All Title Author
Keywords Abstract

PLOS Genetics  2009 

The Drosophila foraging Gene Mediates Adult Plasticity and Gene–Environment Interactions in Behaviour, Metabolites, and Gene Expression in Response to Food Deprivation

DOI: 10.1371/journal.pgen.1000609

Full-Text   Cite this paper   Add to My Lib

Abstract:

Nutrition is known to interact with genotype in human metabolic syndromes, obesity, and diabetes, and also in Drosophila metabolism. Plasticity in metabolic responses, such as changes in body fat or blood sugar in response to changes in dietary alterations, may also be affected by genotype. Here we show that variants of the foraging (for) gene in Drosophila melanogaster affect the response to food deprivation in a large suite of adult phenotypes by measuring gene by environment interactions (GEI) in a suite of food-related traits. for affects body fat, carbohydrates, food-leaving behavior, metabolite, and gene expression levels in response to food deprivation. This results in broad patterns of metabolic, genomic, and behavioral gene by environment interactions (GEI), in part by interaction with the insulin signaling pathway. Our results show that a single gene that varies in nature can have far reaching effects on behavior and metabolism by acting through multiple other genes and pathways.

References

[1]  Via S, Gomulkiewicz R, Dejong G, Scheiner SM, Schlichting CD, et al. (1995) Adaptive phenotypic plasticity - consensus and controversy. Trends Ecol Evol 10: 212–217.
[2]  Sarkar S (2004) From the reaktionsnorm to the evolution of adaptive plasticity: A historical sketch, 1909–1999. In: DeWitt TJ, Scheiner SM, editors. Phenotypic plasticity - functional and conceptual approaches. New York: Oxford University Press. pp. 10–30.
[3]  Windig JJ, de Kovel CGF, de Jong G (2004) Genetics and mechanics of plasticity. In: DeWitt TJ, Scheiner SM, editors. Phenotypic plasticity: Functional and conceptual approaches. New York, N.Y.: Oxford University Press. pp. 31–49.
[4]  Via S, Lande R (1985) Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution 39: 505–522.
[5]  Gutteling EW, Riksen JA, Bakker J, Kammenga JE (2007) Mapping phenotypic plasticity and genotype-environment interactions affecting life-history traits in Caenorhabditis elegans. Heredity 98: 28.
[6]  Sambandan D, Carbone MA, Anholt RRH, Mackay TFC (2008) Phenotypic plasticity and genotype by environment interaction for olfactory behavior in Drosophila melanogaster. Genetics 179: 1079–1088.
[7]  Kalderon D, Rubin GM (1989) cGMP-dependent Protein Kinase genes in Drosophila. J Biol Chem 264: 10738–10748.
[8]  Osborne KA (1997) Natural behavior polymorphism due to a cGMP-dependent Protein Kinase of Drosophila. Science 277: 834–836.
[9]  de Belle JS, Hilliker AJ, Sokolowski MB (1989) Genetic localization of foraging (for): A major gene for larval behavior in Drosophila melanogaster. Genetics 123: 157–164.
[10]  de Belle JS, Sokolowski MB, Hilliker AJ (1993) Genetic analysis of the foraging microregion of Drosophila melanogaster. Genome 36: 94–101.
[11]  Kaun KR, Riedl CAL, Chakaborty-Chatterjee M, Belay AT, Douglas SJ, et al. (2007) Natural variation in food acquisition mediated via a Drosophila cGMP-dependent Protein Kinase. J Exp Biol 210: 3547–3558.
