The MADS-box floral homeotic gene lineages predate the origin of seed plants: Phylogenetic and molecular clock estimates

Flower development in angiosperms is controlled in part by floral homeotic genes, many of which are members of the plant MADS-box regulatory gene family. The evolutionary history of these developmental genes was reconstructed using 74 loci from 15 dicot, three monocot, and one conifer species. Molecular clock estimates suggest that the different floral homeotic gene lineages began to diverge from one another about 450–500 mya, around the time of the origin of land plants themselves. Received: 31 January 1997 / Accepted: 9 April 1997     

Patterns of molecular evolution among paralogous floral homeotic genes.

The plant MADS-box regulatory gene family includes several loci that control different aspects of inflorescence and floral development. Orthologs to the Arabidopsis thaliana MADS-box floral meristem genes APETALA1 and CAULIFLOWER and the floral organ identity genes APETALA3 and PISTILLATA were isolated from the congeneric species Arabidopsis lyrata. Analysis of these loci between these two Arabidopsis species, as well as three other more distantly related taxa, reveal contrasting dynamics of molecular evolution between these paralogous floral regulatory genes. Among the four loci, the CAL locus evolves at a significantly faster rate, which may be associated with the evolution of genetic redundancy between CAL and AP1. Moreover, there are significant differences in the distribution of replacement and synonymous substitutions between the functional gene domains of different floral homeotic loci. These results indicate that divergence in developmental function among paralogous members of regulatory gene families is accompanied by changes in rate and pattern of sequence evolution among loci.     

A characterization of the MADS-box gene family in maize

Studies on distantly related dicot plant species have identified homeotic genes that specify floral meristem identity and determine the fate of floral organ primordia. Most of these genes belong to a family characterized by the presence of a structural motif, the MADS-box, which encodes a protein domain with DNA-binding properties. As part of an effort to understand how such genes may have been recruited during the evolution of flowers with different organ types such as those found in maize, two members of this gene family in maize, ZAG1 and ZAG2, have been characterized previously. Here, the isolation and characterization of four new members of this gene family, designated ZAP1, ZAG3, ZAG4 and ZAG5, are described and the genetic map position of these and 28 additional maize MADS-box genes is determined. The first new member of this family appears to be the Zea mays ortholog of the floral homeotic gene APETALA1 (AP1) and has been designated ZAP1. One of these genes, ZAG4, is unusual in that its deduced protein sequence includes the MADS domain but lacks the K-domain characteristically present in this family of genes. In addition, its copy number and expression varies among different inbreds. A large number of maize MADS-box genes map to duplicated regions of the genome, including one pair characterized here, ZAG3 and ZAG5. These data underscore the complexity of this gene family in maize, and provide the basis for further studies into the regulation of floral organ morphogenesis among the grasses.     

Genomewide Structural Annotation and Evolutionary Analysis of the Type I MADS-Box Genes in Plants

Abstract 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.     

MADS-box genes active in developing pollen cones of Norway spruce (Picea abies) are homologous to the B-class floral homeotic genes in angiosperms.

The reproductive organs of conifers, the pollen cones and seed cones, differ in morphology from the angiosperm flower in several fundamental respects. In this report we present evidence to suggest that the two plant groups, in spite of these morphological differences and the long evolutionary distance between them, share important features in regulating the development of the reproductive organs. We present the cloning of three genes, DAL11, DAL12, and DAL13, from Norway spruce, all of which are related to the angiosperm B-class of homeotic genes. The B-class genes determine the identities of petals and stamens. They are members of a family of MADS-box genes, which also includes C-class genes that act to determine the identity of carpels and, in concert with B genes specify stamens in the angiosperm flower. Phylogenetic analyses and the presence of B-class specific C-terminal motifs in the DAL protein sequences imply homology to the B-class genes. Specific expression of all three genes in developing pollen cones suggests that the genes are involved in one aspect of B function, the regulation of development of the pollen-bearing organs. The different temporal and spatial expression patterns of the three DAL genes in the developing pollen cones indicate that the genes have attained at least in part distinct functions. The DAL11, DAL12, and 13 expression patterns in the pollen cone partly overlap with that of the previously identified DAL2 gene, which is structurally and functionally related to the angiosperm C-class genes. This result supports the hypothesis that an interaction between B- and C-type genes is required for male organ development in conifers like in the angiosperms. Taken together, our data suggests that central components in the regulatory mechanisms for reproductive organ development are conserved between conifers and angiosperms and, thus, among all seed plants.     

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.     

甘蓝型油菜MADS-box基因家族的鉴定与系统进化分析

MADS-box基因家族参与调控开花时间、花器官分化、根系生长、分生组织分化、子房和配子发育、果实膨大及衰老等植物生长发育的重要过程。基于甘蓝型油菜(Brassica napus)基因组测序数据,利用生物信息学方法对甘蓝型油菜MADS-box基因家族进行鉴定和注释及基因结构与系统进化分析。结果显示,在甘蓝型油菜中鉴定出307个MADS-box基因家族成员,根据进化关系可将其分为两大类型,I型(M-type)包含α、β、γ三个亚家族,II型(MIKC-type)包括MIKCC和MIKC*两个亚家族,MIKCC可进一步分为13个小类;甘蓝型油菜A基因组染色体上分布的MADS-box基因多于C基因组。在基因结构上,MIKC-type亚家族基因序列普遍比M-type长且含有较多的外显子;M-type亚家族蛋白序列中的motif数量为2–5个,MIKC-type亚家族蛋白序列中平均含有7个motif。拟南芥(Arabidopsis thaliana)与甘蓝型油菜MADS-box基因共线性分析结果显示,全基因组复制事件对MADS-box基因家族尤其是MIKC亚家族的扩张起重要作用;MIKC亚家族基因在进化过程中受到的选择压力约为M-type的2倍,这表明MIKC-type亚家族在进化过程中被选择性保留。     

Characterization of the Selaginella remotifolia MADS-box gene

Recent progress in plant molecular genetics has revealed that floral organ development is regulated by several homeotic selector genes, most of which belong to the MADS-box gene family. Here we report on SrMADS1,a MIKC(c)-type MADS-box gene from Selaginella, a spikemoss belonging to the lycophytes. SrMADS1 phylogenetically forms a monophyletic clade with genes of the LAMB2 group, which are MIKC(c) genes of the clubmoss Lycopodium, and is expressed in whole sporophytic tissues except roots and rhizophores. Our results and the previous report on Lycopodium MIKC(c) genes suggest that the ancestral MIKC(c )gene of primitive dichotomous plants in the early Devonian was involved in the development of basic sporophytic tissues such as shoot, stem, and sporangium.     

谷子 MADS-box基因家族的鉴定和表达分析

MADS-box基因是真核生物中一类重要的转录因子,参与调控多项植物的生长发育过程。然而关于谷子穗发育的MADS-box基因研究比较少。本研究使用序列相似性检索,在Phytozome 13.0数据库中筛选并且鉴定出了68个谷子MADS家族成员,并对这些家族成员的物理化学性质、系统发育树、染色体定位、表达谱等进行了全面的分析。结果表明,谷子MADS家族成员在染色体上分布不均匀,可以分为5个亚族。通过组织特异性表达谱分析得到,多数MADS基因在穗中表达量要高于其他器官。此外利用转录组测序技术对发育初期的谷穗和成熟期的谷穗进行了转录组测序分析,筛选到数个与谷穗分生组织发育相关MADS-box基因。为进一步揭示MADS-box基因在谷子穗发育过程中的作用奠定了重要的基础。