title: Gene-environment and protein-degradation signatures characterize genomic and phenotypic diversity in wild Caenorhabditis elegans populations.
abstract: BACKGROUND
  Analyzing and understanding the relationship between genotypes and phenotypes is at the heart of genetics. Research on the nematode Caenorhabditis elegans has been instrumental for unraveling genotype-phenotype relations, and has important implications for understanding the biology of mammals, but almost all studies, including forward and reverse genetic screens, are limited by investigations in only one canonical genotype. This hampers the detection and functional analysis of allelic variants, which play a key role in controlling many complex traits. It is therefore essential to explore the full potential of the natural genetic variation and evolutionary context of the genotype-phenotype map in wild C. elegans populations.
  
  
  RESULTS
  We used multiple wild C. elegans populations freshly isolated from local sites to investigate gene sequence polymorphisms and a multitude of phenotypes including the transcriptome, fitness, and behavioral traits. The genotype, transcriptome, and a number of fitness traits showed a direct link with the original site of the strains. The separation between the isolation sites was prevalent on all chromosomes, but chromosome V was the largest contributor to this variation. These results were supported by a differential food preference of the wild isolates for naturally co-existing bacterial species. Comparing polymorphic genes between the populations with a set of genes extracted from 19 different studies on gene expression in C. elegans exposed to biotic and abiotic factors, such as bacteria, osmotic pressure, and temperature, revealed a significant enrichment for genes involved in gene-environment interactions and protein degradation.
  
  
  CONCLUSIONS
  We found that wild C. elegans populations are characterized by gene-environment signatures, and we have unlocked a wealth of genotype-phenotype relations for the first time. Studying natural isolates provides a treasure trove of evidence compared with that unearthed by the current research in C. elegans, which covers only a diminutive part of the myriad of genotype-phenotype relations that are present in the wild.
authors: Laboratory of Nematology, Wageningen University, Droevendaalsesteeg 1, Wageningen 6708PB, The Netherlands. jan.kammenga@wur.nl.
authors: Rita J M
authors: RJ
authors: Volkers
authors: L Basten
authors: LB
authors: Snoek
authors: Caspara J van Hellenberg
authors: CJ
authors: Hubar
authors: Renata
authors: R
authors: Coopman
authors: Wei
authors: W
authors: Chen
authors: Wentao
authors: W
authors: Yang
authors: Mark G
authors: MG
authors: Sterken
authors: Hinrich
authors: H
authors: Schulenburg
authors: Bart P
authors: BP
authors: Braeckman
authors: Jan E
authors: JE
authors: Kammenga
mesh_terms: D000818:Animals; D017173:Caenorhabditis elegans / Q000235:genetics* / Q000378:metabolism; D029742:Caenorhabditis elegans Proteins / Q000235:genetics* / Q000378:metabolism; D018509:DNA, Helminth / Q000235:genetics / Q000302:isolation & purification*; D019143:Evolution, Molecular; D059647:Gene-Environment Interaction; D005828:Genetics, Population; D049751:Genome, Helminth; D005838:Genotype; D010641:Phenotype; D011110:Polymorphism, Genetic; D059467:Transcriptome
chemical_list: D029742:Caenorhabditis elegans Proteins; D018509:DNA, Helminth
references: Mol Cells. 2009 Sep;28(3):209-13
references: 19756391
references: Genome Res. 2010 Jul;20(7):929-37
references: 20488933
references: BMC Genomics. 2009 Apr 14;10:160
references: 19366437
references: Mol Syst Biol. 2012 Jun 05;8:587
references: 22669615
references: Front Genet. 2012 Apr 12;3:50
references: 22529848
references: BMC Syst Biol. 2010 Mar 23;4:32
references: 20331876
references: J Biomed Sci. 2006 Mar;13(2):181-91
references: 16463014
references: Curr Biol. 2013 Apr 8;23(7):607-13
references: 23499532
references: PLoS Biol. 2011 Jul;9(7):e1001115
references: 21814493
references: BMC Evol Biol. 2004 Nov 22;4:49
references: 15555070
references: Nat Genet. 2012 Jan 29;44(3):285-90
references: 22286215
