A Variant in the Neuropeptide Receptor npr-1 is a Major Determinant of Caenorhabditis elegans Growth and Physiology

PLoS Genetics

Volumn 10, Issue 2, 2014, Pages

  Andersen, Erik C ^a,d   Bloom, Joshua S ^a,b   Gerke, Justin P ^a,e   Kruglyak, Leonid ^b,c  

^a PRINCETON UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d NORTHWESTERN UNIVERSITY   (United States)

^e DUPONT COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROPEPTIDE RECEPTOR; CAENORHABDITIS ELEGANS PROTEIN; NEUROPEPTIDE; NEUROPEPTIDE Y RECEPTOR; NPR-1 PROTEIN, C ELEGANS;

ADULT; ALLELE; ARTICLE; BODY SIZE; CAENORHABDITIS ELEGANS; CELL STRAIN; FERTILITY; FOOD INTAKE; GENE; GENE EXPRESSION; GENETIC VARIABILITY; GROWTH RATE; INFECTION SENSITIVITY; NEMATODE LIFE CYCLE STAGE; NONHUMAN; NPR 1 GENE; OXYGEN CONCENTRATION; PHENOTYPE; PHENOTYPIC VARIATION; PROGENY; QUANTITATIVE TRAIT LOCUS; STAPHYLOCOCCUS AUREUS; STARVATION; SURVIVAL; ANIMAL; FEMALE; GENETIC VARIATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; MICROBIOLOGY; MUTATION; PATHOGENICITY;

ALLELES; ANIMALS; BODY SIZE; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; FEMALE; FERTILITY; GENETIC VARIATION; HUMANS; MUTATION; NEUROPEPTIDES; QUANTITATIVE TRAIT LOCI; RECEPTORS, NEUROPEPTIDE Y; STAPHYLOCOCCUS AUREUS;

EID: 84901740617     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004156     Document Type: Article

References (53)

