Thomas Münster

A SHORT HISTORY OF MADS-BOX GENES IN PLANTS

Evolutionary developmental genetics (evodevotics) is a novel scientific endeavor which assumes that changes in developmental control genes are a major aspect of evolutionary changes in morphology. Understanding the phylogeny of developmental control genes may thus help us to understand the evolution of plant and animal form. The principles of evodevotics are exemplified by outlining the role of MADS-box genes in the evolution of plant reproductive structures. In extant eudicotyledonous flowering plants, MADS-box genes act as homeotic selector genes determining floral organ identity and as floral meristem identity genes. By reviewing current knowledge about MADS-box genes in ferns, gymnosperms and different types of angiosperms, we demonstrate that the phylogeny of MADS-box genes was strongly correlated with the origin and evolution of plant reproductive structures such as ovules and flowers. It seems likely, therefore, that changes in MADS-box gene structure, expression and function have been a major cause for innovations in reproductive development during land plant evolution, such as seed, flower and fruit formation.

Characterization of three GLOBOSA-like MADS-box genes from maize : evidence for ancient paralogy in one class of floral homeotic B-function genes of grasses

Floral homeotic B-function genes are involved in specifying the identity of petals and stamens during flower development in higher eudicotyledonous plants. Monocotyledonous plants belonging to the grass family (Poaceae) have very similar B-function genes, except that these genes specify lodicules rather than petals. All B-function genes known so far are members of the MADS-box gene family encoding transcription factors. In some eudicot model systems such as Arabidopsis and Antirrhinum, the B-function is provided by heterodimeric protein complexes encoded by one DEF- and one GLO-like gene. In several different lineages of flowering plant species, however, more than one DEF- or GLO-like gene is found. A known example is the monocot model system rice, which contains two GLO-like genes, termed OSMADS2 and OSMADS4. Duplications of floral homeotic genes may have played a critical role in the diversification of floral homeotic functions and thus the evolution of flowers. In order to date the gene duplication event that gave rise to these two genes, we cloned cDNAs of three different GLO-like genes from maize, a distant relative of rice within the Poaceae family. Phylogeny reconstructions and chromosomal mapping indicate that one of these genes, named ZMM16, is orthologous to OSMADS2, and that the other two, ZMM18 and ZMM29, are probably orthologous to OSMADS4. The gene duplication which gave rise to OSMADS2- and OSMADS4-like genes occurred probably after the split of the lineages that resulted in extant Liliaceae and Poaceae, but before the separation of the lineages that gave rise to extant maize and rice about 50 MYA. Northern and in situ hybridization studies demonstrated that the maize genes are expressed in lodicules, stamens and carpels throughout spikelet development in male and female inflorescences. The GLO-like genes from rice have very similar patterns of mRNA accumulation. In addition, ZMM16 shows also weak expression in vegetative organs. Conservation of the expression in lodicules and stamens is in perfect agreement with a floral homeotic B-function of the GLO-like genes in grasses. The conserved expression in carpels is discussed. Moreover, circumstantial evidence for a functional diversification of GLO-like genes in grasses is provided.

MIKC* MADS-Protein Complexes Bind Motifs Enriched in the Proximal Region of Late Pollen-Specific Arabidopsis Promoters

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.

MADS-complexes regulate transcriptome dynamics during pollen maturation

BackgroundDifferentiation processes are responsible for the diversity and functional specialization of the cell types that compose an organism. The outcome of these processes can be studied at molecular, physiologic, and biochemical levels by comparing different cell types, but the complexity and dynamics of the regulatory processes that specify the differentiation are largely unexplored.ResultsHere we identified the pollen-specific MIKC* class of MADS-domain transcription factors as major regulators of transcriptome dynamics during male reproductive cell development in Arabidopsis thaliana. Pollen transcript profiling of mutants deficient in different MIKC* protein complexes revealed that they control a transcriptional switch that directs pollen maturation and that is essential for pollen competitive ability. We resolved the functional redundancy among the MIKC* proteins and uncovered part of the underlying network by identifying the non-MIKC* MADS-box genes AGL18 and AGL29 as downstream regulators of a subset of the MIKC* MADS-controlled genes.ConclusionOur results provide a first, unique, and compelling insight into the complexity of a transcription factor network that directs cellular differentiation during pollen maturation, a process that is essential for male reproductive fitness in flowering plants.

MIKC* MADS-Box Proteins: Conserved Regulators of the Gametophytic Generation of Land Plants

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 (MADS-box) 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 MADS-box 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* MADS-box proteins have largely preserved molecular roles in the gametophytic generation of land plants.

On the origin of floral morphological novelties

Floral morphological novelties, like homeotic changes of whorl 1 organs, can easily arise by modifying existing regulatory networks. Ectopic expression of B‐function MADS‐box genes in whorl 1 leads to a replacement of sepals by petals, as is found in the Liliaceae. In cases where leaf‐like sepals or even inflated calyces develop, which ultimately envelop the mature fruit as in Physalis, ectopic expression of a vegetative MADS‐box gene seems to be responsible. Current knowledge concerning the origin of such morphological novelties is reviewed.

Molecular genetic basis of pod corn (Tunicate maize)

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.