Genetic variation in the gene foraging (for) is associated with a natural behavioral dimorphism in the fruit fly, Drosophila melanogaster. Some larvae, called ‘rovers’, have increased foraging locomotion compared to others, called ‘sitters’, and this difference is directly related to for-encoded cGMP-dependent protein kinase (PKG) activity. Here we report that larvae with mutations in the gene dgcα1, which encodes a soluble guanylyl cyclase (sGC) subunit, have increases in both PKG activity and foraging locomotion. This is contrary to our original prediction that, based on the role of sGC in the synthesis of cGMP, dgcα1 mutant larvae would have deficient cGMP production leading to decreased PKG activation and thus reduced larval foraging locomotion. We performed DNA microarray analyses to compare transcriptional changes induced by a dgcα1 mutation in both rover and sitter wildtype genetic backgrounds. In either background, we identified many genes that are differentially transcribed, and interestingly, relatively few are affected in both backgrounds. Furthermore, several of these commonly affected genes are enhanced or suppressed in a background-dependent manner. Thus, genetic background has a critical influence on the molecular effects of this mutation. These findings will support future investigations of Drosophila foraging behavior.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
R. R. Anholt T. F. C. Mackay (2004) ArticleTitleQuantitative genetic analyses of complex behaviours in Drosophila Nat. Rev. Genet. 5 838–849 Occurrence Handle15520793 Occurrence Handle1:CAS:528:DC%2BD2cXptFenurk%3D
E. E. Ball J. W. Truman (1998) ArticleTitleDeveloping grasshopper neurons show variable levels of guanylyl cyclase activity on arrival at their targets J. Comp. Neurol. 394 1–13 Occurrence Handle9550138 Occurrence Handle1:CAS:528:DyaK1cXitlSis7Y%3D
H. R. Bourne R. Nicoll (1993) ArticleTitleMolecular machines integrate coincident synaptic signals Cell 72 IssueIDSuppl 65–75 Occurrence Handle8094038
J. E. Casnellie (1991) ArticleTitleAssay of protein kinases using peptides with basic residues for phosphocellulose binding Methods Enzymol. 200 115–120 Occurrence Handle1956315 Occurrence Handle1:CAS:528:DyaK3MXmsFSksLc%3D
B. H. Cheung F. Arellano-Carbajal I. Rybicki M. De Bono (2004) ArticleTitleSoluble guanylate cyclases act in neurons exposed to the body fluid to promote C. elegans aggregation behavior Curr. Biol. 14 1105–1111 Occurrence Handle15203005 Occurrence Handle1:CAS:528:DC%2BD2cXltVOgtbs%3D
J. S. de Belle M. Heisenberg (1996) ArticleTitleExpression of Drosophila mushroom body mutations in alternative genetic backgrounds: a case study of the mushroom body miniature gene (mbm) Proc. Natl. Acad. Sci. USA 93 9875–9880 Occurrence Handle8790424 Occurrence Handle1:CAS:528:DyaK28XlsFehtbc%3D
J. S. de Belle A. J. Hilliker M. B. Sokolowski (1989) ArticleTitleGenetic localization of foraging (for): a major gene for larval behavior in Drosophila melanogaster Genetics 123 157–163 Occurrence Handle2509284 Occurrence Handle1:STN:280:DyaK3c%2FjsVWisg%3D%3D
P. Drain E. Folkers W. G. Quinn (1991) ArticleTitlecAMP-dependent protein kinase and the disruption of learning in transgenic flies Neuron 6 71–82 Occurrence Handle1702651 Occurrence Handle1:CAS:528:DyaK3MXkt1KnsLw%3D