1. Rockman MV, Skrovanek SS, Kruglyak L, (2010) Selection at linked sites shapes heritable phenotypic variation in C. elegans. Science 330: 372-376 doi:10.1126/science.1194208.
2. Seidel HS, Ailion M, Li J, van Oudenaarden A, Rockman MV, et al. (2011) A novel sperm-delivered toxin causes late-stage embryo lethality and transmission ratio distortion in C. elegans. Plos Biol 9: e1001115 doi:10.1371/journal.pbio.1001115.
3. Seidel HS, Rockman MV, Kruglyak L, (2008) Widespread genetic incompatibility in C. elegans maintained by balancing selection. Science 319: 589-594 doi:10.1126/science.1151107.
4. Ghosh R, Andersen EC, Shapiro JA, Gerke JP, Kruglyak L, (2012) Natural variation in a chloride channel subunit confers avermectin resistance in C. elegans. Science 335: 574-578 doi:10.1126/science.1214318.
5. Bendesky A, Tsunozaki M, Rockman MV, Kruglyak L, Bargmann CI, (2011) Catecholamine receptor polymorphisms affect decision-making in C. elegans. Nature 472: 313-318 doi:10.1038/nature09821.
6. Palopoli MF, Rockman MV, TinMaung A, Ramsay C, Curwen S, et al. (2008) Molecular basis of the copulatory plug polymorphism in Caenorhabditis elegans. Nature 454: 1019-1022 doi:10.1038/nature07171.
7. McGrath PT, Rockman MV, Zimmer M, Jang H, Macosko EZ, et al. (2009) Quantitative mapping of a digenic behavioral trait implicates globin variation in C. elegans sensory behaviors. Neuron 61: 692-699 doi:10.1016/j.neuron.2009.02.012.
8. Reddy KC, Andersen EC, Kruglyak L, Kim DH, (2009) A polymorphism in npr-1 is a behavioral determinant of pathogen susceptibility in C. elegans. Science 323: 382-384 doi:10.1126/science.1166527.
9. Glauser DA, Chen WC, Agin R, Macinnis BL, Hellman AB, et al. (2011) Heat avoidance is regulated by transient receptor potential (TRP) channels and a neuropeptide signaling pathway in Caenorhabditis elegans. Genetics 188: 91-103 doi:10.1534/genetics.111.127100.
10. Duveau F, Félix M-A, (2012) Role of pleiotropy in the evolution of a cryptic developmental variation in Caenorhabditis elegans. Plos Biol 10: e1001230 doi:10.1371/journal.pbio.1001230.
11. GAERTNER BE, Parmenter MD, Rockman MV, Kruglyak L, Phillips PC, (2012) More than the sum of its parts: a complex epistatic network underlies natural variation in thermal preference behavior in Caenorhabditis elegans. Genetics 192: 1533-1542 doi:10.1534/genetics.112.142877.
12. Bendesky A, Pitts J, Rockman MV, Chen WC, Tan M-W, et al. (2012) Long-range regulatory polymorphisms affecting a GABA receptor constitute a quantitative trait locus (QTL) for social behavior in Caenorhabditis elegans. PLoS Genet 8: e1003157 doi:10.1371/journal.pgen.1003157.
13. Kammenga JE, Doroszuk A, Riksen JAG, Hazendonk E, Spiridon L, et al. (2007) A Caenorhabditis elegans wild type defies the temperature-size rule owing to a single nucleotide polymorphism in tra-3. PLoS Genet 3: e34 doi:10.1371/journal.pgen.0030034.
14. Andersen EC, Gerke JP, Shapiro JA, Crissman JR, Ghosh R, et al. (2012) Chromosome-scale selective sweeps shape Caenorhabditis elegans genomic diversity. Nat Genet pp. 1-8 doi:10.1038/ng.1050.
15. Rockman MV, Kruglyak L, (2009) Recombinational landscape and population genomics of Caenorhabditis elegans. PLoS Genet 5: e1000419 doi:10.1371/journal.pgen.1000419.
16. GAERTNER BE, Phillips PC, (2010) Caenorhabditis elegans as a platform for molecular quantitative genetics and the systems biology of natural variation. Genet Res 92: 331-348 doi:10.1017/S0016672310000601.
17. Yvert G, Brem RB, Whittle J, Akey JM, Foss E, et al. (2003) Trans-acting regulatory variation in Saccharomyces cerevisiae and the role of transcription factors. Nat Genet 35: 57-64 doi:10.1038/ng1222.
18. Brem RB, Yvert G, Clinton R, Kruglyak L, (2002) Genetic dissection of transcriptional regulation in budding yeast. Science 296: 752-755 doi:10.1126/science.1069516.
19. van Zanten M, Snoek LB, Proveniers MCG, Peeters AJM, (2009) The many functions of ERECTA. Trends Plant Sci 14: 214-218 doi:10.1016/j.tplants.2009.01.010.
20. Rogers C, Reale V, Kim K, Chatwin H, Li C, et al. (2003) Inhibition of Caenorhabditis elegans social feeding by FMRFamide-related peptide activation of NPR-1. Nat Neurosci 6: 1178-1185 doi:10.1038/nn1140.
21. de Bono M, Bargmann CI, (1998) Natural variation in a neuropeptide Y receptor homolog modifies social behavior and food response in C. elegans. Cell 94: 679-689.
22. Macosko EZ, Pokala N, Feinberg EH, Chalasani SH, Butcher RA, et al. (2009) A hub-and-spoke circuit drives pheromone attraction and social behaviour in C. elegans. Nature 458: 1171 doi:10.1038/nature07886.
23. Reddy KC, Andersen EC, Kruglyak L, Kim DH, (2009) A polymorphism in npr-1 is a behavioral determinant of pathogen susceptibility in C. elegans. Science 323: 382-384 doi:10.1126/science.1166527.
24. Chang AJ, Chronis N, Karow DS, Marletta MA, Bargmann CI, (2006) A distributed chemosensory circuit for oxygen preference in C. elegans. Plos Biol 4: e274 doi:10.1371/journal.pbio.0040274.
