Transcriptional regulation of fruit ripening by tomato FRUITFULL homologs and associated MADS box proteins

Plant Cell

Volumn 26, Issue 1, 2014, Pages 89-101

  Fujisawa, Masaki ^a   Shima, Yoko ^a   Nakagawa, Hiroyuki ^a   Kitagawa, Mamiko ^b   Kimbara, Junji ^b   Nakano, Toshitsugu ^a   Kasumi, Takafumi ^c   Ito, Yasuhiro ^a  

^a NATIONAL FOOD RESEARCH INSTITUTE   (Japan)

^b KAGOME CO   (Japan)

^c NIHON UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

FLAVONOID; MADS DOMAIN PROTEIN; VEGETABLE PROTEIN;

BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PROMOTER REGION; SEQUENCE ANALYSIS; TOMATO;

BINDING SITES; CHROMATIN IMMUNOPRECIPITATION; FLAVONOIDS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; LYCOPERSICON ESCULENTUM; MADS DOMAIN PROTEINS; PLANT PROTEINS; PROMOTER REGIONS, GENETIC; SEQUENCE ANALYSIS, RNA;

EID: 84896887017     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.119453     Document Type: Article

References (56)

1. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997). Gapped BLAST and PSIBLAST: A new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402.
2. Ampomah-Dwamena, C., Morris, B.A., Sutherland, P., Veit, B., and Yao, J.L. (2002). Down-regulation of TM29, a tomato SEPALLATA homolog, causes parthenocarpic fruit development and floral reversion. Plant Physiol. 130: 605-617.
3. Bailey, T.L., Williams, N., Misleh, C., and Li, W.W. (2006). MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res. 34: W369-W373.
4. Bemer, M., Karlova, R., Ballester, A.R., Tikunov, Y.M., Bovy, A.G., Wolters-Arts, M., Rossetto, Pde.B., Angenent, G.C., and de Maagd, R.A. (2012). The tomato FRUITFULL homologs TDR4/FUL1 and MBP7/FUL2 regulate ethylene-independent aspects of fruit ripening. Plant Cell 24: 4437-4451.
5. Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate-A practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B Stat. Methodol. 57: 289-300.
6. Daminato, M., Guzzo, F., and Casadoro, G. (2013). A SHATTERPROOFlike gene controls ripening in non-climacteric strawberries, and auxin and abscisic acid antagonistically affect its expression. J. Exp. Bot. 64: 3775-3786.
7. Elitzur, T., Vrebalov, J., Giovannoni, J.J., Goldschmidt, E.E., and 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.
8. Eriksson, E.M., Bovy, A., Manning, K., Harrison, L., Andrews, J., De Silva, J., Tucker, G.A., and Seymour, G.B. (2004). Effect of the Colorless non-ripening mutation on cell wall biochemistry and gene expression during tomato fruit development and ripening. Plant Physiol. 136: 4184-4197.
9. Ferrándiz, C., Liljegren, S.J., and Yanofsky, M.F. (2000). Negative regulation of the SHATTERPROOF genes by FRUITFULL during Arabidopsis fruit development. Science 289: 436-438.
10. Fujisawa, M., Nakano, T., and Ito, Y. (2011). Identification of potential target genes for the tomato fruit-ripening regulator RIN by chromatin immunoprecipitation. BMC Plant Biol. 11: 26.
11. Fujisawa, M., Nakano, T., Shima, Y., and Ito, Y. (2013). A large-scale identification of direct targets of the tomato MADS box transcription factor RIPENING INHIBITOR reveals the regulation of fruit ripening. Plant Cell 25: 371-386.
12. Fujisawa, M., Shima, Y., Higuchi, N., Nakano, T., Koyama, Y., Kasumi, T., and Ito, Y. (2012). Direct targets of the tomato-ripening regulator RIN identified by transcriptome and chromatin immunoprecipitation analyses. Planta 235: 1107-1122.
13. Gapper, N.E., McQuinn, R.P., and Giovannoni, J.J. (2013). Molecular and genetic regulation of fruit ripening. Plant Mol. Biol. 82: 575-591.
14. Giménez, E., Pineda, B., Capel, J., Antón, M.T., Atarés, A., Pérez-Martín, F., García-Sogo, B., Angosto, T., Moreno, V., and Lozano, R. (2010). Functional analysis of the Arlequin mutant corroborates the essential role of the Arlequin/TAGL1 gene during reproductive development of tomato. PLoS ONE 5: e14427.
15. Giovannoni, J.J. (2007). Fruit ripening mutants yield insights into ripening control. Curr. Opin. Plant Biol. 10: 283-289.
