The MADS and the Beauty: Genes Involved in the Development of Orchid Flowers

Since the time of Darwin, biologists have studied the origin and evolution of the Orchidaceae, one of the largest families of flowering plants. In the last two decades, the extreme diversity and specialization of floral morphology and the uncoupled rate of morphological and molecular evolution that have been observed in some orchid species have spurred interest in the study of the genes involved in flower development in this plant family. As part of the complex network of regulatory genes driving the formation of flower organs, the MADS-box represents the most studied gene family, both from functional and evolutionary perspectives. Despite the absence of a published genome for orchids, comparative genetic analyses are clarifying the functional role and the evolutionary pattern of the MADS-box genes in orchids. Various evolutionary forces act on the MADS-box genes in orchids, such as diffuse purifying selection and the relaxation of selective constraints, which sometimes reveals a heterogeneous selective pattern of the coding and non-coding regions. The emerging theory regarding the evolution of floral diversity in orchids proposes that the diversification of the orchid perianth was a consequence of duplication events and changes in the regulatory regions of the MADS-box genes, followed by sub- and neo-functionalization. This specific developmental-genetic code is termed the "orchid code."     

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.     

Antiquity and evolution of the MADS-box gene family controlling flower development in plants

MADS-box genes in plants control various aspects of development and reproductive processes including flower formation. To obtain some insight into the roles of these genes in morphological evolution, we investigated the origin and diversification of floral MADS-box genes by conducting molecular evolutionary genetics analyses. Our results suggest that the most recent common ancestor of today's floral MADS-box genes evolved roughly 650 MYA, much earlier than the Cambrian explosion. They also suggest that the functional classes T (SVP), B (and Bs), C, F (AGL20 or TM3), A, and G (AGL6) of floral MADS-box genes diverged sequentially in this order from the class E gene lineage. The divergence between the class G and E genes apparently occurred around the time of the angiosperm/gymnosperm split. Furthermore, the ancestors of three classes of genes (class T genes, class B/Bs genes, and the common ancestor of the other classes of genes) might have existed at the time of the Cambrian explosion. We also conducted a phylogenetic analysis of MADS-domain sequences from various species of plants and animals and presented a hypothetical scenario of the evolution of MADS-box genes in plants and animals, taking into account paleontological information. Our study supports the idea that there are two main evolutionary lineages (type I and type II) of MADS-box genes in plants and animals.     

Functional conservation of MADS-box factors controlling floral organ identity in rice and Arabidopsis

Studies on MADS-box genes in Arabidopsis and other higher eudicotyledonous flowering plants have shown that they are key regulators of flower development. Since Arabidopsis and monocotyledonous rice are distantly related plant species it is interesting to investigate whether the floral organ identity factors have been conserved in their functions, and if not, to understand the differences. Arabidopsis and rice are very suitable for these studies since they are both regarded as models for plant functional genomics. Both their genomes are sequenced and tools are available for the analysis of gene function. These developments have accelerated experiments and increased our knowledge on rice gene function. Therefore it is the right moment to perform a comparative analysis on MADS-box factors controlling floral organ identity as reported in this review.     

Conservation and diversity in flower land

During the past decade, enormous progress has been made in understanding the molecular regulation of flower development. In particular, homeotic genes that determine the identity of the floral organs have been characterised from different flowering plants, revealing considerable conservation among angiosperm species. On the other hand, evolutionary diversification has led to enormous variation in flower morphology. Increasing numbers of reports have described differences in the regulation, redundancy and function of homeotic genes from various species. These fundamentals of floral organ specification are therefore an ideal subject for comparative analyses of flower development, which will lead to a better understanding of plant evolution, plant development and the complexity of molecular mechanisms that control flower development and morphology.     

