mutualist. Proceedings of the National Academy of Sciences, 107(2), 769-774. https://doi.org/10.1073/pnas.0911476107
Iasur-Kruh, L., Naor, V., Zahavi, T., Ballinger, M.J., Sharon, R., Robinson, W.E. … & Zchori-Fein, E. (2017). Bacterial associates of Hyalesthes obsoletus (Hemiptera: Cixiidae), the insect vector of bois noir disease, with a focus on cultivable bacteria. Research in Microbiology, 168(1), 94-101.
Jović, J., Riedle-Bauer, M., & Chuche, J. (2019). Vector role of cixiids and other planthopper species. In: A. Bertaccini, P.G. Weintraub, G.P. Rao, N. Mori, Phytoplasmas: Plant pathogenic bacteria-II: Transmission and management of Phytoplasma-associated diseases, 79-113, Singapore: Springer.
Ju, J.F., Bing, X.L., Zhao, D.S., Guo, Y., Xi, Z., Hoffmann, A.A. … & Hong, X.Y. (2020). Wolbachia supplement biotin and riboflavin to enhance reproduction in planthoppers. The ISME Journal, 14(3), 676-687. https://doi.org/10.1038/s41396-019-0559-9
Kambris, Z., Cook, P.E., Phuc, H.K., & Sinkins, S.P. (2009). Immune activation by life-shortening Wolbachia and reduced filarial competence in mosquitoes. Science, 326(5949), 134-136. Doi: 10.1126/science.117753
Kaul, C., Seitz, A., Maixner, M., & Johannesen, J. (2009). Infection of Bois-Noir tuf-type-I stolbur phytoplasma in Hyalesthes obsoletus (Hemiptera: Cixiidae) larvae and influence on larval size. Journal of Applied Entomology, 133(8), 596-601. https://doi.org/10.1111/j.1439-0418.2009.01406.x
Kessler, S., Schaerer, S., Delabays, N., Turlings, T.C., Trivellone, V., & Kehrli, P. (2011). Host plant preferences of Hyalesthes obsoletus, the vector of the grapevine yellows disease ‘bois noir’, in Switzerland. Entomologia Experimentalis et Applicata, 139(1), 60-67. https://doi.org/10.1111/j.1570-7458.2011.01107.x
Kosovac, A., Radonjić, S., Hrnčić, S., Krstić, O., Toševski, I., & Jović, J. (2016). Molecular tracing of the transmission routes of bois noir in Mediterranean vineyards of Montenegro and experimental evidence for the epidemiological role of Vitex agnus-castus (Lamiaceae) and associated Hyalesthes obsoletus (Cixiidae). Plant Pathology, 65(2), 285-298. https://doi.org/10.1111/ppa.12409
Kosovac, A., Johannesen, J., Krstić, O., Mitrović, M., Cvrković, T., Toševski, I., & Jović, J. (2018). Widespread plant specialization in the polyphagous planthopper Hyalesthes obsoletus (Cixiidae), a major vector of stolbur phytoplasma: Evidence of cryptic speciation. Plos One, 13(5), e0196969. https://doi.org/10.1371/journal.pone.0196969
Kosovac, A., Jakovljević, M., Krstić, O., Cvrković, T., Mitrović, M., Toševski, I., & Jović, J. (2019). Role of plant-specialized Hyalesthes obsoletus associated with Convolvulus arvensis and Crepis foetida in the transmission of ‘Candidatus Phytoplasma solani’-inflicted bois noir disease of grapevine in Serbia. European Journal of Plant Pathology, 153, 183-195. https://doi.org/10.1007/s10658-018-1553-1
Kosovac, A., Ćurčić, Ž., Stepanović, J., Rekanović, E., & Duduk, B. (2023a). Epidemiological role of novel and already known ‘Ca. P. solani’ cixiid vectors in rubbery taproot disease of sugar beet in Serbia. Scientific Reports, 13(1), 1433. https://doi.org/10.1038/s41598-023-28562-8
Kosovac, A., Rekanović, E., Ćurčić, Ž., Stepanović, J., & Duduk, B. (2023b). Plants under siege: Investigating the relevance of ‘Ca. P. solani’ cixiid vectors through a multi-test study. Plants, 12(24), 4157. https://doi.org/10.3390/plants12244157
Krstić, O. (2017). Uloga evolucionih interakcija između intracelularnog endosimbionta (Wolbachia) i fitoplazme (Flavescence dorée) u promenama komponenti adaptivne vrednosti i pravcima evolucije mitohondrijske DNK u prirodnim populacijama Dictyophara europaea (The role of evolutionary interactions between intracellular endosymbiont (Wolbachia) and phytoplasma (Flavescence dorée) on fitness components and evolution of mitochondrial DNA in natural populations Dictyophara europaea). (Doctoral dissertation). University of Belgrade, Faculty of Biology, Belgrade.
