Abstract
The rate of genomic recombination displays evolutionary plasticity and can even vary in response to environmental factors. The western honey bee (Apis mellifera L.) has an extremely high genomic recombination rate but the mechanistic basis for this genome-wide upregulation is not understood. Based on the hypothesis that meiotic recombination and DNA damage repair share common mechanisms in honey bees as in other organisms, we predicted that oxidative stress leads to an increase in recombination rate in honey bees. To test this prediction, we subjected honey bee queens to oxidative stress by paraquat injection and measured the rates of genomic recombination in select genome intervals of offspring produced before and after injection. The evaluation of 26 genome intervals in a total of over 1750 offspring of 11 queens by microsatellite genotyping revealed several significant effects but no overall evidence for a mechanistic link between oxidative stress and increased recombination was found. The results weaken the notion that DNA repair enzymes have a regulatory function in the high rate of meiotic recombination of honey bees, but they do not provide evidence against functional overlap between meiotic recombination and DNA damage repair in honey bees and more mechanistic studies are needed.
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References
Aamodt RM (2009) Age-and caste-dependent decrease in expression of genes maintaining DNA and RNA quality and mitochondrial integrity in the honeybee wing muscle. Exp Gerontol 44:586–593
Adrian AB, Corchado JC, Comeron JM (2016) Predictive models of recombination rate variation across the Drosophila melanogaster genome. Genome Biol Evol 8:2597–2612
Baudat F, Imai Y, De Massy B (2013) Meiotic recombination in mammals: localization and regulation. Nat Rev Genet 14:794
Bernstein H, Bernstein C, Michod RE (2012) Meiosis as an evolutionary adaptation for DNA repair. In: Kruman I (ed) DNA repair. InTech Publ., pp 357–382
Bessoltane N, Toffano-Nioche C, Solignac M, Mougel F (2012) Fine scale analysis of crossover and non-crossover and detection of recombination sequence motifs in the honeybee (Apis mellifera). PLoS One 7:e36229
Beye M, Gattermeier I, Hasselmann M, Gempe T, Schioett M, Baines JF, Schlipalius D, Mougel F, Emore C, Rueppell O, Sirviö A, Guzmán-Novoa E, Hunt G, Solignac M, Page RE (2006) Exceptionally high levels of recombination across the honey bee genome. Genome Res 16:1339–1344
Blanton HL, Radford SJ, McMahan S, Kearney HM, Ibrahim JG, Sekelsky J. 2005. REC, Drosophila MCM8, drives formation of meiotic crossovers. PLoS Genet 1:e40
Bus JS, Gibson JE (1984) Paraquat—model for oxidant-initiated toxicity. Environ Health Persp 55:37–46
Cadet J, Douki T, Ravanat J-L (2010) Oxidatively generated base damage to cellular DNA. Free Radic Biol Med 49:9–21
Cooke MS, Evans MD, Dizdaroglu M, Lunec J (2003) Oxidative DNA damage: mechanisms, mutation, and disease. FASEB J 17:1195–1214
Corona M, Hughes KA, Weaver DB, Robinson GE (2005) Gene expression patterns associated with queen honey bee longevity. Mech Ageing Dev 126:1230–1238
Corona M, Velarde RA, Remolina S, Moran-Lauter A, Wang Y, Hughes KA, Robinson GE (2007) Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proc Natl Acad Sci USA 104:7128–7133
Dinis-Oliveira R, Duarte J, Sanchez-Navarro A, Remiao F, Bastos M, Carvalho F (2008) Paraquat poisonings: mechanisms of lung toxicity, clinical features, and treatment. Crit Rev Toxicol 38:13–71
Dumont BL, Payseur BA (2011) Evolution of the genomic recombination rate in murid rodents. Genetics 187:643–657
Elsik C, Worley K, Bennett A, Beye M, Camara F, Childers C, de Graaf D, Debyser G, Deng J, Devreese B, Elhaik E, Evans J, Foster L, Graur D, Guigo R, Teams HP, Hoff K, Holder M, Hudson M, Hunt G, Jiang H, Joshi V, Khetani R, Kosarev P, Kovar C, Ma J, Maleszka R, Moritz R, Munoz-Torres M, Murphy T (2014) Finding the missing honey bee genes: lessons learned from a genome upgrade. BMC Genom 15:86
Ghabrial A, Ray RP, Schüpbach T (1998) okra and spindle-B encode components of the RAD52 DNA repair pathway and affect meiosis and patterning in Drosophila oogenesis. Genes Dev 12:2711–2723
Hörandl E, Hadacek F (2013) The oxidative damage initiation hypothesis for meiosis. Plant Reprod 26:351–367
Hunter CM, Huang W, Mackay TF, Singh ND (2016) The genetic architecture of natural variation in recombination rate in Drosophila melanogaster. PLoS Genet 12:e1005951
Keeney S (2008) Spo11 and the formation of DNA double-strand breaks in meiosis. Genome Dyn Stab 2:81–123
Kent CF, Zayed A (2013) Evolution of recombination and genome structure in eusocial insects. Commun Integr Biol 6:e22919
Kent CF, Minaei S, Harpur BA, Zayed A (2012) Recombination is associated with the evolution of genome structure and worker behavior in honey bees. Proc Natl Acad Sci USA 109:18012–18017
Kohl KP, Sekelsky J (2013) Meiotic and mitotic recombination in meiosis. Genetics 194:327–334
