'Why polyploidy is rarer in animals than in plants': myths and mechanisms

Although polyploidy has been involved in speciation in both animals and plants, the general perception is often that it is too rare to have been a significant factor in animal evolution and its role in plant diversification has been questioned. These views have resulted in a bias towards explanations for what deters polyploidy, rather than the somewhat more interesting question of the mechanisms by which polyploidy arises and becomes established in both plants and animals. The evidence for and against some of the traditional views on polyploidy is reviewed, with an attempt to synthesize factors promoting evolution through genome duplication in both groups. It is predicted that polyploidy should be more common in temperate than in tropical breeders because environmental fluctuations may promote unreduced gamete formation, it should be most common in organisms with sufficient numbers of gametes that random meiotic problems can be overcome, and it should be more frequent when mechanisms to promote assortative mating are a direct byproduct of genome duplication.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 453–466.     

Rarely successful polyploids and their legacy in plant genomes

Polyploidy, or whole genome duplication, is recognized as an important feature of eukaryotic genome evolution. Among eukaryotes, polyploidy has probably had the largest evolutionary impact on vascular plants where many contemporary species are of recent polyploid origin. Genomic analyses have uncovered evidence of at least one round of polyploidy in the ancestry of most plants, fueling speculation that genome duplications lead to increases in net diversity. In spite of the frequency of ancient polyploidy, recent analyses have found that recently formed polyploid species have higher extinction rates than their diploid relatives. These results suggest that despite leaving a substantial legacy in plant genomes, only rare polyploids survive over the long term and most are evolutionary dead-ends.     

Polyploid organisms

Polyploids are organisms with three or more complete chromosome sets. Polyploidization is widespread in plants and animals, and is an important mechanism of speciation. Genome sequencing and related molecular systematics and bioinformatics studies on plants and animals in recent years support the view that species have been shaped by whole genome duplication during evolution. The stability of polyploids depends on rapid genome recombination and changes in gene expression after formation. The formation of polyploids and subsequent diploidization are important aspects in long-term evolution. Polyploids can be formed in various ways. Among them, hybrid organisms formed by distant hybridization could produce unreduced gametes and thus generate offspring with doubled chromosomes, which is a fast, efficient method of polyploidization. The formation of fertile polyploids not only promoted the interflow of genetic materials among species and enriched the species diversity, but also laid the foundation for polyploidy breeding. The study of polyploids has both important theoretical significance and valuable applications. The production and application of polyploidy breeding have brought remarkable economic and social benefits.     

Dating and functional characterization of duplicated genes in the apple (<Emphasis Type="Italic">Malus domestica</Emphasis> Borkh.) by analyzing EST data

Background  

Gene duplication is central to genome evolution. In plants, genes can be duplicated through small-scale events and large-scale duplications often involving polyploidy. The apple belongs to the subtribe Pyrinae (Rosaceae), a diverse lineage that originated via allopolyploidization. Both small-scale duplications and polyploidy may have been important mechanisms shaping the genome of this species.     

Polyploidy and its effect on evolutionary success: old questions revisited with new tools

Polyploidy, the condition of possessing more than two complete genomes in a cell, has intrigued biologists for almost a century. Polyploidy is found in many plants and some animal species and today we know that polyploidy has had a role in the evolution of all angiosperms. Despite its widespread occurrence, the direct effect of polyploidy on evolutionary success of a species is still largely unknown. Over the years many attractive hypotheses have been proposed in an attempt to assign functionality to the increased content of a duplicated genome. Among these hypotheses are the proposal that genome doubling confers distinct advantages to a polyploid and that these advantages allow polyploids to thrive in environments that pose challenges to the polyploid''s diploid progenitors. This article revisits these long-standing questions and explores how the integration of recent genomic developments with ecological, physiological and evolutionary perspectives has contributed to addressing unresolved problems about the role of polyploidy. Although unsatisfactory, the current conclusion has to be that despite significant progress, there still isn''t enough information to unequivocally answer many unresolved questions about cause and effect of polyploidy on evolutionary success of a species. There is, however, reason to believe that the increasingly integrative approaches discussed here should allow us in the future to make more direct connections between the effects of polyploidy on the genome and the responses this condition elicits from the organism living in its natural environment.     

