Allele-specific assay reveals functional variation in the Chalcone Synthase promoter of Arabidopsis thaliana that is compatible with neutral evolution

Plant Cell

Volumn 17, Issue 3, 2005, Pages 676-690

  De Meaux, Juliette ^a   Goebel, Ulrike ^a   Pop, Ana ^a   Mitchell Olds, Thomas ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS; ENZYMES; MUTAGENESIS;

ARABIDOPSIS THALIANA; FUNCTIONAL CHANGES; NEUTRAL EVOLUTION; NUCLEOTIDE DIVERSITY;

GENES;

BIOSYNTHESIS; ENZYMES; GENES; MUTATION;

ARABIDOPSIS; ARABIDOPSIS THALIANA; INSECTA;

ACYLTRANSFERASE; CHALCONE SYNTHASE; MESSENGER RNA; PLANT DNA; PLANT RNA;

ALLELE; ANIMAL; ARABIDOPSIS; ARTICLE; CROSS BREEDING; ENZYMOLOGY; GENE; GENE EXPRESSION; GENETIC VARIABILITY; GENETICS; INSECT; LIGHT; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PROMOTER REGION; RADIATION EXPOSURE;

ACYLTRANSFERASES; ALLELES; ANIMALS; ARABIDOPSIS; BASE SEQUENCE; CROSSES, GENETIC; DNA, PLANT; EVOLUTION, MOLECULAR; GENE EXPRESSION; GENES, PLANT; INSECTS; LIGHT; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS (GENETICS); RNA, MESSENGER; RNA, PLANT; VARIATION (GENETICS);

EID: 20444367854     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.104.027839     Document Type: Article

References (64)