[12]  Graf SA, Sokolowski MB (1989) The rover/sitter Drosophila foraging polymorphism as a function of larval development, food patch quality and starvation. J Insect Behav 2: 301–313.
[13]  Pereira HS, Sokolowski MB (1993) Mutations in the larval foraging gene affect adult locomotory behavior after feeding in Drosophila melanogaster. Proc Natl Acad Sci USA 90: 5044–5046.
[14]  Scheiner R, Sokolowski MB, Erber J (2004) Activity of cGMP-dependent Protein Kinase (PKG) affects sucrose responsiveness and habituation in Drosophila melanogaster. Learn Mem 11: 303–311.
[15]  Belay AT, Scheiner R, So AKC, Douglas SJ, Chakaborty-Chatterjee M, et al. (2007) The foraging gene of Drosophila melanogaster: Spatial-expression analysis and sucrose responsiveness. J Comp Neurol 504: 570–582.
[16]  Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, et al. (2003) DAVID: Database for annotation, visualization, and integrated discovery. Genome Biol 4: P3.
[17]  Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci USA 100: 9440–9445.
[18]  Grewal SS (2009) Insulin/Tor signaling in growth and homeostasis: A view from the fly world. Int J Biochem Cell Biol 41: 1006–1010.
[19]  Wu Q, Brown MR (2006) Signaling and function of insulin-like peptides in insects. Annu Rev Entomol 51: 1–24.
[20]  Radimerski T, Montagne J, Rintelen F, Stocker H, van der Kaay J, et al. (2002) dS6K-regulated cell growth is dPKB/dPI(3)K-independent, but requires dPDK1. Nat Cell Biol 4: 251–255.
[21]  Rintelen F, Stocker H, Thomas G, Hafen E (2001) PDK1 regulates growth through Akt1 and S6k in Drosophila. Proc Natl Acad Sci USA 98: 15020–15025.
[22]  Junger MA, Rintelen F, Stocker H, Wasserman JD, Vegh M, et al. (2003) The Drosophila forkhead transcription factor foxo mediates the reduction in cell number associated with reduced insulin signaling. J Biol 2: 2–17.
[23]  Puig O, Marr MT, Ruhf ML, Tjian R (2003) Control of cell number by Drosophila foxo: Downstream and feedback regulation of the insulin receptor pathway. Genes Dev 17: 2006–2020.
[24]  Puig O, Tjian R (2005) Transcriptional feedback control of insulin receptor by dfoxo/foxo1. Genes Dev 19: 2435–2446.
[25]  Williams KD, Busto M, Suster ML, So AKC, Ben-Shahar Y, et al. (2006) Natural variation in Drosophila melanogaster diapause due to the insulin-regulated PI3-kinase. Proc Natl Acad Sci USA 103: 15911–15915.
[26]  Gibson G, Dworkin I (2004) Uncovering cryptic genetic variation. Nat Rev Genet 5: 681–690.
[27]  Mackay TF (2001) Quantitative trait loci in Drosophila. Nat Rev Genet 2: 11–20.
[28]  Buch S, Melcher C, Bauer M, Katzenberger J, Pankratz MJ (2008) Opposing effects of dietary protein and sugar regulate a transcriptional target of Drosophila insulin-like peptide signaling. Cell Metab 7: 321–332.
[29]  Gershman B, Puig O, Hang L, Peitzsch RM, Tatar M, et al. (2007) High-resolution dynamics of the transcriptional response to nutrition in Drosophila: A key role for dfoxo. Physiol Genomics 29: 24–34.
[30]  Guertin DA, Guntur KVP, Bell GW, Thoreen CC, Sabatini DM (2006) Functional genomics identifies Tor-regulated genes that control growth and division. Curr Biol 16: 958–970.
[31]  Engel JE, Xie XJ, Sokolowski MB, Wu CF (2000) A cGMP-dependent protein kinase gene, foraging, modifies habituation-like response decrement of the giant fiber escape circuit in Drosophila. Learn Mem 7: 341–352.
