Characterization of an AGAMOUS-like MADS Box Protein, a Probable Constituent of Flowering and Fruit Ripening Regulatory System in Banana

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Roy Choudhury, Swarup ^a,b   Roy, Sujit ^a,c   Nag, Anish ^a   Singh, Sanjay Kumar ^a   Sengupta, Dibyendu N ^a  

^a BOSE INSTITUTE   (India)

^b DONALD DANFORTH PLANT SCIENCE CENTER   (United States)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGAMOUS MADS BOX PROTEIN; COMPLEMENTARY DNA; HOMODIMER; MA MADS5 PROTEIN; MADS DOMAIN PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BANANA; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONSENSUS SEQUENCE; CONTROLLED STUDY; FLOWER MORPHOLOGY; FLOWERING; FRUIT MORPHOLOGY; FRUIT RIPENING; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; IN VITRO STUDY; IN VIVO STUDY; MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHYLOGENY; PLANT GENE; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN DNA INTERACTION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; BASE SEQUENCE; CELL NUCLEUS; CLONING, MOLECULAR; DIMERIZATION; DNA, COMPLEMENTARY; DNA, PLANT; FLOWERS; FRUIT; GENE EXPRESSION REGULATION, PLANT; MADS DOMAIN PROTEINS; MOLECULAR SEQUENCE DATA; MUSA; PLANT PROTEINS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION FACTORS;

MUSA;

EID: 84866304893     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0044361     Document Type: Article

References (70)