J. Dubnau T. Tully (1998) ArticleTitleGene discovery in Drosophila: new Insights for Learning and Memory Annu. Rev. Neurosci. 21 407–444 Occurrence Handle9530502 Occurrence Handle1:CAS:528:DyaK1cXhsFyhsbc%3D
M. B. Eisen P. T. Spellman P. O. Brown D. Botstein (1998) ArticleTitleCluster analysis and display of genome-wide expression patterns Proc. Natl. Acad. Sci. USA 95 14863–14868 Occurrence Handle9843981 Occurrence Handle1:CAS:528:DyaK1cXotVGmurk%3D
M. R. Elphick I. W. Jones (1998) ArticleTitleLocalization of soluble guanylyl cyclase α-subunit in identified insect neurons Brain Res. 800 174–179 Occurrence Handle9685632 Occurrence Handle1:CAS:528:DyaK1cXksVyqs7s%3D
R. R. Fiscus F. Murad (1988) ArticleTitlecGMP-dependent protein kinase activation in intact tissues Methods Enzymol. 159 150–159 Occurrence Handle10.1016/0076-6879(88)59016-X Occurrence Handle2970577 Occurrence Handle1:CAS:528:DyaL1cXmtVOju7w%3D
D. L. Garbers (1999) ArticleTitleThe guanylyl cyclase receptors Methods 19 477–484 Occurrence Handle10581147 Occurrence Handle1:CAS:528:DyaK1MXns1SksLw%3D
R. Gerlai (1996) ArticleTitleGene-targeting studies of mammalian behavior: is it the mutations or the background genotype? Trends Neurosci. 19 177–181 Occurrence Handle8723200 Occurrence Handle1:CAS:528:DyaK28Xislagsr0%3D
S. M. Gibbs A. Becker R. W. Hardy J. W. Truman (2001) ArticleTitleSoluble guanylate cyclase is required during development for visual system function in Drosophila J. Neurosci. 21 7705–7714 Occurrence Handle11567060 Occurrence Handle1:STN:280:DC%2BD3MritVShsQ%3D%3D
B. S. Gim J. M. Park J. H. Yoon C. Kang Y. J. Kim (2001) ArticleTitleDrosophila Med6 is required for elevated expression of a large but distinct set of developmentally regulated genes Mol. Cell. Biol. 21 5242–5255 Occurrence Handle11438678 Occurrence Handle1:CAS:528:DC%2BD3MXlsVGitbc%3D
S. A. Graf M. B. Sokolowski (1989) ArticleTitleRover/sitter Drosophila melanogaster larval foraging polymorphism as a function of larval development, food-patch quality, and starvation J. Insect Behav. 2 301–313
J. M. Gray D. S. Karow H. Lu A. J. Chang J. S. Chang R. E. Ellis M. A. Marletta C. I. Bargmann (2004) ArticleTitleOxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue Nature 430 317–322 Occurrence Handle15220933 Occurrence Handle1:CAS:528:DC%2BD2cXls1eqs7Y%3D
R. J. Greenspan (1997) ArticleTitleA kinder, gentler genetic analysis of behavior: dissection gives way to modulation Curr. Opin. Neurobiol. 7 805–811 Occurrence Handle9464983 Occurrence Handle1:CAS:528:DyaK1cXpsFGhsQ%3D%3D
J. G. Hardman E. W. Sutherland (1969) ArticleTitleGuanyl Cyclase, an enzyme catalyzing the formation of guanosine 3′,5′-monophosphate from guanosine triphosphate J. Biol. Chem. 244 6363–6370 Occurrence Handle4982201 Occurrence Handle1:CAS:528:DyaE3cXhvVKitA%3D%3D
W. Jin R. M. Riley R. D. Wolfinger K. P. White G. Passador-Gurgel G. Gibson (2001) ArticleTitleThe contributions of sex, genotype and age to transcriptional variance in Drosophila melanogaster Nat. Genet. 29 389–395 Occurrence Handle11726925 Occurrence Handle1:CAS:528:DC%2BD3MXovFarsbg%3D
D. Kalderon G. M. Rubin (1989) ArticleTitlecGMP-dependent protein kinase genes in Drosophila J. Biol. Chem. 264 10738–10748 Occurrence Handle2732245 Occurrence Handle1:CAS:528:DyaK3cXhtlentL4%3D
