h1 is regulated by C1 (Colorless1) and R1 (Red1) transcription factors. The current study demonstrates that, in addition to its role in anthocyanin biosynthesis, the Zmf3-em class="a-plus-plus">h1 gene also participates in the biosynthesis of 3-deoxyflavonoids and phlobaphenes that accumulate in maize pericarps, cob glumes, and silks. Biosynthesis of 3-deoxyflavonoids is regulated by P1 (Pericarp color1) and is independent from the action of C1 and R1 transcription factors. Results In maize, apiforol and luteoforol are the precursors of condensed phlobaphenes. Maize lines with functional alleles of pr1 and p1 (Pr1;P1) accumulate luteoforol, while null pr1 lines with a functional or non-functional p1 allele (pr1;P1 or pr1;p1) accumulate apiforol. Apiforol lacks a hydroxyl group at the 3-position of the flavylium B-ring, while luteoforol has this hydroxyl group. Our biochemical analysis of accumulated compounds in different pr1 genotypes showed that the pr1 encoded ZmF3’H1 has a role in the conversion of mono-hydroxylated to bi-hydroxylated compounds in the B-ring. Steady state RNA analyses demonstrated that Zmf3-em class="a-plus-plus">h1 mRNA accumulation requires a functional p1 allele. Using a combination of EMSA and ChIP experiments, we established that the Zmf3-em class="a-plus-plus">h1 gene is a direct target of P1. Highlighting the significance of the Zmf3-em class="a-plus-plus">h1 gene for resistance against biotic stress, we also show here that the p1 controlled 3-deoxyanthocyanidin and C-glycosyl flavone (maysin) defence compounds accumulate at significantly higher levels in Pr1 silks as compared to pr1 silks. By virtue of increased maysin synthesis in Pr1 plants, corn ear worm larvae fed on Pr1; P1 silks showed slower growth as compared to pr1; P1 silks. Conclusions Our results show that the Zmf3-em class="a-plus-plus">h1 gene participates in the biosynthesis of phlobaphenes and agronomically important 3-deoxyflavonoid compounds under the regulatory control of P1." />
Expression of flavonoid 3-hydroxylase is controlled by P1, the regulator of 3-deoxyflavonoid biosynthesis in maize
详细信息    查看全文
  • 作者：Mandeep Sharma (1)
    Chenglin Chai (2)
    Kengo Morohashi (2)
    Erich Grotewold (2)
    Maurice E Snook (3)
    Surinder Chopra (1)
  • 关键词：Anthocyanins ; Flavones ; Flavonoids ; F3’H ; Maysin ; Phlobaphenes
  • 刊名：BMC Plant Biology
  • 出版年：2012
  • 出版时间：December 2012
  • 年：2012
  • 卷：12
  • 期：1
  • 全文大小：681KB
  • 参考文献：1. Koes R, Verweij W, Quattrocchio F: Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. / Trends Plant Sci 2005,10(5):236-42. CrossRef
    2. Coe EH, Neuffer MG, Hoisington DA: The genetics of corn. In / Corn and corn improvement. Edited by: Sprague GF, Dudley JW. American Society of Agronomy, Crop Science Society of America and Soil Science Society of America, Madison; 1988.
    3. Styles ED, Ceska O: Genetic control of 3-hydroxy- and 3-deoxy-flavonoids in Zea mays [maize]. / Phytochemistry 1975,14(2):413-15. CrossRef
    4. McMullen MD, Frey M, Degenhardt J: Genetics and biochemistry of insect resistance in maize. In / Handbook of Maize: Its Biology. Edited by: Bennetzen J, Hake S. Springer, New York; 2009:271-89. CrossRef
    5. Waiss ACJ, Chan BG, Elliger CA, Wiseman BR, McMillian WW, Widstrom NW, Zuber MS, Keaster AJ: Maysin, a flavone glycoside from corn silks with antibiotic activity toward corn earworm. / J Econ Entomol 1979,72(2):256-58.