25. Davies AG, Bettinger JC, Thiele TR, Judy ME, McIntire SL, (2004) Natural variation in the npr-1 gene modifies ethanol responses of wild strains of C. elegans. Neuron 42: 731-743 doi:10.1016/j.neuron.2004.05.004.
26. Jang H, Kim K, Neal SJ, Macosko E, Kim D, et al. (2012) Neuromodulatory State and Sex Specify Alternative Behaviors through Antagonistic Synaptic Pathways in C. elegans. Neuron 75: 585-592 doi:10.1016/j.neuron.2012.06.034.
27. Hallem EA, Sternberg PW, (2008) Acute carbon dioxide avoidance in Caenorhabditis elegans. Proceedings of the National Academy of Sciences 105: 8038-8043 doi:10.1073/pnas.0707469105.
28. Choi S, Chatzigeorgiou M, Taylor KP, Schafer WR, Kaplan JM, (2013) Analysis of NPR-1 Reveals a Circuit Mechanism for Behavioral Quiescence in C. elegans. Neuron 78: 869-880 doi:10.1016/j.neuron.2013.04.002.
29. Yook K, Harris TW, Bieri T, Cabunoc A, Chan J, et al. (2012) WormBase 2012: more genomes, more data, new website. Nucleic Acids Res 40: D735-D741 doi:10.1093/nar/gkr954.
30. Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, et al. (2003) Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421: 231-237 doi:10.1038/nature01278.
31. Cheung BHH, Arellano-Carbajal F, Rybicki I, de Bono M, (2004) Soluble guanylate cyclases act in neurons exposed to the body fluid to promote C. elegans aggregation behavior. Curr Biol 14: 1105-1111 doi:10.1016/j.cub.2004.06.027.
32. Gray JM, Karow DS, Lu H, Chang AJ, Chang JS, et al. (2004) Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue. Nature 430: 317-322 doi:10.1038/nature02714.
33. Rockman MV, Kruglyak L, (2006) Genetics of global gene expression. Nat Rev Genet 7: 862-872 doi:10.1038/nrg1964.
34. Seidel HS, Kimble J, (2011) The oogenic germline starvation response in C. elegans. PLoS ONE 6: e28074 doi:10.1371/journal.pone.0028074.
35. Jo H, Shim J, Lee JH, Lee J, Kim JB, (2009) IRE-1 and HSP-4 contribute to energy homeostasis via fasting-induced lipases in C. elegans. Cell Metab 9: 440-448 doi:10.1016/j.cmet.2009.04.004.
36. Avery L, Horvitz HR, (1990) Effects of starvation and neuroactive drugs on feeding in Caenorhabditis elegans. J Exp Zool 253: 263-270 doi:10.1002/jez.1402530305.
37. Luedtke S, O'Connor V, Holden-Dye L, Walker RJ, (2010) The regulation of feeding and metabolism in response to food deprivation in Caenorhabditis elegans. Invert Neurosci 10: 63-76 doi:10.1007/s10158-010-0112-z.
38. Hubbard EJA, Korta DZ, Dalfó D, (2013) Physiological control of germline development. Adv Exp Med Biol 757: 101-131 doi:_10.1007/978-1-4614-4015-4_5.
39. Dalfó D, Michaelson D, Hubbard EJA, (2012) Sensory regulation of the C. elegans germline through TGF-β-dependent signaling in the niche. Curr Biol 22: 712-719 doi:10.1016/j.cub.2012.02.064.
40. Gloria-Soria A, Azevedo RBR, (2008) npr-1 Regulates foraging and dispersal strategies in Caenorhabditis elegans. Curr Biol 18: 1694-1699 doi:10.1016/j.cub.2008.09.043.
41. Torii KU, Mitsukawa N, Oosumi T, Matsuura Y, Yokoyama R, et al. (1996) The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell 8: 735-746 doi:10.1105/tpc.8.4.735.
42. Weber KP, De S, Kozarewa I, Turner DJ, Babu MM, et al. (2010) Whole genome sequencing highlights genetic changes associated with laboratory domestication of C. elegans. PLoS ONE 5: e13922 doi:10.1371/journal.pone.0013922.
43. McGrath PT, Xu Y, Ailion M, Garrison JL, Butcher RA, et al. (2011) Parallel evolution of domesticated Caenorhabditis species targets pheromone receptor genes. Nature 477: 321-325 doi:10.1038/nature10378.
44. Rockman MV, (2011) THE QTN PROGRAM AND THE ALLELES THAT MATTER FOR EVOLUTION: ALL THAT'S GOLD DOES NOT GLITTER. Evolution pp. no-no doi:10.1111/j.1558-5646.2011.01486.x.
45. Broman KW, Wu H, Sen S, Churchill GA, (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19: 889-890.
46. Lander E, Botstein D, (1989) Mapping Mendelian Factors Underlying Quantitative Traits Using RFLP Linkage Maps. Genetics 121: 185.
47. Doerge RW, Churchill GA, (1996) Permutation tests for multiple loci affecting a quantitative character. Genetics 142: 285-294.
48. Haley CS, Knott SA, (1992) A simple regression method for mapping quantitative trait loci in line crosses using flanking markers. Heredity 69: 315-324.
49. Bloom JS, Ehrenreich IM, Loo WT, Lite T-LV, Kruglyak L, (2013) Finding the sources of missing heritability in a yeast cross. Nature 494: 234-237 doi:10.1038/nature11867.
50. Brem RB, Kruglyak L, (2005) The landscape of genetic complexity across 5,700 gene expression traits in yeast. Proc Natl Acad Sci USA 102: 1572-1577 doi:10.1073/pnas.0408709102.
51. Smyth GK, (2005) Limma: linear models for microarray data. Bioinformatics and Computational Biology Solutions Using R and Bioconductor Statistics for Biology and Health pp. 397-420.
52. Capra EJ, Skrovanek SM, Kruglyak L, (2008) Comparative developmental expression profiling of two C. elegans isolates. PLoS ONE 3: e4055 doi:10.1371/journal.pone.0004055.
53. Antonov AV, Schmidt T, Wang Y, Mewes HW, (2008) ProfCom: a web tool for profiling the complex functionality of gene groups identified from high-throughput data. Nucleic Acids Res 36: W347-W351 doi:10.1093/nar/gkn239.