Kong A, Thorleifsson G, Frigge ML, Masson G, Gudbjartsson DF, Villemoes R, Magnusdottir E, Olafsdottir SB, Thorsteinsdottir U, Stefansson K (2014) Common and low-frequency variants associated with genome-wide recombination rate. Nat Genet 46:11–16
Laidlaw HH, Page RE (1997) Queen rearing and bee breeding. Wicwas Press, Cheshire
Li X, Heyer W-D (2008) Homologous recombination in DNA repair and DNA damage tolerance. Cell Res 18:99–113
Li-Byarlay H, Huang MH, Simone-Finstrom MD, Strand MK, Tarpy DR, Rueppell O (2016) Honey bee (Apis mellifera) drones survive oxidative stress due to increased tolerance instead of avoidance or repair of oxidative damage. Exp Gerontol 83:15–21
Liu H, Zhang X, Huang J, Chen J-Q, Tian D, Hurst L, Yang S (2015) Causes and consequences of crossing-over evidenced via a high-resolution recombinational landscape of the honey bee. Genome Biol 16:15
Lynch M (2006) The origins of eukaryotic gene structure. Mol Biol Evol 23:450–468
Mannuss A, Trapp O, Puchta H (2012) Gene regulation in response to DNA damage. Biochim Biophys Acta BBA Gene Regul Mech 1819:154–165
Meznar ER, Gadau J, Koeniger N, Rueppell O (2010) Comparative linkage mapping suggests a high recombination rate in all honey bees. J Hered 101:S118–S126
Neale MJ, Keeney S (2006) Clarifying the mechanics of DNA strand exchange in meiotic recombination. Nature 442:153–158
Page RE, Peng Y-SC (2001) Aging and development in social insects with emphasis on the honey bee, Apis mellifera L. Exp Gerontol 36:695–711
Ross CR, DeFelice DS, Hunt GJ, Ihle KE, Amdam GV, Rueppell O (2015) Genomic correlates of recombination rate and its variability across eight recombination maps in the western honey bee (Apis mellifera L.). BMC Genom 16:107
Rueppell O, Amdam GV, Page RE Jr, Carey JR (2004) From genes to society: social insects as models for research on aging. Sci Aging Knowl Environ 5:pe5
Rueppell O, Kuster R, Miller K, Fouks B, Rubio Correa S, Collazo J, Phaincharoen M, Tingek S, Koeniger N (2016) A new metazoan recombination rate record and consistently high recombination rates in the honey bee genus Apis accompanied by frequent inversions but not translocations. Genome Biol Evol 8:3653–3660
Rueppell O, Yousefi B, Collazo J, Smith D (2017) Early life stress affects mortality rate more than social behavio, gene expression or oxidative damage in honey bee workers. Exp Gerontol 90:19–25
Schuermann D, Molinier J, Fritsch O, Hohn B (2005) The dual nature of homologous recombination in plants. Trends Genet 21:172–181
Seehuus SC, Norberg K, Gimsa U, Krekling T, Amdam GV (2006) Reproductive protein protects sterile honey bee workers from oxidative stress. Proc Nat Acad Sci USA 103:962–967
Sim C, Denlinger DL (2011) Catalase and superoxide dismutase-2 enhance survival and protect ovaries during overwintering diapause in the mosquito Culex pipiens. J Insect Physiol 57:628–634
Singh ND, Criscoe DR, Skolfield S, Kohl KP, Keebaugh ES, Schlenke TA (2015) Fruit flies diversify their offspring in response to parasite infection. Science 349:747–750
Slupphaug G, Kavli B, Krokan HE (2003) The interacting pathways for prevention and repair of oxidative DNA damage. Mutat Res Fundam Mol Mech Mutagen 531:231–251
Solignac M, Mougel F, Vautrin D, Monnerot M, Cornuet JM (2007) A third-generation microsatellite-based linkage map of the honey bee, Apis mellifera, and its comparison with the sequence-based physical map. Genome Biol 8:R66
Tokunaga I, Kubo Si, Mikasa H, Suzuki Y, Morita K (1997) Determination of 8-hydroxy-deoxyguanosine formation in rat organs: assessment of paraquat-evoked oxidative DNA damage. Biochem Mol Biol Int 43:73–77
Vispé S, Cazaux C, Lesca C, Defais M (1998) Overexpression of Rad51 protein stimulates homologous recombination and increases resistance of mammalian cells to ionizing radiation. Nucleic Acids Res 26:2859–2864
Wallberg A, Glémin S, Webster MT (2015) Extreme recombination frequencies shape genome variation and evolution in the Honeybee, Apis mellifera. PLoS Genet 11:e1005189
Wilfert L, Gadau J, Schmid-Hempel P (2007) Variation in genomic recombination rates among animal taxa and the case of social insects. Heredity 98:189–197
Winston ML (1987) The biology of the honey bee. Harvard University Press, Cambridge
Acknowledgements
We would like to thank all members of the Social Insect Lab at UNCG for their encouragement and discussion. Financial support for this study was provided by a NIGMS grant to OR (R15GM102753) and the Army Research Office (W911NF1520045).
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Langberg, K., Phillips, M. & Rueppell, O. Testing the effect of paraquat exposure on genomic recombination rates in queens of the western honey bee, Apis mellifera. Genetica 146, 171–178 (2018). https://doi.org/10.1007/s10709-018-0009-z
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DOI: https://doi.org/10.1007/s10709-018-0009-z