Beyond Arabidopsis. Translational biology meets evolutionary developmental biology

Developmental processes shape plant morphologies, which constitute important adaptive traits selected for during evolution. Identifying the genes that act in developmental pathways and determining how they are modified during evolution is the focus of the field of evolutionary developmental biology, or evo-devo. Knowledge of genetic pathways in the plant model Arabidopsis serves as the starting point for investigating how the toolkit of developmental pathways has been used and reused to form different plant body plans. One productive approach is to identify genes in other species that are orthologous to genes known to control developmental pathways in Arabidopsis and then determine what changes have occurred in the protein coding sequence or in the gene's expression to produce an altered morphology. A second approach relies on natural variation among wild populations or crop plants. Natural variation can be exploited to identify quantitative trait loci that underlie important developmental traits and, thus, define those genes that are responsible for adaptive changes. The possibility of applying comparative genomics approaches to Arabidopsis and related species promises profound new insights into the interplay of evolution and development.     

Interpreting the homeobox: metaphors of gene action and activation in development and evolution

SUMMARY Despite countless research efforts to demonstrate the precise developmental and evolutionary nature of homeobox genes, we are far from consensus on the role of this class of genes in development and evolution. This essay attempts to clarify the debate and to nip some problematic interpretations in the bud, by exploring metaphors of homeobox gene function in development and evolution.     

The patterning function of purines in the brine shrimp Artemia

In two Artemia wild-type sibling species originating from the Old and New Worlds, the processes underlying the construction of the naupliar body during embryonic development and the construction of the adult body during postembryonic development are disrupted by specific nutritional deficiencies and/or the administration of metabolic inhibitors. The species-specific phenotypic outcomes of these experimental disruptions on the construction of segments and the establishment of their identity, permit us to outline a model in which Hox genes would act as intermediary cogwheels fastened to a mechanism put in gear upstream by purine-mediated processes which would trigger downstream folic acid-mediated processes. The prevalent view that Hox genes can select for different developmental programmes, is challenged by this model whose relevancy is analysed in the context of our present knowledge on the master functions ascribed to Hox genes in developmental and evolutionary processes.     

The highs and lows of plant life: temperature and light interactions in development

Plants must constantly respond to changes in the environment whilst maintaining developmental and growth processes if they are to survive into the next generation. A complex network of signals from temperature and light must correctly converge to achieve successful development, through vegetative to reproductive growth. Temperature can be thought of as an environmental factor that provides both 'inductive' and 'maintenance' signals in development. It can stimulate developmental processes such as seed dormancy release, germination and vernalization. However, when temperature is not regarded as inductive, an accommodating network of genes work in concert to ensure growth responses occur regardless of fluctuating microclimate conditions. Many of the temperature-regulated developmental pathways are intimately linked with light signaling. For example, light-temperature interactions are major determinants in the timing of reproductive development. Indeed, the ability to process and react to complex environmental cues is crucial for both normal and adaptive development in a changing environment. These responses are frequently mediated by manipulating the phytohormone network, which serves as a powerful, yet adaptable controller of development. This paper illustrates the influential role temperature perception plays throughout plant development and the close interaction between temperature, light and hormone signaling.     

Control of Reproductive Floral Organ Identity Specification in Arabidopsis by the C Function Regulator AGAMOUS

The floral organ identity factor AGAMOUS (AG) is a key regulator of Arabidopsis thaliana flower development, where it is involved in the formation of the reproductive floral organs as well as in the control of meristem determinacy. To obtain insights into how AG specifies organ fate, we determined the genes and processes acting downstream of this C function regulator during early flower development and distinguished between direct and indirect effects. To this end, we combined genome-wide localization studies, gene perturbation experiments, and computational analyses. Our results demonstrate that AG controls flower development to a large extent by controlling the expression of other genes with regulatory functions, which are involved in mediating a plethora of different developmental processes. One aspect of this function is the suppression of the leaf development program in emerging floral primordia. Using trichome initiation as an example, we demonstrate that AG inhibits an important aspect of leaf development through the direct control of key regulatory genes. A comparison of the gene expression programs controlled by AG and the B function regulators APETALA3 and PISTILLATA, respectively, showed that while they control many developmental processes in conjunction, they also have marked antagonistic, as well as independent activities.     

Embryogenomics: developmental biology meets genomics

Fundamental questions in developmental biology are: what genes are expressed, where and when they are expressed, what is the level of expression and how are these programs changed by the functional and structural alteration of genes? These questions have been addressed by studying one gene at a time, but a new research field that handles many genes in parallel is emerging. The methodology is at the interface of large-scale genomics approaches and developmental biology. Genomics needs developmental biology because one of the goals of genomics – collection and analysis of all genes in an organism – cannot be completed without working on embryonic tissues in which many genes are uniquely expressed. However, developmental biology needs genomics – the high-throughput approaches of genomics generate information about genes and pathways that can give an integrated view of complex processes. This article discusses these new approaches and their applications to mammalian developmental biology.     

Looking at the origin of phenotypic variation from pattern formation gene networks

This article critically reviews some widespread views about the overall functioning of development. Special attention is devoted to views in developmental genetics about the superstructure of developmental gene networks. According to these views gene networks are hierarchic and multilayered. The highest layers partition the embryo in large coarse areas and control downstream genes that subsequently subdivide the embryo into smaller and smaller areas. These views are criticized on the bases of developmental and evolutionary arguments. First, these views, although detailed at the level of gene identities, do not incorporate morphogenetic mechanisms nor do they try to explain how morphology changes during development. Often, they assume that morphogenetic mechanisms are subordinate to cell signaling events. This is in contradiction to the evidence reviewed herein. Experimental evidence on pattern formation also contradicts the view that developmental gene networks are hierarchically multilayered and that their functioning is decodable from promoter analysis. Simple evolutionary arguments suggest that, indeed, developmental gene networks tend to be non-hierarchic. Re-use leads to extensive modularity in gene networks while developmental drift blurs this modularity. Evolutionary opportunism makes developmental gene networks very dependent on epigenetic factors.     

