Transcriptional and epigenetic responses to mating and aging in Drosophila melanogaster

BMC Genomics

Robert RH Anholt¹  Trudy FC Mackay¹  Shanshan Zhou¹ 

[1] Department of Biological Sciences, W. M. Keck Center for Behavioral Biology and Program in Genetics, Box 7614, North Carolina State University, Raleigh, NC 27695-7617, USA

关键词: Systems genetics;    Environmental plasticity;    ChipSeq;    Histone modification;    microRNA;   

Others  :  1128430
DOI  :  10.1186/1471-2164-15-927

 received in 2014-07-24, accepted in 2014-10-13,  发布年份 2014

【 摘 要 】

Background

Phenotypic plasticity allows organisms to respond rapidly to changing environmental circumstances, and understanding its genomic basis can yield insights regarding the underlying genes and genetic networks affecting complex phenotypes. Female Drosophila melanogaster undergo dramatic physiological changes mediated by seminal fluid components transferred upon mating, including decreased longevity. Their physiological and behavioral effects have been well characterized, but little is known about resulting changes in regulation of gene expression or the extent to which mating-induced changes in gene expression are the same as those occurring during aging.

Results

We assessed genome-wide mRNA, microRNA, and three common histone modifications implicated in gene activation for young and aged virgin and mated female D. melanogaster in a factorial design. We identified phenotypically plastic transcripts and epigenetic modifications associated with mating and aging. We used these data to derive phenotypically plastic regulatory networks associated with mating of young flies, and aging of virgin and mated flies. Many of the mRNAs, microRNAs and epigenetic modifications associated with mating of young flies also occur with age in virgin flies, which may reflect mating-induced accelerated aging. We functionally tested the plastic regulatory networks by overexpressing environmentally sensitive microRNAs. Overexpression resulted in altered expression of ~70% of candidate target genes, and in all cases affected oviposition.

Conclusions

Our results implicate microRNAs as mediators of phenotypic plasticity associated with mating and provide a comprehensive documentation of the genomic and epigenomic changes that accompany mating- and aging-induced physiological changes in female D. melanogaster.