1. Ahmadian, A., Gharizadeh, B., Gustafsson, A.C., Sterky, F., Nyren, P., Uhlen, M., and Lundeberg, J. (2000). Single-nucleotide polymorphism analysis by pyrosequencing. Anal. Biochem. 280, 103-110.
2. Bamshad, M.J., Mummidi, S., Gonzalez, E., Ahuja, S.S., Dunn, D.M., Watkins, W.S., Wooding, S., Stone, A.C., Jorde, L.B., Weiss, R.B., and Ahuja, S.K. (2002). A strong signature of balancing selection in the 5′ cis-regulatory region of CCR5. Proc. Natl. Acad. Sci. USA 99, 10539-10544.
3. Boffelli, D., McAuliffe, J., Ovcharenko, D., Lewis, K.D., Ovcharenko, I., Pachter, L., and Rubin, E.M. (2003). Phylogenetic shadowing of primate sequences to find functional regions of the human genome. Science 299, 1391-1394.
4. Borevitz, J.O., Xia, Y., Blount, J.W., Dixon, R.A., and Lamb, C. (2000). Activation tagging identifies a conserved MYB regulator of phenyl-propanoid biosynthesis. Plant Cell 12, 2383-2393.
5. Bray, N.J., Buckland, P.R., Owen, M.J., and O'Donovan, M.C. (2003). Cis-acting variation in the expression of a high proportion of genes in human brain. Hum. Genet. 113, 149-153.
6. Brem, R.B., Yvert, G., Clinton, R., and Kruglyak, L. (2002). Genetic dissection of transcriptional regulation in budding yeast. Science 296, 752-755.
7. Brukner, I., Sanchez, R., Suck, D., and Pongor, S. (1995). Sequence-dependent bending propensity of DNA as revealed by DNase-I: Parameters for trinucleotides. EMBO J. 14, 1812-1818.
8. Burbulis, I.E., Iacobucci, M., and Shirley, B.W. (1996). A null mutation in the first enzyme of flavonoid biosynthesis does not affect male fertility in Arabidopsis. Plant Cell 8, 1013-1025.
9. Burbulis, I.E., and Winkel-Shirley, B. (1999). Interactions among enzymes of the Arabidopsis flavonoid biosynthetic pathway. Proc. Natl. Acad. Sci. USA 96, 12929-12934.
10. Clauss, M.J., and Mitchell-Olds, T. (2004). Functional divergence in tandemly duplicated Arabidopsis thaliana trypsin inhibitor genes. Genetics 166, 1419-1436.
11. Cliften, P., Sudarsanam, P., Desikan, A., Fulton, L., Fulton, B., Majors, J., Waterston, R., Cohen, B.A., and Johnston, M. (2003). Finding functional features in Saccharomyces genomes by phylogenetic footprinting. Science 301, 71-76.
12. Cowles, C.R., Hirschhorn, J.N., Altshuler, D., and Lander, E.S. (2002). Detection of regulatory variation in mouse genes. Nat. Genet. 32, 432-437.
13. Crawford, D.L., Segal, J.A., and Barnett, J.L. (1999). Evolutionary analysis of TATA-less proximal promoter function. Mol. Biol. Evol. 16, 194-207.
14. Dermitzakis, E.T., Bergman, C.M., and Clark, A.G. (2003). Tracing the evolutionary history of Drosophila regulatory regions with models that identify transcription factor binding sites. Mol. Biol. Evol. 20, 703-714.
15. Enard, W., et al. (2002). Intra- and interspecific variation in primate gene expression patterns. Science 296, 340-343.
16. Fay, J.C., and Wu, C.I. (2000). Hitchhiking under positive Darwinian selection. Genetics 155, 1405-1413.
17. Gu, Z.L., Rifkin, S.A., White, K.P., and Li, W.H. (2004). Duplicate genes increase gene expression diversity within and between species. Nat. Genet. 36, 577-579.
18. Guo, M., Rupe, M.A., Zinselmeier, C., Habben, J., Bowen, B.A., and Smith, O.S. (2004). Allelic variation of gene expression in maize hybrids. Plant Cell 16, 1707-1716.
19. Gutierrez, R.A., Ewing, R.M., Cherry, J.M., and Green, P.J. (2002). Identification of unstable transcripts in Arabidopsis by cDNA microarray analysis: Rapid decay is associated with a group of touch- and specific clock-controlled genes. Proc. Natl. Acad. Sci. USA 99, 11513-11518.
20. Hartmann, U., Valentine, W.J., Christie, J.M., Hays, J., Jenkins, G.I., and Weisshaar, B. (1998). Identification of UV/blue light-response elements in the Arabidopsis thaliana chalcone synthase promoter using a homologous protoplast transient expression system. Plant Mol. Biol. 36, 741-754.
