The Role of Transposons in Epigenetic Regulation of Ontogenesis

A new insight into the mechanisms underlying implementation of genomic information in the individual development of eukaryotes through interactions of transposons with epigenetic factors dynamically changing during each cell division is described. These mechanisms of stepwise implementation of individual genetic information with characteristic stage- and tissue-specific features in the activities of certain mobile genetic element families are evolutionarily fixed at the species level. In addition, the individual differences caused by their “unscheduled” transpositions can significantly change the regulatory network of the genome altering the phenotype. These changes in individual development can bring about new traits leading to either a disease or better fitness and represent an important component of the variation for natural selection in evolution. A large part of the eukaryotic transposons is altered by mutations and used for formation of the regulatory gene network, changes in the protein-coding genes, and emergence of new nonprotein-coding genes. When inserted into new loci, mobile genetic elements form the basis for microRNA and the domain structures of long noncoding RNA, responding to various types of stress; this is reflected in the specific features of individual development and contributes to variation. The epigenetic factors, including noncoding RNA, DNA methylation, and histone modifications, are tightly associated with mobile genetic elements. The specific features in transposon location in individuals that have emerged owing to spontaneous mutations or those caused by stress impacts can considerably change the interactions in gene networks. This influences the likelihood of survival under changing environmental conditions and reflects a distinct interrelation between the mechanisms of individual development and evolution. There is a parallelism between the mechanisms underlying the rearrangements of genomes caused by transposons in evolution and in individual development. In particular, the responsiveness of transposons to external and internal (microenvironment) factors forms the background for evolutionary construction of transposon-mediated tissue-specific activation patterns of certain transposons during each cell division, which leads to maturation of a reproductive organism. This mechanism is based on tight stage- and tissuespecific interrelation between transposons, epigenetic factors, and protein-coding genes.     

Plant life evoluton: opinions and suppositions

Evolution of plant life has been considered in the context of phylembryogenesis or heterochronia. Hewever, suggested opinions and suppositions regarding the mechanisms, direction and rate of evolutionary changes are opposite. Concepts of phylembryogenesis and heterochronia originally were developed for the different levels of organization and could be distinguished by different modes of morphological evolution. In this connection, interpretations of evolutional changes of shoots morphogenesis, ontogenesis and plant habitus by different types of heterochronia and modes of phylembryogenesis were delineated. It was proposed that evolution of plants life forms could be considered regarding functional specialization of root-shoot (the basic element of life form structure) that appears as metamorphoses of bud, root and shoot. Evolutional changes of root-shoot could take places at the different stages of development due to anabolies (modifications). At the same time epigenetic and episelectional (organic selection) mechanisms of evolution play an important role in the evolution of plant life forms. Moreover, results of modern genetic and molecular phylogenetic investigations produce evidences for the saltations and reversions in the plant life forms evolution.     

Complex evolutionary history and diverse domain organization of SET proteins suggest divergent regulatory interactions

? Plants and animals possess very different developmental processes, yet share conserved epigenetic regulatory mechanisms, such as histone modifications. One of the most important forms of histone modification is methylation on lysine residues of the tails, carried out by members of the SET protein family, which are widespread in eukaryotes. ? We analyzed molecular evolution by comparative genomics and phylogenetics of the SET genes from plant and animal genomes, grouping SET genes into several subfamilies and uncovering numerous gene duplications, particularly in the Suv, Ash, Trx and E(z) subfamilies. ? Domain organizations differ between different subfamilies and between plant and animal SET proteins in some subfamilies, and support the grouping of SET genes into seven main subfamilies, suggesting that SET proteins have acquired distinctive regulatory interactions during evolution. We detected evidence for independent evolution of domain organization in different lineages, including recruitment of new domains following some duplications. ? More recent duplications in both vertebrates and land plants are probably the result of whole-genome or segmental duplications. The evolution of the SET gene family shows that gene duplications caused by segmental duplications and other mechanisms have probably contributed to the complexity of epigenetic regulation, providing insights into the evolution of the regulation of chromatin structure.     

Many-to-One Mapping of Form to Function: A General Principle in Organismal Design?

