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Genome-Wide Patterns of Gene Expression in Nature


Organisms in the wild are subject to multiple, fluctuating environmental factors, and it is in complex natural environments that genetic regulatory networks actually function and evolve. We assessed genome-wide gene expression patterns in the wild in two natural accessions of the model plant Arabidopsis thaliana and examined the nature of transcriptional variation throughout its life cycle and gene expression correlations with natural environmental fluctuations. We grew plants in a natural field environment and measured genome-wide time-series gene expression from the plant shoot every three days, spanning the seedling to reproductive stages. We find that 15,352 genes were expressed in the A. thaliana shoot in the field, and accession and flowering status (vegetative versus flowering) were strong components of transcriptional variation in this plant. We identified between ∼110 and 190 time-varying gene expression clusters in the field, many of which were significantly overrepresented by genes regulated by abiotic and biotic environmental stresses. The two main principal components of vegetative shoot gene expression (PCveg) correlate to temperature and precipitation occurrence in the field. The largest PCveg axes included thermoregulatory genes while the second major PCveg was associated with precipitation and contained drought-responsive genes. By exposing A. thaliana to natural environments in an open field, we provide a framework for further understanding the genetic networks that are deployed in natural environments, and we connect plant molecular genetics in the laboratory to plant organismal ecology in the wild.


Vyšlo v časopise: Genome-Wide Patterns of Gene Expression in Nature. PLoS Genet 8(4): e32767. doi:10.1371/journal.pgen.1002662
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002662

Souhrn

Organisms in the wild are subject to multiple, fluctuating environmental factors, and it is in complex natural environments that genetic regulatory networks actually function and evolve. We assessed genome-wide gene expression patterns in the wild in two natural accessions of the model plant Arabidopsis thaliana and examined the nature of transcriptional variation throughout its life cycle and gene expression correlations with natural environmental fluctuations. We grew plants in a natural field environment and measured genome-wide time-series gene expression from the plant shoot every three days, spanning the seedling to reproductive stages. We find that 15,352 genes were expressed in the A. thaliana shoot in the field, and accession and flowering status (vegetative versus flowering) were strong components of transcriptional variation in this plant. We identified between ∼110 and 190 time-varying gene expression clusters in the field, many of which were significantly overrepresented by genes regulated by abiotic and biotic environmental stresses. The two main principal components of vegetative shoot gene expression (PCveg) correlate to temperature and precipitation occurrence in the field. The largest PCveg axes included thermoregulatory genes while the second major PCveg was associated with precipitation and contained drought-responsive genes. By exposing A. thaliana to natural environments in an open field, we provide a framework for further understanding the genetic networks that are deployed in natural environments, and we connect plant molecular genetics in the laboratory to plant organismal ecology in the wild.


Zdroje

1. GibsonG 2008 The environmental contribution to gene expression profiles. Nat Rev Genet 9 575 581

2. PigliucciMSchlichtingCDJonesCSSchwenkK 1996 Developmental reaction norms: the interactions among allometry, ontogeny and plasticity. Plant Species Biol 11 69 85

3. LeakeyADBAinsworthEABernardSMMarkelzCRJOrtD 2009 Gene expression profiling: opening the black box of plant ecosystem responses to global change. Global Change Biol 15 1201 1213

4. KammengaJEHermanMAOuborgNJJohnsonLBreitlingR 2007 Microarray challenges in ecology. Trends Ecol Evol 22 273 279

5. ChapmanMALeebens-MackJHBurkeJM 2008 Positive Selection and expression divergence following gene duplication in the sunflower CYCLOIDEA gene family. Mol Biol Evol 25 1260 1273

6. RichardsCLHanzawaYEhrenreichIPuruggananMD 2009 Perspectives on ecological and evolutionary systems biology. GutierrezRACoruzziGM Annual Plant Reviews: Plant Systems Biology Oxford, UK Blackwell Publishing

7. AndersonJTMitchell-OldsT 2011 Ecological genetics and genomics of plant defenses: Evidence and approaches. Funct Ecol 25 312 324

