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The evolutionary origin of the angiosperms (f lowering plants sensu stricto) is still enigmatic. Answers to the question of angiosperm origins are intimately connected to the identification of their sister group among extinct and extant taxa. Most phylogenetic analyses based on morphological data agree that among the groups of extant seed plants, the gnetophytes are the sister group of the angiosperms. According to this view, angiosperms and gnetophytes are the only extant members of a clade called ''anthophytes'' to emphasize their shared possession of f lower-like reproductive structures. However, most phylogeny reconstructions based on molecular data so far did not support an anthophyte clade, but also could not clarify the case because support for alternative groupings has been weak or controversial. We have isolated 13 different homologs of MADS-type f loral homeotic genes from the gnetophyte Gnetum gnemon. Five of these genes fall into monophyletic gene clades also comprising putatively orthologous genes from f lowering plants and conifers, among them orthologs of f loral homeotic B and C function genes. Within these clades the Gnetum genes always form distinct subclades together with the respective conifer genes, to the exclusion of the angiosperm genes. This provides strong molecular evidence for a sister-group relationship between gnetophytes and conifers, which is in contradiction to widely accepted interpretations of morphological data for almost a century. Our phylogeny reconstructions and the outcome of expression studies suggest that complex features such as f lower-like reproductive structures and double-fertilization arose independently in gnetophytes and angiosperms.
Characterization of seven MADS-box genes, termed PPM1-PPM4 and PpMADS1-PpMADS3, from the moss model species Physcomitrella patens is reported. Phylogeny reconstructions and comparison of exon-intron structures revealed that the genes described here represent two different classes of homologous, yet distinct, MIKC-type MADS-box genes, termed MIKC(c)-type genes-"(c)" stands for "classic"-(PPM1, PPM2, PpMADS1) and MIKC(*)-type genes (PPM3, PPM4, PpMADS2, PpMADS3). The two gene classes deviate from each other in a characteristic way, especially in a sequence stretch termed intervening region. MIKC(c)-type genes are abundantly present in all land plants which have been investigated in this respect, and give rise to well-known gene types such as floral meristem and organ identity genes. In contrast, LAMB1 from the clubmoss Lycopodium annotinum was identified as the only other MIKC(*)-type gene published so far. Our findings strongly suggest that the most recent common ancestor of mosses and vascular plants contained at least one MIKC(c)-type and one MIKC(*)-type gene. Our studies thus reveal an ancient duplication of an MIKC-type gene that occurred before the separation of the lineages that led to extant mosses and vascular plants more than about 450 MYA. The identification of bona fide K-domains in both MIKC(*)-type and MIKC(c)-type proteins suggests that the K-domain is more ancient than is suggested by a recent alternative hypothesis. MIKC(*)-type genes may have escaped identification in ferns and seed plants so far. It seems more likely, however, that they represent a class of genes which has been lost in the lineage which led to extant ferns and seed plants. The high number of P. patens MADS-box genes and the presence of a K-box in the coding region and of some potential binding sites for MADS-domain proteins and other transcription factors in the putative promoter regions of these genes suggest that MADS-box genes in mosses are involved in complex gene regulatory networks similar to those in flowering plants.
Flowers sensu lato are short, specialized axes bearing closely aggregated sporophylls. They are typical for seed plants (spermatophytes) and are prominent in f lowering plants sensu stricto (angiosperms), where they often comprise an attractive perianth. There is evidence that spermatophytes evolved from gymnosperm-like plants with a fern-like mode of reproduction called progymnosperms. It seems plausible, therefore, that the stamens͞carpels and pollen sacs͞nucelli of spermatophytes are homologous to fern sporophylls and sporangia, respectively. However, the exact mode and molecular basis of early seed and f lower evolution is not yet known. Comparing f lower developmental control genes to their homologs from lower plants that do not f lower may help to clarify the issue. We have isolated and characterized MADS-box genes expressed in gametophytes and sporophytes of the fern Ceratopteris. The data indicate that at least two different MADS-box genes homologous to f loral homeotic genes existed in the last common ancestor of contemporary vascular plants, some descendants of which underwent multiple duplications and diversifications and were recruited into novel developmental networks during the evolution of f loral organs.
The genome of Arabidopsis (Arabidopsis thaliana) encodes over 100 MADS-domain transcription factors, categorized into five phylogenetic subgroups. Most research efforts have focused on just one of these subgroups (MIKCc), whereas the other four remain largely unexplored. Here, we report on five members of the so-called Mδ or Arabidopsis MIKC* (AtMIKC*) subgroup, which are predominantly expressed during the late stages of pollen development. Very few MADS-box genes function in mature pollen, and from this perspective, the AtMIKC* genes are therefore highly exceptional. We found that the AtMIKC* proteins are able to form multiple heterodimeric complexes in planta, and that these protein complexes exhibit a for the MADS-family unusual and high DNA binding specificity in vitro. Compared to their occurrence in promoters genome wide, AtMIKC* binding sites are strongly overrepresented in the proximal region of late pollen-specific promoters. By combining our experimental data with in silico genomics and pollen transcriptomics approaches, we identified a considerable number of putative direct target genes of the AtMIKC* transcription factor complexes in pollen, many of which have known or proposed functions in pollen tube growth. The expression of several of these predicted targets is altered in mutant pollen in which all AtMIKC* complexes are affected, and in vitro germination of this mutant pollen is severely impaired. Our data therefore suggest that the AtMIKC* protein complexes play an essential role in transcriptional regulation during late pollen development.
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