We introduce the concept of many-to-one mapping of form to functionand suggest that this emergent property of complex systems promotesthe evolution of physiological diversity. Our work has focusedon a 4-bar linkage found in labrid fish jaws that transmitsmuscular force and motion from the lower jaw to skeletal elementsin the upper jaws. Many different 4-bar shapes produce the sameamount of output rotation in the upper jaw per degree of lowerjaw rotation, a mechanical property termed Maxillary KT. Weillustrate three consequences of many-to-one mapping of 4-barshape to Maxillary KT. First, many-to-one mapping can partiallydecouple morphological and mechanical diversity within clades.We found with simulations of 4-bars evolving on phylogeniesof 500 taxa that morphological and mechanical diversity wereonly loosely correlated (R² = 0.25). Second, redundant mappingpermits the simultaneous optimization of more than one mechanicalproperty of the 4-bar. Labrid fishes have capitalized on thisflexibility, as illustrated by several species that have MaxillaryKT = 0.8 but have different values of a second property, NasalKT. Finally, many-to-one mapping may increase the influenceof historical factors in determining the evolution of morphology.Using a genetic model of 4-bar evolution we exerted convergentselection on three different starting 4-bar shapes and foundthat mechanical convergence only created morphological convergencein simulations where the starting forms were similar. Many-to-onemapping is widespread in physiological systems and operatesat levels ranging from the redundant mapping of genotypes tophenotypes, up to the morphological basis of whole-organismperformance. This phenomenon may be involved in the uneven distributionof functional diversity seen among animal lineages.     

The evolution of the peculiarities of mammalian sex chromosomes: an epigenetic view

In most discussions of the evolution of sex chromosomes, it is presumed that the morphological differences between the X and Y were initiated by genetic changes. An alternative possibility is that, in the early stages, a key role was played by epigenetic modifications of chromatin structure that did not depend directly on genetic changes. Such modifications could have resulted from spontaneous epimutations at a sex-determining locus or, in mammals, from selection in females for the epigenetic silencing of imprinted regions of the paternally derived sex chromosome. Other features of mammalian sex chromosomes that are easier to explain if the epigenetic dimension of chromosome evolution is considered include the relatively large number of X-linked genes associated with human brain development, and the overrepresentation of spermatogenesis genes on the X. Both may be evolutionary consequences of dosage compensation through X-inactivation.     

Reproductive barrier and genomic imprinting in the endosperm of flowering plants

In flowering plants, success or failure of seed development is determined by various genetic mechanisms. During sexual reproduction, double fertilization produces the embryo and endosperm, which both contain maternally and paternally derived genomes. In endosperm, a reproductive barrier is often observed in inter-specific crosses. Endosperm is a tissue that provides nourishment for the embryo within the seed, in a similar fashion to the placenta of mammals, and for the young seedling after germination. This review considers the relationship between the reproductive barrier in endosperm and genomic imprinting. Genomic imprinting is an epigenetic mechanism that results in mono-allelic gene expression that is parent-of-origin dependent. In Arabidopsis, recent studies of several imprinted gene loci have identified the epigenetic mechanisms that determine genomic imprinting. A crucial feature of genomic imprinting is that the maternally and paternally derived imprinted genes must carry some form of differential mark, usually DNA methylation and/or histone modification. Although the epigenetic marks should be complementary on maternally and paternally imprinted genes within a single species, it is possible that neither the patterns of epigenetic marks nor expression of imprinted genes are the same in different species. Moreover, in hybrid endosperm, the regulation of expression of imprinted genes can be affected by upstream regulatory mechanisms in the male and female gametophytes. Species-specific variations in epigenetic marks, the copy number of imprinted genes, and the epigenetic regulation of imprinted genes in hybrids might all play a role in the reproductive barriers observed in the endosperm of interspecific and interploidy crosses. These predicted molecular mechanisms might be related to earlier models such as the "endosperm balance number" (EBN) and "polar nuclei activation" (PNA) hypotheses.     