Krstić, O., Cvrković, T., Mitrović, M., Radonjić, S., Hrnčić, S., Toševski, I., & Jović, J. (2018). Wolbachia infection in natural populations of Dictyophara europaea, an alternative vector of grapevine Flavescence dorée phytoplasma: Effects and interactions. Annals of Applied Biology, 172(1), 47-64. https://doi.org/10.1111/aab.12400
Langer, M., & Maixner, M. (2004). Molecular characterization of grapevine yellows associated phytoplasmas of the stolbur-group based on RFLP-analysis of non-ribosomal DNA. Vitis, 43(4), 191-199.
Lefoulon, E., Clark, T., Borveto, F., Perriat-Sanguinet, M., Moulia, C., Slatko, B. E., & Gavotte, L. (2020). Pseudoscorpion Wolbachia symbionts: diversity and evidence for a new supergroup S. BMC Microbiology, 20(1), 188.
Lo, N., Casiraghi, M., Salati, E., Bazzocchi, C., & Bandi, C. (2002). How many Wolbachia supergroups exist? Molecular Biology and Evolution, 19(3), 341-346. https://doi.org/10.1093/oxfordjournals.molbev.a004087
Mahuku, G. S. (2004). A simple extraction method suitable for PCR-based analysis of plant, fungal, and bacterial DNA. Plant Molecular Biology Reporter, 22, 71-81. https://doi.org/10.1007/BF02773351
Mitrović, M., Jakovljević, M., Jović, J., Krstić, O., Kosovac, A., Trivellone, V. … & Cvrković, T. (2016). ‘Candidatus phytoplasma solani’ genotypes associated with potato stolbur in Serbia and the role of Hyalesthes obsoletus and Reptalus panzeri (hemiptera, cixiidae) as natural vectors. European Journal of Plant Pathology, 144, 619-630. https://doi.org/10.1007/s10658-015-0800-y
Mori, N., Pozzebon, A., Duso, C., Reggiani, N., & Pavan, F. (2016). Vineyard colonization by Hyalesthes obsoletus (Hemiptera: Cixiidae) induced by stinging nettle cut along surrounding ditches. Journal of Economic Entomology, 109(1), 49-56. https://doi.org/10.1093/jee/tov268
Moussa, A., Maixner, M., Stephan, D., Santoiemma, G., Passera, A., Mori, N., & Quaglino, F. (2021). Entomopathogenic nematodes and fungi to control Hyalesthes obsoletus (Hemiptera: Auchenorrhyncha: Cixiidae). BioControl, 66, 523-534. https://doi.org/10.1007/s10526-020-10076-1
Nickel, H. (2003). The leafhoppers and planthoppers of Germany (Hemiptera, Auchenorrhyncha): Patterns and strategies in a highly diverse group of phytophagous insects. Sofia-Moscow: Pensoft Publishers.
Noda, H., Koizumi, Y., Zhang, Q., & Deng, K. (2001). Infection density of Wolbachia and incompatibility level in two planthopper species, Laodelphax striatellus and Sogatella furcifera. Insect Biochemistry and Molecular Biology, 31, 727-737.
