Deep evolution of MADS-box genes in Archaeplastida

Abstract

MADS-box genes represent a paneukaryotic gene family encoding transcription factors. Given its importance for essential functions in plants, animals and fungi, such as development of organ identity and mating type determination, the phylogeny of MADS-box genes is of great biological interest. It has been well established that a gene duplication in the stem group of extant eukaryotes generated two clades of MADS-box genes, termed Type I and Type II genes. Almost all Type II genes of land plants contain a keratin-like (K) domain in addition to the family-defining, DNA-binding MADS (M) domain and are also termed MIKC-type genes. Due to a lack of sampling of MADS-box genes in Archaeplastida (rhodophytes, glaucophytes, chlorophytes, and streptophytes) except land plants, the deep evolution of MADS-box genes in plants remains poorly understood, however. Here we use the genomic and transcriptomic ressources that have become available in recent years to answer longstanding questions of MADS-box gene evolution in Archaeplastida. Our results reveal that archaeplastid algae likely do not harbour Type I MADS-box genes. However, rhodophytes, glaucophytes, prasinodermophytes and chlorophytes possess Type II MADS-box genes without a K domain. Type II MADS-box genes with a K domain are found only in streptophytes. This corroborates previous views that some Type II gene acquired a K domain in the stem group of extant streptophytes, generating MIKC-type genes. Interestingly, we found both variants of Type II genes - with (MIKC) and without a K domain - in streptophyte algae, but not in land plants (embryophytes), suggesting that Type II genes without a K domain (ancestral Type II genes) were lost in the stem group of land plants. Our data reveal that the deep evolution of MADS-box genes in "plants" (Archaeplastida) was more complex than has previously been thought.

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

“…MIKC-type genes have so far been found in all five major clades of charophytes, but not in chlorophytes yet, corroborating the view that they are a genuine 'synapomorphy' (shared derived trait) of streptophytes (i.e., charophytes + embryophytes) [24][25][26]29]. This finding strongly suggests that MIKC-type genes originated in the stem group of extant streptophytes when a Type II MADS-box gene acquired a K box by unresolved mutation or recombination events.…”

“…These MTFs were hence termed MIKC-type proteins, and the corresponding genes MIKC-type genes. However, the analysis of the genomes of diverse charophytes-a grade of green algae that represents the closest relatives of land plants (embryophytes)-revealed that they contain Type II gene lineages that have K boxes and others that do not [24][25][26], implying that the terms 'Type II genes of plants' and 'MIKC-type genes' should not be used synonymously anymore. This finding also corroborates the view that the absence of a K box is not a sufficient criterion for classifying a plant MADS-box gene as Type I (as, unfortunately, can sometimes be seen in the literature).…”

Cracking the floral quartet code: How do multimers of MIKCC-type MADS-domain transcription factors recognize their target genes?

“…MIKC-type genes have so far been found in all the five major clades of charophytes, but not in chlorophytes yet, corroborating the view that they are a genuine 'synapomorphy' (shared derived trait) of streptophytes (that is charophytes + embryophytes) [21][22][23]27]. This finding strongly suggests that MIKC-type genes originated in the stem group of extant streptophytes when a Type II MADS-box gene acquired a K box by unresolved mutation or recombination events.…”

“…These MTFs were hence termed MIKC-type proteins, the corresponding genes MIKC-type genes. However, the analysis of the genomes of diverse charophytes -a grade of green algae that represents the closest relatives of land plants (embryophytes) -revealed that they contain Type II gene lineages that have K boxes and others that do not [21][22][23], implying that the terms 'Type II genes of plants' and 'MIKC-type genes' should not be used synonymously anymore. This finding also corroborates the view that the absence of a K-box is not a sufficient criterion for classifying a plant MADS-box gene as Type I (as, unfortunately, can sometimes be seen in the literature).…”

“…This finding strongly suggests that MIKC-type genes originated in the stem group of extant streptophytes when a Type II MADS-box gene acquired a K box by unresolved mutation or recombination events. Whole genome analyses revealed that there are very few MIKC-type genes in extant charophyte species [22, 23, 27], suggesting that there possibly might have been just one MIKC-type gene in the most recent common ancestor (MRCA) of extant land plants.…”