    6. Casati P, Walbot V: Differential accumulation of maysin and rhamnosylisoorientin in leaves of high-altitude landraces of maize after UV-B exposure. / Plant Cell Environ 2005,28(6):788-99. CrossRef
    7. Cone KC, Cocciolone SM, Burr FA, Burr B: Maize anthocyanin regulatory gene pl is a duplicate of c1 that functions in the plant. / Plant Cell 1993,5(12):1795-805.
    8. Ludwig SR, Wessler SR: Maize R gene family: Tissue-specific helix-loop-helix proteins. / Cell 1990,62(5):849-51. CrossRef
    9. Chandler VL, Radicella JP, Robbins TP, Chen J, Turks D: Two regulatory genes of the maize anthocyanin pathway are homologous: isolation of B utilizing R genomic sequences. / Plant Cell 1989,1(12):1175-183.
    10. Goff SA, Cone KC, Chandler VL: Functional analysis of the transcriptional activator encoded by the maize B gene: evidence for a direct functional interaction between two classes of regulatory proteins. / Genes Dev 1992,6(5):864-75. CrossRef
    11. Grotewold E, Sainz MB, Tagliani L, Hernandez JM, Bowen B, Chandler VL: Identification of the residues in the Myb domain of maize C1 that specify the interaction with the bHLH cofactor R. / Proc Natl Acad Sci USA 2000,97(25):13579-3584. CrossRef
    12. Grotewold E, Drummond BJ, Bowen B, Peterson T: The myb-homologous P gene controls phlobaphene pigmentation in maize floral organs by directly activating a flavonoid biosynthetic gene subset. / Cell 1994,76(3):543-53. CrossRef
    13. Zhang P, Chopra S, Peterson T: A segmental gene duplication generated differentially expressed myb-homologous genes in maize. / Plant Cell 2000,12(12):2311-322.
    14. Zhang P, Wang Y, Zhang J, Maddock S, Snook M, Peterson T: A maize QTL for silk maysin levels contains duplicated Myb-homologous genes which jointly regulate flavone biosynthesis. / Plant Mol Biol 2003,52(1):1-5. CrossRef
    15. Byrne PF, McMullen MD, Snook ME, Musket TA, Theuri JM, Widstrom NW, Wiseman BR, Coe EH: Quantitative trait loci and metabolic pathways: genetic control of the concentration of maysin, a corn earworm resistance factor, in maize silks. / Proc Natl Acad Sci USA 1996,93(17):8820-825. CrossRef
    16. McMullen MD, Snook M, Lee EA, Byrne PF, Kross H, Musket TA, Houchins K, Coe EH Jr: The biological basis of epistasis between quantitative trait loci for flavone and 3-deoxyanthocyanin synthesis in maize (Zea mays L.). / Genome 2001,44(4):667-76.
    17. Grotewold E, Chamberlin M, Snook M, Siame B, Butler L, Swenson J, Maddock S, Clair G, Bowen B: Engineering secondary metabolism in maize cells by ectopic expression of transcription factors. / Plant Cell 1998,10(5):721-40.
    18. Quattrocchio F, Baudry A, Lepiniec L, Grotewold E: The regulation of flavonoid biosynthesis. In / The science of flavonoids. Edited by: Grotewold E. Springer, New York; 2006:97-22. CrossRef
    19. Pooma W, Gersos C, Grotewold E: Transposon insertions in the promoter of the Zea mays a1 gene differentially affect transcription by the Myb factors P and C1. / Genetics 2002,161(2):793-01.
    20. Tuerck JA, Fromm ME: Elements of the maize A1 promoter required for transactivation by the anthocyanin B/C1 or phlobaphene P regulatory genes. / Plant Cell 1994,6(11):1655-663.
