A Genome-Wide Association Study Identifies Variants Underlying the Shade Avoidance Response
Shade avoidance is an ecologically and molecularly well-understood set of plant developmental responses that occur when the ratio of red to far-red light (R∶FR) is reduced as a result of foliar shade. Here, a genome-wide association study (GWAS) in Arabidopsis thaliana was used to identify variants underlying one of these responses: increased hypocotyl elongation. Four hypocotyl phenotypes were included in the study, including height in high R∶FR conditions (simulated sun), height in low R∶FR conditions (simulated shade), and two different indices of the response of height to low R∶FR. GWAS results showed that variation in these traits is controlled by many loci of small to moderate effect. A known PHYC variant contributing to hypocotyl height variation was identified and lists of significantly associated genes were enriched in a priori candidates, suggesting that this GWAS was capable of generating meaningful results. Using metadata such as expression data, GO terms, and other annotation, we were also able to identify variants in candidate de novo genes. Patterns of significance among our four phenotypes allowed us to categorize associations into three groups: those that affected hypocotyl height without influencing shade avoidance, those that affected shade avoidance in a height-dependent fashion, and those that exerted specific control over shade avoidance. This grouping allowed for the development of explicit hypotheses about the genetics underlying shade avoidance variation. Additionally, the response to shade did not exhibit any marked geographic distribution, suggesting that variation in low R∶FR–induced hypocotyl elongation may represent a response to local conditions.
Vyšlo v časopise:
A Genome-Wide Association Study Identifies Variants Underlying the Shade Avoidance Response. PLoS Genet 8(3): e32767. doi:10.1371/journal.pgen.1002589
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002589
Souhrn
Shade avoidance is an ecologically and molecularly well-understood set of plant developmental responses that occur when the ratio of red to far-red light (R∶FR) is reduced as a result of foliar shade. Here, a genome-wide association study (GWAS) in Arabidopsis thaliana was used to identify variants underlying one of these responses: increased hypocotyl elongation. Four hypocotyl phenotypes were included in the study, including height in high R∶FR conditions (simulated sun), height in low R∶FR conditions (simulated shade), and two different indices of the response of height to low R∶FR. GWAS results showed that variation in these traits is controlled by many loci of small to moderate effect. A known PHYC variant contributing to hypocotyl height variation was identified and lists of significantly associated genes were enriched in a priori candidates, suggesting that this GWAS was capable of generating meaningful results. Using metadata such as expression data, GO terms, and other annotation, we were also able to identify variants in candidate de novo genes. Patterns of significance among our four phenotypes allowed us to categorize associations into three groups: those that affected hypocotyl height without influencing shade avoidance, those that affected shade avoidance in a height-dependent fashion, and those that exerted specific control over shade avoidance. This grouping allowed for the development of explicit hypotheses about the genetics underlying shade avoidance variation. Additionally, the response to shade did not exhibit any marked geographic distribution, suggesting that variation in low R∶FR–induced hypocotyl elongation may represent a response to local conditions.