1. Messenguy F, Dubois E, (2003) Role of MADS box proteins and their cofactors in combinatorial control of gene expression and cell development. Gene 316: 1-21.
2. Cho SC, Jang SH, Chae SJ, Chung KM, Moon YH, et al. (1999) Analysis of the C-terminal region of Arabidopsis thaliana APETALA1 as a transcription activation domain. Plant Mol Biol 40: 419-29.
3. de Folter S, Angenent GC, (2006) Trans meets cis in MADS science. Trends Plant Sci 11: 224-231.
4. Yanofsky MH, Ma H, Bowman JL, Drews GN, Feldman KA, et al. (1990) The protein encoded by the Arabidopsis thaliana homeotic gene agamous resembles transcription factors. Nature 346: 35-39.
5. Honma T, Goto K, (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409: 525-529.
6. Theissen G, Saedler H, (2001) Plant biology. Floral quartets. Nature 409: 469-471.
7. Giovannoni JJ, (2007) Fruit ripening mutants yield insights into ripening control. Curr Opin Plant Biol 10: 283-289.
8. Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, et al. (2002) A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. Science 296: 343-346.
9. Seymour GB, Ryder CD, Cevik V, Hammond JP, Popovich A, et al. (2011) A SEPALLATA gene is involved in the development and ripening of strawberry (Fragaria X ananassa Duch.) fruit, a non-climacteric tissue. J Exp Bot 62: 1179-1188.
10. Yao J, Kvarnheden A, Morris B, (1999) Seven MADS-box genes in apple are expressed in different parts of the fruit. J Am Soc Hortic Sci 124: 8-13.
11. Boss PK, Vivier M, Matsumoto S, Dry IB, Thomas MR, (2001) A cDNA from grapevine (Vitis vinifera L.), which shows homology to AGAMOUS and SHATTERPROOF, is not only expressed in flowers but also throughout berry development. Plant Mol Biol 45: 541-553.
12. Tadiello A, Pavanello A, Zanin D, Caporali E, Colombo L, et al. (2009) A PLENA-like gene of peach is involved in carpel formation and subsequent transformation into a fleshy fruit. J Exp Bot 60: 651-661.
13. Elitzur T, Vrebalov J, Giovannoni JJ, Goldschmidt EE, Friedman H, (2010) The regulation of MADS-box gene expression during ripening of banana and their regulatory interaction with ethylene. J Exp Bot 61: 1523-1535.
14. Huang H, Mizukami Y, Ma H, (1993) Isolation and characterization of the binding sequences for the product of the Arabidopsis floral homeotic gene AGAMOUS. Nucleic Acids Res 21: 4769-4776.
15. Shiraishi H, Okada K, Shimura Y, (1993) Nucleotide sequences recognized by the AGAMOUS MADS domain of Arabidopsis thaliana in vitro. Plant J 4: 385-398.
16. Lockhart SR, Nguyen M, Srikantha T, Soll DR, (1998) A MADS Box protein consensus binding site is necessary and sufficient for activation of the opaque-phase-specific gene OP4 of Candida albicans. J Bacteriology 180: 6607-6616.
17. Huang H, Tudor M, Weiss C, Hu Y, Ma H, (1995) The Arabidopsis MADS-box gene AGL3 is widely expressed and encodes a sequence-specific DNA-binding protein. Plant Mol Biol 28: 549-567.
18. Huang H, Tudor M, Su T, Zhang Y, Hu Y, et al. (1996) DNA binding properties of two Arabidopsis MADS domain proteins: binding consensus and dimer formation. Plant Cell 8: 81-94.
19. West AG, Sharrocks AD, Causier BE, Davies B, (1998) DNA binding and dimerisation determinants of Antirrhinum majus MADS-box transcription factors. Nucleic Acids Res 26: 5277-5287.
20. Tang W, Perry SE, (2003) Binding site selection for the plant MADS-domain protein AGL15: an in vitro and in vivo study. J Biol Chem 278: 28154-28159.
21. Ito Y, Kitagawa M, Ihashi N, Yabe K, Kimbara J, et al. (2008) DNA-binding specificity, transcriptional activation potential, and the rin mutation effect for the tomato fruit-ripening regulator RIN. Plant J 55: 212-223.
22. Marchler-Bauer A, Anderson JB, Derbyshire MK, DeWeese-Scott C, Gonzales NR, et al. (2007) CDD: a conserved domain database for interactive domain family analysis. Nucleic Acids Res 35: D237-D240.
23. Letunic I, Copley RR, Schmidt S, Ciccarelli FD, Doerks T, et al. (2004) SMART 4.0: towards genomic data integration. Nucleic Acids Res 32: D142-D144.
24. Theissen G, Becker A, Rosa AD, Kanno A, Kim JT, et al. (2000) A short history of MADS-box genes in plants. Plant Mol Biol 42: 115-149.
25. Santelli E, Richmond TJ, (2000) Crystal structure of MEF2A core bound to DNA at 1.5 A° resolution. J Mol Biol 297: 437-449.
26. Liu J, Xu B, Hu L, Li M, Su W, et al. (2009) Involvement of a banana MADS-box transcription factor gene in ethylene-induced fruit ripening. Plant Cell Rep 28: 103-111.
27. Sharrocks AD, Shore P, (1995) DNA bending in the ternary nucleoprotein complex at the c-fos promoter. Nucleic Acids Res 23: 2442-2449.
28. Manning K, Tor M, Poole M, Hong Y, Thompson A, et al. (2006) A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat Genet 38: 948-952.
29. Roy Choudhury S, Roy S, Saha PP, Singh SK, Sengupta DN, (2008a) Characterization of differential ripening pattern in association with ethylene biosynthesis in the fruits of five naturally occurring banana cultivars and detection of a GCC-box specific DNA binding protein. Plant Cell Rep 27: 1235-49.
30. Wang XL, Peng XX, (2001a) Cloning of promoter of fruit-specific ACC synthase gene and primary study on its function. Chin J Biotechnol 17: 293-296.
31. Wang XL, Peng XX, (2001b) Cloning of banana fruit ripening-related ACO1 and primary study on its function. Chin J Biotechnol 17: 428-431.
32. Trivedi P, Nath P, (2004) MaExp1, an ethylene-induced expansin from ripening banana fruit. Plant Sci 6: 1351-1358.
33. Xu BY, Liu G, Jin ZQ, (2006) Isolation, sequencing analysis and characterization of the promoter of banana lectin gene. Chin J Biotechnol 22: 945-949.
34. Roy Choudhury S, Roy S, Das R, Sengupta DN, (2008b) Differential transcriptional regulation of banana sucrose phosphate synthase gene in response to ethylene, auxin, wounding, low temperature and different photoperiods during fruit ripening and functional analysis of banana SPS gene promoter. Planta 229: 207-23.