Polyploidy and self-fertilization in flowering plants

Mating systems directly control the transmission of genes across generations, and understanding the diversity and distribution of mating systems is central to understanding the evolution of any group of organisms. This basic idea has been the motivation for many studies that have explored the relationships between plant mating systems and other biological and/or ecological phenomena, including a variety of floral and environmental characteristics, conspecific and pollinator densities, growth form, parity, and genetic architecture. In addition to these examples, a potentially important but poorly understood association is the relationship between plant mating systems and genome duplication, i.e., polyploidy. It is widely held that polyploid plants self-fertilize more than their diploid relatives, yet a formal analysis of this pattern does not exist. Data from 235 species of flowering plants were used to analyze the association between self-fertilization and ploidy. Phylogenetically independent contrasts and cross-species analyses both lend support to the hypothesis that polyploids self-fertilize more than diploids. Because polyploidy and self-fertilization are so common among angiosperms, these results contribute not only to our understanding of the relationship between mating systems and polyploidy in particular, but more generally, to our understanding of the evolution of flowering plants.     

Extensive variation in chromosome number and genome size in sexual and parthenogenetic species of the jumping‐bristletail genus Machilis (Archaeognatha)

Parthenogenesis in animals is often associated with polyploidy and restriction to extreme habitats or recently deglaciated areas. It has been hypothesized that benefits conferred by asexual reproduction and polyploidy are essential for colonizing these habitats. However, while evolutionary routes to parthenogenesis are manifold, study systems including polyploids are scarce in arthropods. The jumping‐bristletail genus Machilis (Insecta: Archaeognatha) includes both sexual and parthenogenetic species, and recently, the occurrence of polyploidy has been postulated. Here, we applied flow cytometry, karyotyping, and mitochondrial DNA sequencing to three sexual and five putatively parthenogenetic Eastern‐Alpine Machilis species to investigate whether (1) parthenogenesis originated once or multiply and (2) whether parthenogenesis is strictly associated with polyploidy. The mitochondrial phylogeny revealed that parthenogenesis evolved at least five times independently among Eastern‐Alpine representatives of this genus. One parthenogenetic species was exclusively triploid, while a second consisted of both diploid and triploid populations. The three other parthenogenetic species and all sexual species were diploid. Our results thus indicate that polyploidy can co‐occur with parthenogenesis, but that it was not mandatory for the emergence of parthenogenesis in Machilis. Overall, we found a weak negative correlation of monoploid genome size (Cx) and chromosome base number (x), and this connection is stronger among parthenogenetic species alone. Likewise, monoploid genome size decreased with elevation, and we therefore hypothesize that genome downsizing could have been crucial for the persistence of alpine Machilis species. Finally, we discuss the evolutionary consequences of intraspecific chromosomal rearrangements and the presence of B chromosomes. In doing so, we highlight the potential of Alpine Machilis species for research on chromosomal and genome‐size alterations during speciation.     

The influence of experimentally induced polyploidy on the relationships between endopolyploidy and plant function in Arabidopsis thaliana

Whole genome duplication, leading to polyploidy and endopolyploidy, occurs in all domains and kingdoms and is especially prevalent in vascular plants. Both polyploidy and endopolyploidy increase cell size, but it is unclear whether both processes have similar effects on plant morphology and function, or whether polyploidy influences the magnitude of endopolyploidy. To address these gaps in knowledge, fifty‐five geographically separated diploid accessions of Arabidopsis thaliana that span a gradient of endopolyploidy were experimentally manipulated to induce polyploidy. Both the diploids and artificially induced tetraploids were grown in a common greenhouse environment and evaluated with respect to nine reproductive and vegetative characteristics. Induced polyploidy decreased leaf endopolyploidy and stem endopolyploidy along with specific leaf area and stem height, but increased days to bolting, leaf size, leaf dry mass, and leaf water content. Phenotypic responses to induced polyploidy varied significantly among accessions but this did not affect the relationship between phenotypic traits and endopolyploidy. Our results provide experimental support for a trade‐off between induced polyploidy and endopolyploidy, which caused induced polyploids to have lower endopolyploidy than diploids. Though polyploidy did not influence the relationship between endopolyploidy and plant traits, phenotypic responses to experimental genome duplication could not be easily predicted because of strong cytotype by accession interactions.     

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.     

The Battle to Sequence the Bread Wheat Genome:A Tale of the Three Kingdoms

In the year 2018, the world witnessed the finale of the race to sequence the genome of the world’s most widely grown crop, the common wheat. Wheat has been known to bear a notoriously large and complicated genome of a polyploidy nature. A decade competition to sequence the wheat genome initiated with a single consortium of multiple countries, taking a conventional strategy similar to that for sequencing Arabidopsis and rice, became ferocious over time as both sequencing technologies and genome assembling methodologies advanced. At different stages, multiple versions of genome sequences of the same variety (e.g., Chinese Spring) were produced by several groups with their special strategies. Finally, 16 years after the rice genome was finished and 9 years after that of maize, the wheat research community now possesses its own reference genome. Armed with these genomics tools, wheat will reestablish itself as a model for polyploid plants in studying the mechanisms of polyploidy evolution, domestication, genetic and epigenetic regulation of homoeolog expression, as well as defining its genetic diversity and breeding on the genome level. The enhanced resolution of the wheat genome should also help accelerate development of wheat cultivars that are more tolerant to biotic and/or abiotic stresses with better quality and higher yield.     

