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Günter Theissen

Publications and source records attributed to Günter Theissen.

At least 19 recordsLinked to original sources

Catching a 'hopeful monster': shepherd's purse (Capsella bursa-pastoris) as a model system to study the evolution of flower development.

Capsella is a small genus within the mustard family (Brassicaceae). Its three species, however, show many evolutionary trends also observed in other Brassicaceae (including Arabidopsis) and far beyond, including transitions from a diploid, self-incompatible, obligatory outcrossing species with comparatively large and attractive flowers but a restricted distribution to a polyploid, self-compatible, predominantly selfing, invasive species with floral reductions. All these evolutionary transitions may have contributed to the fact that Capsella bursa-pastoris (shepherd's purse) has become one of the most widely distributed flowering plants on our planet. In addition, Capsella bursa-pastoris shows a phenomenon that, although rare, could be of great evolutionary importance, specifically the occurrence of a homeotic variety found in relatively stable populations in the wild. Several lines of evidence suggest that homeotic changes played a considerable role in floral evolution, but how floral homeotic varieties are established in natural populations has remained a highly controversial topic among evolutionary biologists. Due to its close relationship with the model plant Arabidopsis thaliana, numerous experimental tools are available for studying the genus Capsella, and further tools are currently being developed. Hence, Capsella provides great opportunities to investigate the evolution of flower development from molecular developmental genetics to field ecology and biogeography, and from morphological refinements to major structural transitions.

Biological Evolution↗

Petaloidy and petal identity MADS-box genes in the balsaminoid genera Impatiens and Marcgravia.

Impatiens and Marcgravia have striking morphological innovations associated with the flowers. One of the sepals in Impatiens is spurred and petaloid, while in Marcgravia the petals are fused into a cap and nectary cups are associated with the inflorescence. Balsaminaceae (Impatiens) and Marcgraviaceae have surprisingly been shown to be closely related, since both belong to the balsaminoid clade of Ericales (basal asterids). However, several thorough morphological studies thus far have not revealed shared derived characters (synapomorphies) that support a close relationship between these families. In the balsaminoid clade, transitions from entirely green flowers to flowers with heterotopic petaloid organs can be observed. The primary role of class B genes in core eudicots is to specify the identity of petal and stamen floral organs. E-class genes, of which SEP3 is a representative, have been identified as redundant mediators that confer transcriptional activation potential on protein complexes that specify organ identity. Given the conserved function of organ-identity MADS-box genes in model plants, but the rapid molecular evolution in angiosperms, it remains controversial whether these genes have been involved in shaping floral diversity. We have identified a SEP3-like gene and a total of five class B genes from Impatiens hawkeri and Marcgravia umbellata and report their quantitative expression in the floral organs. In Impatiens, two AP3/DEF-like genes were identified with strongly divergent C-terminal domains, one truncated and one unusually long. Both genes show a gradual decrease in expression towards the outer perianth organs, but no GLO-like gene expression is observed in the petaloid sepal. Remarkably, SEP3-like gene expression in the Impatiens perianth is absent from the green sepals but present in the petaloid sepal and in the petals. Dimeric protein interactions of the cloned Impatiens genes were studied in yeast and by using gel retardation. In Marcgravia, strong overlapping class B gene expression is limited to the stamens, but a SEP3-like gene is strongly expressed in the Marcgravia nectary, indicating that both Impatiens and Marcgravia show heterotopic expression of a SEP3-like gene. We discuss several candidate mechanisms for heterotopic petaloidy involving modified gene expression and protein interaction of SEP3-like and class B genes.

Amino Acid Sequence↗

The proper place of hopeful monsters in evolutionary biology.

Hopeful monsters are organisms with a profound mutant phenotype that have the potential to establish a new evolutionary lineage. The Synthetic Theory of evolutionary biology has rejected the evolutionary relevance of hopeful monsters, but could not fully explain the mechanism and mode of macroevolution. On the other hand, several lines of evidence suggest that hopeful monsters played an important role during the origin of key innovations and novel body plans by saltational rather than gradual evolution. Homeotic mutants are identified as an especially promising class of hopeful monsters. Examples for animal and plant lineages that may have originated as hopeful monsters are given. Nevertheless, a brief review of the history of the concept of hopeful monsters reveals that it needs refinements and empirical tests if it is to be a useful addition to evolutionary biology. While evolutionary biology is traditionally zoocentric, hopeful monsters might be more relevant for plant than for animal evolution. Even though during recent years developmental genetics has provided detailed knowledge about how hopeful monsters can originate in the first place, we know almost nothing about their performance in natural populations and thus the ultimate difference between hopeful and hopeless. Studying the fitness of candidate hopeful monsters (suitable mutants with profound phenotype) in natural habitats thus remains a considerable challenge for the future.

