Precise spatio-temporal regulation of the anthocyanin biosynthetic pathway leads to petal spot formation in Clarkia gracilis (Onagraceae)

New Phytologist

Volumn 197, Issue 3, 2013, Pages 958-969

  Martins, Talline R ^a,b   Berg, Jeremy J ^a   Blinka, Steven ^a   Rausher, Mark D ^b   Baum, David A ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b DUKE UNIVERSITY   (United States)

Author keywords

Clarkia; Dihydroflavonol 4 reductase (Dfr); Flower color; Petal spot; Pigment pattern

Indexed keywords

ANTHOCYANIN; MESSENGER RNA; PLANT DNA;

ALLELE; COLOR; DICOTYLEDON; ENZYME ACTIVITY; FLOWER; GENE EXPRESSION; LEAF; PIGMENT; POLLINATOR; POLYMERASE CHAIN REACTION; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; REAL TIME; SPATIOTEMPORAL ANALYSIS;

ARTICLE; BIOSYNTHESIS; CHEMISTRY; CROSS BREEDING; DNA SEQUENCE; FLOWER; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HISTOLOGY; METABOLISM; ONAGRACEAE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANTHOCYANINS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CROSSES, GENETIC; DNA, PLANT; FLOWERS; GENOTYPE; ONAGRACEAE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEQUENCE ANALYSIS, DNA;

CLARKIA; CLARKIA GRACILIS; MAGNOLIOPHYTA; ONAGRACEAE;

EID: 84872152274     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12062     Document Type: Article

References (53)

