Genome evolution in polyploids

Polyploidy is a prominent process in plants and has been significant in the evolutionary history of vertebrates and other eukaryotes. In plants, interdisciplinary approaches combining phylogenetic and molecular genetic perspectives have enhanced our awareness of the myriad genetic interactions made possible by polyploidy. Here, processes and mechanisms of gene and genome evolution in polyploids are reviewed. Genes duplicated by polyploidy may retain their original or similar function, undergo diversification in protein function or regulation, or one copy may become silenced through mutational or epigenetic means. Duplicated genes also may interact through inter-locus recombination, gene conversion, or concerted evolution. Recent experiments have illuminated important processes in polyploids that operate above the organizational level of duplicated genes. These include inter-genomic chromosomal exchanges, saltational, non-Mendelian genomic evolution in nascent polyploids, inter-genomic invasion, and cytonuclear stabilization. Notwithstanding many recent insights, much remains to be learned about many aspects of polyploid evolution, including: the role of transposable elements in structural and regulatory gene evolution; processes and significance of epigenetic silencing; underlying controls of chromosome pairing; mechanisms and functional significance of rapid genome changes; cytonuclear accommodation; and coordination of regulatory factors contributed by two, sometimes divergent progenitor genomes. Continued application of molecular genetic approaches to questions of polyploid genome evolution holds promise for producing lasting insight into processes by which novel genotypes are generated and ultimately into how polyploidy facilitates evolution and adaptation.     

Genomic change and gene silencing in polyploids

Combining the genomes of two species through hybridization and chromosome doubling can create a new allopolyploid species virtually overnight. Although common in Nature, such genetic mergers might not be easy. Recent studies, mostly in plants, suggest that polyploidization can induce a flurry of genetic and epigenetic events that include DNA sequence elimination and gene silencing.     

Reproductive and genetic roles of the maternal progenitor in the origin of common wheat (Triticum aestivum L.)

Common wheat (Triticum aestivum L., AABBDD genome) is thought to have emerged through natural hybridization between Triticum turgidum L. (AABB genome) and Aegilops tauschii Coss. (DD genome). Hybridization barriers and doubling of the trihaploid F₁ hybrids’ genome (ABD) via unreduced gamete fusion had key roles in the process. However, how T. turgidum, the maternal progenitor, was involved in these mechanisms remains unknown. An artificial cross‐experiment using 46 cultivated and 31 wild T. turgidum accessions and a single Ae. tauschii tester with a very short genetic distance to the common wheat D genome was conducted. Cytological and quantitative trait locus analyses of F₁ hybrid genome doubling were performed. The crossability and ability to cause hybrid inviability did not greatly differ between the cultivars and wild accessions. The ability to cause hybrid genome doubling was higher in the cultivars. Three novel T. turgidum loci for hybrid genome doubling, which influenced unreduced gamete production in F₁ hybrids, were identified. Cultivated T. turgidum might have increased the probability of the emergence of common wheat through its enhanced ability to cause genome doubling in F₁ hybrids with Ae. tauschii. The ability enhancement might have involved alterations at a relatively small number of loci.     

Evolutionary significance of hybridization in Onosma (Boraginaceae): analyses of stabilized hemisexual odd polyploids and recent sterile hybrids