    21. Morohashi K, Casas MI, Ferreyra LF, Mejía-Guerra MK, Pourcel L, Yilmaz A, Feller A, Carvalho B, Emiliani J, Rodriguez E, Pellegrinet S, McMullen M, Casati P, Grotewold E: A genome-wide regulatory framework identifies maize Pericarp Color1 (P1) controlled genes. / Plant Cell 2012,24(7):2745-764. CrossRef
    22. Forkmann G: Flavonoids as flower pigments: the formation of the natural spectrum and its extension by genetic engineering. / Plant Breed 1991,106(2):1-6. CrossRef
    23. Larson RL, Bussard JB: Microsomal flavonoid 3-monooxygenase from maize seedlings. / Plant Physiol 1986,80(2):483-86. CrossRef
    24. Sharma M, Cortes-Cruz M, Ahern KR, McMullen M, Brutnell TP, Chopra S: Identification of the pr1 gene product completes the anthocyanin biosynthesis pathway of maize. / Genetics 2011,188(1):69-9. CrossRef
    25. Lee EA, Byrne PF, McMullen MD, Snook ME, Wiseman BR, Widstrom NW, Coe EH: Genetic mechanisms underlying apimaysin and maysin synthesis and corn earworm antibiosis in maize (Zea mays L.). / Genetics 1998,149(4):1997-006.
    26. Cortes-Cruz M, Snook M, McMullen MD: The genetic basis of C-glycosyl flavone B-ring modification in maize (Zea mays L.) silks. / Genome 2003,46(2):182-94. CrossRef
    27. Boddu J, Svabek C, Sekhon R, Gevens A, Nicholson R, Jones DJP, Gustine D, Chopra S: Expression of a putative flavonoid 3-hydroxylase in sorghum mesocotyls synthesizing 3-deoxyanthocyanidin phytoalexins. / Physiol Mol Plant Pathol 2004,65(2):101-13. CrossRef
    28. McMullen MD, Kross H, Snook ME, Cortes-Cruz M, Houchins KE, Musket TA, Coe EH Jr: Salmon silk genes contribute to the elucidation of the flavone pathway in maize (Zea mays L.). / J Hered 2004,95(3):225-33. CrossRef
    29. Meyers MT: A second recessive factor for brown pericarp in maize. / Ohio J Sci 1927, 27:295-00.
    30. Emerson RA, Beadle GW, Fraser AC: A summary of linkage studies in maize. / Cornell Univ Agric Exp Stn Mem 1935, 180:1-0.
    31. Winkel-Shirley B: Biosynthesis of flavonoids and effects of stress. / Curr Opin Plant Biol 2002,5(3):218-23. CrossRef
    32. Ferreyra ML, Rius S, Emiliani J, Pourcel L, Feller A, Morohashi K, Casati P, Grotewold E: Cloning and characterization of a UV-B-inducible maize flavonol synthase. / Plant J 2010,62(1):77-1. CrossRef
    33. Chopra S, Gevens A, Svabek C, Wood KV, Peterson T, Nicholson RL: Excision of the Candystripe1 transposon from a hyper-mutable Y1-cs allele shows that the sorghum y1 gene control the biosynthesis of both 3-deoxyanthocyanidin phytoalexins and phlobaphene pigments. / Physiol Mol Plant Pathol 2002,60(6):321-30.