16. Gu, Q., Ferrándiz, C., Yanofsky, M.F., and Martienssen, R. (1998). The FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development. Development 125: 1509-1517.
17. Honma, T., and Goto, K. (2001). Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409: 525-529.
18. Iijima, Y., et al. (2008). Metabolite annotations based on the integration of mass spectral information. Plant J. 54: 949-962.
19. Immink, R.G., Tonaco, I.A., de Folter, S., Shchennikova, A., van Dijk, A.D., Busscher-Lange, J., Borst, J.W., and Angenent, G.C. (2009). SEPALLATA3: The 'glue' for MADS box transcription factor complex formation. Genome Biol. 10: R24.
20. Ireland, H.S., Yao, J.L., Tomes, S., Sutherland, P.W., Nieuwenhuizen, N., Gunaseelan, K., Winz, R.A., David, K.M., and Schaffer, R.J. (2013). Apple SEPALLATA1/2-like genes control fruit flesh development and ripening. Plant J. 73: 1044-1056.
21. Itkin, M., Seybold, H., Breitel, D., Rogachev, I., Meir, S., and Aharoni, A. (2009). TOMATO AGAMOUS-LIKE 1 is a component of the fruit ripening regulatory network. Plant J. 60: 1081-1095.
22. Ito, Y., Kitagawa, M., Ihashi, N., Yabe, K., Kimbara, J., Yasuda, J., Ito, H., Inakuma, T., Hiroi, S., and Kasumi, T. (2008). DNA-binding specificity, transcriptional activation potential, and the rin mutation effect for the tomato fruit-ripening regulator RIN. Plant J. 55: 212-223.
23. Ito, Y., Ozawa, A., Sawasaki, T., Endo, Y., Ochi, K., and Tozawa, Y. (2002). OsRALyase1, a putative F-box protein identified in rice, Oryza sativa, with enzyme activity identical to that of wheat RALyase. Biosci. Biotechnol. Biochem. 66: 2727-2731.
24. Jaakola, L., Poole, M., Jones, M.O., Kämäräinen-Karppinen, T., Koskimäki, J.J., Hohtola, A., Häggman, H., Fraser, P.D., Manning, K., King, G.J., Thomson, H., and Seymour, G.B. (2010). A SQUAMOSA MADS box gene involved in the regulation of anthocyanin accumulation in bilberry fruits. Plant Physiol. 153: 1619-1629.
25. Kaufmann, K., Muiño, J.M., Jauregui, R., Airoldi, C.A., Smaczniak, C., Krajewski, P., and Angenent, G.C. (2009). Target genes of the MADS transcription factor SEPALLATA3: Integration of developmental and hormonal pathways in the Arabidopsis flower. PLoS Biol. 7: e1000090.
26. Langmead, B., and Salzberg, S.L. (2012). Fast gapped-read alignment with Bowtie 2. Nat. Methods 9: 357-359.
27. Leseberg, C.H., Eissler, C.L., Wang, X., Johns, M.A., Duvall, M.R., and Mao, L. (2008). Interaction study of MADS-domain proteins in tomato. J. Exp. Bot. 59: 2253-2265.
28. Liljegren, S.J., Ditta, G.S., Eshed, Y., Savidge, B., Bowman, J.L., and Yanofsky, M.F. (2000). SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404: 766-770.
29. Martel, C., Vrebalov, J., Tafelmeyer, P., and Giovannoni, J.J. (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.
30. Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L., and Wold, B. (2008). Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5: 621-628.
31. Muir, S.R., Collins, G.J., Robinson, S., Hughes, S., Bovy, A., Ric De Vos, C.H., van Tunen, A.J., and Verhoeyen, M.E. (2001). Overexpression of petunia chalcone isomerase in tomato results in fruit containing increased levels of flavonols. Nat. Biotechnol. 19: 470-474.
32. Pan, I.L., McQuinn, R., Giovannoni, J.J., and Irish, V.F. (2010). Functional diversification of AGAMOUS lineage genes in regulating tomato flower and fruit development. J. Exp. Bot. 61: 1795-1806.
33. Pelaz, S., Ditta, G.S., Baumann, E., Wisman, E., and Yanofsky, M.F. (2000). B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405: 200-203.
34. Pnueli, L., Hareven, D., Broday, L., Hurwitz, C., and Lifschitz, E. (1994a). The TM5 MADS box gene mediates organ differentiation in the three inner whorls of tomato flowers. Plant Cell 6: 175-186.
35. Pnueli, L., Hareven, D., Rounsley, S.D., Yanofsky, M.F., and Lifschitz, E. (1994b). Isolation of the tomato AGAMOUS gene TAG1 and analysis of its homeotic role in transgenic plants. Plant Cell 6: 163-173.
