Natural diversity in daily rhythms of gene expression contributes to phenotypic variation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 3, 2015, Pages 905-910

  De Montaigu, Amaury ^a   Giakountis, Antonis ^a,c   Rubin, Matthew ^b   Tóth, Réka ^a,d   Cremer, Frédéric ^a   Sokolova, Vladislava ^a   Porri, Aimone ^a   Reymond, Matthieu ^a,e   Weinig, Cynthia ^b   Coupland, George ^a  

^a MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^b UNIVERSITY OF WYOMING   (United States)

^c Institute of Molecular Oncology   (Greece)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e AGROPARISTECH   (France)

Author keywords

Arabidopsis; Circadian; Diurnal; GIGANTEA; Rhythms

Indexed keywords

PHYTOCHROME; PHYTOCHROME INTERACTING FACTOR 4; UNCLASSIFIED DRUG;

ALLELE; ARABIDOPSIS; ARTICLE; BIODIVERSITY; CIRCADIAN RHYTHM; CONTROLLED STUDY; GENE; GENE EXPRESSION; GENETIC VARIABILITY; LIGHT; NONHUMAN; PHENOTYPE; PHENOTYPIC VARIATION; PLANT; PRIORITY JOURNAL; WAVEFORM; GENE EXPRESSION REGULATION; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ARABIDOPSIS;

ARABIDOPSIS; CIRCADIAN RHYTHM; GENE EXPRESSION REGULATION, PLANT; LIGHT; SIGNAL TRANSDUCTION;

EID: 84921324621     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1422242112     Document Type: Article

References (56)