21. Higo, K., Ugawa, Y., Iwamoto, M., and Korenaga, T. (1999). Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res. 27, 297-300.
22. Hoeren, F.U., Dolferus, R., Wu, Y.R., Peacock, W.J., and Dennis, E.S. (1998). Evidence for a role for AtMYB2 in the induction of the Arabidopsis alcohol dehydrogenase gene (ADH1) by low oxygen. Genetics 149, 479-490.
23. Hofacker, I.L. (2003). Vienna RNA secondary server. Nucleic Acids Res. 13, 3429-3431.
24. Hudson, R.R., Kreitman, M., and Aguade, M. (1987). A test of neutral molecular evolution based on nucleotide data. Genetics 116, 153-159.
25. Jacobsen, S.E., and Meyerowitz, E.M. (1997). Hypermethylated SUPERMAN epigenetic alleles in Arabidopsis. Science 277, 1100-1103.
26. Jenkins, G.I., Long, J.C., Wade, H.K., Shenton, M.R., and Bibikova, T.N. (2001). UV and blue light signalling: Pathways regulating chalcone synthase gene expression in Arabidopsis. New Phytol. 151, 121-131.
27. Johnson, E.T., and Dowd, P.F. (2004). Differentially enhanced insect resistance, at a cost, in Arabidopsis thaliana constitutively expressing a transcription factor of defensive metabolites. J. Agric. Food Chem. 52, 5135-5138.
28. Khaitovich, P., Weiss, G., Lachmann, M., Hellmann, I., Enard, W., Muetzel, B., Wirkner, U., Ansorge, W., and Paabo, S. (2004). A neutral model of transcriptome evolution. PLoS Biology 2, 682-689.
29. Koch, M.A., Haubold, B., and Mitchell-Olds, T. (2000). Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol. Biol. Evol. 17, 1483-1498.
30. Koch, M.A., Weisshaar, B., Kroymann, J., Haubold, B., and Mitchell-Olds, T. (2001). Comparative genomics and regulatory evolution: Conservation and function of the Chs and Apetala3 promoters. Mol. Biol. Evol. 18, 1882-1891.
31. Lerman, D.N., Michalak, P., Helin, A.B., Bettencourt, B.R., and Feder, M.E. (2003). Modification of heat-shock gene expression in Drosophila melanogaster populations via transposable elements. Mol. Biol. Evol. 20, 135-144.
32. Liu, C.-J., Blount, J.W., Steele, C.L., and Dixon, R.A. (2002). Bottle-necks for metabolic engineering of isoflavone glycoconjugates in Arabidopsis. Proc. Natl. Acad. Sci. USA 99, 14578-14583.
33. Logemann, E., and Hahlbrock, K. (2002). Crosstalk among stress responses in plants: Pathogen defense overrides UV protection through an inversely regulated ACE/ACE type of light-responsive gene promoter unit. Proc. Natl. Acad. Sci. USA 99, 2428-2432.
34. Lomvardas, S., and Thanos, D. (2002). Modifying gene expression programs by altering core promoter chromatin structure. Cell 110, 261-271.
35. Ludwig, M.Z., Bergman, C., Patel, N.H., and Kreitman, M. (2000). Evidence for stabilizing selection in a eukaryotic enhancer element. Nature 403, 564-567.
36. Maleck, K., Levine, A., Eulgem, T., Morgan, A., Schmid, J., Lawton, K.A., Dangl, J.L., and Dietrich, R.A. (2000). The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat. Genet. 26, 403-410.
37. Michalak, P., Minkov, I., Helin, A., Lerman, D.N., Bettencourt, B.R., Feder, M.E., Korol, A.B., and Nevo, E. (2001). Genetic evidence for adaptation-driven incipient speciation of Drosophila melanogaster along a microclimatic contrast in "Evolution Canyon," Israel. Proc. Natl. Acad. Sci. USA 98, 13195-13200.
38. Miyashita, N.T. (2001). DNA variation in the 5′ upstream region of the Adh locus of the wild plants Arabidopsis thaliana and Arabis gemmifera. Mol. Biol. Evol. 18, 164-171.
39. Mol, J., Jenkins, G., Schafer, E., and Weiss, D. (1996). Signal perception, transduction, and gene expression involved in anthocyanin biosynthesis. Crit. Rev. Plant Sci. 15, 525-557.
40. Nei, M. (1987). Molecular Evolutionary Genetics. (New York: Columbia University Press).
41. Neve, B., Froguel, P., Corset, L., Vaillant, E., Vatin, V., and Boutin, P. (2002). Rapid SNP allele frequency determination in genomic DNA pools by pyrosequencing. Biotechniques 32, 1138-1142.
42. Ngai, N., Tsai, F.Y., and Coruzzi, G. (1997). Light-induced transcriptional repression of the pea AS1 gene: Identification of cis-elements and transfactors. Plant J. 12, 1021-1034.