【 授权许可】

   
2014 Zhou et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

【 参考文献 】

• [1]Lakowski B, Hekimi S: The genetics of caloric restriction in Caenorhabditis elegans. Proc Natl Acad Sci U S A 1998, 95(22):13091-13096.
• [2]Magwire MM, Yamamoto A, Carbone MA, Roshina NV, Symonenko AV, Pasyukova EG, Morozova TV, Mackay TFC: Quantitative and molecular genetic analyses of mutations increasing Drosophila life span. PLoS Genet 2010, 6(7):e1001037.
• [3]Weindruch R, Kayo T, Lee CK, Prolla TA: Microarray profiling of gene expression in aging and its alteration by caloric restriction in mice. J Nutr 2001, 131(3):918S-923S.
• [4]Zhou S, Campbell TG, Stone EA, Mackay TFC, Anholt RRH: Phenotypic plasticity of the Drosophila transcriptome. PLoS Genet 2012, 8(3):e1002593.
• [5]Sambandan D, Carbone MA, Anholt RRH, Mackay TFC: Phenotypic plasticity and genotype by environment interaction for olfactory behavior in Drosophila melanogaster. Genetics 2008, 179(2):1079-1088.
• [6]Bourc’his D, Voinnet O: A small-RNA perspective on gametogenesis, fertilization, and early zygotic development. Science 2010, 330(6004):617-622.
• [7]Bushati N, Cohen SM: MicroRNA functions. Annu Rev Cell Dev Biol 2007, 23:175-205.
• [8]Kato M, Slack FJ: Ageing and the small, non-coding RNA world. Ageing Res Rev 2013, 12(1):429-435.
• [9]Liu N, Landreh M, Cao K, Abe M, Hendriks GJ, Kennerdell JR, Zhu Y, Wang LS, Bonini NM: The microRNA miR-34 modulates ageing and neurodegeneration in Drosophila. Nature 2012, 482(7386):519-523.
• [10]Duncan EJ, Gluckman PD, Dearden PK: Epigenetics, plasticity, and evolution: How do we link epigenetic change to phenotype? J Exp Zool B Mol Dev Evol 2014, 322(4):208-220.
• [11]Gardner KE, Allis CD, Strahl BD: Operating on chromatin, a colorful language where context matters. J Mol Biol 2011, 409(1):36-46.
• [12]Spencer VA, Davie JR: Role of covalent modifications of histones in regulating gene expression. Gene 1999, 240(1):1-12.
• [13]McGraw LA, Clark AG, Wolfner MF: Post-mating gene expression profiles of female Drosophila melanogaster in response to time and to four male accessory gland proteins. Genetics 2008, 179(3):1395-1408.
• [14]Pletcher SD, Macdonald SJ, Marguerie R, Certa U, Stearns SC, Goldstein DB, Partridge L: Genome-wide transcript profiles in aging and calorically restricted Drosophila melanogaster. Curr Biol 2002, 12(9):712-723.
• [15]McCarroll SA, Murphy CT, Zou S, Pletcher SD, Chin CS, Jan YN, Kenyon C, Bargmann CI, Li H: Comparing genomic expression patterns across species identifies shared transcriptional profile in aging. Nat Genet 2004, 36(2):197-204.
• [16]Lai CQ, Parnell LD, Lyman RF, Ordovas JM, Mackay TFC: Candidate genes affecting Drosophila life span identified by integrating microarray gene expression analysis and QTL mapping. Mech Ageing Dev 2007, 128(3):237-249.
• [17]Smith G, Fang Y, Liu X, Kenny J, Cossins AR, de Oliveira CC, Etges WJ, Ritchie MG: Transcriptome-wide expression variation associated with environmental plasticity and mating success in cactophilic Drosophila mojavensis. Evolution 2013, 67(7):1950-1963.
• [18]Dalton JE, Kacheria TS, Knott SR, Lebo MS, Nishitani A, Sanders LE, Stirling EJ, Winbush A, Arbeitman MN: Dynamic, mating-induced gene expression changes in female head and brain tissues of Drosophila melanogaster. BMC Genomics 2010, 11:541. BioMed Central Full Text
• [19]McGraw LA, Gibson G, Clark AG, Wolfner MF: Genes regulated by mating, sperm, or seminal proteins in mated female Drosophila melanogaster. Curr Biol 2004, 14(16):1509-1514.
• [20]Lai CQ, Leips J, Zou W, Roberts JF, Wollenberg KR, Parnell LD, Zeng ZB, Ordovas JM, Mackay TFC: Speed-mapping quantitative trait loci using microarrays. Nat Methods 2007, 4(10):839-841.
• [21]Wolfner MF: Battle and ballet: molecular interactions between the sexes in Drosophila. J Hered 2009, 100(4):399-410.
• [22]Chapman T: Seminal fluid-mediated fitness traits in Drosophila. Heredity (Edinb) 2001, 87(Pt 5):511-521.
• [23]Wolfner MF: The gifts that keep on giving: physiological functions and evolutionary dynamics of male seminal proteins in Drosophila. Heredity (Edinb) 2002, 88(2):85-93.
• [24]Chapman T, Liddle LF, Kalb JM, Wolfner MF, Partridge L: Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 1995, 373(6511):241-244.
• [25]Rubinstein CD, Wolfner MF: Drosophila seminal protein ovulin mediates ovulation through female octopamine neuronal signaling. Proc Natl Acad Sci U S A 2013, 110(43):17420-17425.
• [26]Yapici N, Kim YJ, Ribeiro C, Dickson BJ: A receptor that mediates the post-mating switch in Drosophila reproductive behaviour. Nature 2008, 451(7174):33-37.
• [27]Wilson RH, Lai CQ, Lyman RF, Mackay TFC: Genomic response to selection for postponed senescence in Drosophila. Mech Ageing Dev 2013, 134(3–4):79-88.
• [28]Norga KK, Gurganus MC, Dilda CL, Yamamoto A, Lyman RF, Patel PH, Rubin GM, Hoskins RA, Mackay TFC, Bellen HJ: Quantitative analysis of bristle number in Drosophila mutants identifies genes involved in neural development. Curr Biol 2003, 13(16):1388-1396.