Unlocking the Black Box between Genotype and Phenotype: Cell Condensations as Morphogenetic (modular) Units

Embryonic development and ontogeny occupy whatis often depicted as the black box betweengenes – the genotype – and the features(structures, functions, behaviors) of organisms– the phenotype; the phenotype is not merelya one-to-one readout of the genotype. Thegenes home, context, and locus of operation isthe cell. Initially, in ontogeny, that cell isthe single-celled zygote. As developmentensues, multicellular assemblages of like cells(modules) progressively organized as germlayers, embryonic fields, anlage,condensations, or blastemata, enable genes toplay their roles in development and evolution.As modules, condensations are fundamentaldevelopmental and selectable units ofmorphology (morphogenetic units) that mediateinteractions between genotype and phenotype viaevolutionary developmental mechanisms. In ahierarchy of emergent processes, gene networksand gene cascades (genetic modules) link thegenotype with morphogenetic units such ascondensations, while epigenetic processes suchas embryonic inductions, tissue interactionsand functional integration, link morphogeneticunits to the phenotype. To support theseconclusions I distinguish units of heredityfrom units of transmission and discussepigenetic inheritance by tracing the historyof relationship between embryology andevolution, especially the role(s) assigned tocells or to cellular components in generatingtheories of morphological change in evolution.The concept of cells as modular morphogeneticunits is modeled and illustrated using themammalian dentary bone.     

Three epigenetic information channels and their different roles in evolution

There is increasing evidence for epigenetically mediated transgenerational inheritance across taxa. However, the evolutionary implications of such alternative mechanisms of inheritance remain unclear. Herein, we show that epigenetic mechanisms can serve two fundamentally different functions in transgenerational inheritance: (i) selection-based effects, which carry adaptive information in virtue of selection over many generations of reliable transmission; and (ii) detection-based effects, which are a transgenerational form of adaptive phenotypic plasticity. The two functions interact differently with a third form of epigenetic information transmission, namely information about cell state transmitted for somatic cell heredity in multicellular organisms. Selection-based epigenetic information is more likely to conflict with somatic cell inheritance than is detection-based epigenetic information. Consequently, the evolutionary implications of epigenetic mechanisms are different for unicellular and multicellular organisms, which underscores the conceptual and empirical importance of distinguishing between these two different forms of transgenerational epigenetic effect.     

Epigenetic germline inheritance

Our increased knowledge of epigenetic reprogramming supports the idea that epigenetic marks are not always completely cleared between generations. Incomplete erasure at genes associated with a measurable phenotype can result in unusual patterns of inheritance from one generation to the next. It is also becoming clear that the establishment of epigenetic marks during development can be influenced by environmental factors. In combination, these two processes could provide a mechanism for a rapid form of adaptive evolution.     

Dynamics of DNA Methylation in Recent Human and Great Ape Evolution

DNA methylation is an epigenetic modification involved in regulatory processes such as cell differentiation during development, X-chromosome inactivation, genomic imprinting and susceptibility to complex disease. However, the dynamics of DNA methylation changes between humans and their closest relatives are still poorly understood. We performed a comparative analysis of CpG methylation patterns between 9 humans and 23 primate samples including all species of great apes (chimpanzee, bonobo, gorilla and orangutan) using Illumina Methylation450 bead arrays. Our analysis identified ∼800 genes with significantly altered methylation patterns among the great apes, including ∼170 genes with a methylation pattern unique to human. Some of these are known to be involved in developmental and neurological features, suggesting that epigenetic changes have been frequent during recent human and primate evolution. We identified a significant positive relationship between the rate of coding variation and alterations of methylation at the promoter level, indicative of co-occurrence between evolution of protein sequence and gene regulation. In contrast, and supporting the idea that many phenotypic differences between humans and great apes are not due to amino acid differences, our analysis also identified 184 genes that are perfectly conserved at protein level between human and chimpanzee, yet show significant epigenetic differences between these two species. We conclude that epigenetic alterations are an important force during primate evolution and have been under-explored in evolutionary comparative genomics.     