Interspecific hybridization is an important evolutionary force promoting plant speciation. In the genus Onosma, one of three main evolutionary lineages presumably evolved by hybrid speciation. The assumed hybrid lineage (Heterotricha) consists of two species complexes with bimodal karyotypes containing different numbers of large (L) and small (S) chromosomes, the tetraploid Onosma pseudoarenaria (2n = 12 L + 14S) and the triploid Onosma arenaria (2n = 12 L + 8S). The latter represents a rare case of hemisexual, asymmetrically compensating allopolyploids. Representatives of the other two lineages of the genus, Haplotricha (2n = 12 L) and Asterotricha (2n = 14S), have been considered to be the ancestral taxa of O. pseudoarenaria and O. arenaria, although this has yet to be investigated critically. In the present study, we examined genetic [amplified fragment length polymorphism (AFLP), internal transcribed spacer (ITS) , and chloroplast (cp)DNA)], reproductive (pollen viability and seed production) and cytogenetic (chromosome counts, genome size assessment) patterns to resolve the hypothesized allopolyploid formations in the Heterotricha group, single or polytopic allopolyploid origins, as well as ongoing interspecific gene flow as one piece of evidence for understanding past hybrid speciation events in the genus. Discordant patterns in maternally inherited cpDNA (Heterotricha accessions bearing the haplotypes related to asterotrichous species) and the nuclear ITS and AFLP markers (Heterotricha clustering with haplotrichous Onosma fastigiata), as well as karyological features, support the hybrid origin of the stabilized Heterotricha lineage. Genetic variation that is both large and geographically correlated indicates multiple origins of Heterotricha allopolyploids or, less likely, a single origin with recurring introgression from the progenitor species. The nuclear markers and cytogenetic features also provide evidence for the ongoing hybridization between O. arenaria and Onosma echioides (2n = 14S), which gives rise to sterile triploids of 2n = 6 L + 15S. We contrast the two cases of triploids with LLS (hemisexual O. arenaria from the stabilized Heterotricha lineage) and LSS (recent sterile hybrids) karyotypes, which could help to understand the mechanisms ensuring the establishment and reproductive fitness of the odd allopolyploids in Onosma. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112 , 89–107.     

Stochastic and epigenetic changes of gene expression in Arabidopsis polyploids

Polyploidization is an abrupt speciation mechanism for eukaryotes and is especially common in plants. However, little is known about patterns and mechanisms of gene regulation during early stages of polyploid formation. Here we analyzed differential expression patterns of the progenitors' genes among successive selfing generations and independent lineages. The synthetic Arabidopsis allotetraploid lines were produced by a genetic cross between A. thaliana and A. arenosa autotetraploids. We found that some progenitors' genes are differentially expressed in early generations, whereas other genes are silenced in late generations or among different siblings within a selfing generation, suggesting that the silencing of progenitors' genes is rapidly and/or stochastically established. Moreover, a subset of genes is affected in autotetraploid and multiple independent allotetraploid lines and in A. suecica, a natural allotetraploid derived from A. thaliana and A. arenosa, indicating locus-specific susceptibility to ploidy-dependent gene regulation. The role of DNA methylation in silencing progenitors' genes is tested in DNA-hypomethylation transgenic lines of A. suecica using RNA interference (RNAi). Two silenced genes are reactivated in both ddm1- and met1-RNAi lines, consistent with the demethylation of centromeric repeats and gene-specific regions in the genome. A rapid and stochastic process of differential gene expression is reinforced by epigenetic regulation during polyploid formation and evolution.     

Genomic markers on synthetic genomes

Genome synthesis endows scientists the ability of de novo creating genomes absent in nature, by thorough redesigning DNA sequences and introducing numerous custom features. However, the genome synthesis is a labor‐ and time‐consuming work, and thus it is a challenge to verify and quantify the synthetic genome rapidly and precisely. Thus, specific DNA sequences different from native genomic sequences are designed into synthetic genomes during synthesis, namely genomic markers. Genomic markers can be easily detected by PCR reaction, whole‐genome sequencing (WGS) and a variety of methods to identify the synthetic genome from native one. Here, we review types and applications of genomic markers utilized in synthetic genomes, with the hope of providing a guidance for future works.     

A new seed-based assay for meiotic recombination in Arabidopsis thaliana

Meiotic recombination is a fundamental biological process that plays a central role in the evolution and breeding of plants. We have developed a new seed-based assay for meiotic recombination in Arabidopsis. The assay is based on the transformation of green and red fluorescent markers expressed under a seed-specific promoter. A total of 74 T-DNA markers were isolated, sequenced and mapped both physically and genetically. Lines containing red and green markers that map 1-20 cM apart were crossed to produce tester lines with the two markers linked in cis yielding seeds that fluoresced both in red and green. We show that these lines can be used for efficient scoring of recombinant types (red only or green only fluorescing seeds) in a seed population derived from a test cross (backcross) or self-pollination. Two tester lines that were characterized during several generations of backcross and self-pollination, one in the background of ecotype Landsberg and one in the ecotype Columbia, are described. We discuss the number of plants and seeds to be scored in order to obtain reliable and reproducible crossing over rate values. This assay offers a relatively high-throughput method, with the benefit of seed markers (similar to the maize classical genetic markers) combined with the advantages of Arabidopsis. It advances the prospect to better understand the factors that affect the rate of meiotic crossover in plants and to stimulate this process for more efficient breeding and mapping.     