• [29]Barckmann B, Simonelig M: Control of maternal mRNA stability in germ cells and early embryos. BBA-Gene Regul Mech 2013, 1829(6–7):714-724.
• [30]Tadros W, Lipshitz HD: The maternal-to-zygotic transition: a play in two acts. Development 2009, 136(18):3033-3042.
• [31]Ruby JG, Stark A, Johnston WK, Kellis M, Bartel DP, Lai EC: Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs. Genome Res 2007, 17(12):1850-1864.
• [32]Bushati N, Stark A, Brennecke J, Cohen SM: Temporal reciprocity of miRNAs and their targets during the maternal-to-zygotic transition in Drosophila. Curr Biol 2008, 18(7):501-506.
• [33]Lyko F, Ramsahoye BH, Jaenisch R: DNA methylation in Drosophila melanogaster. Nature 2000, 408(6812):538-540.
• [34]Allis CD, Berger SL, Cote J, Dent S, Jenuwien T, Kouzarides T, Pillus L, Reinberg D, Shi Y, Shiekhattar R, Shilatifard A, Workman J, Zhang Y: New nomenclature for chromatin-modifying enzymes. Cell 2007, 131(4):633-636.
• [35]Kouzarides T: SnapShot: Histone-modifying enzymes. Cell 2007, 131(4):822.
• [36]Nègre N, Brown CD, Ma L, Bristow CA, Miller SW, Wagner U, Kheradpour P, Eaton ML, Loriaux P, Sealfon R, Li Z, Ishii H, Spokony RF, Chen J, Hwang L, Cheng C, Auburn RP, Davis MB, Domanus M, Shah PK, Morrison CA, Zieba J, Suchy S, Senderowicz L, Victorsen A, Bild NA, Grundstad AJ, Hanley D, MacAlpine DM, Mannervik M, et al.: A cis-regulatory map of the Drosophila genome. Nature 2011, 471(7339):527-531.
• [37]Murali T, Pacifico S, Yu J, Guest S, Roberts GG 3rd, Finley RL Jr: DroID 2011: a comprehensive, integrated resource for protein, transcription factor, RNA and gene interactions for Drosophila. Nucleic Acids Res 2011, 39(Database issue):D736-D743.
• [38]Brand AH, Perrimon N: Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993, 118(2):401-415.
• [39]Giraldez AJ, Mishima Y, Rihel J, Grocock RJ, Van Dongen S, Inoue K, Enright AJ, Schier AF: Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 2006, 312(5770):75-79.
• [40]De Renzis S, Elemento O, Tavazoie S, Wieschaus EF: Unmasking activation of the zygotic genome using chromosomal deletions in the Drosophila embryo. PLoS Biol 2007, 5(5):e117.
• [41]Yin H, Sweeney S, Raha D, Snyder M, Lin H: A high-resolution whole-genome map of key chromatin modifications in the adult Drosophila melanogaster. PLoS Genet 2011, 7(12):e1002380.
• [42]Nagarajan M, Veyrieras JB, de Dieuleveult M, Bottin H, Fehrmann S, Abraham AL, Croze S, Steinmetz LM, Gidrol X, Yvert G: Natural single-nucleosome epi-polymorphisms in yeast. PLoS Genet 2010, 6(4):e1000913.
• [43]Benoit B, He CH, Zhang F, Votruba SM, Tadros W, Westwood JT, Smibert CA, Lipshitz HD, Theurkauf WE: An essential role for the RNA-binding protein Smaug during the Drosophila maternal-to-zygotic transition. Development 2009, 136(6):923-932.
• [44]Jin H, Kim VN, Hyun S: Conserved microRNA miR-8 controls body size in response to steroid signaling in Drosophila. Genes Dev 2012, 26(13):1427-1432.
• [45]Kucherenko MM, Barth J, Fiala A, Shcherbata HR: Steroid-induced microRNA let-7 acts as a spatio-temporal code for neuronal cell fate in the developing Drosophila brain. EMBO J 2012, 31(24):4511-4523.
• [46]Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL: TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 2013, 14(4):R36. BioMed Central Full Text
• [47]Langmead B, Salzberg SL: Fast gapped-read alignment with Bowtie 2. Nat Methods 2012, 9(4):357-359.
• [48]Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L: Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 2012, 7(3):562-578.
• [49]Griffiths-Jones S, Grocock RJ, van Dongen S, Bateman A, Enright AJ: miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 2006, 34:D140-D144.
• [50]Wang WC, Lin FM, Chang WC, Lin KY, Huang HD, Lin NS: miRExpress: Analyzing high-throughput sequencing data for profiling microRNA expression. BMC Bioinformatics 2009, 10:328. BioMed Central Full Text
• [51]Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I: Controlling the false discovery rate in behavior genetics research. Behav Brain Res 2001, 125(1–2):279-284.
• [52]Kheradpour P, Stark A, Roy S, Kellis M: Reliable prediction of regulator targets using 12 Drosophila genomes. Genome Res 2007, 17(12):1919-1931.
• [53]Schnall-Levin M, Zhao Y, Perrimon N, Berger B: Conserved microRNA targeting in Drosophila is as widespread in coding regions as in 3ʹUTRs. Proc Natl Acad Sci U S A 2010, 107(36):15751-15756.
• [54]Egelhofer TA, Minoda A, Klugman S, Lee K, Kolasinska-Zwierz P, Alekseyenko AA, Cheung MS, Day DS, Gadel S, Gorchakov AA, Gu T, Kharchenko PV, Kuan S, Latorre I, Linder-Basso D, Luu Y, Ngo Q, Perry M, Rechtsteiner A, Riddle NC, Schwartz YB, Shanower GA, Vielle A, Ahringer J, Elgin SC, Kuroda MI, Pirrotta V, Ren B, Strome S, Park PJ, et al.: An assessment of histone-modification antibody quality. Nat Struct Mol Biol 2011, 18(1):91-93.
• [55]Feng J, Liu T, Qin B, Zhang Y, Liu XS: Identifying ChIP-seq enrichment using MACS. Nat Protoc 2012, 7(9):1728-1740.
• [56]da Huang W, Sherman BT, Lempicki RA: Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4(1):44-57.