36. Qin, G., Wang, Y., Cao, B., Wang, W., and Tian, S. (2012). Unraveling the regulatory network of the MADS box transcription factor RIN in fruit ripening. Plant J. 70: 243-255.
37. Rice, P., Longden, I., and Bleasby, A. (2000). EMBOSS: The European Molecular Biology Open Software Suite. Trends Genet. 16: 276-277.
38. Riechmann, J.L., Krizek, B.A., and Meyerowitz, E.M. (1996). Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS. Proc. Natl. Acad. Sci. USA 93: 4793-4798.
39. Robinson, M.D., McCarthy, D.J., and Smyth, G.K. (2010). edgeR: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140.
40. Robinson, M.D., and Oshlack, A. (2010). A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 11: R25.
41. Robles, J.A., Qureshi, S.E., Stephen, S.J., Wilson, S.R., Burden, C.J., and Taylor, J.M. (2012). Efficient experimental design and analysis strategies for the detection of differential expression using RNA-Sequencing. BMC Genomics 13: 484.
42. Ruepp, A., Zollner, A., Maier, D., Albermann, K., Hani, J., Mokrejs, M., Tetko, I., Güldener, U., Mannhaupt, G., Münsterkötter, M., and Mewes, H.W. (2004). The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res. 32: 5539-5545.
43. Schaffer, R.J., Ireland, H.S., Ross, J.J., Ling, T.J., and David, K.M. (2013). SEPALLATA1/2-suppressed mature apples have low ethylene, high auxin and reduced transcription of ripening-related genes. AoB Plants 5: pls047.
44. Schultz, D.J., Craig, R., Cox-Foster, D.L., Mumma, R.O., and Medford, J.I. (1994). RNA isolation from recalcitrant plant tissues. Plant Mol. Biol. Rep. 12: 310-316.
45. Seymour, G.B., Ryder, C.D., Cevik, V., Hammond, J.P., Popovich, A., King, G.J., Vrebalov, J., Giovannoni, J.J., and Manning, K. (2011). A SEPALLATA gene is involved in the development and ripening of strawberry (Fragaria x ananassa Duch.) fruit, a nonclimacteric tissue. J. Exp. Bot. 62: 1179-1188.
46. Shima, Y., Fujisawa, M., Kitagawa, M., Nakano, T., Kimbara, J., Nakamura, N., Shiina, T., Sugiyama, J., Nakamura, T., Kasumi, T., and Ito, Y. (2014). Tomato FRUITFULL homologs regulate fruit ripening via ethylene biosynthesis. Biosci. Biotechnol. Biochem., in press.
47. Shima, Y., Kitagawa, M., Fujisawa, M., Nakano, T., Kato, H., Kimbara, J., Kasumi, T., and Ito, Y. (2013). Tomato FRUITFULL homologues act in fruit ripening via forming MADS-box transcription factor complexes with RIN. Plant Mol. Biol. 82: 427-438.
48. Smaczniak, C., Immink, R.G., Angenent, G.C., and Kaufmann, K. (2012a). Developmental and evolutionary diversity of plant MADS-domain factors: Insights from recent studies. Development 139: 3081-3098.
49. Smaczniak, C., et al. (2012b). Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development. Proc. Natl. Acad. Sci. USA 109: 1560-1565.
50. Theissen, G., and Saedler, H. (2001). Plant biology. Floral quartets. Nature 409: 469-471.
51. Tigchelaar, E.C., Mcglasson, W.B., and Buescher, R.W. (1978). Geneticregulation of tomato fruit ripening. HortScience 13: 508-513.
52. Tomato Genome Consortium (2012). The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485: 635-641.
53. Vrebalov, J., Pan, I.L., Arroyo, A.J., McQuinn, R., Chung, M., Poole, M., Rose, J., Seymour, G., Grandillo, S., Giovannoni, J., and Irish, V.F. (2009). Fleshy fruit expansion and ripening are regulated by the tomato SHATTERPROOF gene TAGL1. Plant Cell 21: 3041-3062.
54. Vrebalov, J., Ruezinsky, D., Padmanabhan, V., White, R., Medrano, D., Drake, R., Schuch, W., and Giovannoni, J. (2002). A MADSbox gene necessary for fruit ripening at the tomato ripeninginhibitor (rin) locus. Science 296: 343-346.
55. West, A.G., Causier, B.E., Davies, B., and Sharrocks, A.D. (1998). DNA binding and dimerisation determinants of Antirrhinum majus MADS-box transcription factors. Nucleic Acids Res. 26: 5277-5287.
56. Zhong, S., Fei, Z., Chen, Y.R., Zheng, Y., Huang, M., Vrebalov, J., McQuinn, R., Gapper, N., Liu, B., Xiang, J., Shao, Y., and Giovannoni, J.J. (2013). Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat. Biotechnol. 31: 154-159.