The origin, evolution and diversification of MADS-box transcription factors in green plants

MADS-box genes acted as one of the most important regulatory elements in eukaryotes and particularly diversified throughout the evolution of green plants (Viridiplantae). Although the evolution and function of MADS-box genes have been extensively studied, it remains incomplete regarding the picture of the origin and diversification of MADS-box genes in Viridiplantae. Here, we employed genomic data of 551 representative eukaryotes for systematical analyses on both sequences and protein structures, aiming to clarify the evolutionary footprint of MADS-box genes across green plant lineages. Our analyses suggested the polyphyletic origin of plant Type I genes, and the two subfamilies of plant Type II genes (i.e., MIKCC and MIKC∗ genes) have arisen from an ancient gene duplication in the stem group of streptophytes rather than in land plants. The sphere-like structures of MIKCC proteins were uncovered in chlorophytes and charophytes, likely being an ancestral feature as physical constraint to tetramerization. The architectures of MIKCC proteins largely evolved in land plants with significantly shortened C-termini where key domains fully exposed, offering a structural necessity for shaping tetramer. Meanwhile, we recovered the diversification of MIKCC genes in ferns, implying a preacquisition of raw genetic basis for their explosive functional diversity in seed plants.