Generality and characteristics of genetic and epigenetic changes in newly synthesized allotetraploid wheat lines

Previous studies have shown rapid and extensive genomic instability associated with early stages of allopolyploidization in wheat.However, these studies are based on either a few pre-selected genomic loci or genome-wide analysis of a single plant individual for a given cross combination, thus making the extent and generality of the changes uncertain.To further study the generality and characteristics of allopolyploidization-induced genomic instability in wheat, we investigated genetic and epigenetic changes from a genome-wide perspective (by using the AFLP and MSAP markers) in four sets of newly synthesized allotetraploid wheat lines with various genome constitutions, each containing three randomly chosen individual plants at the same generation.We document that although general chromosomal stability was characteristic of all four sets of allotetraploid wheat lines, genetic and epigenetic changes at the molecular level occurred in all these plants, with both kinds of changes classifiable into two distinct categories, i.e., stochastic and directed.The abundant type of genetic change is loss of parental bands while the prevalent cytosine methylation pattern alteration is hypermethylation at the CHG sites.Our results have extended previous studies regarding allopolyploidization-induced genomic dynamics in wheat by demonstrating the generality of both genetic and epigenetic changes associated with multiple nascent allotetraploid wheat lines, and providing novel insights into the characteristics of the two kinds of induced genomic instabilities.     

Allopolyploidization lays the foundation for evolution of distinct populations: evidence from analysis of synthetic Arabidopsis allohexaploids

Polyploidization is an important mechanism for introducing diversity into a population and promoting evolutionary change. It is believed that most, if not all, angiosperms have undergone whole genome duplication events in their evolutionary history, which has led to changes in genome structure, gene regulation, and chromosome maintenance. Previous studies have shown that polyploidy can coincide with meiotic abnormalities and somatic cytogenetic mosaics in Arabidopsis allotetraploids, but it is unclear whether this phenomenon can contribute to novel diversity or act as a mechanism for speciation. In this study we tested the hypothesis that mosaic aneuploidy contributes to the formation of incipient diversity in neoallopolyploids. We generated a population of synthesized Arabidopsis allohexaploids and monitored karyotypic and phenotypic variation in this population over the first seven generations. We found evidence of sibling line-specific chromosome number variations and rapidly diverging phenotypes between lines, including flowering time, leaf shape, and pollen viability. Karyotypes varied between sibling lines and between cells within the same tissues. Cytotypic variation correlates with phenotypic novelty, and, unlike in allotetraploids, remains a major genomic destabilizing factor for at least the first seven generations. While it is still unclear whether new stable aneuploid lines will arise from these populations, our data are consistent with the notion that somatic aneuploidy, especially in higher level allopolyploids, can act as an evolutionary relevant mechanism to induce rapid variation not only during the initial allopolyploidization process but also for several subsequent generations. This process may lay the genetic foundation for multiple, rather than just a single, new species.     

Spartina anglica C. E. Hubbard: a natural model system for analysing early evolutionary changes that affect allopolyploid genomes

Spartina anglica arose during the end of the 19th century in England by hybridization between the indigenous Spartina maritima and the introduced East American Spartina alterniflora and following genome duplication of the hybrid ( S.  ×  townsendii ). This system allows investigations of the early evolutionary changes that accompany stabilization of a new allopolyploid species in natural populations. Various molecular data indicate that S. anglica has resulted from a unique parental genotype. This young species contains two distinctly divergent homoeologous genomes that have not undergone extensive change since their reunion. No burst of retroelements has been encountered in the F₁ hybrid or in the allopolyploid, suggesting a 'structural genomic stasis' rather than 'rapid genomic changes'. However, modifications of the methylation patterns in the genomes of S.  ×  townsendii and S. anglica indicate that in this system, epigenetic changes have followed both hybridization and polyploidization.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 475–484.     

