Germline-dependent Gene Expression in Distant Non-gonadal Somatic Tissues of Drosophila

Overview

Journal BMC Genomics

Publisher Biomed Central

Specialty Genetics

Date 2010 Jun 3

PMID 20515475

Citations 19

Authors

Michael J Parisi

Vaijayanti Gupta

David Sturgill

James T Warren

Jean-Marc Jallon

John H Malone

Yu Zhang

Lawrence I Gilbert

Brian Oliver

Affiliations

Soon will be listed here.

Abstract

Background: Drosophila females commit tremendous resources to egg production and males produce some of the longest sperm in the animal kingdom. We know little about the coordinated regulation of gene expression patterns in distant somatic tissues that support the developmental cost of gamete production.

Results: We determined the non-gonadal gene expression patterns of Drosophila females and males with or without a germline. Our results show that germline-dependent expression in the non-gonadal soma is extensive. Interestingly, gene expression patterns and hormone titers are consistent with a hormone axis between the gonads and non-gonadal soma.

Conclusions: The germline has a long-range influence on gene expression in the Drosophila sexes. We suggest that this is the result of a germline/soma hormonal axis.

Citing Articles

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References

Beissbarth T, Speed T . GOstat: find statistically overrepresented Gene Ontologies within a group of genes. Bioinformatics. 2004; 20(9):1464-5. DOI: 10.1093/bioinformatics/bth088. View

Barnes A, Wigby S, Boone J, Partridge L, Chapman T . Feeding, fecundity and lifespan in female Drosophila melanogaster. Proc Biol Sci. 2008; 275(1643):1675-83. PMC: 2452982. DOI: 10.1098/rspb.2008.0139. View

Edgar R, Domrachev M, Lash A . Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2001; 30(1):207-10. PMC: 99122. DOI: 10.1093/nar/30.1.207. View

Bult C, Eppig J, Kadin J, Richardson J, Blake J . The Mouse Genome Database (MGD): mouse biology and model systems. Nucleic Acids Res. 2007; 36(Database issue):D724-8. PMC: 2238849. DOI: 10.1093/nar/gkm961. View

Arbeitman M, Fleming A, Siegal M, Null B, Baker B . A genomic analysis of Drosophila somatic sexual differentiation and its regulation. Development. 2004; 131(9):2007-21. DOI: 10.1242/dev.01077. View

Miura S, Gan J, Brzostowski J, Parisi M, Schultz C, Londos C . Functional conservation for lipid storage droplet association among Perilipin, ADRP, and TIP47 (PAT)-related proteins in mammals, Drosophila, and Dictyostelium. J Biol Chem. 2002; 277(35):32253-7. DOI: 10.1074/jbc.M204410200. View

Kadener S, Villella A, Kula E, Palm K, Pyza E, Botas J . Neurotoxic protein expression reveals connections between the circadian clock and mating behavior in Drosophila. Proc Natl Acad Sci U S A. 2006; 103(36):13537-42. PMC: 1557390. DOI: 10.1073/pnas.0605962103. View

Bauer M, Katzenberger J, Hamm A, Bonaus M, Zinke I, Jaekel J . Purine and folate metabolism as a potential target of sex-specific nutrient allocation in Drosophila and its implication for lifespan-reproduction tradeoff. Physiol Genomics. 2006; 25(3):393-404. DOI: 10.1152/physiolgenomics.00009.2006. View

Spradling A . Stem cells and their progeny respond to nutritional changes during Drosophila oogenesis. Dev Biol. 2001; 231(1):265-78. DOI: 10.1006/dbio.2000.0135. View

10.

Cui X, Hwang J, Qiu J, Blades N, Churchill G . Improved statistical tests for differential gene expression by shrinking variance components estimates. Biostatistics. 2004; 6(1):59-75. DOI: 10.1093/biostatistics/kxh018. View

11.

Wolfinger R, GIBSON G, Wolfinger E, Bennett L, Hamadeh H, Bushel P . Assessing gene significance from cDNA microarray expression data via mixed models. J Comput Biol. 2001; 8(6):625-37. DOI: 10.1089/106652701753307520. View

12.

Hochberg Y, Benjamini Y . More powerful procedures for multiple significance testing. Stat Med. 1990; 9(7):811-8. DOI: 10.1002/sim.4780090710. View

13.

Bownes M, Scott A, Shirras A . Dietary components modulate yolk protein gene transcription in Drosophila melanogaster. Development. 1988; 103(1):119-28. DOI: 10.1242/dev.103.1.119. View

14.

Parisi M, Nuttall R, Edwards P, Minor J, Naiman D, Lu J . A survey of ovary-, testis-, and soma-biased gene expression in Drosophila melanogaster adults. Genome Biol. 2004; 5(6):R40. PMC: 463073. DOI: 10.1186/gb-2004-5-6-r40. View

15.

. The FlyBase database of the Drosophila Genome Projects and community literature. Nucleic Acids Res. 1998; 27(1):85-8. PMC: 148103. DOI: 10.1093/nar/27.1.85. View

16.

Fujii S, Amrein H . Genes expressed in the Drosophila head reveal a role for fat cells in sex-specific physiology. EMBO J. 2002; 21(20):5353-63. PMC: 129088. DOI: 10.1093/emboj/cdf556. View

17.

McGraw L, Gibson G, Clark A, Wolfner M . Genes regulated by mating, sperm, or seminal proteins in mated female Drosophila melanogaster. Curr Biol. 2004; 14(16):1509-14. DOI: 10.1016/j.cub.2004.08.028. View

18.

Lyne R, Smith R, Rutherford K, Wakeling M, Varley A, Guillier F . FlyMine: an integrated database for Drosophila and Anopheles genomics. Genome Biol. 2007; 8(7):R129. PMC: 2323218. DOI: 10.1186/gb-2007-8-7-r129. View

19.

Akam M, Carlson J . The detection of Jonah gene transcripts in Drosophila by in situ hybridization. EMBO J. 1985; 4(1):155-61. PMC: 554164. DOI: 10.1002/j.1460-2075.1985.tb02330.x. View

20.

Parisi M, Nuttall R, Naiman D, Bouffard G, Malley J, Andrews J . Paucity of genes on the Drosophila X chromosome showing male-biased expression. Science. 2003; 299(5607):697-700. PMC: 1363366. DOI: 10.1126/science.1079190. View