Transcriptome and miRNAs analyses enhance our understanding of the evolutionary advantages of polyploidy

Polyploid organisms have more than two sets of chromosomes, including autopolyploid via intraspecific genome doubling, and allopolyploid via merging genomes of distinct species by hybridization. Polyploid organisms are widespread in plants, indicating that polyploidy has some evolutionary advantages over its diploid ancestor. Actually, polyploidy is always tightly associated with hybrid vigor and adaptation to adverse environmental conditions. However, why polyploidy can develop such advantages is poorly known. MicroRNAs (miRNAs) are endogenous ～21?nt small RNAs which can play important regulatory roles in animals and plants by targeting mRNAs for cleavage or translational repression. MicroRNAs are essential for cell development, differentiation, signal transduction, and show an adaptive response to biotic and abiotic stresses. Environmental stresses cause plants to over- or under-express certain miRNAs or synthesize new miRNAs to cope with stress. We have here reviewed our current knowledge on the molecular mechanisms, which can account for the evolutionary advantages of polyploidy over its diploid ancestor from genome-wide gene expression and microRNAs expression perspectives.     

Size is not everything: rates of genome size evolution,not C-value,correlate with speciation in angiosperms

Angiosperms represent one of the key examples of evolutionary success, and their diversity dwarfs other land plants; this success has been linked, in part, to genome size and phenomena such as whole genome duplication events. However, while angiosperms exhibit a remarkable breadth of genome size, evidence linking overall genome size to diversity is equivocal, at best. Here, we show that the rates of speciation and genome size evolution are tightly correlated across land plants, and angiosperms show the highest rates for both, whereas very slow rates are seen in their comparatively species-poor sister group, the gymnosperms. No evidence is found linking overall genome size and rates of speciation. Within angiosperms, both the monocots and eudicots show the highest rates of speciation and genome size evolution, and these data suggest a potential explanation for the megadiversity of angiosperms. It is difficult to associate high rates of diversification with different types of polyploidy, but it is likely that high rates of evolution correlate with a smaller genome size after genome duplications. The diversity of angiosperms may, in part, be due to an ability to increase evolvability by benefiting from whole genome duplications, transposable elements and general genome plasticity.     

An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV

Advances in recent years have revolutionized our understanding of both the context and occurrence of polyploidy in plants. Molecular phylogenetics has vastly improved our understanding of plant relationships, enabling us to better understand trait and character evolution, including chromosome number changes. This, in turn, has allowed us to appreciate better the frequent occurrence and extent of polyploidy throughout the history of angiosperms, despite the occurrence of low chromosome numbers in some groups, such as in Arabidopsis (A. thaliana was the first plant genome to be sequenced and assembled). In tandem with an enhanced appreciation of phylogenetic relationships, the accumulation of genomic data has led to the conclusion that all angiosperms are palaeopolyploids, together with better estimates of the frequency and type of polyploidy in different angiosperm lineages. The focus therefore becomes when a lineage last underwent polyploidization, rather than simply whether a plant is ‘diploid’ or ‘polyploid’. This legacy of past polyploidization in plants is masked by large‐scale genome reorganization involving repetitive DNA loss, chromosome rearrangements (including fusions and fissions) and complex patterns of gene loss, a set of processes that are collectively termed ‘diploidization’. We argue here that it is the diploidization process that is responsible for the ‘lag phase’ between polyploidization events and lineage diversification. If so, diploidization is important in determining chromosome structure and gene content, and has therefore made a significant contribution to the evolutionary success of flowering plants. © 2015 The Authors. Botanical Journal of the Linnean Society published by John Wiley & Sons Ltd on behalf of Linnean Society of London, 2016, 180 , 1–5.     

