Characterization of MADS-box genes in charophycean green algae and its implication for the evolution of MADS-box genes

Abstract

The MADS-box genes of land plants are extensively diverged to form a superfamily and are important in various aspects of development including the specification of floral organs as homeotic selector genes. The closest relatives of land plants are the freshwater green algae charophyceans. To study the origin and evolution of land plant MADS-box genes, we characterized these genes in three charophycean green algae: the stonewort Chara globularis, the coleochaete Coleochaete scutata, and the desmid Closterium peracerosum-strigosum-littorale complex. Phylogenetic analyses suggested that MADS-box genes diverged extensively in the land plant lineage after the separation of charophyceans from land plants. The stonewort C. globularis mRNA was specifically detected in the oogonium and antheridium together with the egg and spermatozoid during their differentiation. The expression of the C. peracerosum-strigosum-littorale-complex gene increased when vegetative cells began to differentiate into gametangial cells and decreased after fertilization. These expression patterns suggest that the precursors of land plant MADS-box genes originally functioned in haploid reproductive cell differentiation and that the haploid MADS-box genes were recruited into a diploid generation during the evolution of land plants.charophytes ͉ land plants ͉ Chara ͉ Coleochaete ͉ Closterium D iversity in form, a hallmark of extant species, is probably caused by modifications of ancestral gene networks regulating development and by the generation of novel developmental processes (1). The evolution of transcription factors, which have critical functions in development, through gene duplication and subsequent functional divergence has been hypothesized to be a major force in developmental evolution (reviewed in ref.2). The adaptation of green plants to a terrestrial environment and their subsequent diversification are tightly linked to the evolution of the body plan of land plants (3, 4). Members of the MADS-box gene family regulate various aspects of development in flowering plants and therefore were probably involved in the evolution of the morphology of land plants.MADS-box genes are characterized by the conserved MADS domain and are found in a wide range of eukaryotes including metazoans, fungi, slime mold, and green plants (5). These genes have been classified into several groups (6). MIKC C -and MIKC*-type MADS-box genes contain intervening (I), keratinlike (K), and C-terminal (C) domains (7,8). They are present in all major land plant taxa including seed plants, pteridophytes, and bryophytes but have not been found in other organisms such as green algae (5, 6, 9). The Arabidopsis genome (10) contains Ϸ38 MIKC C -type and 5 MIKC*-type genes (6, 9). The MIKC*-type genes tend to form a monophyletic group, including several subgroups of genes with unknown functions (9), but the MIKC Ctype MADS-box genes have been classified into about a dozen subfamilies with diverse functions and expression patterns (reviewed in ref. 6). The floral homeotic genes ar...

The MADS-domain protein PPM2 preferentially occurs in gametangia and sporophytes of the moss Physcomitrella patens

“…In ferns like Ceratopteris richardii more than 30 genes seem to be present in the genome (W. F. and T. M., unpublished data), at least a similar number of genes exist in the gymnosperm Gnetum gnemon (whereas this is likely an underestimation due to limited samplings) and about 40 genes have been identified in the eudicotyledonous model plant A. thaliana (Kofuji et al, 2003;Pařenicová et al, 2003). On the other hand, only one MIKC c gene was shown to be present in the genomes of Charophycean green algae (Tanabe et al, 2005). These data suggest a common trend of increasing MIKC c gene numbers in the evolutionary history of green plants.…”

“…The fact that sporophyte-dominant plants evolved from gametophyte-dominant ancestors suggests that the precursors of land plant MADS-box genes, like the precursors of many other genes, originated from genes which were active in the haploid generation and were recruited into a functional context in the diploid phase during the evolution of land plants (Nishiyama et al, 2003;Kofuji et al, 2003;Tanabe et al, 2005). To verify this hypothesis, information on a number of informative non-seed plant lineages, which have been analyzed for their MADS-box gene families and the respective gene expression patterns, was collected and scrutinized.…”

“…Charophycean green algae display what may be considered as the ancestral state of MADS-box gene expression (Tanabe et al, 2005). In both the unicellular charophycean green alga Closterium peracerosum-strigosum-littorale complex and the multicellular representative Chara globularis MADS-box gene expression is basically restricted to haploid cells.…”

“…One important finding for the reconstruction of the evolutionary history of the MADS-box gene family was the identification of angiosperm gene orthologs in gymnosperms showing a high degree of functional conservation (Sundström & Engström, 2002). So far MIKC c MADS-box genes have been characterized from different representatives of lycophytes (Svensson & Engström, 2002;Tanabe et al, 2003), pteridophytes (Münster et al, 1997;Hasebe et al, 1998;Münster et al, 2002), bryophytes (Krogan and Ashton, 2000;Henschel et al, 2002;Hohe et al, 2002) and green algae (Tanabe et al, 2005). However, no evidence for the existence of seed plant gene orthologs could be obtained from non-seed plants.…”

“…Information on MADS-domain protein distribution or putative gene functions is completely lacking. An obvious evolutionary trend of MIKC c MADS-box genes in plants is the increase in gene family size, ranging from just one gene in Charophycean green algae to about 40 in flowering plants (Kofuji et al, 2003;Tanabe et al, 2005). Because no MIKC c MADS-box genes could be identified in the genomes of the chlorophycean green alga Chlamydomonas reinhardtii (Tanabe et al, 2005) and the red alga Cyanidioschyzon merolae (Matsuzaki et al, 2004), MIKC c MADS-box genes very likely originated in a common ancestor of charophytes and land plants at least 500 million years ago (MYA).…”