references: PLoS One. 2010 Nov 11;5(11):e13922
references: 21085631
references: PLoS Genet. 2010 Mar 12;6(3):e1000877
references: 20300655
references: Nature. 2008 Aug 21;454(7207):1019-22
references: 18633349
references: PLoS One. 2011;6(9):e25476
references: 21980473
references: Arch Biochem Biophys. 2001 Nov 15;395(2):158-68
references: 11697852
references: Genetics. 2012 Dec;192(4):1533-42
references: 23086219
references: Front Genet. 2013 Jan 10;3:317
references: 23335938
references: J Exp Zool B Mol Dev Evol. 2007 Jul 15;308(4):409-16
references: 17377952
references: Proc Natl Acad Sci U S A. 2007 Jan 30;104(5):1708-13
references: 17237218
references: PLoS Genet. 2013;9(2):e1003315
references: 23437011
references: G3 (Bethesda). 2012 May;2(5):597-605
references: 22670229
references: Science. 2010 Oct 15;330(6002):372-6
references: 20947766
references: BMC Genomics. 2011 Oct 17;12:510
references: 22004469
references: PLoS One. 2010 Feb 02;5(2):e9010
references: 20126308
references: Nucleic Acids Res. 2013 Jan;41(Database issue):D738-43
references: 23180786
references: Nature. 2012 Feb 08;482(7384):173-8
references: 22318601
references: Environ Toxicol Chem. 2004 Feb;23(2):480-8
references: 14982397
references: Heredity (Edinb). 2007 Apr;98(4):206-13
references: 17203010
references: PLoS One. 2011;6(9):e24619
references: 21931778
references: Exp Gerontol. 2012 Aug;47(8):581-7
references: 22613270
references: Microbiol Immunol. 2012 Dec;56(12):825-35
references: 22957781
references: Mol Cell Endocrinol. 2011 Mar 1;334(1-2):49-55
references: 20438802
references: Parasitology. 2004 Apr;128(Pt 4):433-43
references: 15151149
references: Dev Comp Immunol. 2010 Jun;34(6):690-8
references: 20149819
references: BMC Biol. 2008 Oct 06;6:42
references: 18837995
references: Scand J Infect Dis. 2011 Apr;43(4):286-95
references: 21254954
references: PLoS One. 2008;3(12):e4055
references: 19116648
references: Genetics. 2009 Oct;183(2):685-92, 1SI-19SI
references: 19667133
references: PLoS One. 2012;7(5):e38200
references: 22675448
references: Nucleic Acids Res. 2009 Sep;37(16):e110
references: 19542186
references: PLoS One. 2011;6(9):e24676
references: 21931806
references: Genetics. 2010 Sep;186(1):405-10
references: 20610403
references: Genetics. 2006 Jan;172(1):127-43
references: 16291650
references: Immunobiology. 2008;213(3-4):237-50
references: 18406370
references: PLoS Genet. 2007 Mar 2;3(3):e34
references: 17335351
references: BMC Genomics. 2010 Jan 25;11:62
references: 20100350
references: Heredity (Edinb). 2013 Oct;111(4):306-13
references: 23715016
references: PLoS Pathog. 2008 Jul 18;4(7):e1000105
references: 18636113
references: PLoS One. 2012;7(12):e52493
references: 23300685
references: Genetics. 2006 Jan;172(1):171-84
references: 16272415
references: Heredity (Edinb). 2007 Jan;98(1):28-37
references: 16955112
references: Genetics. 2003 Jan;163(1):147-57
references: 12586703
references: PLoS Genet. 2009 Mar;5(3):e1000419
references: 19283065
references: PLoS Genet. 2006 Dec 29;2(12):e222
references: 17196041
references: Curr Biol. 2005 Jul 12;15(13):1176-84
references: 16005289
references: Mol Biol Evol. 2005 Jan;22(1):160-73
references: 15371529
references: Ann N Y Acad Sci. 2001 Dec;948:32-42
references: 11795393
references: Bioinformatics. 2011 Feb 15;27(4):592-3
references: 21169378
references: J Basic Microbiol. 2011 Oct;51(5):540-9
references: 21656805
references: Genome Res. 2006 Aug;16(8):1005-16
references: 16809667
references: PLoS One. 2012;7(9):e44255
references: 23028509
references: PLoS Genet. 2009 Jun;5(6):e1000503
references: 19503598
references: Trends Genet. 2008 Apr;24(4):178-85
references: 18325626
references: PLoS Genet. 2006 Nov 10;2(11):e183
references: 17096597
references: Genome Biol. 2007;8(6):R122
references: 17592649
references: PLoS Pathog. 2010 Jul 01;6:e1000982
references: 20617181
references: Genome Res. 2000 Nov;10(11):1690-6
references: 11076854
references: Methods. 2003 Dec;31(4):265-73
references: 14597310
references: Neuron. 2009 Mar 12;61(5):692-9
references: 19285466
references: Folia Microbiol (Praha). 2011 Sep;56(5):373-80
references: 21853381
references: BMC Genomics. 2009 Apr 29;10:202
references: 19402892