Function and evolution of the plant MADS-box gene family

The function of MADS-box genes in flower and fruit development has been uncovered at a rapid pace over the past decade. Evolutionary biologists can now analyse the expression pattern of MADS-box genes during the development of different plant species, and study the homology of body parts and the evolution of body plans. These studies have shown that floral development is conserved among divergent species, and indicate that the basic mechanism of floral patterning might have evolved in an ancient flowering plant.     

Evolutionary dynamics of genes controlling floral development

Advances in the understanding of floral developmental genetics in model species such as Arabidopsis continue to provide an important foundation for comparative studies in other flowering plants. In particular, floral organ identity genes are the focus of many projects that are addressing both ancient and recent evolutionary questions. Expanded analyses of the evolution of these gene lineages have highlighted the dynamic nature of the gene birth-and-death process, and may have significant implications for the evolution of genetic pathways. Crucial functional studies of floral organ identity genes in diverse taxa are allowing the first real insight into the conservation of gene function, while findings on the genetic control of organ elaboration offer to open up new avenues for investigation. Taken together, these trends show that the field of floral developmental evolution continues to make significant progress towards elucidating the processes that have shaped the evolution of flower development and morphology.     

The genetics of plant morphological evolution.

Considerable progress has been made in identifying genes that are involved in the evolution of plant morphologies. Elements of the ABC model of flower development are conserved throughout angiosperms, and homologous MADS-box genes function in gymnosperm reproduction. Candidate gene and mapping analyses of floral symmetry, sex determination, inflorescence architecture, and compound leaves provide intriguing glimpses into the evolution of morphological adaptations.     

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.     

MADS-box基因家族基因重复及其功能的多样性

基因的重复(duplication)及其功能的多样性(diversification)为生物体新的形态进化提供了原材料。MADS-box基因在植物(特别是被子植物)的进化过程中发生了大规模的基因重复事件而形成一个多基因家族。MADS-box基因家族的不同成员在植物生长发育过程中起着非常重要的作用,在调控开花时间、决定花分生组织和花器官特征以及调控根、叶、胚珠及果实的发育中起着广泛的作用。探讨MADS-box基因家族的进化历史有助于深入了解基因重复及随后其功能分化的过程和机制。本文综述了MADS-box基因家族基因重复及其功能分化式样的研究进展。     

Overexpression of the cucumber LEAFY homolog CFL and hormone treatments alter flower development in gloxinia (Sinningia speciosa)

Leafy (LFY) and LFY-like genes control the initiation of floral meristems and regulate MADS-box genes in higher plants. The Cucumber-FLO-LFY (CFL) gene, a LFY homolog in Cucumis sativus L. is expressed in the primordia, floral primordia, and each whirl of floral organs during the early stage of flower development. In this study, functions of CFL in flower development were investigated by overexpressing the CFL gene in gloxinia (Sinningia speciosa). Our results show that constitutive CFL overexpression significantly promote early flowering without gibberellin (GA(3)) supplement, suggesting that CFL can serve functionally as a LFY homolog in gloxinia. Moreover, GA(3) and abscisic acid (ABA) treatments could modulate the expression of MADS-box genes in opposite directions. GA(3) resembles the overexpression of CFL in the expression of MADS-box genes and the regeneration of floral buds, but ABA inhibits the expression of MADS-box genes and flower development. These results suggest that CFL and downstream MADS-box genes involved in flower development are regulated by GA(3) and ABA.     

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。     

MADS-box 基因家族基因重复及其功能的多样性

基因的重复(duplication)及其功能的多样性(diversification)为生物体新的形态进化提供了原材料。MADS-box基因在植物(特别是被子植物)的进化过程中发生了大规模的基因重复事件而形成一个多基因家族。MADS-box基因家族的不同成员在植物生长发育过程中起着非常重要的作用, 在调控开花时间、决定花分生组织和花器官特征以及调控根、叶、胚珠及果实的发育中起着广泛的作用。探讨MADS-box基因家族的进化历史有助于深入了解基因重复及随后其功能分化的过程和机制。本文综述了MADS-box基因家族基因重复及其功能分化式样的研究进展。