8. De BoerTEBirlutiuABochdanovitsZTimmermansMJTNDijkstraTMH 2011 Transcriptional plasticity of a soil arthropod across different ecological conditions. Mol Ecol 20 1144 1154

9. VandersteenW 2011 Detecting gene expression profiles associated with environmental stressors within an ecological context. Mol Ecol 20 1322 1323

10. KoornneefMAlonso-BlancoCVreugdenhilD 2004 Naturally ocurring genetic variation in Arabidopsis thaliana. Ann Rev Plant Biol 55 141 172

11. ShimizuKKPuruggananMD 2005 Evolutionary and ecological genomics of Arabidopsis. Plant Physiol 138 578 584

12. ShindoCBernasconiGHardtkeCS 2007 Natural genetic variation in Arabidopsis: Tools, traits and prospects for evolutionary ecology. Ann Bot 99 1043 1054

13. HoffmannMHGlaßASTomiukJSchmuthsHFritschRM 2003 Analysis of molecular data of Arabidopsis thaliana (L.) Heynh. (Brassicaceae) with Geographical Information Systems (GIS). Mol Ecol 12 1007 1019

14. SamisKEHeathKDStinchcombeJR 2008 Discordant longitudinal clines in flowering time and phytochrome C in Arabidopsis thaliana. Evolution 62 2971 2983

15. PigliucciM 1998 Developmental phenotypic plasticity: Where internal programming meets the external environment. Curr Op Plant Biol 1 87 91

16. GossEBergelsonJ 2007 Fitness consequences of infection of Arabidopsis thaliana with its natural bacterial pathogen Pseudomonas viridiflava. Oecologia 152 71 81

17. KliebensteinDPedersenDBarkerBMitchell-OldsT 2002 Comparative analysis of quantitative trait loci controlling glucosinolates, myrosinase and insect resistance in Arabidopsis thaliana. Genetics 161 325 332

18. BenningtonCStrattonD 1998 Field tests of density-and frequency-dependent selection in Erigeron annuus (Compositae). Am J Bot 85 540

19. MauricioRRausherMD 1997 Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant defense. Evolution 78 1301 1310

20. MauricioRRausherMDBurdickDS 1997 Variation in the defense strategies of plants: Are resistance and tolerance mutually exclusive? Ecology 78 1301 1311

21. MauricioR 1998 Cost of resistance to natural enemies in field populations of the annual Arabidopsis thaliana. Am Nat 151 20 28

22. DonohueKDornLGriffithCKimEAguileraA 2005 The evolutionary ecology of seed germination of Arabidopsis thaliana: Variable natural selection on germination timing. Evolution 59 758 770

23. TianDTrawMBChenJQKreitmanMBergelsonJ 2003 Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423 74 77

24. MalmbergRLHeldSWaitsAMauricioR 2005 Epistasis for fitness-related quantitative traits in Arabidopsis thaliana grown in the field and in the greenhouse. Genetics 171 2013 2027

25. WeinigCUngererMCDornLAKaneNCToyonagaY 2002 Novel loci control variation in reproductive timing in Arabidopsis thaliana in natural environments. Genetics 162 1875 1884

26. CaicedoALStinchcombeJROlsenKMSchmittJPuruggananMD 2004 Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait. Proc Nat Acad Sci USA 101 15670 15675

27. HarmerSLHogeneschJBStraumeMChangH-SHanB 2000 Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290 2110 2113

28. BirnbaumKShashaDEWangJYJungJWLambertGM 2003 A gene expression map of the Arabidopsis root. Science 302 1956 1960

29. SchmidMDavisonTSHenzSRPapeUJDemarM 2005 A gene expression map of Arabidopsis thaliana development. Nat Genet 37 501 506

30. BradySMLongTABenfeyPN 2006 Unraveling the dynamic transcriptome. Plant Cell 18 2101 2111

31. GalbraithDWBirnbaumK 2006 Global studies of cell type-specific gene expression in plants. Ann Rev Plant Biol 57 451 475