Developmental changes in crossover frequency in Arabidopsis

Parental genomes are generally rearranged by two processes during meiosis: one is the segregation of homologous chromosomes and the other is crossing over between such chromosomes. Although the mechanisms underlying chromosome segregation and crossing over are well understood because of numerous genetic and molecular investigations, their contributions to the rearrangement of genetic information have not yet been analysed at a genome-wide level in Arabidopsis thaliana. We established 343 CAPS or SSLP markers to identify polymorphisms between two different Arabidopsis ecotypes, Col and Ler, which are distributed at an average distance of approximately 400kb between pairs of markers throughout the entire genome. Using these markers, crossover frequencies and chromosome segregation were quantified with respect to sex and age. Our large-scale analysis demonstrated that: (i) crossover frequencies during pollen formation were 1.79 and 1.37 times higher than those during megaspore formation in early and late flowers, respectively (P<0.001); (ii) the crossover frequencies during pollen formation were not significantly different between early and late flowers of main shoots (P>0.05), whereas the frequencies increased 1.30 times with shoot age during megaspore formation (P<0.001); (iii) the effect of aging depended on the developmental age of the individual shoot rather than on the age of the whole plant; and (iv) five chromosomes were randomly selected and mixed during meiosis.     

Rapid genomic changes in polyploid wheat and related species:implications for genome evolution and genetic improvement

A polyploid organism by possessing more than two sets of chromosomes from one species （autopolyploidy） or two or more species （allopolyploidy） is known to have evolutionary advantages. However, by what means a polyploid accommodates increased genetic dosage or divergent genomes （allopolyploidy） in one cell nucleus and cytoplasm constitutes an enormous challenge. Recent years have witnessed efforts and progress in exploring the possible mechanisms by which these seemingly intangible hurdles of polyploidy may be ameliorated or eventually overcome. In particular, the documentation of rapid and extensive non-Mendelian genetic and epigenetic changes that often accompany nascent polyploidy is revealing： the resulting non-additive and novel gene expression at global, regional and local levels, and timely restoration of meiotic chromosomal behavior towards bivalent pairing and disomic inheritance may ensure rapid establishment and stabilization as well as its long-term evolutionary success. Further elucidation on these novel mechanisms underpinning polyploidy will promote our understanding on fundamental issues in evolutionary biology and in our manipulation capacities in future genetic improvement of important crops that are currently polyploids in genomic constitution. This review is intended to provide an updated discussion on these interesting and important issues within the scope of a specific yet one of the most important plant groups--polyploid wheat and its related species.     

Genome evolution in Oryza allopolyploids of various ages: Insights into the process of diploidization

The prevalence and recurrence of whole-genome duplication in plants and its major role in evolution have been well recognized. Despite great efforts, many aspects of genome evolution, particularly the temporal progression of genomic responses to allopolyploidy and the underlying mechanisms, remain poorly understood. The rice genus Oryza consists of both recently formed and older allopolyploid species, representing an attractive system for studying the genome evolution after allopolyploidy. In this study, through screening BAC libraries and sequencing and annotating the targeted BAC clones, we generated orthologous genomic sequences surrounding the DEP1 locus, a major grain yield QTL in cultivated rice, from four Oryza polyploids of various ages and their likely diploid genome donors or close relatives. Based on sequenced DEP1 region and published data from three other genomic regions, we investigated the temporal evolutionary dynamics of four polyploid genomes at both genetic and expression levels. In the recently formed BBCC polyploid, Oryza minuta, genome dominance was not observed and its short-term responses to allopolyploidy are mainly manifested as a high proportion of homoeologous gene pairs showing unequal expression. This could partly be explained by parental legacy, rewiring of divergent regulatory networks and epigenetic modulation. Moreover, we detected an ongoing diploidization process in this genus, and suggest that the expression divergence driven by changes of selective constraint probably plays a big role in the long-term diploidization. These findings add novel insights into our understanding of genome evolution after allopolyploidy, and could facilitate crop improvements through hybridization and polyploidization.     