Animals↗

Mutant analysis, protein-protein interactions and subcellular localization of the Arabidopsis B sister (ABS) protein.

Recently, close relatives of class B floral homeotic genes, termed B(sister) genes, have been identified in both angiosperms and gymnosperms. In contrast to the B genes themselves, B(sister) genes are exclusively expressed in female reproductive organs, especially in the envelopes or integuments surrounding the ovules. This suggests an important ancient function in ovule or seed development for B(sister) genes, which has been conserved for about 300 million years. However, investigation of the first loss-of-function mutant for a B(sister) gene (ABS/TT16 from Arabidopsis) revealed only a weak phenotype affecting endothelium formation. Here, we present an analysis of two additional mutant alleles, which corroborates this weak phenotype. Transgenic plants that ectopically express ABS show changes in the growth and identity of floral organs, suggesting that ABS can interact with floral homeotic proteins. Yeast-two-hybrid and three-hybrid analyses indicated that ABS can form dimers with SEPALLATA (SEP) floral homeotic proteins and multimeric complexes that also include the AGAMOUS-like proteins SEEDSTICK (STK) or SHATTERPROOF1/2 (SHP1, SHP2). These data suggest that the formation of multimeric transcription factor complexes might be a general phenomenon among MIKC-type MADS-domain proteins in angiosperms. Heterodimerization of ABS with SEP3 was confirmed by gel retardation assays. Fusion proteins tagged with CFP (Cyan Fluorescent Protein) and YFP (Yellow Fluorescent Protein) in Arabidopsis protoplasts showed that ABS is localized in the nucleus. Phylogenetic analysis revealed the presence of a structurally deviant, but closely related, paralogue of ABS in the Arabidopsis genome. Thus the evolutionary developmental genetics of B(sister) genes can probably only be understood as part of a complex and redundant gene network that may govern ovule formation in a conserved manner, which has yet to be fully explored.

Alleles↗

Birth, life and death of developmental control genes: new challenges for the homology concept.

Understanding the interrelationship between the phylogeny of developmental control genes and the evolution of morphological features is a central goal of evolutionary developmental biology (evo-devo). It requires that one distinguishes properly between gene genealogy and function. Gene duplication, gene loss and speciation in combination with differential changes in gene function can generate complex evolutionary scenarios that require additional terms beyond homology for a proper description. Use and possible misuse of these terms, including "orthology", "paralogy" and "subfunctionalization", is exemplified with AGAMOUS-like genes encoding transcription factors involved in flower and fruit development. This MADS-box gene subfamily demonstrates that homologous genes in different species with (almost) identical functions can be paralogues rather than orthologues, corroborating that functional similarity of genes is not a valid criterion for orthology. Homeosis fails some tests of homology, but might be of greater evolutionary importance than previously assumed, justifying yet another term, "homocracy". It describes organs that share the expression of the same patterning genes, irrespective of the homology of these organs. All in all this article opts for a careful use of a limited and well-chosen set of terms describing gene relationships and function, rather than the inflationary production of novel terms that may seem to be precise, but whose obscurity hampers communication.

Animals↗

Characterization of candidate class A, B and E floral homeotic genes from the perianthless basal angiosperm Chloranthus spicatus (Chloranthaceae).