Unique patterns of evolutionary conservation of imprinted genes

During mammalian evolution, complex systems of epigenetic gene regulation have been established: Epigenetic mechanisms control tissue-specific gene expression, X chromosome inactivation in females and genomic imprinting. Studying DNA sequence conservation in imprinted genes, it becomes evident that evolution of gene function and evolution of epigenetic gene regulation are tightly connected. Furthermore, comparative studies allow the identification of DNA sequence features that distinguish imprinted genes from biallelically expressed genes. Among these features are CpG islands, tandem repeats and retrotransposed elements that are known to play major roles in epigenetic gene regulation. Currently, more and more genetic and epigenetic data sets become available. In future, such data sets will provide the basis for more complex investigations on epigenetic variation in human populations. Therein, an exciting topic will be the genetic and epigenetic variability of imprinted genes and its input on human disease.     

Epigenetic “Drivers” of Cancer

Genetics is at the basis of cancer initiation and evolution, but emerging evidence indicates that mutations are not sufficient to produce cancer, indicating a role for epigenetic contributions to the different stages of tumorigenesis. While the genetic tracks of cancer have been widely investigated, the epigenetic “drivers” remain a vague definition. Gene-environment interactions can produce gene-regulatory programs that dictate pathogenesis; this implies a reciprocal relationship where environmental factors contribute to genetic mechanisms of tumorigenesis (i.e. mutagenesis) and genetic factors influence the cellular response to extrinsic stress. In this review article, we attempt to summarise the most remarkable findings demonstrating a contribution of epigenetic factors as proper “drivers” of tumorigenesis. We also try to pose attention on the relevance of epigenetic mechanisms as downstream consequences of genes versus environment interaction.     

花、基因、禾本科

进化发育生物学的一个重要任务就是揭示形态多样性的分子基础,该领域的研究包含形态、形态发育相关基因和形态所属类群等三个要素。花/花序是进化发育生物学研究的首要对象,系统发育重建和个体发育剖析的结合将促进认知花的形态进化。发育相关基因的进化表现为等位基因遗传或表观遗传的突变,基因家族生与死的进化,不同基因组拥有独特的基因。运用形态学或序列分析方法很大程度揭示了禾本科植物花进化过程中的基因进化。试从学科问题、思路方法以及具体例子介绍植物进化发育生物学。     

花、基因、禾本科

进化发育生物学的一个重要任务就是揭示形态多样性的分子基础, 该领域的研究包含形态、形态发育相关基因和形态所属类群等三个要素。花/花序是进化发育生物学研究的首要对象, 系统发育重建和个体发育剖析的结合将促进认知花的形态进化。发育相关基因的进化表现为等位基因遗传或表观遗传的突变, 基因家族生与死的进化, 不同基因组拥有独特的基因。运用形态学或序列分析方法很大程度揭示了禾本科植物花进化过程中的基因进化。试从学科问题、思路方法以及具体例子介绍植物进化发育生物学。     

PHENOTYPIC PLASTICITY AND EPIGENETIC MARKING: AN ASSESSMENT OF EVIDENCE FOR GENETIC ACCOMMODATION

The relationship between genotype (which is inherited) and phenotype (the target of selection) is mediated by environmental inputs on gene expression, trait development, and phenotypic integration. Phenotypic plasticity or epigenetic modification might influence evolution in two general ways: (1) by stimulating evolutionary responses to environmental change via population persistence or by revealing cryptic genetic variation to selection, and (2) through the process of genetic accommodation, whereby natural selection acts to improve the form, regulation, and phenotypic integration of novel phenotypic variants. We provide an overview of models and mechanisms for how such evolutionary influences may be manifested both for plasticity and epigenetic marking. We point to promising avenues of research, identifying systems that can best be used to address the role of plasticity in evolution, as well as the need to apply our expanding knowledge of genetic and epigenetic mechanisms to our understanding of how genetic accommodation occurs in nature. Our review of a wide variety of studies finds widespread evidence for evolution by genetic accommodation.     