    34. Aguero ME, Gevens A, Nicholson RL: Interaction of Cochliobolus heterostrophus with phytoalexin inclusions in Sorghum bicolor. / Physiol Mol Plant Pathol 2002,61(5):267-71. CrossRef
    35. Snyder BA, Nicholson RL: Synthesis of phytoalexins in sorghum as a site-specific response to fungal ingress. / Science 1990,248(4963):1637-639. CrossRef
    36. Snook ME, Gueldner RC, Widstrom NW, Wiseman BR, Himmelsbach DS, Harwood JS, Costello CE: Levels of maysin and maysin analogs in silks of maize germplasm. / J Agric Food Chem 1993,41(9):1481-485. CrossRef
    37. Larson R, Bussard JB, Coe EH Jr: Gene-dependent flavonoid 3-hydroxylation in maize. / Biochem Genet 1986,24(7-):615-24. CrossRef
    38. Winkel-Shirley B: Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. / Plant Physiol 2001,126(2):485-93. CrossRef
    39. Chopra S, Hoshino A, Boddu J, Iida S: Flavonoid pigments as tools in molecular genetics. In / The science of flavonoids. Edited by: Grotewold E. Springer, New York; 2006:147-73. CrossRef
    40. Hahlbrock K, Scheel D: Physiology and molecular biology of phenylpropanoid metabolism. / Annu Rev Plant Physiol Plant Mol Biol 1989, 40:347-69. CrossRef
    41. Byrne PF, Darrah LL, Snook M, Wiseman BR, Widstrom NW, Moellenbeck DJ, Barry BD: Maize silk-browning, maysin content, and antibiosis to the corn earworm, Helicoverpa zea (Boddie). / Maydica 1996,41(1):13-8.
    42. Ibraheem F, Gaffoor I, Chopra S: Flavonoid phytoalexin-dependent resistance to anthracnose leaf blight requires a functional yellow seed1 in Sorghum bicolor. / Genetics 2010,184(4):915-26. CrossRef
    43. Nicholson RL, Kollipara SS, Vincent JR, Lyons PC, Cadena-Gomez G: Phytoalexin synthesis by the sorghum mesocotyl in response to infection by pathogenic and nonpathogenic fungi. / Proc Natl Acad Sci USA 1987,84(16):5520-524. CrossRef
    44. Lo SC, Verdier KD, Nicholson RL: Accumulation of 3-deoxyanthocyanidin phytoalexins and resistance to Colletotrichum sublineolum in sorghum. / Physiol Mol Plant Pathol 1999,55(5):263-73. CrossRef
    45. Zanta CA, Yang X, Axtell JD, Bennetzen JL: The candystripe locus, y-cs, determines mutable pigmentation of the sorghum leaf, flower, and pericarp. / J Hered 1994,85(1):23-9.
    46. Boddu J, Svabek C, Ibraheem F, Jones AD, Chopra S: Characterization of a deletion allele of a sorghum Myb gene yellow seed1 showing loss of 3-deoxyflavonoids. / Plant Sci 2005,169(3):542-52. CrossRef
    47. Lindroth R, Peterson SS: Effects of plant phenols on performance of southern armyworm larvae. / Oecologia 1988,75(2):185-98. CrossRef
    48. Elliger CA, Chan BG, Waiss ACJ: Flavonoids as larval growth inhibitors. / Naturwissenschaften 1980,67(7):358-60. CrossRef
    49. Snook ME, Widstrom NW, Wiseman BR, Gueldner RC, Wilson RL, Himmelsbach DS, Harwood JS, Costello CE: New flavoneC-glycosides from corn (Zea maysL.) for the control of the corn earworm (Helicoverpa zea). In / Bioregulators for Crop protection and pest control symposium. Edited by: Hedin PA. American Chemical Society Symposium Series #557, Washington, D.C; 1994:122-35. CrossRef
    50. Duffey SS, Stout MJ: Antinutritive and toxic components of plant defense against insects. / Arch Insect Biochem 1996,32(1):3-7. CrossRef
    51. Szalma SJ, Buckler ES, Snook ME, McMullen MD: Association analysis of candidate genes for maysin and chlorogenic acid accumulation in maize silks. / Theor Appl Genet 2005,110(7):1324-333. CrossRef
    52. Szalma SJ, Snook ME, Bushman BS, Houchins KE, McMullen MD: Duplicate loci as QTL: the role of chalcone synthase loci in flavone and phenylpropanoid biosynthesis in maize. / Crop Sci 2002,42(5):1679-687. CrossRef
    53. Byrne PF, McMullen MD, Wiseman BR, Snook ME, Musket TA, Theuri JM, Widstrom NW, Coe EH: Maize silk maysin concentration and corn earworm antibiosis: Qtls and genetic mechanisms. / Crop Sci 1998,38(2):461-71. CrossRef
    54. Halbwirth H, Fischer TC, Roemmelt S, Spinelli F, Schlangen K, Peterek S, Sabatini E, Messina C, Speakman JB, Andreotti C, Rademacher W, Bazzi C, Costa G, Treutter D, Forkmann G, Stich K: Induction of antimicrobial 3-deoxyflavonoids in pome fruit trees controls fire blight. / Z Naturforsch [C] 2003,58(11-2):765-70.