43. Noh, B., and Spalding, E.P. (1998). Anion channels and the stimulation of anthocyanin accumulation by blue light in Arabidopsis seedlings. Plant Physiol. 116, 503-509.
44. Piano, F., Parisi, M.J., Karess, R., and Kambysellis, M.P. (1999). Evidence for redundancy but not trans factor-cis element coevolution in the regulation of Drosophila Yp genes. Genetics 152, 605-616.
45. Ramos-Onsins, S.E., Stranger, B.E., Mitchell-Olds, T., and Aguade, M. (2004). Multilocus analysis of variation and speciation in the closely related species Arabidopsis halleri and A. lyrata. Genetics 166, 373-388.
46. Reymond, P., Weber, H., Damond, M., and Farmer, E.E. (2000). Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12, 707-719.
47. Rockman, M.V., Hahn, M.W., Soranzo, N., Goldstein, D.B., and Wray, G.A. (2003). Positive selection on a human-specific transcription factor binding site regulating IL4 expression. Curr. Biol. 13, 2118-2123.
48. Rozas, J., and Rozas, R. (1999). DnaSP version 3: An integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15, 174-175.
49. Sandelin, A., and Wasserman, W.W. (2004). Constrained binding site diversity within families of transcription factors enhances pattern discovery bioinformatics. J. Mol. Biol. 338, 207-215.
50. Schmid, K.J., Ramos-Onsins, S.E., Ryngis-Beckstein, H., Weisshaar, B., and Mitchell-Olds, T. (January 16, 2005). A multi-locus sequence survey in Arabidopsis thaliana reveals a genome-wide departure from the standard neutral model of sequence evolution. Genetics 10.1534/genetics.104.033795.
51. Schulte, P.M., Glemet, H.C., Fiebig, A.A., and Powers, D.A. (2000). Adaptive variation in lactate dehydrogenase-B gene expression: Role of a stress-responsive regulatory element. Proc. Natl. Acad. Sci. USA 97, 6597-6602.
52. Stone, J.R., and Wray, G.A. (2001). Rapid evolution of cis-regulatory sequences via local point mutations. Mol. Biol. Evol. 18, 1764-1770.
53. Tajima, F. (1983). Evolutionary relationship of DNA sequences in finite populations. Genetics 105, 437-460.
54. Tajima, F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585-595.
55. Thastrom, A., Lowary, P.T., Widlund, H.R., Cao, H., Kubista, M., and Widom, J. (1999). Sequence motifs and free energies of selected natural and non-natural nucleosome positioning DNA sequences. J. Mol. Biol. 288, 213-229.
56. Townsend, J.P. (2004). Resolution of large and small differences in gene expression using models for the Bayesian analysis of gene expression levels and spotted DNA microarrays. BMC Bioinformatics 5, 54.
57. Von Dassow, G., and Odell, G.M. (2002). Design and constraints of the Drosophila segment polarity module: Robust spatial patterning emerges from intertwined cell state switches. J. Exp. Zool. 294, 179-215.
58. Wade, H.K., Bibikova, T.N., Valentine, W.J., and Jenkins, G.I. (2001). Interactions within a network of phytochrome, cryptochrome and UV-B phototransduction pathways regulate chalcone synthase gene expression in Arabidopsis leaf tissue. Plant J. 25, 675-685.
59. Wang, R.L., Stec, A., Hey, J., Lukens, L., and Doebley, J. (1999). The limits of selection during maize domestication. Nature 398, 236-239.
60. Watterson, G.A. (1975). Number of segregating sites in genetic models without recombination. Theor. Popul. Biol. 7, 256-276.
61. Winkel-Shirley, B. (2001). Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol. 126, 485-493.
62. Wittkopp, P.J., Haerum, B.K., and Clark, A.G. (2004). Evolutionary changes in cis and frans gene regulation. Nature 430, 85-88.
63. Wray, G.A., Hahn, M.W., Abouheif, E., Balhoff, J.P., Pizer, M., Rockman, M.V., and Romano, L.A. (2003). The evolution of transcriptional regulation in eukaryotes. Mol. Biol. Evol. 20, 1377-1419.
64. Yan, H., Yuan, W.S., Velculescu, V.E., Vogelstein, B., and Kinzler, K.W. (2002). Allelic variation in human gene expression. Science 297, 1143.