Evolution of Reproductive Organs in Land Plants

LEAFY gene is the positive regulator of the MADS-box genes in flower primordia. The number of MADS-box genes presumably increased by gene duplications before the divergence of ferns and seed plants. Most MADS-box genes in ferns are expressed similarly in both vegetative and reproductive organs, while in gymnosperms, some MADS-box genes are specifically expressed in reproductive organs. This suggests that (1) the increase in the number of MADS-box genes and (2) the subsequent recruitment of some MADS-box genes as homeotic selector genes were important for the evolution of complex reproductive organs. The phylogenetic tree including both angiosperm and gymnosperm MADS-box genes indicates the loss of the A-function genes in the gymnosperm lineage, which is presumably related to the absence of perianths in extant gymnosperms. Comparison of expression patterns of orthologous MADS-box genes in angiosperms, Gnetales, and conifers supports the sister relationship of Gnetales and conifers over that of Gnetales and angiosperms predicted by phylogenetic trees based on amino acid and nucleotide sequences. Received 30 July 1999/ Accepted in revised form 9 September 1999     

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.     

MADS-BOX GENES: DEVELOPMENT AND EVOLUTION OF PLANT BODY PLANS

We review functional data on MADS-box genes, recent phylogenetic analyses of these coding regions, and their roles in the development and evolution of key morphological innovations in plants. We map the origin of important morphological structures in particular diverse stages of the life cycle in different plant clades onto organismal phylogenies, and present relevant molecular genetic aspects of development related to the MADS-box genes. We focus on reproductive structures of the sporophyte because most functional characterizations have been done of MADS-box genes involved in flower development. We discuss MADS-box evolution in flowering plants, but we also review studies in the other nonflowering vascular plants, gymnosperms (conifers and gnetales), and ferns and preliminary data from the algae. We suggest that floral (e.g. flowering time, inflorescence, and flower meristem identity) MADS-box and nonfloral plant MADS-box genes should be the focus of future comparative research. Cloning and functional analyses of MADS-box genes in bryophytes, particularly in the experimental system Physcomitrella patens (Hedw.) B.S.G., are needed. The ABC model of floral organ specification is an excellent general representation of an important network of genes; however, formal analytical tools are required to integrate data on complex gene interaction in comparative analyses. This and other analytical approaches to constructing gene network models will help to frame homology hypotheses in an evolutionary and developmental framework.     

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.     

Gymnosperm Orthologues of Class B Floral Homeotic Genes and Their Impact on Understanding Flower Origin

Class B floral homeotic genes play a key role in specifying the identity of male reproductive organs (stamens) and petals during the development of flowers. Recently, close relatives (orthologues) of these genes have been found in diverse gymnosperms, the sister group of the flowering plants (angiosperms). The fact that such genes have not been found so far, despite considerable efforts, in mosses, ferns or algae, has been taken as evidence to suggest that B genes originated 300–400 million years ago in a lineage that led to extant seed plants. Gymnosperms do not develop petals, and their male reproductive organs deviate considerably from angiosperm stamens. So what is the function of gymnosperm B genes? Recent experiments revealed that B genes from diverse extant gymnosperms are exclusively expressed in male reproductive organs (microsporophylls). At least for some of these genes it has been shown that they can partially substitute for the Arabidopsis B genes AP3 and PI in ectopic expression experiments, or even partially substitute these genes in different class B floral organ identity gene mutants. This functional complementation, however, is restricted to male organ development. These findings strongly suggest that gymnosperm and angiosperm B genes have highly related interaction partners and equivalent functions in the male organs of their different host species. It seems likely that in extant gymnosperms B genes have a function in specifying male reproductive organs. This function was probably established already in the most recent common ancestor of extant gymnosperms and angiosperms (seed plants) 300 million years ago and thus represents the ancestral function of seed plant B genes, from which other functions (e.g., in specifying petal identity) might have been derived. This suggests that the B gene function is part of an ancestral sex determination system in which B gene expression specifies male reproductive organ development, while the absence of B gene expression leads to the formation of female reproductive organs. Such a simple switch mechanism suggests that B genes might have played a central role during the origin of flowers. In the out-of-male and out-of-female hypotheses changes in B gene expression led to the origin of hermaphroditic flower precursors out of male or female gymnosperm reproductive cones, respectively. We compare these hypotheses with other recent molecular hypotheses on the origin of flowers, in which C/D and FLORICAULA/LEAFY-like genes is given a more prominent role, and we suggest how these hypotheses might be tested in the future.     

One MADS-box gene does not a flower make

Tandre, K., Svenson, M., Svensson, M.E. and Engström, P. (1998) Conservation of gene structure and activity in the regulation of reproductive organ development of conifers and angiosperms, Plant J. 15, 615–623Rutledge, R., Regan, S., Nicolas, O., Fobert, P., Côté, C., Bosnich, W., Kauffeldt, C., Sunohara, G., Séguin, A. and Stewart, D. (1998) Characterization of an AGAMOUS homologue from the conifer black spruce (Picea mariana) that produces floral homeotic conversions when expressed in Arabidopsis, Plant J. 15, 625–634     

植物MADS-box基因的研究进展

MADS-box基因是一类重要的转录调控因子,在动物、植物、真菌中都有分布。在植物中从根、茎、叶到花的发育,果实的成熟MADS-box基因都起作用,尤其是在开花植物中花的发育,开花时间的控制等方面起着重要的作用。综述了MADS-box基因的分类、进化、结构、以及MADS-box基因在植物花器官发育,开花时间的控制,果实的成熟等方面的作用。     

Comparative analysis of rice MADS-box genes expressed during flower development

MADS-box genes involved in flower development have been isolated and studied in a wide variety of plant species. However, most of these studies are related to dicot species like Antirrhinum majus, Arabidopsis thaliana and Petunia hybrida. Although the floral structures of typical monocot and dicot flowers differ substantially, previous studies indicate that MADS-box genes controlling floral organ identity in dicots can also be identified in monocot plants like rice and maize. To extend this study further to obtain a more global picture of monocot and dicot MADS-box gene evolution, we performed a phylogenetic study using MADS-box genes from A. thaliana and Oryza sativa. Furthermore, we investigated whether the identified orthologues of Arabidopsis and rice have a conserved expression profile that could indicate conservation of function.