Zdroje
1. KamiCLorrainSHornitschekPFankhauserC 2010 Light-regulated plant growth and development. Current Topics in Developmental Biology 91 29 66
2. FranklinKA 2008 Shade avoidance. New Phytol 179 930 944
3. MorganDCSmithH 1979 A systematic relationship between phytochrome-controlled development and species habitat, for plants grown in simulated natural radiation. Planta 145 253 258
4. DudleySASchmittJ 1996 Testing the adaptive plasticity hypothesis: density-dependent selection on manipulated stem length in Impatiens capensis. The American Naturalist 147 445 465
5. SchmittJMcCormacACSmithH 1995 A Test of the Adaptive Plasticity Hypothesis Using Transgenic and Mutant Plants Disabled in Phytochrome-Mediated Elongation Responses to Neighbors. The American Naturalist 146 937 953
6. DornLAPyleEHSchmittJ 2000 Plasticity to light cues and resources in Arabidopsis thaliana: testing for adaptive value and costs. Evolution 54 1982 94
7. BottoJFSmithH 2002 Differential genetic variation in adaptive strategies to a common environmental signal in Arabidopsis accessions: phytochrome-mediated shade avoidance. Plant, Cell & Environment 25 53 63
8. KebromBrutnell 2007 The molecular analysis of the shade avoidance syndrome in the grasses has begun. J Exp Bot 58 3079 3089
9. HornitschekPLorrainSZoeteVMichielinOFankhauserC 2009 Inhibition of the shade avoidance response by formation of non-DNA binding bHLH heterodimers. EMBO J 28 3893 3902
10. SessaGCarabelliMSassiMCiolfiAPossentiM 2005 A dynamic balance between gene activation and repression regulates the shade avoidance response in Arabidopsis. Genes Dev 19 2811 5
11. CarabelliMSessaGBaimaSMorelliGRubertiI 1993 The Arabidopsis Athb-2 and -4 genes are strongly induced by far-red-rich light. Plant J 4 469 479
12. SalterMGFranklinKAWhitelamGC 2003 Gating of the rapid shade-avoidance response by the circadian clock in plants. Nature 426 680 683
13. StammPKumarPP 2010 The phytohormone signal network regulating elongation growth during shade avoidance. J Exp Bot 61 2889 903
14. TaoYFerrerJLLLjungKPojerFHongF 2008 Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133 164 176
15. WonCShenXMashiguchiKZhengZDaiX 2011 Conversion of tryptophan to indole-3-acetic acid by TRYPTOPHAN AMINOTRANSFERASES OF ARABIDOPSIS and YUCCAs in Arabidopsis. Proc Natl Acad Sci U S A 108 18518 18523
16. KanyukaKPraekeltUFranklinKABillinghamOEHooleyR 2003 Mutations in the huge Arabidopsis gene BIG affect a range of hormone and light responses. Plant J 35 57 70
17. KeuskampDPollmannSVoesenekLPeetersAPierikR 2010 Auxin transport through PINFORMED 3 (PIN3) controls shade avoidance and fitness during competition. Proc Natl Acad Sci U S A 107 22740
18. KozukaTKobayashiJHoriguchiGDemuraTSakakibaraH 2010 Involvement of auxin and brassinosteroid in the regulation of petiole elongation under the shade. Plant Physiol 153 1608 18
19. HisamatsuTKingRWHelliwellCAKoshiokaM 2005 The involvement of gibberellin 20-oxidase genes in phytochrome-regulated petiole elongation of Arabidopsis. Plant Physiol 138 1106 1116
20. Djakovic-PetrovicTde WitMVoesenekLACJPierikR 2007 DELLA protein function in growth responses to canopy signals. Plant J 51 117 26
21. BorevitzJOMaloofJNLutesJDabiTRedfernJL 2002 Quantitative trait loci controlling light and hormone response in two accessions of Arabidopsis thaliana. Genetics 160 683 96
22. ColuccioMPSanchezSEKasulinLYanovskyMJBottoJF 2010 Genetic mapping of natural variation in a shade avoidance response: ELF3 is the candidate gene for a QTL in hypocotyl growth regulation. J Exp Bot 62 167 176
23. Jiménez-GómezJMWallaceADMaloofJN 2010 Network analysis identifies ELF3 as a QTL for the shade avoidance response in Arabidopsis. PLoS Genet 6 e1001100 doi:10.1371/journal.pgen.1001100
