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Genome-wide characterization of Ficus carica MADS-box transcription factors with a focus on their roles during fruit development

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Abstract

MCM1-AGAMOUS-DEFICIENS-SRF (MADS)-box transcription factors (TFs) regulate a variety of plant developmental processes, particularly floral organ identity and fruit ripening. However, little is known about the MADS-box TF family in the common fig (Ficus carica L.), a vital fruit crop of Mediterranean countries. Here, we report a comprehensive overview of the MADS-box genes and their TF products in fig, describing their classification, physicochemical properties, protein and gene architectures, phylogenetic relationships, selection mode and differential expression during fruit development. A total of 64 MADS-box members were identified in F. carica and phylogenetically categorized as either type I (30) or type II (34). Type I MADS-box TFs were divided into three families (Mα, Mβ and Mγ, with 16, 4 and 10 members, respectively), whereas type II TFs were classified into two families (MIKCC and MIKC*, with 29 and 5 members, respectively). MIKCC TFs could be further classified into 12 subfamilies. Most FcMADS genes within the same clade were characterized by similar exon–intron organizations and motif compositions. Comparative phylogenetic analysis using mulberry (Morus notabilis) identified 24 (18 type II and 6 type I) orthologs between F. carica and M. notabilis. In addition, 11 paralogous MADS-box gene pairs were identified in F. carica, which evolved under purifying selection, except for two recent paralogs from the TM3 (SOC1) subfamily. RNA-seq results indicated that 28 and 34 FcMADS genes were differentially expressed in fruit peel and female flowers, respectively, during six successive stages of fruit development. According to their expression profiles, genes were grouped into four clusters (I, II, III and IV) in both tissues. FcMADS genes from fruit peel expression cluster IV (FcMADS13, -23, -32, -40 and -60) and female flower expression cluster III (FcMADS9, -49 and -58) were upregulated during fruit ripening in the corresponding tissues, suggesting a potential, tissue-specific role of these candidate genes in fruit ripening. Our findings provide the first genome-wide extended characterization of the MADS-box TF family in F. carica, laying the groundwork for future research on its molecular roles in fruit ripening.

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All data analyzed during this study are included in this article and its supplementary files.

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Acknowledgements

This work is part of a doctoral thesis prepared by Narjes Kmeli. The authors thank all lab members for assistance. Special thanks to Judith Risse (Wageningen University, The Netherlands) for helpful assistance in RNA-Seq data analysis.

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NK contributed by analyzing data and writing the original draft. JH helped in performing bioinformatics analyses and contributed to discussions. DB contributed to the conceptualization, methodology, software, data curation, supervision and manuscript editing. All authors have read and approved the final manuscript.

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Correspondence to Dhia Bouktila.

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The authors state that there is no conflict of interest in the publishing of this work. The text and its contents have not been published or submitted anywhere else.

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Communicated by Seon-In Yeom.

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Kmeli, N., Hamdi, J. & Bouktila, D. Genome-wide characterization of Ficus carica MADS-box transcription factors with a focus on their roles during fruit development. Hortic. Environ. Biotechnol. 64, 311–329 (2023). https://doi.org/10.1007/s13580-022-00478-8

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  • DOI: https://doi.org/10.1007/s13580-022-00478-8

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