The Origin of Floral Quartet Formation—Ancient Exon Duplications Shaped the Evolution of MIKC-type MADS-domain Transcription Factor Interactions

Abstract

During development of flowering plants, some MIKC-type MADS-domain transcription factors (MTFs) exert their regulatory function as heterotetrameric complexes bound to two sites on the DNA of target genes. This way they constitute „floral quartets“or related „floral quartet-like complexes“(FQCs), involving a unique multimeric system of paralogous protein interactions. Tetramerisation of MTFs is brought about mainly by interactions of keratin-like (K) domains. The K-domain associated with the more ancient DNA-binding MADS-domain during evolution in the stem group of extant streptophytes (charophyte green algae + land plants). However, whether this was sufficient for MTF tetramerisation and FQC formation to occur, remains unknown. Here, we provide biophysical and bioinformatic data indicating that FQC formation likely originated in the stem group of land plants in a sublineage of MIKC-type genes termed MIKCC-type genes. In the stem group of this gene lineage, the duplication of the most downstream exon encoding the K-domain led to a C-terminal elongation of the second K-domain helix, thus, generating the tetramerisation interface found in extant MIKCC type proteins. In the stem group of the sister lineage of the MIKCC-type genes, termed MIKC*-type genes, the duplication of two other K-domain exons occurred, extending the K-domain at its N-terminal end. Our data indicate that this structural change prevents heterodimerisation between MIKCC-type and MIKC*-type proteins. This way, two largely independent gene regulatory networks could be established, featuring MIKCC-type or MIKC*-type proteins, respectively, that control different aspects of plant development.

Genomes of multicellular algal sisters to land plants illuminate signaling network evolution

“…16 ). This suggests the presence of two MADS-domain TFs in the Zygnematophyceae ancestor: (1) an ancestral Type II without a K domain (probably unable to form FQCs), and (2) the MIKC type, with (in vitro) demonstrated ability to form FQCs 57 .…”

Reflections on the ABC model of flower development

“…3B ) ( Henschel et al 2002 ; Kofuji et al 2003 ; Wellmer et al 2014 ; Qiu et al 2023 ). Land plant MIKC C -MADS proteins can form quartets in vitro, with a duplication of sequence within the K domain critical for forming the interface required for tetramer formation ( Rümpler et al 2023 ). Hence, quartet emergence predates the MADS-boxes learning their ABCs.…”

“…Hence, quartet emergence predates the MADS-boxes learning their ABCs. The ability to form tetramers combined with expansion and diversification of MADS-box genes in the ancestral seed plant, and more dramatically within the ancestral angiosperm, enhanced the combinatorial power of MIKC C complexes ( Rümpler et al 2023 ) and may have contributed to the evolution of tissue and organ types during development. In the ancestral land plant, sex was determined during the haploid generation ( Bowman 2022 ), but in seed plants the sporophyte largely controls gametophyte development, including sex expression.…”

Cracking the Floral Quartet Code: How Do Multimers of MIKCC-Type MADS-Domain Transcription Factors Recognize Their Target Genes?

“…The ancestral MIKC-type gene present in charophytes was duplicated in the stem group of extant embryophytes (land plants), resulting in the lineages of MIKC C -type and MIKC*-type genes [17,[29][30][31].…”

“…FQC formation depends on some remarkable structural features of the K domain [7], but not all MIKC-type proteins can accomplish this. Recent data suggest that some MIKCtype proteins of charophyte algae are capable of FQC formation, but that an exon duplication that led to an elongation of the K domain in the stem group of extant MIKC C -type genes strongly favored it [31]. In contrast, MIKC*-type proteins appear to bind to DNA only as dimers, not as tetramers [31].…”