D. Koesling (1998) ArticleTitleModulators of soluble guanylyl cyclase Naunyn Schmiedebergs Arch. Pharmacol. 358 123–126 Occurrence Handle9721013 Occurrence Handle1:CAS:528:DyaK1cXktlyisLg%3D
D. Koesling M. Russwurm E. Mergia F. Mullershausen A. Friebe (2004) ArticleTitleNitric oxide-sensitive guanylyl cyclase: structure and regulation Neurochem. Int. 45 813–819 Occurrence Handle15312975 Occurrence Handle1:CAS:528:DC%2BD2cXmslOiurs%3D
S. C. LaGraize J. Borzan M. M. Rinker J. L. Kopp P. N. Fuchs (2004) ArticleTitleBehavioral evidence for competing motivational drives of nociception and hunger Neurosci. Lett. 372 30–34 Occurrence Handle15531083 Occurrence Handle1:CAS:528:DC%2BD2cXpsFWhs74%3D
K. K. Langlais J. A. Stewart D. B. Morton (2004) ArticleTitlePreliminary characterization of two atypical soluble guanylyl cyclases in the central and peripheral nervous system of Drosophila melanogaster J. Exp. Biol. 207 IssueIDPt 13 2323–2338 Occurrence Handle15159437 Occurrence Handle1:CAS:528:DC%2BD2cXmsl2ltbs%3D
J. Lee S. W. Kim T. K. Jung Y. Oh C. S. Park S. K. Ma N. H. Kim K. C. Choi (2004) ArticleTitleIndomethacin decreases particulate guanylyl cyclase activity in rat kidney Clin. Exp. Pharmacol. Physiol. 31 207–211 Occurrence Handle15053815 Occurrence Handle1:CAS:528:DC%2BD2cXjsFelsbc%3D
D. L. Lindsey G. G. Zimm (1992) The genome of Drosophila Melanogaster Academic Press NY, USA
W. Liu J. Yoon M. Burg L. Chen W. L. Pak (1995) ArticleTitleMolecular characterization of two Drosophila guanylate cyclases expressed in the nervous system J. Biol. Chem. 270 12418–12427 Occurrence Handle7759483 Occurrence Handle1:CAS:528:DyaK2MXlvFOit7o%3D
K. A. Lucas G. M. Pitari S. Kazerounian I. Ruiz-Stewart J. Park S. Schultz K. P. Chepenik S. A. Waldman (2000) ArticleTitleGuanylyl cyclases and signaling by cyclic GMP Pharmacol. Rev. 52 375–413 Occurrence Handle10977868 Occurrence Handle1:CAS:528:DC%2BD3cXntFCmsbg%3D
D. B. Morton (2004a) ArticleTitleInvertebrates yield a plethora of atypical guanylyl cyclases Mol. Neurobiol. 29 97–115 Occurrence Handle1:CAS:528:DC%2BD2cXkslCns7g%3D
D. B. Morton (2004b) ArticleTitleAtypical soluble guanylyl cyclases in Drosophila can function as molecular oxygen sensors J. Biol. Chem. 279 50651–50653 Occurrence Handle1:CAS:528:DC%2BD2cXhtVaru7rP
U. Müller H. Hildebrandt (2002) ArticleTitleNitric oxide/cGMP-mediated protein kinase A activation in the antennal lobes plays an important role in appetitive reflex habituation in the honeybee J. Neurosci. 22 8739–8747 Occurrence Handle12351749
S. J. Neal M. L. Gibson A. K.-C. So J. T. Westwood (2003) ArticleTitleConstruction of a cDNA-based microarray for Drosophila melanogaster: a comparison of gene transcription profiles from SL2 and Kc167 cells Genome 46 879–892 Occurrence Handle14608405 Occurrence Handle1:CAS:528:DC%2BD3sXpsFChtbo%3D
A. Nighorn K. A. Byrnes D. B. Morton (1999) ArticleTitleIdentification and characterization of a novel β subunit of soluble guanylyl cyclase that is active in the absence of a second subunit and is relatively insensitive to nitric oxide J. Biol. Chem. 274 2525–2531 Occurrence Handle9891024 Occurrence Handle1:CAS:528:DyaK1MXovVGqug%3D%3D
A. Nighorn N. J. Gibson D. M. Rivers J. G. Hildebrand D. B Morton (2000) ArticleTitleThe nitric oxide-cGMP pathway may mediate communication between sensory afferents and projection neurons in the antennal lobe of Manduca sexta J. Neurosci. 18 7244–7255