The classic ABC model explains the activities of each class of floral homeotic genes in specifying the identity of floral organs. Thus, changes in these genes may underlay the origin of floral diversity during evolution. In this study, three MADS-box genes were isolated from the perianthless basal angiosperm Chloranthus spicatus. Sequence and phylogenetic analyses revealed that they are AP1-like, AP3-like and SEP3-like genes, and hence these genes were termed CsAP1, CsAP3 and CsSEP3, respectively. Due to these assignments, they represent candidate class A, class B and class E genes, respectively. Expression patterns suggest that the CsAP1, CsAP3 and CsSEP3 genes function during flower development of C. spicatus. CsAP1 is expressed broadly in the flower, which may reflect the ancestral function of SQUA-like genes in the specification of inflorescence and floral meristems rather than in patterning of the flower. CsAP3 is exclusively expressed in male floral organs, providing the evidence that AP3-like genes have ancestral function in differentiation between male and female reproductive organs. CsSEP3 expression is not detectable in spike meristems, but its mRNA accumulates throughout the flower, supporting the view that SEP-like genes have conserved expression pattern and function throughout angiosperm. Studies of synonymous vs nonsynonymous nucleotide substitutions indicate that these genes have not evolved under changes in evolutionary forces. All the data above suggest that the genes may have maintained at least some ancestral functions despite the lack of perianth in the flowers of C. spicatus.

Amino Acid Sequence↗

MIKC-type MADS-domain proteins: structural modularity, protein interactions and network evolution in land plants.

MIKC-type proteins represent a class of MADS-domain transcription factors and are defined by a unique domain structure: in addition to the highly conserved DNA-binding MADS-domain, they have three other domains ('I', 'K' and 'C'), with the keratin-like K-domain being the most highly conserved and characteristic one. The number and functional diversity of MIKC-type proteins increased considerably during land plant evolution, culminating in higher flowering plants, where they dominate the control of reproductive development from early to late stages. We wonder how one special class of proteins became important in the control of essentially all stages of a morphogenetic process. All MADS-domain proteins appear to bind to DNA as homo- or heterodimers and may function as part of ternary transcription factor complexes involving non-MADS-domain proteins. Only MIKC-type proteins, however, generate complex intrafamily interaction networks. These are based on the special potential of MIKC-type proteins to form complexes involving more than two homologous proteins constituting transcriptional regulators. We speculate that the potential to form heteromultimers of homologous proteins was achieved by the acquisition of the K-domain during evolution. There is emerging evidence that organismal complexity arises from progressively more elaborate regulation of gene expression. We hypothesize that combinatorial multimer formation of MIKC-type MADS-domain proteins facilitated an unusually efficient and rapid functional diversification based on gene duplication, sequence divergence and fixation. This 'networking' may have enabled a more sophisticated transcriptional control of target genes which was recruited for controlling increasingly complex and diverse developmental pathways during the rapid origin and diversification of plant reproductive structures. Therefore, MIKC-type proteins may owe their evolutionary 'success' and present-day developmental importance in part to their modular domain structure. Investigating the evolution of MIKC-type genes may thus help to better understand origin and diversification of gene regulatory networks.

Amino Acid Sequence↗

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

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.

Algal Proteins↗

A simple method for predicting the functional differentiation of duplicate genes and its application to MIKC-type MADS-box genes.

A simple statistical method for predicting the functional differentiation of duplicate genes was developed. This method is based on the premise that the extent of functional differentiation between duplicate genes is reflected in the difference in evolutionary rate because the functional change of genes is often caused by relaxation or intensification of functional constraints. With this idea in mind, we developed a window analysis of protein sequences to identify the protein regions in which the significant rate difference exists. We applied this method to MIKC-type MADS-box proteins that control flower development in plants. We examined 23 pairs of sequences of floral MADS-box proteins from petunia and found that the rate differences for 14 pairs are significant. The significant rate differences were observed mostly in the K domain, which is important for dimerization between MADS-box proteins. These results indicate that our statistical method may be useful for predicting protein regions that are likely to be functionally differentiated. These regions may be chosen for further experimental studies.

Data Interpretation, Statistical↗

Distinct MADS-box gene expression patterns in the reproductive cones of the gymnosperm Gnetum gnemon.

Expression patterns from in situ hybridization of four MADS-box genes (GGM7, GGM9, GGM11, and GGM15) from the gymnosperm species Gnetum gnemon are presented. Together with previously published data about putative orthologs of floral homeotic genes from G. gnemon (GGM2, GGM3, GGM13), we describe seven temporally and spatially distinct expression patterns in male, female or both types of reproductive units which very likely reflect the diversity of MADS-box gene function in gymnosperm cones. There is evidence that some aspects of the observed differential expression have been conserved since the last common ancestor of extant angiosperms and gymnosperms about 300 million years ago.

