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Tomato FRUITFULL homologues act in fruit ripening via forming MADS-box transcription factor complexes with RIN

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Abstract

The tomato MADS-box transcription factor RIN acts as a master regulator of fruit ripening. Here, we identified MADS-box proteins that interact with RIN; we also provide evidence that these proteins act in the regulation of fruit ripening. We conducted a yeast two-hybrid screen of a cDNA library from ripening fruit, for genes encoding proteins that bind to RIN. The screen identified two MADS-box genes, FUL1 and FUL2 (previously called TDR4 and SlMBP7), both of which have high sequence similarity to Arabidopsis FRUITFULL. Expression analyses revealed that the FUL1 mRNA and FUL1 protein accumulate in a ripening-specific manner in tomato fruits and FUL2 mRNA and protein accumulate at the pre-ripening stage and throughout ripening. Biochemical analyses confirmed that FUL1 and FUL2 form heterodimers with RIN; this interaction required the FUL1 and FUL2 C-terminal domains. Also, the heterodimers bind to a typical target DNA motif for MADS-box proteins. Chromatin immunoprecipitation assays revealed that FUL1 and FUL2 bind to genomic sites that were previously identified as RIN-target sites, such as the promoter regions of ACS2, ACS4 and RIN. These findings suggest that RIN forms complexes with FUL1 and FUL2 and these complexes regulate expression of ripening-related genes. In addition to the functional redundancy between FUL1 and FUL2, we also found they have potentially divergent roles in transcriptional regulation, including a difference in genomic target sites.

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Acknowledgments

This work was supported in part by the Program for Promotion of Basic and Applied Researches for Innovations in the Bio-oriented Technology Research Advancement Institution (BRAIN) of Japan to Y. I.

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Authors and Affiliations

  1. National Food Research Institute, National Agriculture and Food Research Organization (NARO), 2-1-12 Kannondai, Tsukuba, Ibaraki, 305-8642, Japan

    Yoko Shima, Masaki Fujisawa, Toshitsugu Nakano, Hiroki Kato & Yasuhiro Ito

  2. Research Institute, Kagome Co., Ltd., 17 Nishitomiyama, Nasushiobara, Tochigi, 329-2762, Japan

    Mamiko Kitagawa & Junji Kimbara

  3. Department of Applied Biological Science, Tokyo University of Science, 2641 Yamazaki, Noda, Chiba, 278-8510, Japan

    Hiroki Kato

  4. Department of Chemistry and Life Science, Nihon University, 1866 Kameino, Fujisawa, Kanagawa, 252-0880, Japan

    Takafumi Kasumi

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  1. Yoko Shima
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  2. Mamiko Kitagawa
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  8. Yasuhiro Ito
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Correspondence to Yasuhiro Ito.

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Shima, Y., Kitagawa, M., Fujisawa, M. et al. Tomato FRUITFULL homologues act in fruit ripening via forming MADS-box transcription factor complexes with RIN. Plant Mol Biol 82, 427–438 (2013). https://doi.org/10.1007/s11103-013-0071-y

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