    55. Nicholson RL, Hammerschmidt R: Phenolic compounds and their role in disease resistance. / Ann Rev Phytopathol 1992, 30:369-89. CrossRef
    56. Polacco M: Maize genetic nomenclature guide. In / TIG genetic nomenclature guide. vol. S.20–S.21 edition. Edited by: Wood R. Elsevier Science, Amsterdam; 1998:1-9.
    57. Brink RA, Styles ED: A collection of pericarp factors. / Maize Genet Coop News Lett 1966, 40:149-60.
    58. Cocciolone SM, Chopra S, Flint-Garcia SA, McMullen MD, Peterson T: Tissue-specific patterns of a maize Myb transcription factor are epigenetically regulated. / Plant J 2001,27(5):467-78. CrossRef
    59. Emerson RA: Genetic studies of variegated pericarp in maize. / Genetics 1917,2(1):1-5.
    60. Anderson EG: Pericarp studies in maize: II. The allelomorphism of a series of factors for pericarp color. / Genetics 1924,9(5):442-53.
    61. Grotewold E, Athma P, Peterson T: A possible hot spot for Ac insertion in the maize P gene. / Mol Gen Genet 1991,230(1-):329-31. CrossRef
    62. Athma P, Peterson T: Ac induces homologous recombination at the maize P locus. / Genetics 1991,128(1):163-73.
    63. Zhang J, Peterson T: Genome rearrangements by nonlinear transposons in maize. / Genetics 1999,153(3):1403-410.
    64. Watterson JJ, Butler LJ: Occurance of an unusual leucoanthocyanidin and absence of proanthocyanidins in sorghum leaves. / J Agric Food Chem 1983,31(1):41-5. CrossRef
    65. Stich K, Forkmann G: Biosynthesis of 3-deoxyanthocyanins in flower extracts from Sinningia cardinalis. / Phytochemistry 1988,27(3):785-89. CrossRef
    66. Stafford HA: / Flavonoid metabolism. CRC press, Boca Raton, FL; 1990.
    67. Wienand U, Weydemann U, Niesbach-Klosgen U, Peterson PA, Saedler H: Molecular cloning of the c2 locus of Zea mays, the gene coding for chalcone synthase. / Mol Gen Genet 1986,203(2):202-07. CrossRef
    68. Grotewold E, Peterson T: Isolation and characterization of a maize gene encoding chalcone flavonone isomerase. / Mol Gen Genet 1994,242(1):1-.
    69. Schwarz-Sommer Z, Shepherd N, Tacke E, Gierl A, Rohde W, Leclercq L, Mattes M, Berndtgen R, Peterson PA, Saedler H: Influence of transposable elements on the structure and function of the A1 gene of Zea mays. / EMBO J 1987,6(2):287-94.
