A Preliminary Study on the Transfer Mode and Biological Significance of Endosymbiont Arsenophonus in Nilaparvata lugens

doi:10.3969/j.issn.1001-7216.2014.01.013

Abstract

Abstract: According to direct and reciprocal cross test, Arsenophonus offspring infection was determined by female parents rather than male parents,which indicated Arsenophonus was maternally inherited in the brown planthopper (BPH), Nilaparvata lugens. The newly emerged Arsenophonusinfected (positive) and uninfected (negative) BPH were paired respectively, the number and sex of offsprings were recorded. The results indicated Arsenophonus infection did not significantly impact reproduction and sex ratio of BPH. It suggested that Arsenophonus had no malekilling function to BPH. The results showed that the infection rate of negative population to M. anisopliae ARSEF1764 (55.2 %) was significantly higher than that of positive population (32.5 %), which indicated Arsenophonus could improve the resistance of BPH to M. anisopliae.

Key words: Arsenophonus, Nilaparvata lugens, transfer mode, malekilling, Metarhizium anisopliae

摘要： 通过阳性（含Arsenophonus）与阴性（不含Arsenophonus）褐飞虱初羽化成虫的正反交试验，发现子代感染Arsenophonus的情况由其母本决定，而与父本无关，表明褐飞虱体内的Arsenophonus可由母体垂直传递给子代。初羽化阳性和阴性成虫的配对实验结果表明，Arsenophonus对褐飞虱后代数量及性比没有显著的作用，无雄性致死作用。通过黄绿绿僵菌ARSEF1764菌株对初羽化雌成虫褐飞虱的接种实验，发现阴性试虫的感病率为55.2% ，显著高于阳性试虫的32.5% ，表明感染Arsenophonus有助于提高褐飞虱对黄绿绿僵菌ARSEF1764菌株的抵抗能力。

关键词: Arsenophonus, 褐飞虱, 传递方式, 雄性致死, 黄绿绿僵菌

CLC Number:

CHEN Yu, CHEN Yang, WANG Weixia, LAI Fengxiang, FU Qiang*. A Preliminary Study on the Transfer Mode and Biological Significance of Endosymbiont Arsenophonus in Nilaparvata lugens[J]. Chinese Journal of Rice Science, 2014, 28(1): 92-96.

陈宇,陈洋,王渭霞,赖凤香,傅强*. 褐飞虱杀雄菌属共生菌Arsenophonus的传递方式与生物学意义初探[J]. 中国水稻科学, 2014, 28(1): 92-96.

References

\[1\]Gherna R L, Werren J H, Weisburg W, et al. Arsenophonus nasoniae gen. nov., sp. nov., the causative agent of the sonkiller trait in the parasitic wasp Nasonia vitripennis. Int J Syst Bacteriol, 1991, 41(4): 563565.

\[2\]Duron O, Bouchon D, Boutin S, et al.The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol, 2008, 6(1): 27.

\[3\]陈宇, 王渭霞, 陈洋, 等. 昆虫Arsenophonus属共生菌的研究进展. 浙江农业学报, 2014， 26（2）（印刷中）.

\[4\]Duron O, Wilkes TE, Hurst GDD. Interspecific transmission of a malekilling bacterium on an ecological timescale. Ecol Lett, 2010, 13(9): 11391148.

\[5\]刘巍巍, 杨璞, 陈晓鸣, 等. 白蜡虫体内杀雄菌属共生菌的分子检测. 微生物学报, 2012, 52(8): 10021010.

\[6\]Skinner S W. Sonkiller: a third extrachromosomal factor affecting sex ratios in the parasitoid wasp Nasonia vitripennis. Genetics, 1985, 109(4): 745759.

\[7\]Huger A M, Skinner S W, Werren J H. Bacterial infections associated with the sonkiller trait in the parasitoid wasp Nasonia (=Mormeniella) vitripennis (Hymenoptera: Pteronalidae). J Invertebr Pathol, 1985, 46(3): 272280.