K. A. Osborne A. Robichon E. Burgess S. Butland R. A. Shaw A. Coulthard H. S. Pereira R. J. Greenspan M. B. Sokolowski (1997) ArticleTitleNatural behavior polymorphism due to a cGMP-dependent protein kinase of Drosophila Science 277 834–836 Occurrence Handle9242616 Occurrence Handle1:CAS:528:DyaK2sXlt1ersrw%3D
D. A. Pelligrino Q. Wang (1998) ArticleTitleCyclic nucleotide crosstalk and the regulation of cerebral vasodilation Prog. Neurobiol. 56 1–18 Occurrence Handle9723128 Occurrence Handle1:CAS:528:DyaK1cXlsVOru74%3D
H. S. Pereira D. E. MacDonald A. J. Hilliker M. B. Sokolowski (1995) ArticleTitleChaser (Csr), a new gene affecting larval foraging behavior in Drosophila melanogaster Genetics 141 263–270 Occurrence Handle8536975 Occurrence Handle1:CAS:528:DyaK28Xht1Cmt7w%3D
S. Prabhakar D. B. Short N. L. Scholz M. F. Goy (1997) ArticleTitleIdentification of nitric oxide-sensitive and -insensitive forms of cytoplasmic guanylate cyclase J. Neurochem. 69 1650–1660 Occurrence Handle9326294 Occurrence Handle1:CAS:528:DyaK2sXmsVCksbc%3D Occurrence Handle10.1046/j.1471-4159.1997.69041650.x
C. Ramakers J. M. Ruijter R. H. Lekanne Deprez A. F. M. Moorman (2003) ArticleTitleAssumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data Neurosci. Lett. 339 62–66 Occurrence Handle12618301 Occurrence Handle1:CAS:528:DC%2BD3sXhs1Kks70%3D
A. Redkozubov (2000) ArticleTitleGuanosine 3′,5′-cyclic monophosphate reduces the response of the Moth’s olfactory receptor neuron to pheromone Chem. Senses. 25 381–385 Occurrence Handle10944500 Occurrence Handle1:CAS:528:DC%2BD3cXmsVOmtbo%3D
F. J. Rivero-Vilches S. de Frutos M. Saura D. Rodriguez-Puyol M. Rodriguez-Puyol (2003) ArticleTitleDifferential relaxing responses to particulate or soluble guanylyl cyclase activation on endothelial cells: a mechanism dependent on PKG-I alpha activation by NO/cGMP Am. J. Physiol. Cell Physiol. 285 C891–C898 Occurrence Handle12814915 Occurrence Handle1:CAS:528:DC%2BD3sXosV2rtb8%3D
S. Rozen H. Skaletsky (2000) ArticleTitlePrimer3 on the WWW for general users and for biologist programmers Methods Mol. Biol. 132 365–386 Occurrence Handle10547847 Occurrence Handle1:CAS:528:DyaK1MXmslKqsbo%3D
J. Sambrook D. Russell (2001) Molecular cloning. A laboratory manual EditionNumber3 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY, USA
InstitutionalAuthorNameSAS Institute Inc. (1999) SAS/STAT user’s guide, version 8 SAS Institute Inc Cary, NC
S. Shah D. R. Hyde (1995) ArticleTitleTwo Drosophila genes that encode the α and β subunits of the brain soluble guanylyl cyclase J. Biol. Chem. 270 15368–15376 Occurrence Handle7797526 Occurrence Handle1:CAS:528:DyaK2MXmsFKqtbc%3D
S. A. Shaver C. A. L. Riedl T. L. Parkes M. B. Sokolowski A. J. Hilliker (2000) ArticleTitleIsolation of larval behavioral mutants in Drosophila melanogaster J. Neurogenet. 14 193–205 Occurrence Handle11342381 Occurrence Handle1:CAS:528:DC%2BD3MXktVamu7c%3D
M. B. Sokolowski (1980) ArticleTitleForaging strategies of Drosophila melanogaster: a chromosomal analysis Behav. Genet. 10 291–302 Occurrence Handle6783027 Occurrence Handle1:STN:280:DyaL3M7lvFyrsg%3D%3D
M. B. Sokolowski (2001) ArticleTitleDrosophila: genetics meets behaviour Nat. Rev. Genet. 2 879–890 Occurrence Handle11715043 Occurrence Handle1:CAS:528:DC%2BD38Xmt1Wgtrs%3D