Quaglino, F., Zhao, Y., Casati, P., Bulgari, D., Bianco, P.A., Wei, W., & Davis, R.E. (2013). ‘Candidatus Phytoplasma solani’, a novel taxon associated with stolbur-and bois noir-related diseases of plants. International journal of systematic and evolutionary microbiology, 63(8), 2879-2894. https://doi.org/10.1099/ijs.0.044750-0
Rees, D.J., Emerson, B.C., Oromi, P., & Hewitt, G.M. (2001). Mitochondrial DNA, ecology and morphology: interpreting the phylogeography of the Nesotes (Coleoptera: Tenebrionidae) of Gran Canaria (Canary Islands). Molecular Ecology, 10(2), 427-434. https://doi.org/10.1046/j.1365-294X.2001.01227.x
Riedle-Bauer, M., & Brader, G. (2023). Effects of insecticides and repellents on the spread of ‘Candidatus Phytoplasma solani’ under laboratory and field conditions. Journal of Plant Diseases and Protection, 130(5), 1057-1074. https://doi.org/10.1007/s41348-023-00768-y
Rinklef, A., Behrmann, S.C., Loff ler, D., Erner, J., Meyer, M.V., Lang, C. … Lee, K.Z. (2024). Prevalence in potato of ‘Candidatus Arsenophonus Phytopathogenicus’ and ‘Candidatus Phytoplasma Solani ’ and their transmission via adult Pentastiridius leporinus. Insects, 15(4), p.275. https://doi.org/10.3390/insects15040275
Ross, P.A., Turelli, M., & Hoffmann, A.A. (2019). Evolutionary ecology of Wolbachia releases for disease control. Annual Review of Genetics, 53, 93-116. https://doi.org/10.1146/annurev-genet-112618-043609
Schulenburg, J.H.G., Hurst, G.D.D., Huigens, T.M.E., van Meer, M.M.M., Jiggins, F.M., & Majerus, M.E.N. (2000). Molecular evolution and phylogenetic utility of Wolbachia ftsZ and wsp gene sequences with special reference to the origin of male-killing. Molecular Biology and Evolution, 17(4), 584-600. https://doi.org/10.1093/oxfordjournals.molbev.a026338
Sforza, R., Bourgoin, T., Wilson, S.W., & Boudon-Padieu, E. (1999). Field observations, laboratory rearing and descriptions of immatures of the planthopper Hyalesthes obsoletus (Hemiptera: Cixiidae). European Journal of Entomology, 96(4), 409-418.
Sharon, R., Soroker, V., Wesley, S.D., Zahavi, T., Harari, A., & Weintraub, P.G. (2005). Vitex agnus-castus is preferred host plant for Hyalesthes obsoletus. Journal of Chemical Ecology, 31, 1051-1063. https://doi.org/10.1007/s10886-005-4247-z
Shropshire, J. D., Leigh, B., & Bordenstein, S. R. (2020). Symbiont-mediated cytoplasmic incompatibility: what have we learned in 50 years? Elife, 9, e61989. https://doi.org/10.7554/eLife.61989
Stouthamer R., Breeuwer J.A.J, & Hurst G.D.D (1999). Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annual Review of Microbiology, 53, 71-102. https://doi.org/10.1146/annurev.micro.53.1.71
Sullivan, W. (2020). Vector control: Wolbachia expands its protective reach from humans to plants. Current Biology, 30(24), R1469–R1499. https://doi.org/10.1016/j.cub.2020.11.005
Tamura, K., Stecher, G., & Kumar, S. (2021). MEGA11: molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution, 38(7), 3022-3027. https://doi.org/10.1093/molbev/msab120
Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22(22), 4673-4680. https://doi.org/10.1093/nar/22.22.4673
Werren, J.H. (1997). Biology of Wolbachia. Annual Review of Entomology, 42, 587-609. https://doi.org/10.1146/annurev.ento.42.1.587
Werren, J.H., Baldo, L., & Clark, M.E. (2008). Wolbachia: master manipulators of invertebrate biology. Nature Reviews Microbiology, 6(10), 741-751. https://doi.org/10.1038/nrmicro1969
Zug, R., & Hammerstein, P. (2015). Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts. Biological Reviews, 90(1), 89-111.
Sva prava zadržana (c) 2024 Autori
Ovaj rad je pod Creative Commons Autorstvo-Deli pod istim uslovima 4.0 međunarodnom licencom.
Autori koji objavljuju u ovom časopisu pristaju na sledeće uslove:- Autori zadržavaju autorska prava i pružaju časopisu pravo prvog objavljivanja rada i licenciraju ga "Creative Commons Attribution licencom" koja omogućava drugima da dele rad, uz uslov navođenja autorstva i izvornog objavljivanja u ovom časopisu.
- Autori mogu izraditi zasebne, ugovorne aranžmane za neekskluzivnu distribuciju članka objavljenog u časopisu (npr. postavljanje u institucionalni repozitorijum ili objavljivanje u knjizi), uz navođenje da je članak izvorno objavljen u ovom časopisu.
- Autorima je dozvoljeno i podstiču se da postave objavljeni članak onlajn (npr. u institucionalni repozitorijum ili na svoju internet stranicu) pre ili tokom postupka prijave rukopisa, s obzirom da takav postupak može voditi produktivnoj razmeni ideja i ranijoj i većoj citiranosti objavljenog članka (Vidi Efekti otvorenog pristupa).