    70. Grotewold E, Athma P, Peterson T: Alternatively spliced products of the maize P gene encode proteins with homology to the DNA-binding domain of myb-like transcription factors. / Proc Natl Acad Sci USA 1991,88(11):4587-591. CrossRef
    71. Boddu J, Jiang C, Sangar V, Olson T, Peterson T, Chopra S: Comparative structural and functional characterization of sorghum and maize duplications containing orthologous myb transcription regulators of 3-deoxyflavonoid biosynthesis. / Plant Mol Biol 2006,60(2):185-99. CrossRef
    72. Mejia-Guerra MK, Pomeranz M, Morohashi K, Grotewold E: From plant gene regulatory grids to network dynamics. / Biochim Biophys Acta 2012,1819(5):454-65. CrossRef
    73. Hernandez JM, Heine GF, Irani NG, Feller A, Kim MG, Matulnik T, Chandler VL, Grotewold E: Different mechanisms participate in the R-dependent activity of the R2R3 MYB transcription factor C1. / J Biol Chem 2004,279(46):48205-8213. CrossRef
    74. Snook ME, Widstrom NW, Gueldner RC: Reversed phase high-performance liquid chromatographic procedure for the determination of maysin in corn silks. / J Chromatogr 1989, 477:439-47. CrossRef
    75. Jacob D, Chippendale GM: Growth and development of the southwestern corn borer, Diatraea grandiosella, on a meridic diet. / Ann Entomol Soc Am 1971,64(2):485-88.
  • 作者单位：Mandeep Sharma (1)
    Chenglin Chai (2)
    Kengo Morohashi (2)
    Erich Grotewold (2)
    Maurice E Snook (3)
    Surinder Chopra (1)

    1. Department of Plant Science, Pennsylvania State University, University Park, Pennsylvania, PA, 16802, USA
    2. Center for Applied Plant Sciences and Department of Molecular Genetics, Ohio State University, Columbus, OH, 43210, USA
    3. USDA-ARS, Russell Research Center, 950 College Station Road, Athens, GA, 30605, USA
文摘
Background The maize (Zea mays) red aleurone1 (pr1) encodes a CYP450-dependent flavonoid 3-hydroxylase (ZmF3’H1) required for the biosynthesis of purple and red anthocyanin pigments. We previously showed that Zmf3-em class="a-plus-plus">h1 is regulated by C1 (Colorless1) and R1 (Red1) transcription factors. The current study demonstrates that, in addition to its role in anthocyanin biosynthesis, the Zmf3-em class="a-plus-plus">h1 gene also participates in the biosynthesis of 3-deoxyflavonoids and phlobaphenes that accumulate in maize pericarps, cob glumes, and silks. Biosynthesis of 3-deoxyflavonoids is regulated by P1 (Pericarp color1) and is independent from the action of C1 and R1 transcription factors. Results In maize, apiforol and luteoforol are the precursors of condensed phlobaphenes. Maize lines with functional alleles of pr1 and p1 (Pr1;P1) accumulate luteoforol, while null pr1 lines with a functional or non-functional p1 allele (pr1;P1 or pr1;p1) accumulate apiforol. Apiforol lacks a hydroxyl group at the 3-position of the flavylium B-ring, while luteoforol has this hydroxyl group. Our biochemical analysis of accumulated compounds in different pr1 genotypes showed that the pr1 encoded ZmF3’H1 has a role in the conversion of mono-hydroxylated to bi-hydroxylated compounds in the B-ring. Steady state RNA analyses demonstrated that Zmf3-em class="a-plus-plus">h1 mRNA accumulation requires a functional p1 allele. Using a combination of EMSA and ChIP experiments, we established that the Zmf3-em class="a-plus-plus">h1 gene is a direct target of P1. Highlighting the significance of the Zmf3-em class="a-plus-plus">h1 gene for resistance against biotic stress, we also show here that the p1 controlled 3-deoxyanthocyanidin and C-glycosyl flavone (maysin) defence compounds accumulate at significantly higher levels in Pr1 silks as compared to pr1 silks. By virtue of increased maysin synthesis in Pr1 plants, corn ear worm larvae fed on Pr1; P1 silks showed slower growth as compared to pr1; P1 silks. Conclusions Our results show that the Zmf3-em class="a-plus-plus">h1 gene participates in the biosynthesis of phlobaphenes and agronomically important 3-deoxyflavonoid compounds under the regulatory control of P1.

© 2004-2018 中国地质图书馆版权所有 京ICP备05064691号 京公网安备11010802017129号

地址：北京市海淀区学院路29号 邮编：100083

电话：办公室：(+86 10)66554848；文献借阅、咨询服务、科技查新：66554700