[32]  Mery F, Belay AT, Sokolowski MB, Kawecki TJ (2006) Antagonistic effects of natural polymorphism at the foraging locus on short-term learning and long-term memory. J Neurogenet 20: 177–177.
[33]  Kaun KR, Hendel T, Gerber B, Sokolowski MB (2007) Natural variation in Drosophila larval reward learning and memory due to a cGMP-dependent protein kinase. Learn Mem 14: 342–349.
[34]  Mery F, Belay AT, So AK, Sokolowski MB, Kawecki TJ (2007) Natural polymorphism affecting learning and memory in Drosophila. Proc Natl Acad Sci USA 104: 13051–13055.
[35]  Kaun KR, Riedl CAL, Chakaborty-Chatterjee M, Belay AT, Douglas SJ, et al. (2008) Natural variation in plasticity of glucose homeostasis and food intake. J Exp Biol 211: 3160–3166.
[36]  Fitzpatrick MJ, Sokolowski MB (2004) In search of food: Exploring the evolutionary link between cGMP-dependent protein kinase (PKG) and behaviour. Integr Comp Biol 44: 28–36.
[37]  You YJ, Kim J, Raizen DM, Avery L (2008) Insulin, cGMP, and TGF-beta signals regulate food intake and quiescence in C. elegans: A model for satiety. Cell Metab 7: 249–257.
[38]  Gray JM (2004) Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue. Nature 430: 317–322.
[39]  Ben-Shahar Y, Leung HT, Pak WL, Sokolowski MB, Robinson GE (2003) cGMP-dependent changes in phototaxis: A possible role for the foraging gene in honey bee division of labor. J Exp Biol 206: 2507–2515.
[40]  Ingram KK, Oefner P, Gordon DM (2005) Task-specific expression of the foraging gene in harvester ants. Mol Ecol 14: 813–818.
[41]  Lucas C, Sokolowski MB (2009) Molecular basis for changes in behavioral state in ant social behaviors. Proc Natl Acad Sci USA 106: 6351–6356.
[42]  Lasko P, Sonenberg N (2007) Coordinated transcriptional and translational control in metabolic homeostasis in flies. Genes Dev 21: 235–237.
[43]  Ceddia RB, Bikopoulos GJ, Hilliker AJ, Sweeney G (2003) Insulin stimulates glucose metabolism via the pentose phosphate pathway in Drosophila Kc cells. FEBS Letters 555: 307–310.
[44]  Teleman AA, Chen YW, Cohen SM (2005) Drosophila melted modulates foxo and Tor activity. Dev Cell 9: 271–281.
[45]  Brogiolo W, Stocker H, Ikeya T, Rintelen F, Fernandez R, et al. (2001) An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control. Curr Biol 11: 213–221.
[46]  Bohni R, Riesgo-Escovar J, Oldham S, Brogiolo W, Stocker H, et al. (1999) Autonomous control of cell and organ size by chico, a Drosophila homolog of vertebrate IRS1-4. Cell 97: 865–875.
[47]  Britton JS, Lockwood WK, Li L, Cohen SM, Edgar BA (2002) Drosophila's insulin/PI3-Kinase pathway coordinates cellular metabolism with nutritional conditions. Dev Cell 2: 239–249.
[48]  Kramer JM, Davidge JT, Lockyer JM, Staveley BE (2003) Expression of Drosophila foxo regulates growth and can phenocopy starvation. BMC Dev Biol 3: 1–14.
[49]  Hwangbo DS, Gershman B, Tu MP, Palmer M, Tatar M (2004) Drosophila dfoxo controls lifespan and regulates insulin signalling in brain and fat body. Nature 429: 562–566.
[50]  Cohen P, Alessi DR, Cross DA (1997) PDK1, one of the missing links in insulin signal transduction? FEBS Letters 410: 3–10.
[51]  Nayar JK, Vanhande E (1971) Fuel for sustained mosquito flight. J Insect Physiol 17: 471–5.
[52]  Rowley WA (1970) Interval flights and glycogen utilization by mosquito Culex tarsalis. J Insect Physiol 16: 1839–&.