1. de Montaigu A, Tóth R, Coupland G (2010) Plant development goes like clockwork. Trends Genet 26(7):296-306.
2. Wang W, et al. (2011) Timing of plant immune responses by a central circadian regulator. Nature 470(7332):110-114.
3. Harmer SL (2009) The circadian system in higher plants. Annu Rev Plant Biol 60: 357-377.
4. Michael TP, et al. (2003) Enhanced fitness conferred by naturally occurring variation in the circadian clock. Science 302(5647):1049-1053.
5. Dodd AN, et al. (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309(5734):630-633.
6. Somers DE, Devlin PF, Kay SA (1998) Phytochromes and cryptochromes in the entrainment of the Arabidopsis circadian clock. Science 282(5393):1488-1490.
7. Michael TP, Salome PA, McClung CR (2003) Two Arabidopsis circadian oscillators can be distinguished by differential temperature sensitivity. Proc Natl Acad Sci USA 100(11):6878-6883.
8. Salomé PA, To JP, Kieber JJ, McClung CR (2006) Arabidopsis response regulators ARR3 and ARR4 play cytokinin-independent roles in the control of circadian period. Plant Cell 18(1):55-69.
9. Millar AJ, Kay SA (1996) Integration of circadian and phototransduction pathways in the network controlling CAB gene transcription in Arabidopsis. Proc Natl Acad Sci USA 93(26):15491-15496.
10. Fowler SG, Cook D, Thomashow MF (2005) Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock. Plant Physiol 137(3):961-968.
11. Li G, et al. (2011) Coordinated transcriptional regulation underlying the circadian clock in Arabidopsis. Nat Cell Biol 13(5):616-622.
12. Hayama R, Yokoi S, Tamaki S, Yano M, Shimamoto K (2003) Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422(6933): 719-722.
13. Turner A, Beales J, Faure S, Dunford RP, Laurie DA (2005) The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310(5750): 1031-1034.
14. Böhlenius H, et al. (2006) CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312(5776):1040-1043.
15. Izawa T, et al. (2011) Os-GIGANTEA confers robust diurnal rhythms on the global transcriptome of rice in the field. Plant Cell 23(5):1741-1755.
16. Kloosterman B, et al. (2013) Naturally occurring allele diversity allows potato cultivation in northern latitudes. Nature 495(7440):246-250.
17. Slotte T, Holm K, McIntyre LM, Lagercrantz U, Lascoux M (2007) Differential expression of genes important for adaptation in Capsella bursa-pastoris (Brassicaceae). Plant Physiol 145(1):160-173.
18. Swarup K, et al. (1999) Natural allelic variation identifies new genes in the Arabidopsis circadian system. Plant J 20(1):67-77.
19. Edwards KD, Lynn JR, Gyula P, Nagy F, Millar AJ (2005) Natural allelic variation in the temperature-compensation mechanisms of the Arabidopsis thaliana circadian clock. Genetics 170(1):387-400.
20. Boikoglou E, et al. (2011) Environmental memory from a circadian oscillator: The Arabidopsis thaliana clock differentially integrates perception of photic vs. thermal entrainment. Genetics 189(2):655-664.
21. Anwer MU, et al. (2014) Natural variation reveals that intracellular distribution of ELF3 protein is associated with function in the circadian clock. eLife 3:3.
22. Darrah C, et al. (2006) Analysis of phase of LUCIFERASE expression reveals novel circadian quantitative trait loci in Arabidopsis. Plant Physiol 140(4):1464-1474.
23. Eimert K, Wang SM, Lue WI, Chen J (1995) Monogenic Recessive Mutations Causing Both Late Floral Initiation and Excess Starch Accumulation in Arabidopsis. Plant Cell 7(10):1703-1712.
24. Kurepa J, Smalle J, Van Montagu M, Inzé D (1998) Oxidative stress tolerance and longevity in Arabidopsis: The late-flowering mutant gigantea is tolerant to paraquat. Plant J 14(6):759-764.
25. Park DH, et al. (1999) Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. Science 285(5433):1579-1582.
26. Fowler S, et al. (1999) GIGANTEA: A circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. EMBO J 18(17):4679-4688.
27. Huq E, Tepperman JM, Quail PH (2000) GIGANTEA is a nuclear protein involved in phytochrome signaling in Arabidopsis. Proc Natl Acad Sci USA 97(17):9789-9794.
28. Dalchau N, et al. (2011) The circadian oscillator gene GIGANTEA mediates a long-term response of the Arabidopsis thaliana circadian clock to sucrose. Proc Natl Acad Sci USA 108(12):5104-5109.
29. Kim WY, et al. (2013) Release of SOS2 kinase from sequestration with GIGANTEA determines salt tolerance in Arabidopsis. Nat Commun 4:1352.
30. Dunford RP, Griffiths S, Christodoulou V, Laurie DA (2005) Characterisation of a barley (Hordeum vulgare L.) homologue of the Arabidopsis flowering time regulator GIGANTEA. Theor Appl Genet 110(5):925-931.
31. Zhao XY, Liu MS, Li JR, Guan CM, Zhang XS (2005) The wheat TaGI1, involved in photoperiodic flowering, encodes an Arabidopsis GI ortholog. Plant Mol Biol 58(1): 53-64.
32. Hecht V, et al. (2007) Pea LATE BLOOMER1 is a GIGANTEA ortholog with roles in photoperiodic flowering, deetiolation, and transcriptional regulation of circadian clock gene homologs. Plant Physiol 144(2):648-661.
33. Onai K, et al. (2004) Large-scale screening of Arabidopsis circadian clock mutants by a high-throughput real-time bioluminescence monitoring system. Plant J 40(1):1-11.
34. Ding Z, Millar AJ, Davis AM, Davis SJ (2007) TIME FOR COFFEE encodes a nuclear regulator in the Arabidopsis thaliana circadian clock. Plant Cell 19(5):1522-1536.
35. Palágyi A, et al. (2010) Functional analysis of amino-terminal domains of the photoreceptor phytochrome B. Plant Physiol 153(4):1834-1845.
36. Dalchau N, et al. (2010) Correct biological timing in Arabidopsis requires multiple light-signaling pathways. Proc Natl Acad Sci USA 107(29):13171-13176.
37. Filiault DL, et al. (2008) Amino acid polymorphisms in Arabidopsis phytochrome B cause differential responses to light. Proc Natl Acad Sci USA 105(8):3157-3162.
38. Locke JC, et al. (2005) Extension of a genetic network model by iterative experimentation and mathematical analysis. Mol Syst Biol 1:2005.0013.
39. Paltiel J, Amin R, Gover A, Ori N, Samach A (2006) Novel roles for GIGANTEA revealed under environmental conditions that modify its expression in Arabidopsis and Medicago truncatula. Planta 224(6):1255-1268.
40. Salomé PA, et al. (2002) The out of phase 1 mutant defines a role for PHYB in circadian phase control in Arabidopsis. Plant Physiol 129(4):1674-1685.
41. Nozue K, et al. (2007) Rhythmic growth explained by coincidence between internal and external cues. Nature 448(7151):358-361.
42. Nusinow DA, et al. (2011) The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature 475(7356):398-402.
43. Kim Y, et al. (2012) GIGANTEA and EARLY FLOWERING 4 in Arabidopsis exhibit differential phase-specific genetic influences over a diurnal cycle. Mol Plant 5(3): 678-687.
44. Kim Y, et al. (2013) ELF4 regulates GIGANTEA chromatin access through subnuclear sequestration. Cell Reports 3(3):671-677.
45. Sawa M, Nusinow DA, Kay SA, Imaizumi T (2007) FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science 318(5848): 261-265.
46. Fornara F, et al. (2009) Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response. Dev Cell 17(1):75-86.
47. Mizoguchi T, et al. (2005) Distinct roles of GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis. Plant Cell 17(8):2255-2270.
48. Martin-Tryon EL, Kreps JA, Harmer SL (2007) GIGANTEA acts in blue light signaling and has biochemically separable roles in circadian clock and flowering time regulation. Plant Physiol 143(1):473-486.
49. Oliverio KA, et al. (2007) GIGANTEA regulates phytochrome A-mediated photomorphogenesis independently of its role in the circadian clock. Plant Physiol 144(1): 495-502.
50. Kroymann J, Mitchell-Olds T (2005) Epistasis and balanced polymorphism influencing complex trait variation. Nature 435(7038):95-98.
51. Joseph B, et al. (2013) Hierarchical nuclear and cytoplasmic genetic architectures for plant growth and defense within Arabidopsis. Plant Cell 25(6):1929-1945.
52. Rockman MV (2012) The QTN program and the alleles that matter for evolution: All that's gold does not glitter. Evolution 66(1):1-17.
53. Narang RA, Bruene A, Altmann T (2000) Analysis of phosphate acquisition efficiency in different Arabidopsis accessions. Plant Physiol 124(4):1786-1799.
54. Rédei GP (1962) Supervital Mutants of Arabidopsis. Genetics 47(4):443-460.
55. Reed JW, Nagpal P, Poole DS, Furuya M, Chory J (1993) Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development. Plant Cell 5(2):147-157.
56. Clough SJ, Bent AF (1998) Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735-743.