Gene Expression↗

Structural diversification and neo-functionalization during floral MADS-box gene evolution by C-terminal frameshift mutations.

Frameshift mutations generally result in loss-of-function changes since they drastically alter the protein sequence downstream of the frameshift site, besides creating premature stop codons. Here we present data suggesting that frameshift mutations in the C-terminal domain of specific ancestral MADS-box genes may have contributed to the structural and functional divergence of the MADS-box gene family. We have identified putative frameshift mutations in the conserved C-terminal motifs of the B-function DEF/AP3 subfamily, the A-function SQUA/AP1 subfamily and the E-function AGL2 subfamily, which are all involved in the specification of organ identity during flower development. The newly evolved C-terminal motifs are highly conserved, suggesting a de novo generation of functionality. Interestingly, since the new C-terminal motifs in the A- and B-function subfamilies are only found in higher eudicotyledonous flowering plants, the emergence of these two C-terminal changes coincides with the origin of a highly standardized floral structure. We speculate that the frameshift mutations described here are examples of co-evolution of the different components of a single transcription factor complex. 3' terminal frameshift mutations might provide an important but so far unrecognized mechanism to generate novel functional C-terminal motifs instrumental to the functional diversification of transcription factor families.

Amino Acid Motifs↗

Genomewide structural annotation and evolutionary analysis of the type I MADS-box genes in plants.

The type I MADS-box genes constitute a largely unexplored subfamily of the extensively studied MADS-box gene family, well known for its role in flower development. Genes of the type I MADS-box subfamily possess the characteristic MADS box but are distinguished from type II MADS-box genes by the absence of the keratin-like box. In this in silico study, we have structurally annotated all 47 members of the type I MADS-box gene family in Arabidopsis thaliana and exerted a thorough analysis of the C-terminal regions of the translated proteins. On the basis of conserved motifs in the C-terminal region, we could classify the gene family into three main groups, two of which could be further subdivided. Phylogenetic trees were inferred to study the evolutionary relationships within this large MADS-box gene subfamily. These suggest for plant type I genes a dynamic of evolution that is significantly different from the mode of both animal type I (SRF) and plant type II (MIKC-type) gene phylogeny. The presence of conserved motifs in the majority of these genes, the identification of Oryza sativa MADS-box type I homologues, and the detection of expressed sequence tags for Arabidopsis thaliana and other plant type I genes suggest that these genes are indeed of functional importance to plants. It is therefore even more intriguing that, from an experimental point of view, almost nothing is known about the function of these MADS-box type I genes.

Amino Acid Motifs↗

And then there were many: MADS goes genomic.

During the past decade, MADS-box genes have become known as key regulators in both reproductive and vegetative plant development. Traditional genetics and functional genomics tools are now available to elucidate the expression and function of this complex gene family on a much larger scale. Moreover, comparative analysis of the MADS-box genes in diverse flowering and non-flowering plants, boosted by bioinformatics, contributes to our understanding of how this important gene family has expanded during the evolution of land plants. Therefore, the recent advances in comparative and functional genomics should enable researchers to identify the full range of MADS-box gene functions, which should help us significantly in developing a better understanding of plant development and evolution.

Evolution, Molecular↗

The major clades of MADS-box genes and their role in the development and evolution of flowering plants.