1. Abdel-Hameed F, Snow R. 1972. The origin of the allotetraploid Clarkia gracilis. Evolution 26: 74-83.
2. Albert NW, Lewis DH, Zhang H, Schwinn KE, Jameson PE, Davies KM. 2011. Members of an R2R3-MYB transcription factor family in Petunia are developmentally and environmentally regulated to control complex floral and vegetative pigmentation patterning. The Plant Journal 65: 771-784.
3. Beldade P, Brakefield PM, Long AD. 2002. Contribution of Distal-less to quantitative variation in butterfly eyespots. Nature 415: 315-318.
4. Borevitz JO, Xia YJ, Blount J, Dixon RA, Lamb C. 2000. Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12: 2383-2393.
5. Carey CC, Strahle JT, Selinger DA, Chandler VL. 2004. Mutations in the pale aleurone color1 regulatory gene of the Zea mays anthocyanin pathway have distinct phenotypes relative to the functionally similar TRANSPARENT TESTA GLABRA1 gene in Arabidopsis thaliana. Plant Cell 16: 450-464.
6. Carroll SB, Gates J, Keys DN, Paddock SW, Panganiban GB, Selegue JE, Williams JA. 1994. Pattern formation and eyespot determination in butterfly wings. Science 265: 109-114.
7. Cone K, Burr F, Burr B. 1986. Molecular analysis of the maize anthocyanin regulatory locus C1. Proceedings of the National Academy of Sciences, USA 83: 9631-9635.
8. DesMarais D, Rausher MD. 2008. Escape from adaptive conflict after duplication in an anthocyanin pathway gene. Nature 454: 762-766.
9. Dorn P, Bloom W. 1984. Anthocyanin variation in an introgressive complex in Clarkia. Biochemical Systematics and Ecology 12: 311-314.
10. Doyle JJ, Doyle JL. 1987. A rapid DNA isolation procedure from small quantities of fresh leaf tissues. Phytochemical Bulletin 19: 11-15.
11. Eckhart M, Rushing S, Hart M. 2006. Frequency dependent pollinator foraging in polymorphic Clarkia xantiana ssp. xantiana populations: implications for flower colour evolution and pollinator interactions. Oikos 112: 412-421.
12. Elomaa P, Mehto M, Kotilainen M, Helariutta Y, Nevalainen L, Teeri T. 1998. A bHLH transcription factor mediates organ, region and flower type specific signals on dihydroflavonol-4-reductase (dfr) gene expression in the inflorescence of Gerbera hybrida (Asteraceae). The Plant Journal 16: 93-99.
13. Fischer T, Halbwirth H, Meisel B, Stich K. 2003. Molecular cloning, substrate specificity of the functionally expressed dihydroflavonol 4-reductases from Malus domestica and Pyrus communis cultivars and the consequences for flavonoid metabolism. Archives of Biochemistry and Biophysics 412: 223-230.
14. Gerats AGM, de Vlaming P, Doodeman M, Al B, Schram AW. 1982. Genetic control of the conversion of dihydroflavonols into flavonols and anthocyanins in flowers of Petunia hybrida. Planta 155: 364-368.
15. Gonzalez A, Zhao M, Leavitt JM, Lloyd AM. 2008. Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. The Plant Journal 53: 814-827.
16. Goodrich J, Carpenter R, Coen ES. 1992. A common gene regulates pigmentation pattern in diverse plant species. Cell 68: 955-964.
17. Gottlieb L, Ford V. 1988. Genetic studies of the pattern of floral pigmentation in Clarkia gracilis. Heredity 60: 237-246.
18. Goulson D, Mcguire K, Munro EE, Adamson S, Colliar L, Park KJ, Tinsley MC, Gilburn AS. 2009. Functional significance of the dark central floret of Daucus carota (Apiaceae) L.; is it an insect mimic? Plant Species Biology 24: 77-82.
19. Harborne JB. 1984. Phytochemical methods: a guide to modern techniques of plant analysis, 2nd edn. London, UK: Chapman and Hall.
20. Hopkins R, Rausher MD. 2011. Indentification of two genes causing reinforcement in the Texas wildflower Phlox drummondii. Nature 469: 411-414.
21. Jackson D, Roberts K, Martin C. 1992. Temporal and spatial control of expression of anthocyanin biosynthetic genes in developing flowers of Antirrhinum majus. The Plant Journal 2: 425-434.
22. Johnson S, Midgley J. 1997. Fly pollination of Gorteria diffusa (Asteraceae), and a possible mimetic function for dark spots on the capitulum. American Journal of Botany 84: 429-436.
23. Johnson E, Ryu S, Yi H, Shin B, Cheong H, Choi G. 2001. Alteration of a single amino acid changes the substrate specificity of dihydroflavonol-4-reductase. The Plant Journal 25: 325-333.
24. Jones K. 1996. Pollinator behavior and postpollination reproductive success in alternative floral phenotypes of Clarkia gracilis (Onagraceae). International Journal of Plant Sciences 157: 733-738.
25. Keys DN, Lewis DL, Selegue JE, Pearson BJ, Goodrich LV, Johnson RL, Gates J, Scott MP, Carroll SB. 1999. Recruitment of a hedgehog regulatory circuit in butterfly eyespot evolution. Science 283: 532-534.
26. Lin-Wang K, Bolitho K, Grafton K, Kortstee A, Karunairetnam S, McGhie TK, Espley RV, Hellens RP, Allan AC. 2010. An R2R3 MYB transcription factor associated with regulation of the anthocyanin biosynthetic pathway in Rosaceae. BMC Plant Biology 10: 50.
27. Ludwig SR, Habera LF, Dellaporta SL, Wessler SR. 1989. Lc, a member of the maize R gene family responsible for tissue-specific anthocyanin production, encodes a protein similar to transcriptional activators and contains the Myc-homology region. Proceedings of the National Academy of Sciences, USA 86: 7092-7096.