Polyploidy does not control all: Lineage‐specific average chromosome length constrains genome size evolution in ferns

Recent studies investigating the evolution of genome size diversity in ferns have shown that they have a distinctive genome profile compared with other land plants. Ferns are typically characterized by possessing medium‐sized genomes, although a few lineages have evolved very large genomes. Ferns are different from other vascular plant lineages as they are the only group to show evidence for a correlation between genome size and chromosome number. In this study, we aim to explore whether the evolution of fern genome sizes is not only shaped by chromosome number changes arising from polyploidy but also by constraints on the average amount of DNA per chromosome. We selected the genus Asplenium L. as a model genus to study the question because of the unique combination of a highly conserved base chromosome number and a high frequency of polyploidy. New genome size data for Asplenium taxa were combined with existing data and analyzed within a phylogenetic framework. Genome size varied substantially between diploid species, resulting in overlapping genome sizes among diploid and tetraploid spleenworts. The observed additive pattern indicates the absence of genome downsizing following polyploidy. The genome size of diploids varied non‐randomly and we found evidence for clade‐specific trends towards larger or smaller genomes. The 578‐fold range of fern genome sizes have arisen not only from repeated cycles of polyploidy but also through clade‐specific constraints governing accumulation and/or elimination of DNA.     

Is lack of cycad (Cycadales) diversity a result of a lack of polyploidy?

Many hypotheses exist for the relative diversity of seed plant taxa. We discuss one of them: how the relative dearth of cycad diversity throughout their 300 million year history may be a result of a lack of duplication of their entire nuclear genome, often termed polyploidy. We show theoretically how polyploidy causes speciation via cryptic reproductive isolation. Polyploidy can also cause radiations via epigenetically induced heterochrony and plasticity. Most cycads have only a few large chromosomes because of a lack of whole genome duplication or, except possibly in the genus Zamia, chromosomal fission. Large chromosomes and extremely small effective population sizes result in substantial linkage disequilibrium, genetic hitchhiking and genetic drift in cycads. By contrast, other seed plants have higher incidences of polyploidy and may therefore have been more prone to radiations. © 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 165 , 156–167.     

Karyotypic Changes through Dysploidy Persist Longer over Evolutionary Time than Polyploid Changes

Chromosome evolution has been demonstrated to have profound effects on diversification rates and speciation in angiosperms. While polyploidy has predated some major radiations in plants, it has also been related to decreased diversification rates. There has been comparatively little attention to the evolutionary role of gains and losses of single chromosomes, which may or not entail changes in the DNA content (then called aneuploidy or dysploidy, respectively). In this study we investigate the role of chromosome number transitions and of possible associated genome size changes in angiosperm evolution. We model the tempo and mode of chromosome number evolution and its possible correlation with patterns of cladogenesis in 15 angiosperm clades. Inferred polyploid transitions are distributed more frequently towards recent times than single chromosome gains and losses. This is likely because the latter events do not entail changes in DNA content and are probably due to fission or fusion events (dysploidy), as revealed by an analysis of the relationship between genome size and chromosome number. Our results support the general pattern that recently originated polyploids fail to persist, and suggest that dysploidy may have comparatively longer-term persistence than polyploidy. Changes in chromosome number associated with dysploidy were typically observed across the phylogenies based on a chi-square analysis, consistent with these changes being neutral with respect to diversification.     

植物多倍体基因组的形成与进化

多倍化是植物进化变异的自然现象,也是促进植物发生进化改变的重要力量。在被子植物中,约 70％的种类在进化史中曾发生过一次或多次多倍化的过程。目前的研究结果表明,自然界绝大多数多倍体是通过未减数配子的融合而形成的,并且很多多倍体种是通过多次独立的多倍化过程而重复发生的。由多倍化所导致的重复基因在多倍体基因组中可能有三种不同的命运,即：保持原有的功能、基因沉默或分化并执行新的功能。多倍化以后,重复基因组的进化动态则主要表现在染色体重排和“染色体二倍化”、不同基因组之间的相互渗透、以及核-质之间的相互作用等方面。     

Induced polyploidization in Brassica campestris L. (Brassicaceae)

Present experimental design has been made up to obtain crop with higher ploidy level via synthetic polyploidization. Since ploidy manipulation is generally associated with the obtainment of some increased enviable traits of the crop and also provides them greater adaptability to unfavorable or harsh circumstances as compared to its diploids counterparts. Thus, herein present research autotetraploids of Brassica campestris L. have been lucratively achieved by the application of colchicine. Two methods of treatment were utilized i.e. seed treatment and seedling treatment. No polyploidy could be obtained through seed treatment while seedling treatment responded well towards polyploidy. However, the status of autotetraploidy has been confirmed by cytomorphological investigations of treated plants as against its diploids counterparts. For the purpose, morphological parameters such as increased stomata size, pollen diameter, flower size, reproductive organs whereas reduction in plant height, leaf length, leaf breadth, stomata frequency, number of flowers/inflorescence etc. were appraised. Further, cytological observations were made that had clearly revealed the doubling of genome in the autotetraploids as compared to diploids. Meanwhile, pollen fertility and size of pollen grains were evaluated as well.