How MIKC* MADS-Box Genes Originated and Evidence for Their Conserved Function Throughout the Evolution of Vascular Plant Gametophytes

Abstract

Land plants have a remarkable life cycle that alternates between a diploid sporophytic and a haploid gametophytic generation, both of which are multicellular and changed drastically during evolution. Classical MIKC MADS-domain (MIKCC) transcription factors are famous for their role in sporophytic development and are considered crucial for its evolution. About the regulation of gametophyte development, in contrast, little is known. Recent evidence indicated that the closely related MIKC* MADS-domain proteins are important for the functioning of the Arabidopsis thaliana male gametophyte (pollen). Furthermore, also in bryophytes, several MIKC* genes are expressed in the haploid generation. Therefore, that MIKC* genes have a similar role in the evolution of the gametophytic phase as MIKCC genes have in the sporophyte is a tempting hypothesis. To get a comprehensive view of the involvement of MIKC* genes in gametophyte evolution, we isolated them from a broad variety of vascular plants, including the lycophyte Selaginella moellendorffii, the fern Ceratopteris richardii, and representatives of several flowering plant lineages. Phylogenetic analysis revealed an extraordinary conservation not found in MIKCC genes. Moreover, expression and interaction studies suggest that a conserved and characteristic network operates in the gametophytes of all tested model organisms. Additionally, we found that MIKC* genes probably evolved from an ancestral MIKCC-like gene by a duplication in the Keratin-like region. We propose that this event facilitated the independent evolution of MIKC* and MIKCC protein networks and argue that whereas MIKCC genes diversified and attained new functions, MIKC* genes retained a conserved role in the gametophyte during land plant evolution.

Discovery of novel transcripts and gametophytic functions via RNA-seq analysis of maize gametophytic transcriptomes

“…In Arabidopsis, MIKC* MADS genes are overrepresented in the MP [13,15,55], whereas the type I class α and β genes are overrepresented in the ES [53]. In maize, all MIKC* MADS genes are enriched in MP, supporting the conclusion for an ancient role for these genes in the male gametophyte [56]. Other MPenriched maize MADS genes fall into the MIKC and the type 1 class α groups.…”

Developmental and evolutionary diversity of plant MADS-domain factors: insights from recent studies

“…In the moss Physcomitrella patens, MIKC C -type genes function in the gametophyte as well as in specific tissues of the sporophyte, whereas MIKC*-type genes are specifically expressed in the gametophyte (Singer et al, 2007;Kwantes et al, 2012). This gametophytic expression appears to be highly conserved across land plant evolution and might reflect an ancestral, conserved role of MIKC*-type genes in gametophyte development (Verelst et al, 2007a;Zobell et al, 2010;Kwantes et al, 2012). The enigmatic origin and success of seed plants and, more recently, of flowering plants (angiosperms), is one of the biggest evolutionary mysteries.…”

“…1B). The latter are characterized by an altered protein domain structure, possibly linked to the duplication of exons encoding a subregion of the K domain (Kwantes et al, 2012). Moreover, we can divide MIKC C -type MADS-box genes into several distinctive subfamilies based on their phylogeny ( Phylogenetic analyses and the domain structure of selected representatives of (A) type I and (B) type II MADS-box transcription factors from thale cress (Arabidopsis thaliana, At), grape (Vitis vinifera, Vv) and tomato (Solanum lycopersicum, Sl).…”

“…Plant type II MADS-box transcription factors have four domains: the DNA-binding MADS, the intervening (I, green), the keratin-like (K, orange/purple) and the C-terminal (C, blue) domains. MIKC*-type proteins are usually longer than MIKC C -type proteins, probably owing to a longer K domain (MIKC*, orange; MIKC C , purple) (Kwantes et al, 2012). REVIEW Development 139 (17) are often characterized by distinct sequence motifs in their Cterminal domains, which further diversified during evolution by frameshift mutations (see Vandenbussche et al, 2003a).…”

“…Prior to the origin of the most primitive extant lineages of land plants, the bryophytes, a gene duplication event led to the origin of MIKC C -type and MIKC*-type genes (Henschel et al, 2002). In the moss Physcomitrella patens, MIKC C -type genes function in the gametophyte as well as in specific tissues of the sporophyte, whereas MIKC*-type genes are specifically expressed in the gametophyte (Singer et al, 2007;Kwantes et al, 2012). This gametophytic expression appears to be highly conserved across land plant evolution and might reflect an ancestral, conserved role of MIKC*-type genes in gametophyte development (Verelst et al, 2007a;Zobell et al, 2010;Kwantes et al, 2012).…”