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Dual specificity and target gene selection by the MADS-domain protein FRUITFULL

Nature Plants volume 9, pages 473–485 (2023)Cite this article

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Abstract

How transcription factors attain their target gene specificity and how this specificity may be modulated, acquiring different regulatory functions through the development of plant tissues, is an open question. Here we characterized different regulatory roles of the MADS-domain transcription factor FRUITFULL (FUL) in flower development and mechanisms modulating its activity. We found that the dual role of FUL in regulating floral transition and pistil development is associated with its different in vivo patterns of DNA binding in both tissues. Characterization of FUL protein complexes by liquid chromatography–tandem mass spectrometry and SELEX-seq experiments shows that aspects of tissue-specific target site selection can be predicted by tissue-specific variation in the composition of FUL protein complexes with different DNA binding specificities, without considering the chromatin status of the target region. This suggests a role for dynamic changes in FUL TF complex composition in reshaping the regulatory functions of FUL during flower development.

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Fig. 1: Tissue-specific gene regulation by FUL.
Fig. 2: Tissue-specific DNA binding patterns of FUL.
Fig. 3: In planta FUL protein interactions.
Fig. 4: DNA binding specificity of FUL dimers.
Fig. 5: Prediction of in vivo FUL DNA binding.

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Data availability

The RNA-seq, ChIP–seq and SELEX-seq data have been deposited in the GEO database under accession numbers GSE194055, GSE108455 and GSE199643, respectively. The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium via the PRIDE partner repository with the dataset identifier PXD037091.

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Acknowledgements

The authors would like to thank E. Schijlen and B. te Lintel Hekkert for generating the HiSeq 2000 data, and M. Busscher for assistance in the laboratory. We thank A. Pajoro for advice on ChIP–seq experiments, and A. Jolma and J. Taipale for providing barcoded single-stranded DNA. This work was supported by an NWO-VIDI grant to K.K., a DFG grant (407463262) to J.M.M. and financial support of China Scholarship Council (CSC201906910064) to P.C.

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  1. These authors contributed equally: Hilda van Mourik, Peilin Chen.

Authors and Affiliations

  1. Laboratory of Molecular Biology, Wageningen University & Research, Wageningen, the Netherlands

    Hilda van Mourik, Marian Bemer & Gerco C. Angenent

  2. Plant Cell and Molecular Biology, Institute of Biology, Humboldt-Universität zu Berlin, Berlin, Germany

    Peilin Chen, Cezary Smaczniak, Kerstin Kaufmann & Jose M. Muino

  3. Laboratory of Biochemistry, Wageningen University & Research, Wageningen, the Netherlands

    Sjef Boeren

  4. Department of Bioscience, Wageningen University & Research, Wageningen, the Netherlands

    Marian Bemer & Gerco C. Angenent

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Contributions

H.v.M., J.M.M., G.C.A. and K.K. jointly conceived and designed the study. P.C. and J.M.M. performed the computational analysis. H.v.M., P.C., C.S., M.B. and S.B. performed experiments. H.v.M., P.C. and J.M.M. wrote the manuscripts with input from all authors.

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Correspondence to Jose M. Muino.

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Supplementary Figs. 1–12.

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Supplementary Table

Supplementary Table 1. Summary of the sequenced and mapped reads; differentially expressed genes (ful versus WT) analysis by DESeq2 in inflorescence meristems and pistils. Supplementary Table 2. Results of the Biological Process GO enrichment analysis for different group of DEGs or targets. Supplementary Table 3. Summary of mapped reads; lists of FUL DNA binding sites detect by CSAR in IM and pistils (IP versus control); list of FUL DNA binding sites with a quantitative difference detected by DESeq2 between IM versus pistils (IP IM versus IP pistils). Supplementary Table 4. Complete IP LC–MS/MS analysis for FUL TF in IM versus pistils. Supplementary Table 5. Summary of SELEX sequencing result; quantile normalized DNA binding specificity based on SELEX-seq. Supplementary Table 6. Combined analysis of ChIP–seq and SELEX-seq. Supplementary Table 7. Primer and oligo sequences used in this study.

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van Mourik, H., Chen, P., Smaczniak, C. et al. Dual specificity and target gene selection by the MADS-domain protein FRUITFULL. Nat. Plants 9, 473–485 (2023). https://doi.org/10.1038/s41477-023-01351-x

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