Evolution and Divergence of the MADS-Box Gene Family Based on Genome-Wide Expression Analyses

Abstract

MADS-box genes encode transcription factors involved in various important aspects of development and differentiation in land plants, metazoans, and other organisms. Three types of land plant MADS-box genes have been reported. MIKCC- and MIKC*-type genes both contain conserved MADS and K domains but have different exon/intron structures. M-type genes lack a K domain. Most MADS-box genes previously analyzed in land plants are expressed in the sporophyte (diploid plant body); few are expressed in the gametophyte (haploid plant body). Land plants are believed to have evolved from a gametophyte (haploid)-dominant ancestor without a multicellular sporophyte (diploid plant body); most genes expressed in the sporophyte probably originated from those used in the gametophyte during the evolution of land plants. To analyze the evolution and diversification of MADS-box genes in land plants, gametophytic MADS-box genes were screened using macroarray analyses for 105 MADS-box genes found in the Arabidopsis genome. Eight MADS-box genes were predominantly expressed in pollen, the male gametophyte; all but one of their expression patterns was confirmed by Northern analyses. Analyses of the exon/intron structure of these seven genes revealed that they included two MIKCC-type, one M-type, and four MIKC*-type MADS-box genes. Previously, MIKC*-type genes have been reported only from a moss and a club moss, and this is the first record in seed plants. These genes can be used to investigate the unknown ancestral functions of MADS-box genes in land plants. The macroarray analyses did not detect expression of 56 of 61 M-type MADS-box genes in any tissues examined. A phylogenetic tree including all three types of Arabidopsis MADS-box genes with representative genes from other organisms showed that M-type genes were polyphyletic and that their branch lengths were much longer than for the other genes. This finding suggests that most M-type genes are pseudogenes, although further experiments are necessary to confirm this possibility. Our global phylogenetic analyses of MADS-box genes did not support the previous classification of MADS-box genes into type I and II groups, based on smaller scale analyses. An evolutionary scenario for the evolution of MADS-box genes in land plants is discussed.

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).…”

“…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.…”

“…MIKC c MADS-box genes in seed plants are nearly absent from gametophytic tissues. Out of 38 genes in A. thaliana only one, AGL18, is detectable in pollen (Kofuji et al, 2003). To date it is unclear whether it has been retained in the haploid generation or was re-recruited from the sporophyte.…”

“…Well known are MADS-box genes responsible for the definition of organ identity in angiosperm flowers; their functional interplay is summarized in combinatorial models based on the "ABC-model" of floral development (Coen & Meyerowitz, 1991). However, in a typical seed plant like Arabidopsis thaliana the socalled MIKC c MADS-box genes, of which the ABC function genes are typical representatives, constitute less than half of the more than 100 MADS-box genes which have been identified in genome-wide surveys (Kofuji et al, 2003;Pařenicová et al, 2003). To date, the MIKC c genes are by far the best analyzed MADS-box genes in plants, and a number of mutant phenotypes have been described so far.…”

“…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).…”