32. MiyazakySFredricksenMHollisKCPoroykoVShepleyD 2004 Transcript expression profiles of Arabidopsis thaliana grown under controlled conditions and open-air elevated concentrations of CO2 and of O3. Field Crops Res 90 47 59

33. GuptaPDuplessisSWhiteHKarnoskyDFMartinF 2005 Gene expression patterns of trembling aspen trees following long-term exposure to interacting elevated CO2 and tropospheric O3. New Phytol 167 129 142

34. TaylorGStreetNRTrickerPJSjodinAGrahamL 2005 The transcriptome of Populus in elevated CO2. New Phytol 167 143 154

35. YangSHLoopstraCA 2005 Seasonal variation in gene expression for loblolly pines (Pinus taeda) from different geographical regions. Tree Physiol 25 1063 1073

36. AinsworthEARogersAVodkinLOWalterASchurrU 2006 The effects of elevated CO2 concentration on soybean gene expression. An analysis of growing and mature leaves. Plant Physiol 142 135 147

37. DruartNRodriuez-BueyMBarron-GraffordGSjodinABhaleraoR 2006 Molecular targets of elevated [CO2] in leaves and stems of Pupolus deltoides: implications for future tree growth and carbon sequestration. Func Plant Biol 33 121 131

38. SchmidtDDBaldwinIT 2006 Transcriptional responses of Solanum nigrum to methyl jasmonate and competition: A glasshouse and field study. Func Ecol 20 500 508

39. LiPAinsworthEALeakeyADBUlanovALozovayaV 2008 Arabidopsis transcript and metabolite profiles: Ecotype-specific responses to open-air elevated CO2. Plant Cell Env 31 1673 1687

40. LeakeyADBXuFGillespieKMMcGrathJMAinsworthEA 2009 Genomic basis for stimulated respiration by plants growing under elevated carbon dioxide. Proc Nat Acad Sci USA 106 3597 3602

41. TallisMJLinYRogersAZhangJStreetNR 2010 The transcriptome of Populus in elevated CO2 reveals increades anthocyanin biosynthesis during delayed autumnal senescence. New Phytol 186 415 428

42. TraversSETangZCarageaDGarrettKAHulbertSH 2010 Variation in gene expression of Andropogon gerardii in response to altered environmental conditions associated with climate change. J Ecol 98 374 383

43. AikawaSKobayashiMJSatakeAShimizuKKKudohH 2010 Robust control of the seasonal expression of the Arabidopsis FLC gene in a fluctuating environment. Proc Nat Acad Sci USA 107 11632 11637

44. LoudetOChaillouSCamilleriCBouchezDDaniel-VedeleF 2002 Bay-0×Shahdara recombinant inbred line population: a powerful tool for the genetic dissection of complex traits in Arabidopsis. Theor Appl Genet 104 1173 1184

45. NordborgMHuTTIshinoYJhaveriJToomajianC 2005 The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol 3 e196 doi:10.1371/journal.pbio.0030196

46. CaoJSchneebergerKOssowskiSGuntherTBenderS 2011 Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat Genet 43 956 963

47. GentlemanRCareyVBatesDBolstadBDettlingM 2004 Bioconductor: Open software development for computational biology and bioinformatics. Genome Biol 5 R80

48. MandelMAGustafson-BrownCSavidgeBYanofskyMF 1992 Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360 273 277

49. JackTBrockmanLLMeyerowitzEM 1992 The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens. Cell 68 683 697

50. GotoKMeyerowitzEM 1994 Function and regulation of the Arabidopsis floral homeotic gene PISTILLATA. Genes Dev 8 1548 1560

51. YanofskyMFMaHBowmanJLDrewsGNFeldmannKA 1990 The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346 35 39

52. RounsleySDDittaGSYanofskyMF 1995 Diverse roles for MADS Box genes in Arabidopsis development. Plant Cell 7 1259 1269

53. MaHYanofskyMFMeyerowitzEM 1991 AGL1-AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. Genes Dev 5 484 495

54. LiJBushelPRChuT-MWolfingerRD 2009 Principal variance components analysis: Estimating batch effects in microarray gene expression data. SchererA Batch Effects and Noise in Microarray Experiments Chichester, UK John Wiley & Sons, Ltd 141 154