Snail shell coiling (re-)evolution and the evo-devo revolution

During the last two decades evolutionary developmental biology has become a major research programme whose findings put into question some concepts lying at the core of the 'Synthetic Theory'. However, some authors are waiting for a 'revolution' in biology, one in which the existing genetic determinism will give way to a new conceptual understanding of the complexity of living organisms. This 'revolution' should necessarily pass through the elaboration of an appropriate theoretical framework integrating the non-linear dynamics of development as its fundamental basis. This objective implies a drastic shift in the way causality is generally understood as well as a purge of numerous convenient but misleading metaphors such as genetic or developmental programmes. Although most authors do not take these metaphors too literally, some persist in employing such 'instructionist' notions in a more literal perspective, and, in doing so, deny some concepts at the core of evolutionary developmental biology. We critically review two recent studies suggesting that shell coiling has re-evolved in a family of limpets (Calyptraeidae, Gastropoda). We stress that this putative re-evolution of snail shell coiling results only from an arbitrary scoring procedure leading us to consider shell coiling as a binary discrete character. We show that the way in which these authors connect this case study to evolutionary theories stems from the unwarranted premise of a linear mapping of genes onto phenotypes where particulate inheritance of morphological characters seems implicitly assumed. We illustrate how the persisting unclear role of genes in morphogenesis allows the maintenance of the adaptationist programme.     

Maternal control of seed development

Maternal control of higher plant seed development is likely to involve female sporophytic as well as female gametophytic genes. While numerous female sporophytic mutants control the production of the ovule and the embryo sac true maternal effect mutations affecting embryo and endosperm development are rare in plants. A new class of female gametophytic mutants has been isolated that controls autonomous development of endosperm. Molecular analyses of these genes, known as FIS class genes, suggest that they repress downstream seed development genes by chromatin remodelling. Expression of the FIS genes in turn is modulated by parent specific expression or genomic imprinting which in turn is controlled by DNA methylation. Thus maternal control of seed development is a complex developmental event influenced by both genetic and epigenetic processes.     

Genome-wide analysis of the SET DOMAIN GROUP family in grapevine

The SET DOMAIN GROUP (SDG) proteins represent an evolutionarily-conserved family of epigenetic regulators present in eukaryotes and are putative candidates for the catalysis of lysine methylation in histones. Plant genomes analyses of this family have been performed in arabidopsis, maize, and rice and functional studies have shown that SDG genes are involved in the control of plant development. In this work, we describe the identification and structural characterization of SDG genes in the Vitis vinifera genome. This analysis revealed the presence of 33 putative SDG genes that can be grouped into different classes, as it has been previously described for plants. In addition to the SET domain, the proteins identified possessed other domains in the different classes. As part of our study regarding the growth and development of grapevine, we selected eight genes and their expression levels were analyzed in representative vegetative and reproductive organs of this species. The selected genes showed different patterns of expression during inflorescence and fruit development, suggesting that they participate in these processes. Furthermore, we showed that the expression of selected SDGs changes during viral infection, using as a model Grapevine Leafroll Associated Virus 3-infected symptomatic grapevine leaves and fruits. Our results suggest that developmental changes caused by this virus could be the result of alterations in SDG expression.     

Organ-specific expression of Arabidopsis genome during development

The development of complex eukaryotic organisms can be viewed as the selective expression of distinct fractions of the genome in different organs or tissue types in response to developmental and environmental cues. Here, we generated a genome expression atlas of 18 organ or tissue types representing the life cycle of Arabidopsis (Arabidopsis thaliana). We showed that each organ or tissue type had a defining genome expression pattern and that the degree to which organs share expression profiles is highly correlated with the biological relationship of organ types. Further, distinct fractions of the genome exhibited expression changes in response to environmental light among the three seedling organs, despite the fact that they share the same photo-perception and transduction systems. A significant fraction of the genes in the Arabidopsis genome is organized into chromatin domains exhibiting coregulated expression patterns in response to developmental or environmental signals. The knowledge of organ-specific expression patterns and their response to the changing environment provides a foundation for dissecting the molecular processes underlying development.     

MicroRNAs: Small regulators with a big impact

MicroRNAs (miRNA) are non-coding small (approximately 22nt) RNAs that regulate diverse physiological and developmental processes. In animals, they regulate target genes by binding imperfectly to 3'UTR sequences in mRNAs and attenuate translation. There are hundreds of miRNA genes in animals, and current studies show they constitute a minimum of 1% of known genes. We are just beginning to understand the diverse roles they play in cellular processes, which include signaling pathways, developmental pathways, and possibly various types of cancers.     

A new dawn for an old connection: development meets the cell

Increasingly, the attention of developmental biologists is being drawn from genes and their products towards cells, from processes mediated by linear pathways in which one protein regulates the activity of another to events that rely on multimolecular machines. Some components of these machines are partially redundant, and some have essential functions in general cellular processes. These observations invite a reassessment of the uses of genetics for analyzing the cell biology of development. In addition, the increasing ability to image live cells and their proteins reveals a complex and interesting world, forcing us to deal with new variables and objects of study. Here, we provide a glimpse of these changes and the challenges they raise.