35. Fujisawa M, Nakano T, Ito Y, (2011) Identification of potential target genes for the tomato fruit-ripening regulator RIN by chromatin immunoprecipitation. BMC Plant Biol 11: 26.
36. Roy Choudhury S, Roy S, Sengupta DN, (2008c) Characterization of transcriptional profiles of MA-ACS1 and MA-ACO1 genes in response to ethylene, auxin, wounding, cold and different photoperiods during ripening in banana fruit. J Plant Physiol 165: 1865-78.
37. Pellegrini L, Tan S, Richmond TJ, (1995) Structure of serum response factor core bound to DNA. Nature 376: 490-498.
38. Riechmann JL, Krizek BA, Meyerowitz EM, (1996) Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS. Proc Natl Acad Sci U S A 93: 4793-4798.
39. West AG, Shore P, Sharrocks AD, (1997) DNA binding by MADS-box transcription factors: a molecular mechanism for differential DNA bending. Mol Cell Biol 17: 2876-2887.
40. Garcia-Maroto F, Carmona M-J, Garrido J-A, Vilches-Ferron M, Rodriguez-Ruiz J, et al. (2003) New roles for MADS-box genes in higher plants. Biol Plant 46: 321-330.
41. Busi MV, Bustamante C, D'Angelo C, Hidalgo-Cuevas M, Boggio SB, et al. (2003) MADS-box genes expressed during tomato seed and fruit development. Plant Molecular Biology 52: 801-815.
42. Martel C, Vrebalov J, Tafelmeyer P, Giovannoni JJ, (2011) The tomato MADS-Box transcription factor RIPENING INHIBITOR interacts with promoters involved in numerous ripening processes in a COLORLESS NONRIPENING-dependent manner. Plant Physiol 157: 1568-1579.
43. Roy Choudhury S, Roy S, Sengupta DN, (2009) A comparative study of cultivar differences in sucrose phosphate synthase gene expression and sucrose formation during banana fruit ripening. Postharvest Biol Technol 54: 15-24.
44. Peumans WJ, Zhang W, Barre A, Houles-Astoul C, Balint-Kurti P, et al. (2000) Fruit-specific lectins from banana and plantain. Planta 211: 546-554.
45. Kramer EM, Jaramillo MA, Di Stilio VS, (2004) Patterns of gene duplication and functional evolution during the diversification of the AGAMOUS subfamily of MADS box genes in angiosperms. Genetics 166: 1011-23.
46. Causier B, Castillo R, Zhou J, Ingram R, Xue Y, et al. (2005) Evolution in action: Following function in duplicated floral homeotic genes. Curr Biol 15: 1508-1512.
47. Bradley D, Carpenter R, Sommer H, Hartley N, Coen E, (1993) Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of Antirrhinum. Cell 72: 85-95.
48. Davies B, Motte P, Keck E, Saedler H, Sommer H, et al. (1999) PLENA and FARINELLI: redundancy and regulatory interactions between two Antirrhinum MADS-box factors controlling flower development. EMBO J 18: 4023-34.
49. Ito T, Ng KH, Lim TS, Yu H, Meyerowitz EM, (2007) The homeotic protein AGAMOUS controls late stamen development by regulating a jasmonate biosynthetic gene in Arabidopsis. Plant Cell 19: 3516-3529.
50. Liljegren SJ, Ditta GS, Eshed Y, Savidge B, Bowman JL, et al. (2000) SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404: 766-770.
51. Flanagan CA, Hu Y, Ma H, (1996) Specific expression of the AGL1 MADS-box gene suggests regulatory functions in Arabidopsis gynoecium and ovule development. Plant J 10: 343-353.
52. Pinyopich A, Ditta GS, Baumann E, Wisman E, Yanofsky MF, (2003) Unraveling the redundant roles of MADS-box genes during carpel and fruit development. Nature 424: 85-88.
53. Hileman LC, Sundstrom JF, Litt A, Chen M, Shumba T, et al. (2006) Molecular and phylogenetic analyses of the MADS-box gene family in tomato. Mol Biol Evol 23: 2245-2258.
54. Pnueli L, Hareven D, Rounsley SD, Yanofsky MF, Lifschitz E, (1994) Isolation of the tomato AGAMOUS gene TAG1 and analysis of its homeotic role in transgenic plants. Plant Cell 6: 163-173.
55. Itkin M, Seybold H, Breitel D, Rogachev I, Meir S, et al. (2009) TOMATO AGAGAMOUS-LIKE1 is a component of the fruit ripening regulatory network. Plant J 60: 1081-1095.
56. Pan IL, McQuinn R, Giovannoni JJ, Irish VF, (2010) Functional diversification of AGAMOUS lineage genes in regulating tomato flower and fruit development. J Exp Bot 61: 1795-1806.
57. Inaba A, Nakamura R, (1986) Effect of exogenous ethylene concentration and fruit temperature on the minimum treatment time necessary to induce ripening in banana fruit. J Jpn Soc Hortic Sci 55: 348-354.
58. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York.
59. Chattopadhyay S, Ang LH, Puente P, Deng XW, Wei N, (1998) Arabidopsis bZIP protein HY5 directly interacts with light-responsive promoters in mediating light control of gene expression. Plant Cell 10: 673-684.
60. Stenger D, Gruissem W, Baginsky S, (2004) Mass spectrometric identification of RNA binding proteins from dried EMSA gels. J Proteome Res 3: 662-664.
61. Shevchenko A, Wilm M, Vorm O, Mann M, (1996) Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal Chem 68: 850-858.
62. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
63. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higguns DG, (1997) The CLUSTAL X Windows Interface: Flexible stratgies for multiple sequene alignment aided by quality analysis tools. Nucleic Acids Res 24: 4876-4882.
64. Kumar S, Tamura K, Jakobsen IB, Masatoshi N, (2001) MEGA2: Molecular evolutionary genetics analysis software. Bioinformatics 17: 1244-1245.
65. Kerppola TK, Curran T, (1993) Selective DNA bending by a variety of bZIP proteins. Mol Cell Biol 13: 5479-5489.
66. Drak J, Crothers DM, (1991) Helical repeat and chirality effects on DNA gel electrophoretic mobility. Proc Natl Acad Sci U S A 88: 3074-3078.
67. Lane D., Harlow E. (1988) Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
68. Paciorek T, Friml J, (2006) Auxin signalling. J Cell Sci 119: 1199-1202.
69. Bhattacharya J, Das KP, (1998) α-Crystallin does not require temperature activation for its function as molecular chaperone. Biochem Mol Biol Int 48: 249-258.
70. Bowler C, Benvenuto G, Laflamme P, Molino D, Probst AV, et al. (2004) Chromatin techniques for plant cells. Plant J 39: 776-789.