Land plants (embryophytes) are characterized by an alternation of two generations, the haploid gametophyte and the diploid sporophyte. The development of the small and simple male gametophyte of the flowering plant Arabidopsis (Arabidopsis thaliana) critically depends on the action of five MIKC* group MCM1-AGAMOUS-DEFICIENS-SRF-box (MADSbox) proteins. In this study, these MIKC* MADS-box genes were isolated from land plants with relatively large and complex gametophyte bodies, namely the bryophytes. We found that although the gene family expanded in the mosses Sphagnum subsecundum, Physcomitrella patens, and Funaria hygrometrica, only a single homologue, Marchantia polymorpha MADSbox gene 1 (MpMADS1), has been retained in the liverwort M. polymorpha. Liverworts are the earliest diverging land plants, and so a comparison of MpMADS1 with its angiosperm homologues addresses the molecular evolution of an embryophyte-specific transcription factor over the widest phylogenetic distance. MpMADS1 was found to form a homodimeric DNA-binding complex, which is in contrast to the Arabidopsis proteins that are functional only as heterodimeric complexes. The M. polymorpha homodimer, nevertheless, recognizes the same DNA sequences as its angiosperm counterparts and can functionally replace endogenous MIKC* complexes to a significant extent when heterologously expressed in Arabidopsis pollen. The 11 MIKC* homologues from the moss F. hygrometrica are highly and almost exclusively expressed in the gametophytic generation. Taken together, these findings suggest that MIKC* MADSbox proteins have largely preserved molecular roles in the gametophytic generation of land plants.
Pod corn is a classic morphological mutant of maize in which the mature kernels of the cob are covered by glumes, in contrast to generally grown maize varieties in which kernels are naked. Pod corn, known since pre-Columbian times, is the result of a dominant gain-of-function mutation at the Tunicate ( Tu ) locus. Some classic articles of 20th century maize genetics reported that the mutant Tu locus is complex, but molecular details remained elusive. Here, we show that pod corn is caused by a cis -regulatory mutation and duplication of the ZMM19 MADS-box gene. Although the WT locus contains a single-copy gene that is expressed in vegetative organs only, mutation and duplication of ZMM19 in Tu lead to ectopic expression of the gene in the inflorescences, thus conferring vegetative traits to reproductive organs.
The MIKC-type MADS-box genes of seed plants encode transcription factors which are typically expressed in a tissue-or organ-specific way. In contrast, the MIKC genes of the fern Ceratopteris isolated so far, show fairly ubiquitous expression in both reproductive and non-reproductive organs. In order to determine whether this is a feature which is unique to a lineage of highly derived, leptosporangiate ferns, we initiated a characterization of the family of MIKC-type MADS-box genes of the eusporangiate ªfernº Ophioglossum. Within the large clade of ferns and their allies, Ophioglossum is only very distantly related to Ceratopteris. cDNAs were isolated which represent at least four different Ophioglossum MIKC-type genes, termed OPM1, OPM3 ± OPM5. Hybridization of genomic DNA gel blots, however, revealed that appreciably more MADS-box genes are present in the Ophioglossum genome. As for the MIKC-type genes from Ceratopteris, phylogeny reconstructions did not reveal orthology to seed plant genes for any of these. For OPM1 and OPM5, however, a relatively close relationship to some Ceratopteris genes was moderately supported. Semi-quantitative RT-PCR revealed that OPM1, OPM3 and OPM5 are expressed in both the vegetative (trophophore) and the reproductive (sporophore) part of the Ophioglossum leaf. In contrast, expression of OPM4 is restricted to the sporophore, suggesting a specific role in generative development for that gene. These findings suggest that relatively ubiquitous expression is a typical, but not absolute, feature of MIKC-type MADS-box genes from ferns and their allies. Taken together, the data outlined here corroborate the view that the phylogeny of MIKC-type MADS-box genes took different pathways in ferns and their allies on the one hand, and seed plants on the other hand, involving numerous independent gene duplications in both lineages, and distinct differences in the ubiquity of the expression patterns and, by inference, function. The implications of these findings for a better understanding of the evolution of vascular plants are discussed.
To date, the function of MADS-domain transcription factors in non-seed plants remains largely elusive, although a number of genes have been isolated and characterized from a variety of species. In our study we analyzed PPM2, a classical MIKC-type MADS-box gene from the moss Physcomitrella patens, taking advantage of the unique technical properties Physcomitrella offers in terms of efficient homologous recombination. We determined mRNA and protein distribution and performed targeted disruption of the genomic locus for functional analysis of PPM2. Despite weak ubiquitous expression, PPM2 protein is mostly found in male and female gametangia and basal parts of developing sporophytes. Therefore, PPM2 seems to function in both the haploid and the diploid phase of the moss life cycle. This situation reflects an evolutionary transition state of gene recruitment from an ancestral gametophytic generation into a derived sporophytic generation which became dominating in tracheophytes. However, a knock-out of the PPM2 gene did not cause visible phenotypical changes in the respective structures. The implications of our findings for the understanding of the evolutionary history of MADS-box transcription factors in plants are discussed.
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