M. B. Sokolowski H. S. Pereira K. Hughes (1997) ArticleTitleEvolution of foraging behavior in Drosophila by density-dependent selection Proc. Natl. Acad. Sci. USA 94 7373–7377 Occurrence Handle9207098 Occurrence Handle1:CAS:528:DyaK2sXksFOmtL0%3D
M .B. Sokolowski C. A. L. Riedl (1999) Behaviour-genetic and molecular analysis of naturally occurring variation in Drosophila larval foraging behaviour R. Gerlai W. Crusio (Eds) Molecular-genetic techniques for brain and behaviour Elsevier Scientific London 517–532
J. R. Stone M. A. Marletta (1994) ArticleTitleSoluble guanylate cyclase from bovine lung: activation with nitric oxide and carbon monoxide and spectral characterization of the ferrous and ferric states Biochemistry 33 5636–5640 Occurrence Handle7910035 Occurrence Handle1:CAS:528:DyaK2cXivFaltr8%3D
J. W. Truman J. De Vente E. E. Ball (1996) ArticleTitleNitric oxide-sensitive guanylate cyclase activity is associated with the maturational phase of neuronal development in insects Development 122 3949–3958 Occurrence Handle9012515 Occurrence Handle1:CAS:528:DyaK2sXhtVOqtLY%3D
T. Tully (1996) ArticleTitleDiscovery of genes involved with learning and memory: an experimental synthesis of Hirschian and Benzerian perspectives Proc. Natl. Acad. Sci. USA 93 13460–13467 Occurrence Handle8942957 Occurrence Handle1:CAS:528:DyaK28Xnt1Gitbs%3D
V. G. Tusher R. Tibshirani G. Chu (2001) ArticleTitleSignificance analysis of microarrays applied to the ionizing radiation response Proc. Natl. Acad. Sci. USA 98 5116–5121 Occurrence Handle11309499 Occurrence Handle1:CAS:528:DC%2BD3MXjt1Ons7w%3D
X. Wang P. J. Robinson (1997) ArticleTitleCyclic GMP-dependent protein kinase and cellular signaling in the nervous system J. Neurochem. 68 443–456 Occurrence Handle9003029 Occurrence Handle1:CAS:528:DyaK2sXot1ynsA%3D%3D Occurrence Handle10.1046/j.1471-4159.1997.68020443.x
B. J. Wedel D. L. Garbers (2001) ArticleTitleThe guanylyl cyclase family at Y2K Annu. Rev. Physiol. 63 215–233 Occurrence Handle11181955 Occurrence Handle1:CAS:528:DC%2BD3MXjtFKmtL0%3D
B. Wildemann G. Bicker (1999a) ArticleTitleDevelopmental expression of nitric oxide/cyclic GMP synthesizing cells in the nervous system of Drosophila melanogaster J. Neurobiol. 38 1–15 Occurrence Handle1:CAS:528:DyaK1MXlsVWgug%3D%3D
B. Wildemann G. Bicker (1999b) ArticleTitleNitric oxide and cyclic GMP induce vesicle release at Drosophila neuromuscular junction J. Neurobiol. 39 337–346 Occurrence Handle1:CAS:528:DyaK1MXjvVCnu7k%3D
S. Yoshikawa I. Miyamoto J. Aruga T. Furuichi H. Okano K. Mikoshiba (1993) ArticleTitleIsolation of a Drosophila gene encoding a head-specific guanylyl cyclase J. Neurochem. 60 1570–1573 Occurrence Handle8095978 Occurrence Handle1:CAS:528:DyaK3sXit12isro%3D
L. Zhang S. Tinette A. Robichon (2002) ArticleTitleDrosophila NO-dependent guanylyl cyclase is finely regulated by sequential order of coincidental signaling J. Cell. Biochem. 85 392–402 Occurrence Handle11948694 Occurrence Handle1:CAS:528:DC%2BD38XivVyqs7o%3D
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Riedl, C.A.L., Neal, S.J., Robichon, A. et al. Drosophila soluble guanylyl cyclase mutants exhibit increased foraging locomotion: behavioral and genomic investigations. Behav Genet 35, 231–244 (2005). https://doi.org/10.1007/s10519-005-3216-1
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s10519-005-3216-1