MADS-box genes encode a family of transcription factors which control diverse developmental processes in flowering plants ranging from root to flower and fruit development. Sequencing of (almost) the complete Arabidopsis genome enabled the identification of (almost) all of the Arabidopsis MADS-box genes. MADS-box genes have been divided in two large groups, termed type I and type II genes. The type II genes comprise the MEF2-like genes of animals and fungi and the MIKC-type genes of plants. The majority of MIKC-type genes are of the MIKC(c)-type, which includes all plant MADS-box genes for which expression patterns or mutant phenotypes are known. By phylogeny reconstruction, almost all of the MIKC(c)-type genes can be subdivided into 12 major gene clades, each clade comprising 1-6 paralogs from Arabidopsis and putative orthologs from other seed plants. Here we first briefly describe the deep branching of the MADS-box gene tree to place the MIKC(c)-type genes into an evolutionary context. For every clade of MIKC(c)-type genes we then review what is known about its members from Arabidopsis and well-studied members from other phylogenetically informative plant species. By gene sampling and phylogeny reconstructions we provide minimal estimates for the ages of the different clades. It turns out that 7 of the 12 major gene clades, i.e., AG-, AGL6-, AGL12-, DEF+GLO- (B), GGM13- (B(s)), STMADS11- and TM3-like genes very likely existed already in the most recent common ancestor of angiosperms and gymnosperms about 300MYA. Three of the other clades, i.e., AGL2-, AGL17-, and SQUA-like genes, existed at least already in the most recent common ancestor of monocots and eudicots about 200 MYA. Only for two gene clades, AGL15-like genes (2 genes in Arabidopsis) and FLC-like genes (6 genes) members from plants other than Brassicaceae have not been reported yet. Similarly, only one ancient clade known from other flowering plant species, TM8-like genes, is not represented in Arabidopsis. These findings reveal that the diversity of MADS-box genes in Arabidopsis is rather ancient and representative for other flowering plants. Our studies may thus help to predict the set of MADS-box genes in all other flowering plants, except for relatively young paralogs. For the different gene clades we try to identify ancestral and derived gene functions and review the importance of these clades for seed plant development and evolution. We put special emphasis on gene clades for which insights into their importance has rapidly increased just recently.

Arabidopsis↗

Heterotopic expression of class B floral homeotic genes supports a modified ABC model for tulip (Tulipa gesneriana).

In higher eudicotyledonous angiosperms the floral organs are typically arranged in four different whorls, containing sepals, petals, stamens and carpels. According to the ABC model, the identity of these organs is specified by floral homeotic genes of class A, A+B, B+C and C, respectively. In contrast to the sepal and petal whorls of eudicots, the perianths of many plants from the Liliaceae family have two outer whorls of almost identical petaloid organs, called tepals. To explain the Liliaceae flower morphology, van Tunen et al. (1993) proposed a modified ABC model, exemplified with tulip. According to this model, class B genes are not only expressed in whorls 2 and 3, but also in whorl 1. Thus the organs of both whorls 1 and 2 express class A plus class B genes and, therefore, get the same petaloid identity. To test this modified ABC model we have cloned and characterized putative class B genes from tulip. Two DEF- and one GLO-like gene were identified, named TGDEFA, TGDEFB and TGGLO. Northern hybridization analysis showed that all of these genes are expressed in whorls 1, 2 and 3 (outer and inner tepals and stamens), thus corroborating the modified ABC model. In addition, these experiments demonstrated that TGGLO is also weakly expressed in carpels, leaves, stems and bracts. Gel retardation assays revealed that TGGLO alone binds to DNA as a homodimer. In contrast, TGDEFA and TGDEFB cannot homodimerize, but make heterodimers with PI. Homodimerization of GLO-like protein has also been reported for lily, suggesting that this phenomenon is conserved within Liliaceae plants or even monocot species.

Amino Acid Sequence↗

Ancestry and diversity of BEL1-like homeobox genes revealed by gymnosperm ( Gnetum gnemon) homologs.

BEL1-like homeobox genes encode plant-specific transcription factors, at least some of which are important for ovule development. Here we report MELBEL1-MELBEL4,the first BEL1-like genes from a non-flowering plant, the gymnosperm Gnetum gnemon. Our analyses suggest that there was already at least one BEL1-like gene present in the most recent common ancestor of extant seed plants about 300 million years ago. Multiple sequence alignments revealed that since this time, not only the DNA-binding homeodomain, but also a protein-protein interaction domain upstream of the homeodomain, termed the BEL domain, has been highly conserved. Sequence comparison of the BEL domain with upstream domains that have been conserved in other TALE homeodomain proteins, i.e. MEIS, KNOX, and PBC, revealed only weak sequence similarity. However, since homology has been shown for MEIS, KNOX, and PBC domains and since KNOX and BEL domains directly interact in vivo, it appears likely that the BEL domain was also derived from an ancestral upstream (MEINOX) domain.

Amino Acid Sequence↗