Discordance between morphological and mechanical diversity in the feeding mechanism of centrarchid fishes

Morphological diversity is routinely used to infer ecological variation among species because differences in form underlie variation in functional performance of ecological tasks like capturing prey, avoiding predators, or defending territories. However, many functions have complex morphological bases that can weaken associations between morphological and functional diversification. We investigate the link between these levels of diversity in a mechanically explicit model of fish suction-feeding performance, where the map of head morphology to feeding mechanics is many-to-one: multiple, alternative forms can produce the same mechanical property. We show that many-to-one mapping leads to discordance between morphological and mechanical diversity in the freshwater fish family, the Centrarchidae, despite close associations between morphological changes and their mechanical effects. We find that each of the model's five morphological variables underlies evolution of suction capacity. Yet, the major centrarchid clades exhibit an order of magnitude range in diversity of suction mechanics in the absence of any clear difference in diversity of the morphological variables. This cryptic pattern of mechanical diversity suggests an evolutionary history for suction performance that is unlike the one inferred from comparisons of morphological diversity. Because many-to-one mapping is likely to be common in functional systems, this property of design may lead to widespread discordance between functional and morphological diversity. Although we focus on the interaction between morphology and mechanics, many-to-one mapping can decouple diversity between levels of organization in any hierarchical system.     

Cryptic individual scaling relationships and the evolution of morphological scaling

Morphological scaling relationships between organ and body size—also known as allometries—describe the shape of a species, and the evolution of such scaling relationships is central to the generation of morphological diversity. Despite extensive modeling and empirical tests, however, the modes of selection that generate changes in scaling remain largely unknown. Here, we mathematically model the evolution of the group‐level scaling as an emergent property of individual‐level variation in the developmental mechanisms that regulate trait and body size. We show that these mechanisms generate a “cryptic individual scaling relationship” unique to each genotype in a population, which determines body and trait size expressed by each individual, depending on developmental nutrition. We find that populations may have identical population‐level allometries but very different underlying patterns of cryptic individual scaling relationships. Consequently, two populations with apparently the same morphological scaling relationship may respond very differently to the same form of selection. By focusing on the developmental mechanisms that regulate trait size and the patterns of cryptic individual scaling relationships they produce, our approach reveals the forms of selection that should be most effective in altering morphological scaling, and directs researcher attention on the actual, hitherto overlooked, targets of selection.     

Genome-wide survey and developmental expression mapping of zebrafish SET domain-containing genes

SET domain-containing proteins represent an evolutionarily conserved family of epigenetic regulators, which are responsible for most histone lysine methylation. Since some of these genes have been revealed to be essential for embryonic development, we propose that the zebrafish, a vertebrate model organism possessing many advantages for developmental studies, can be utilized to study the biological functions of these genes and the related epigenetic mechanisms during early development. To this end, we have performed a genome-wide survey of zebrafish SET domain genes. 58 genes total have been identified. Although gene duplication events give rise to several lineage-specific paralogs, clear reciprocal orthologous relationship reveals high conservation between zebrafish and human SET domain genes. These data were further subject to an evolutionary analysis ranging from yeast to human, leading to the identification of putative clusters of orthologous groups (COGs) of this gene family. By means of whole-mount mRNA in situ hybridization strategy, we have also carried out a developmental expression mapping of these genes. A group of maternal SET domain genes, which are implicated in the programming of histone modification states in early development, have been identified and predicted to be responsible for all known sites of SET domain-mediated histone methylation. Furthermore, some genes show specific expression patterns in certain tissues at certain stages, suggesting the involvement of epigenetic mechanisms in the development of these systems. These results provide a global view of zebrafish SET domain histone methyltransferases in evolutionary and developmental dimensions and pave the way for using zebrafish to systematically study the roles of these genes during development.     

The great escape

Epigenetic mechanisms precisely regulate sex chromosome inactivation as well as genes that escape the silencing process. In male germ cells, DNA damage response factor RNF8 establishes active epigenetic modifications on the silent sex chromosomes during meiosis, and activates escape genes during a state of sex chromosome-wide silencing in postmeiotic spermatids. During the course of evolution, the gene content of escape genes in postmeiotic spermatids recently diverged on the sex chromosomes. This evolutionary feature mirrors the epigenetic processes of sex chromosomes in germ cells. In this article, we describe how epigenetic processes have helped to shape the evolution of sex chromosome-linked genes. Furthermore, we compare features of escape genes on sex chromosomes in male germ cells to escape genes located on the single X chromosome silenced during X-inactivation in females, clarifying the distinct evolutionary implications between male and female escape genes.