24. AukermanMJHirschfeldMWesterLWeaverMClackT 1997 A deletion in the PHYD gene of the Arabidopsis Wassilewskija ecotype defines a role for phytochrome D in red/far-red light sensing. Plant Cell 9 1317 1326
25. BrockMTMaloofJNWeinigC 2010 Genes underlying quantitative variation in ecologically important traits: PIF4 (phytochrome interacting factor 4) is associated with variation in internode length, owering time, and fruit set in Arabidopsis thaliana. Mol Ecol 19 1187 1199
26. ViaSLandeR 1987 Evolution of genetic variability in a spatially heterogeneous environment: effects of genotype-environment interaction. Genetical research 49 147 56
27. ScheinerSM 1993 Genetics and Evolution of Phenotypic Plasticity. Annual Review of Ecology and Systematics 24 35 68
28. MaloofJNBorevitzJODabiTLutesJNehringRB 2001 Natural variation in light sensitivity of Arabidopsis. Nat Genet 29 441 446
29. StenøienHKFensterCBKuittinenHSavolainenO 2002 Quantifying latitudinal clines to light responses in natural populations of Arabidopsis thaliana (Brassicaceae). American Journal of Botany 89 1604 8
30. BalasubramanianSSureshkumarSAgrawalMMichaelTPWessingerC 2006 The PHYTOCHROME C photoreceptor gene mediates natural variation in owering and growth responses of Arabidopsis thaliana. Nat Genet 38 711 715
31. PlattAHortonMHuangYSLiYAnastasioAE 2010 The scale of population structure in Arabidopsis thaliana. PLoS Genet 6 e1000843 doi:10.1371/journal.pgen.1000843
32. SmithH 1982 Light quality, photopercetion, and plant strategy. Annual Review of Plant Physiology 33 481 518
33. Fournier-LevelAKorteACooperMDNordborgMSchmittJ 2011 A Map of Local Adaptation in Arabidopsis thaliana. Science 334 86 89
34. DudleySASchmittJ 1995 Genetic Differentiation in Morphological Responses to Simulated Foliage Shade between Populations of Impatiens capensis from Open and Woodland Sites. Functional Ecology 9 655 666
35. WeinigC 2000 Plasticity versus canalization: population di_erences in the timing of shadeavoidance responses. Evolution Int J Org Evolution 54 441 451
36. AtwellSHuangYSVilhjálmssonBJWillemsGHortonM 2010 Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465 627 631
37. KangHMZaitlenNAWadeCMKirbyAHeckermanD 2008 Efficient control of population structure in model organism association mapping. Genetics 178 1709 23
38. BaxterIBrazeltonJNYuDHuangYSLahnerB 2010 A Coastal Cline in Sodium Accumulation in Arabidopsis thaliana Is Driven by Natural Variation of the Sodium Transporter AtHKT1;1. PLoS Genet 6 e1001193 doi:10.1371/journal.pgen.1001193
39. FiliaultDLWessingerCADinnenyJRLutesJBorevitzJO 2008 Amino acid polymorphisms in Arabidopsis phytochrome B cause differential responses to light. Proc Natl Acad Sci U S A 105 3157 3162
40. NordborgMHuTTIshinoYJhaveriJToomajianC 2005 The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol 3 e196 doi:10.1371/journal.pbio.0030196
41. TatematsuKKumagaiSMutoHSatoAWatahikiMK 2004 MASSUGU2 encodes Aux/IAA19, an auxin-regulated protein that functions together with the transcriptional activator NPH4/ARF7 to regulate differential growth responses of hypocotyl and formation of lateral roots in Arabidopsis thaliana. The Plant Cell 16 379 93
42. FengSMartinezCGusmaroliGWangYZhouJ 2008 Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451 475 9
43. SteindlerCMatteucciASessaGWeimarTOhgishiM 1999 Shade avoidance responses are mediated by the ATHB-2 HD-zip protein, a negative regulator of gene expression. Development 126 4235 45
44. TeppermanJMHwangYSQuailPH 2006 phyA dominates in transduction of red-light signals to rapidly responding genes at the initiation of Arabidopsis seedling de-etiolation. Plant J 48 728 42