[53]  Wigglesworth VB (1949) The utilization of reserve substances in Drosophila during flight. J Exp Biol 26: 150–163.
[54]  Gade G, Auerswald L (2003) Mode of action of neuropeptides from the adipokinetic hormone family. Gen Comp Endocrinol 132: 10.
[55]  Graves JL, Toolson EC, Jeong C, Vu LN, Rose MR (1992) Desiccation, flight, glycogen, and postponed senescence in Drosophila melanogaster. Physiol Zool 65: 268–286.
[56]  Gibbs AG, Chippindale AK, Rose MR (1997) Physiological mechanisms of evolved desiccation resistance in Drosophila melanogaster. J Exp Biol 200: 1821–1832.
[57]  Hoffmann AA, Parsons PA (1989) Selection for increased desiccation resistance in Drosophila melanogaster: Additive genetic control and correlated responses for other stresses. Genetics 122: 837.
[58]  Hoffmann AA, Harshman LG (1999) Desiccation and starvation resistance in Drosophila: Patterns of variation at the species, population and intrapopulation levels. Heredity 83(Pt 6): 637.
[59]  Ballard JWO, Melvin RG, Simpson SJ (2008) Starvation resistance is positively correlated with body lipid proportion in five wild caught drosophila simulans populations. J Insect Physiol 54: 1371–1376.
[60]  Zhao Z, Zera AJ (2002) Differential lipid biosynthesis underlies a tradeoff between reproduction and flight capability in a wing-polymorphic cricket. Proc Natl Acad Sci USA 99: 16829–16834.
[61]  Zera AJ, Zhao Z (2003) Morph-dependent fatty acid oxidation in a wing-polymorphic cricket: implications for the trade-off between dispersal and reproduction. J Insect Physiol 49: 933–943.
[62]  Houle D (1991) Genetic covariance of fitness correlates: What genetic correlations are made of and why it matters. Evolution 45: 630–648.
[63]  Ota KT, Pierre VJ, Ploski JE, Queen K, Schafe GE (2008) The NO-cGMP-PKG signaling pathway regulates synaptic plasticity and fear memory consolidation in the lateral amygdala via activation of ERK/MAP Kinase. Learn Mem 15: 792–805.
[64]  Feil R, Hofmann F, Kleppisch T (2005) Function of cGMP-dependent protein kinases in the nervous system. Rev Neurosci 16: 23–41.
[65]  Liu S, Rao Y, Daw N (2003) Roles of Protein Kinase A and Protein Kinase G in synaptic plasticity in the visual cortex. Cereb Cortex 13: 864–869.
[66]  Wang X, Robinson P (1997) Cyclic GMP-dependent protein kinase and cellular signaling in the nervous system. J Neurochem 68: 443–456.
[67]  Dostmann WR, Tegge W, Frank R, Nickl CK, Taylor MS, et al. (2002) Exploring the mechanisms of vascular smooth muscle tone with highly specific, membrane-permeable inhibitors of cyclic GMP-dependent Protein Kinase I-alpha. Pharmacol Ther 93: 203–215.
[68]  Stuart JM, Segal E, Koller D, Kim SK (2003) A gene-coexpression network for global discovery of conserved genetic modules. Science 302: 249–255.
[69]  Engel JE, Wu CF (1996) Altered habituation of an identified escape circuit in Drosophila memory mutants. J Neurosci 16: 3486–3499.
[70]  Engel JE, Wu CF (1998) Genetic dissection of functional contributions of specific potassium channel subunits in habituation of an escape circuit in Drosophila. J Neurosci 18: 2254–2267.
[71]  Renger JJ, Yao WD, Sokolowski MB, Wu CF (1999) Neuronal polymorphism among natural alleles of a cGMP-dependent kinase gene, foraging, in drosophila. J Neurosci 19: RC28.