\[8\]Ferree P M, Avery A, Azpurua J, et al. A bacterium targets maternally inherited centrosomes to kill males in Nasonia. Curr Biol, 2008, 18(18): 14091414.

\[9\]Werren J H, Skinner S W, Huger A M. Malekilling bacteria in a parasitic wasp. Science, 1986, 231: 990992.

\[10\]Hansen A K, Jeong G, Paine T D, et al. Frequency of secondary symbiont infection in an invasive psyllid relates to parasitism pressure on a geographic scale in California. App Environ Microbiol, 2007, 73(23): 75317535.

\[11\]Chiel E, Gottlieb Y, ZchoriFein E, et al. Biotypedependent secondary symbiont communities in sympatric populations of Bemisia tabaci. Bull Entomol Res, 2007, 97(4): 407413.

\[12\]王渭霞, 罗举, 赖凤香,等. 水稻褐飞虱内生共生细菌Arsenophonus的鉴定和系统分析. 昆虫学报，2010, 53(6): 647654.

\[13\]Thao M L L, Baumann P. Evidence for multiple acquisition of Arsenophonus by whitefly species (Sternorrhyncha: Aleyrodidae). Curr Microbiol, 2004, 48(2)： 140144.

\[14\]Murad G, Svetlana K. Susceptibility to insecticides in the Q biotype of Bemisia tabaci is correlated with bacterial symbiont densities. Pest Manag Sci, 2009, 65(9): 939942.

\[15\]Tang Q Y, Zhang C X. Data Processing System (DPS) software with experimental design, statistical analysis and data mining developed for use in entomological research. Insect Science, 2013, 20(2): 254260.

\[16\]Taylor G P, Coghlin P C, Floate K D, et al. The host range of the malekilling symbiont Arsenophonus nasoniae in filth fly parasitioids. J Inverteb Pathol, 2011, 106(3): 371379.

\[17\]Clay K, Klyachko O, Grindle N, et al. Microbial communities and interactions in the lone star tick, Amblyomma americanum. Mol Ecol, 2008, 17(19): 43714381.

\[18\] Hypa V, Dale C. In vitro culture and phylogenetic analysis of “Candidatus Arsenophonus triatominarum”, an intracellular bacterium from the triatomine bug, Triatoma infestans. Int J Syst Bacteriol, 1997, 47(4): 11401144.

\[19\] Dale C, Beeton M, Harbison C, et al. Isolation, pure culture, and characterization of “Candidatus Arsenophonus arthropodicus” an intracellular secondary endosymbiont from the hippoboscid louse fly Pseudolynchia canariensis. Appl Environ Microbiol, 2006, 72(4): 29973004.

\[20\]Ferrari J, Darby A C, Daniell T J, et al. Linking the bacterial community in pea aphids with hostplant use and natural enemy resistance. Ecol Entomol, 2004, 29 (1): 6065.

\[21\] Moran N A, Russell J A, Koga R, et al. Evolutionary relationships of three new species of Enterobacteriaceae living as symbionts of aphids and other insects. Appl Environ Microbiol, 2005, 71 (6): 33023310.

\[22\] Scarborough C L, Ferrari J, Godfray H C J. Aphid protected from pathogen by endosymbiont. Science, 2005, 310(5755): 1781.

\[23\]Panteleev D Y, Goryacheva I I, Andrianov B V, et al. The endosymbiotic bacterium Wolbachia enhances the nonspecific resistance to insect pathogens and alters behavior of Drosophila melanogaster. Rus J Gene, 2007, 43(9): 10661069.

\[24\]Jaenike J, Stahlhut J K, Boelio L M, et al. Association between Wolbachia and Spiroplasma within Drosophila neotestacea: An emerging symbiotic mutualism. Mol Ecol, 2010, 19 (2): 414425.

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