45. RichterRBehringerCMüllerIKSchwechheimerC 2010 The GATA-type transcription factors GNC and GNL/CGA1 repress gibberellin signaling downstream from DELLA proteins and PHYTOCHROME-INTERACTING FACTORS. Genes Dev 24 2093 104
46. QuaedvliegNDockxJRookFWeisbeekPSmeekensS 1995 The homeobox gene ATH1 of Arabidopsis is derepressed in the photomorphogenic mutants cop1 and det1. Plant Cell 7 117 29
47. Gómez-MenaCde FolterSCostaMMRAngenentGCSablowskiR 2005 Transcriptional program controlled by the oral homeotic gene AGAMOUS during early organogenesis. Development 132 429 38
48. RutjensBBaoDvan Eck-StoutenEBrandMSmeekensS 2009 Shoot apical meristem function in Arabidopsis requires the combined activities of three BEL1-like homeodomain proteins. Plant J 58 641 54
49. LinRWangH 2004 Arabidopsis FHY3/FAR1 gene family and distinct roles of its members in light control of Arabidopsis development. Plant Physiol 136 4010 22
50. HudsonMELischDRQuailPH 2003 The FHY3 and FAR1 genes encode transposase-related proteins involved in regulation of gene expression by the phytochrome A-signaling pathway. Plant J 34 453 71
51. LinRDingLCasolaCRipollDRFeschotteC 2007 Transposase-derived transcription factors regulate light signaling in Arabidopsis. Science 318 1302 5
52. FranklinKAQuailPH 2010 Phytochrome functions in Arabidopsis development. Journal of experimental botany 61 11 24
53. DevlinPFYanovskyMJKaySA 2003 A genomic analysis of the shade avoidance response in Arabidopsis. Plant Physiol 133 1617 29
54. ChanEKFRoweHCHansenBGKliebensteinDJ 2010 The Complex Genetic Architecture of the Metabolome. PLoS Genet 6 e1001198 doi:10.1371/journal.pgen.1001198
55. BrachiBFaureNHortonMFlahauwEVazquezA 2010 Linkage and association mapping of Arabidopsis thaliana owering time in nature. PLoS Genet 6 e1000940 doi:10.1371/journal.pgen.1000940
56. LiYHuangYBergelsonJNordborgMBorevitzJO 2010 Association mapping of local climatesensitive quantitative trait loci in Arabidopsis thaliana. Proc Natl Acad Sci U S A 107 21199 204
57. BrachiBMorrisGPBorevitzJO 2011 Genome-wide association studies in plants: the missing heritability is in the field. Genome Biology 12 232
58. SchmittJDudleySAPigliucciM 1999 Manipulative Approaches to Testing Adaptive Plasticity: PhytochromeMediated ShadeAvoidance Responses in Plants. The American Naturalist 154 S43 S54
59. SchmittJStinchcombeJRHeschelMSHuberH 2003 The adaptive evolution of plasticity: phytochrome-mediated shade avoidance responses. Integrative and Comparative Biology 43 459 69
60. CaoJSchneebergerKOssowskiSGüntherTBenderS 2011 Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nature Genetics 43 956 963
61. RasbandW 1997–2011 ImageJ. U. S. National Institutes of Health, Bethesda, Maryland, USA, http://imagej.nih.gov/ij/edition
62. R Development Core Team 2010 R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria
63. BatesDMaechlerM 2010 lme4: Linear mixed-effects models using S4 classes
64. FalconerDSMackayTFC 1996 Introduction to Quantitative Genetics (4th Edition) Prentice Hall
65. WarnesGLeischFManM with contributions from Gregor Gorjanc 2008 genetics: Population Genetics
66. SmythGK 2005 Limma: linear models for microarray data. GentlemanRCareyVDudoitSR IrizarryWH Bioinformatics and Computational Biology Solutions using R and Bioconductor New York Springer 397 420
67. GentlemanRCCareyVJBatesDM 2004 Bioconductor: Open software development for computational biology and bioinformatics. Genome Biology 5 R80
68. CarlsonMFalconSPagesHLiN org.At.tair.db: Genome wide annotation for Arabidopsis
69. BeissbarthTSpeedTP 2004 GOstat: find statistically overrepresented Gene Ontologies within a group of genes. Bioinformatics 20 1464 5
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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