55. KliebensteinDJWestMALvan LeeuwenHKimKDoergeRW 2006 Genomic survey of gene expression diversity in Arabidopsis thaliana. Genetics 172 1179 1189

56. GanXStegleOBehrJSteffenJGDreweP 2011 Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477 419 423

57. StoreyJDXiaoWLeekJTTompkinsRGDavisRW 2005 Significance analysis of time course microarray experiments. Proc Natl Acad Sci USA 102 12837 12842

58. LeekJTMonsenEDabneyARStoreyJD 2006 EDGE: Extraction and analysis of differential gene expression. Bioinformatics 22 507 508

59. KaufmanLRousseeuwPJ 1990 Finding groups in data: An introduction to cluster analysis Hoboken John Wiley & Sons

60. RosselJBWilsonIWPogsonBJ 2002 Global changes in gene expression in response to high light in Arabidopsis. Plant Physiol 130 1109 1120

61. KilianJWhiteheadDHorakJWankeDWeinlS 2007 The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. The Plant Journal 50 347 363

62. WhithamSAQuanSChangH-SCooperBEstesB 2003 Diverse RNA viruses elicit the expression of common sets of genes in susceptible Arabidopsis thaliana plants. Plant J 33 271 283

63. BabuMGriffithsJHuangT-SWangA 2008 Altered gene expression changes in Arabidopsis leaf tissues and protoplasts in response to Plum pox virus infection. BMC Genomics 9 325

64. De VosMVan OostenVRVan PoeckeRMPVan PeltJAPozoMJ 2005 Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol Plant-Microbe Interact 18 923 937

65. KatariMSNowickiSDAceitunoFFNeroDKelferJ 2010 VirtualPlant: A software platform to support systems biology research. Plant Physiol 152 500 515

66. PauwelsLBarberoGFGeerinckJTillemanSGrunewaldW 2010 NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 464 788 791

67. BerberichTHaradaMSugawaraKKodamaHIbaK 1998 Two maize genes encoding ω-3 fatty acid desaturase and their differential expression to temperature. Plant Mol Biol 36 297 306

68. KumarSVWiggePA 2010 H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140 136 147

69. KoborMSVenkatasubrahmanyamSMeneghiniMDGinJWJenningsJL 2004 A protein complex containing the conserved Swi2/Snf2-related ATPase Swr1p deposits histone variant H2A.Z into euchromatin. PLoS Biol 2 e131 doi:10.1371/journal.pbio.0020131

70. MizuguchiGShenXLandryJWuW-HSenS 2004 ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 303 343 348

71. SungDYVierlingEGuyCL 2001 Comprehensive expression profile analysis of the Arabidopsis Hsp70 gene family. Plant Physiol 126 789 800

72. SaeedAIBhagabatiNKBraistedJCLiangWSharovVHoweEA 2006 TM4 microarray software suite. Methods Enzymol 411 134 193

73. ZhengZ-LNafisiMTamALiHCrowellDN 2002 Plasma membrane-associated ROP10 small GTPase is a specific negative regulator of abscisic acid responses in Arabidopsis. Plant Cell 14 2787 2797

74. XinZZhaoYZhengZ-L 2005 Transcriptome analysis reveals specific modulation of abscisic acid signaling by ROP10 small GTPase in Arabidopsis. Plant Physiol 139 1350 1365

75. SeoMPeetersAJMKoiwaiHOritaniTMarion-PollA 2000 The Arabidopsis aldehyde oxidase 3 (AAO3) gene product catalyzes the final step in abscisic acid biosynthesis in leaves. Proc Natl Acad Sci USA 97 12908 12913

76. AbrahamERigoGSzekelyGNagyRKonczC 2003 Light-dependent induction of proline biosynthesis by abscisic acid and salt stress is inhibited by brassinosteroid in Arabidopsis. Plant Mol Biol 51 363 372