Major transitions in evolution by genome fusions: from prokaryotes to eukaryotes,metazoans, bilaterians and vertebrates

Journal of Structural and Functional Genomics - The major transitions in human evolution from prokaryotes toeukaryotes, from protozoans to metazoans, from the first animals tobilaterians and...     

Transposable elements and microevolutionary changes in natural populations

Transposable elements (TEs) usually represent the most abundant and dynamic fraction of genomes in almost all living organisms. The overall capacity of such ‘junk DNA’ to induce mutations and foster the reorganization of functional genomes suggests that TE may be of central evolutionary significance. However, to what extent TE dynamics drive and is driven by the evolutionary trajectory of host taxa remains poorly known. Further work addressing the fate of TE insertions in natural populations is necessary to shed light on their impact on microevolutionary processes. Here, we highlight methodological approaches (i.e. transposon displays and high‐throughput sequencing), tracking TE insertions across large numbers of individuals and discuss their pitfalls and benefits for molecular ecology surveys.     

种间杂种染色体配对所揭示的披碱草属植物StY基因组分化及其进化意义

在同倍体(homoploid)植物杂交-分化的物种形成(speciation)过程中,杂交后代与亲本之间的有效生殖隔离是新物种形成的关键。杂种与亲本在时间、空间、生态环境和基因水平上的隔离,保证了杂种后代的分化和稳定,并逐渐形成新物种。为了研究披碱草属(Elymus)含StY基因组四倍体物种的系统演化关系,本文对来自亚洲不同地理分布区的26种披碱草属植物进行了大规模的种间杂交和杂种F1减数分裂染色体配对行为的分析。结果表明各物种之间有不同程度的杂交亲合力,杂交结实率在各杂交组合之间有较大的变异(在4．8％-100％之间);但各物种之间的杂种F1完全不育。证明各物种之间形成了明显的生殖隔离。种间杂种F1减数分裂中期-I染色体配对分析的结果进一步表明,StY基因组随各披碱草属物种地理分布的不同而有不同程度的分化。来自同一分布区(如东亚或西亚分布区之内)物种的StY基因组分化程度较低,但来自不同分布区(如东亚和西亚)物种之间相同的StY基因组具有显著的分化。表明地理隔离对含StY基因组物种的分化起到了十分重要的作用。通过对种间和种内杂种F1的减数分裂异常现象和染色体配对频率变化规律的分析,作者认为细胞学水平的变化,如基因组同源性的分化和染色体结构的变异等都在杂种后代与亲本之间产生生殖隔离并逐渐形成新物种的进化过程中起到了积极的作用。     

芸薹属多倍体植物基因组进化的RAPD分析

多倍化是促进高等植物发生进化的重要力量。为了更清楚地了解多倍体在形成之后其基因组是如何进化的,利用38个随机引物对芸薹属Brassica L.禹氏三角（U’Triangle）中的多倍体物种及其祖先二倍体物种进行了研究。根据扩增出的273条带计算了遗传距离,并用UPGMA法进行了聚类分析。结果发现,二倍体物种B.campestris（AA）与B.oleracea（CC）的亲缘关系比与B.nigra（BB）的要近;异源多倍体B.napus（AACC）比起其二倍体祖先之一B.campestris（AA）与另一个     

Associated chromosomal DNA changes in polyploids.

The 2C and 4C nuclear DNA amounts were estimated in eight diploid species, belonging to three diverse genera (Vicia, Tephrosia, and Phlox) and their corresponding colchitetraploids. In P. drummondii, T. purpurea, and T. oxygona tetraploids the deviation from the expectation was highly significant. The DNA in P. drummondii was further discarded in subsequent (C1, C2) generations, thus attaining an overall reduction of about 25%. The DNA content in the subsequent generations was the same as that of C2. It is concluded that rapid DNA loss in the first and subsequent generations was not only associated with the substantial increase (30-66%) in the seed set, but it also helped in the establishment and stabilization of the tetraploid. The possible relationship between such a nucleotypic change and success of polyploids is discussed. The DNA change from the expected value in the P. drummondii tetraploid was achieved by equal decrement to each chromosome independent of size, i.e., small chromosomes loose the same amount of DNA as the large chromosomes.