[72]  Dawson-Scully K, Armstrong GA, Kent C, Robertson RM, Sokolowski MB (2007) Natural variation in the thermotolerance of neural function and behavior due to a cGMP-dependent protein kinase. PLoS ONE 2: e773. doi:10.1371/journal.pone.0000773.
[73]  Greenspan RJ (2001) The flexible genome. Nature Rev Genet 2: 383–387.
[74]  Featherstone DE, Broadie K (2002) Wrestling with pleiotropy: genomic and topological analysis of the yeast gene expression network. BioEssays 24: 267–274.
[75]  van Swinderen B, Greenspan RJ (2005) Flexibility in a gene network affecting a simple behavior in Drosophila melanogaster. Genetics 169: 2151–2163.
[76]  Promislow DE (2004) Protein networks, pleiotropy and the evolution of senescence. Proc Biol Sci 271: 1225–1234.
[77]  Benfey PN, Mitchell-Olds T (2008) From genotype to phenotype: systems biology meets natural variation. Science 320: 495–497.
[78]  Greenspan RJ (1997) A kinder, gentler genetic analysis of behavior: Dissection gives way to modulation. Curr Opin Neurobiol 7: 805–811.
[79]  Fitzpatrick MJ, Feder E, Rowe L, Sokolowski MB (2007) Maintaining a behaviour polymorphism by frequency-dependent selection on a single gene. Nature 447: 210–212.
[80]  Toma DP, White KP, Hirsch J, Greenspan RJ (2002) Identification of genes involved in Drosophila melanogaster geotaxis, a complex behavioral trait. Nat Genet 31: 349–353.
[81]  Oldham S, Stocker H, Laffargue M, Wittwer F, Wymann M, et al. (2002) The Drosophila insulin/IGF receptor controls growth and size by modulating PTDinsP(3) levels. Development 129: 4103–4109.
[82]  Clancy DJ, Gems D, Harshman LG, Oldham S, Stocker H, et al. (2001) Extension of life-span by loss of chico, a Drosophila insulin receptor substrate protein. Science 292: 104–106.
[83]  Weinkove D, Neufeld TP, Twardzik T, Waterfield MD, Leevers SJ (1999) Regulation of imaginal disc cell size, cell number and organ size by Drosophila class I(a) Phosphoinositide 3-Kinase and its adaptor. Curr Biol 9: 1019–1029.
[84]  Zulak KG, Cornish A, Daskalchuk TE, Deyholos MK, Goodenowe DB, et al. (2007) Gene transcript and metabolite profiling of Elicitor-induced opium poppy cell cultures reveals the coordinate regulation of primary and secondary metabolism. Planta 225: 1085–1106.
[85]  Gray GR, Heath D (2005) A global reorganization of the metabolome in Arabidopsis during cold acclimation is revealed by metabolic fingerprinting. Physiol Plantarum 124: 236–248.
[86]  Kanehisa M, Goto S, Hattori M, Aoki-Kinoshita KF, Itoh M, et al. (2006) From genomics to chemical genomics: new developments in KEGG. Nucl Acids Res 34: D354–D357.
[87]  Smith CA, O'Maille G, Want EJ, Qin C, Trauger SA, et al. (2005) Metlin: A metabolite mass spectral database. Ther Drug Monit 27: 747–751.
[88]  Clark AG (1989) Causes and consequences of variation in energy storage in Drosophila melanogaster. Genetics 123: 131–144.
[89]  Kunst A, et al. (1984) Metabolites 1: Carbohydrates. In: Bergmeyer HU, editor. Weinheim: Verlag Chemie. 163p p. 3rd – ed.
[90]  Dierick HA, Greenspan RJ (2006) Molecular analysis of flies selected for aggressive behavior. Nat Genet 38: 1023–1031.
[91]  Bolstad BM, Irizarry RA, Astrand M, Speed TP (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185–193.
[92]  Schwarz G (1978) Estimating the dimension of a model. Ann Statist 6: 461–464.

Full-Text

comments powered by Disqus