77. SzékelyGÁbrahámECséplőÁRigóGZsigmondL 2008 Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. Plant J 53 11 28

78. ShinozakiKYamaguchi-ShinozakiK 2007 Gene networks involved in drought stress response and tolerance. J Exp Bot 58 221 227

79. SwindellWHuebnerMWeberA 2007 Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways. BMC Genomics 8 125

80. SwindellWRHuebnerMWeberAP 2007 Plastic and adaptive gene expression patterns associated with temperature stress in Arabidopsis thaliana. Heredity 99 143 150

81. Yamaguchi-ShinozakiKShinozakiK 2006 Trascriptional regulatory networks in cellular responses and tolerance to dehydration and cold stress. Ann Rev Plant Biol 57 781 803

82. DenbyKGehringC 2005 Engineering drought and salinity tolerance in plants: lessons from genome-wide expression profiling in Arabidopsis. Trends Biotech 23 547 552

83. RabelloAGuimaraesCRangelPda SilvaFSeixasD 2008 Identification of drought-responsive genes in roots of upland rice (Oryza sativa L). BMC Genomics 9 485

84. van de MortelJEAlmar VillanuevaLSchatHKwekkeboomJCoughlanS 2006 Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiol 142 1127 1147

85. OgawaINakanishiHMoriSNishizawaN 2009 Time course analysis of gene regulation under cadmium stress in rice. Plant and Soil 325 97 108

86. PalencharPKouranovALejayLCoruzziG 2004 Genome-wide patterns of carbon and nitrogen regulation of gene expression validate the combined carbon and nitrogen (CN)-signaling hypothesis in plants. Genome Biol 5 R91

87. LianXWangSZhangJFengQZhangL 2006 Expression profiles of 10,422 genes at early stage of low nitrogen stress in rice assayed using a cDNA microarray. Plant Mol Biol 60 617 631

88. SchenkPMKazanKWilsonIAndersonJPRichmondT 2000 Coordinated plant defense response in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 97 11655 11660

89. EhltingJChowriraSMattheusNAeschlimanDArimuraG-I 2008 Comparative transcriptome analysis of Arabidopsis thaliana infested by diamond back moth (Plutella xylostella) larvae reveals signatures of stress response, secondary metabolism, and signalling. BMC Genomics 9 154

90. Martin-TrilloMLázaroAPoethigRSGómez-MenaCPiñeiroMA 2006 EARLY IN SHORT DAYS 1 (ESD1) encodes ACTIN-RELATED PROTEIN 6 (AtARP6), a putative component of chromatin remodelling complexes that positively regulates FLC accumulation in Arabidopsis. Development 133 1241 1252

91. Fournier-LevelAKorteACooperMDNordborgMSchmittJ 2011 A map of local adaptation in Arabidopsis thaliana. Science 334 86 89

92. HancockAMBrachiBFaureNHortonMWJarymowyczLB 2011 Adaptation to climate across the Arabidopsis thaliana genome. Science 334 83 86

93. Korves ToniaMSchmid KarlJCaicedo AnaLMaysCStinchcombe JohnR 2007 Fitness effects associated with the major flowering time gene FRIGIDA in Arabidopsis thaliana in the field. Am Nat 169 E141 E157

94. WeinigCDornLAKaneNCGermanZMHalldorsdottirSS 2003 Heterogeneous selection at specific loci in natural environments in Arabidopsis thaliana. Genetics 165 321 329

95. StinchcombeJRWeinigCUngererMOlsenKMMaysC 2004 A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA. Proc Natl Acad Sci USA 101 4712 4717

96. AFFYMETRIXAffymetrix, editor 2002 Affymetrix Microarray Suite User Guide; Santa Clara, CA

97. BorevitzJOHazenSPMichaelTPMorrisGPBaxterIR 2007 Genome-wide patterns of single-feature polymorphism in Arabidopsis thaliana. Proc Nat Acad Sci USA 104 12057 12062

98. RousseeuwPJ 1987 Silhouettes: A graphical aid to the interpretation and validation of cluster analysis. J Compt Appl Math 20 53 65

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