28. Maddison DR, Maddison WP. 2000. MacClade 4: analysis of phylogeny and character evolution. Sunderland, MA, USA: Sinauer Associates.
29. Martin C, Prescott A, Mackay S, Bartlett J, Vrijlandt E. 1991. Control of anthocyanin biosynthesis in flowers of Antirrhinum majus. The Plant Journal 1: 37-49.
30. Morita Y, Saitoh M, Hoshino A, Nitasaka E, Iida S. 2006. Isolation of cDNAs for R2R3-MYB, bHLH and WDR transcriptional regulators and identification of c and ca mutations conferring white flowers in the Japanese morning glory. Plant and Cell Physiology 47: 457-470.
31. Nijhout HF. 1980. Pattern formation on Lepidopteran wings: determination of an eyespot. Developmental Biology 80: 267-274.
32. Niu S-S, Xu C-J, Zhang W-S, Zhang B, Li X, Lin-Wang K, Ferguson IB, Allan AC, Chen K-S. 2010. Coordinated regulation of anthocyanin biosynthesis in Chinese bayberry (Myrica rubra) fruit by a R2R3 MYB transcription factor. Planta 231: 887-899.
33. Parker HG, VonHoldt BM, Quignon P, Margulies EH, Shao S, Mosher DS, Spady TC, Elkahloun A, Cargill M, Jones PG et al. 2009. An expressed Fgf4 retrogene is associated with breed-defining chondrodysplasia in domestic dogs. Science 325: 995-998.
34. Paz-Ares J, Ghosal D, Wienand U, Peterson PA, Saedler H. 1987. The regulatory c1 locus of Zea mays encodes a protein with homology to myb proto-oncogene products and with structural similarities to transcriptional activators. EMBO Journal 6: 3553-3558.
35. Paz-Ares J, Wienand U, Peterson P, Saedler H. 1986. Molecular cloning of the c locus of Zea mays: a locus regulating the anthocyanin pathway. EMBO Journal 9: 315-321.
36. Pichersky E, Raguso R, Lewinsohn E. 1994. Floral scent production in Clarkia (Onagraceae) (I. Localization and developmental modulation of monoterpene emission and linalool synthase activity). Plant Physiology 106: 1533-1540.
37. Quattrocchio F, Wing J, van der Woude K, Mol J, Koes R. 1998. Analysis of bHLH and MYB domain proteins: species-specific regulatory differences are caused by divergent evolution of target anthocyanin genes. The Plant journal 13: 475-488.
38. Quattrocchio F, Wing J, van der Woude K, Souer E, de Vetten N, Mol J, Koes R. 1999. Molecular analysis of the anthocyanin2 gene of petunia and its role in the evolution of flower color. Plant Cell 11: 1433-1444.
39. Reed RD, Serfas MS. 2004. Butterfly wing pattern evolution is associated with changes in a Notch/Distal-less temporal pattern formation process. Current Biology 14: 1159-1166.
40. Robinson G, Robinson R. 1931. CLXXXII. A survey of anthocyanins. I. Biochemical Journal 25: 1687-1705.
41. Schwinn K, Venail J, Shang Y, Mackay S, Alm V. 2006. A small family of MYB-regulatory genes controls floral pigmentation intensity and patterning in the genus Antirrhinum. The Plant Cell 18: 831-851.
42. Shang Y, Venail J, Mackay S, Bailey PC, Schwinn KE, Jameson PE, Martin CR, Davies KM. 2011. The molecular basis for venation patterning of pigmentation and its effect on pollinator attraction in flowers of Antirrhinum. New Phytologist 189: 602-615.
43. Shimada N, Sasaki R, Sato S. 2005. A comprehensive analysis of six dihydroflavonol 4-reductases encoded by a gene cluster of the Lotus japonicus genome. Journal of Experimental Botany 56: 2573-2585.
44. Smith S, Rausher MD. 2011. Gene loss and parallel evolution contribute to species difference in flower color. Molecular Biology and Evolution 28: 2799-2810.
45. Soltis P. 1986. Anthocyanidin variation in Clarkia. Biochemical Systematics and Ecology 14: 487-489.
46. Spelt C, Quattrocchio F, Mol JNM, Koes R. 2000. Anthocyanin1 of petunia encodes a basic helix-loop-helix protein that directly activates transcription of structural anthocyanin genes. Plant Cell 12: 1619-1631.
47. Spelt C, Quattrocchio F, Mol J, Koes R. 2002. ANTHOCYANIN1 of petunia controls pigment synthesis, vacuolar pH, and seed coat development by genetically distinct mechanisms. Plant Cell 14: 2121-2135.
48. Swofford DL. 2002. PAUP* phylogenetic analysis using parsimony (*and other methods), version 4.0b10. Sunderland, MA, USA: Sinauer Associates.
49. Tornielli G, Koes R, Quattrocchio F. 2009 The genetics of flower color. In: Gerats T, Strommer J, eds. Petunia, evolutionary, developmental and physiological genetics. New York, NY, USA: Springer, 269-299.
50. Van Kleunen M, Nänni I, Donaldson J, Manning J. 2007. The role of beetle marks and flower colour on visitation by monkey beetles (Hopliini) in the greater cape floral region, South Africa. Annals of Botany 100: 1483-1489.
51. de Vetten N, Quattrocchio F, Mol J, Koes R. 1997. The an11 locus controlling flower pigmentation in petunia encodes a novel WD-repeat protein conserved in yeast, plants, and animals. Genes & Development 11: 1422-1434.
52. Walker AR. 1999. The TRANSPARENT TESTA GLABRA1 Locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 Repeat protein. Plant Cell 11: 1337-1349.
53. Xiao H, Jiang N, Schaffner E, Stockinger EJ, van der Knaap E. 2008. A retrotransposon-mediated gene duplication underlies morphological variation of tomato fruit. Science 319: 1527-1530.