Comparative analysis reveals that polyploidy does not decelerate diversification in fish

While the proliferation of the species‐rich teleost fish has been ascribed to an ancient genome duplication event at the base of this group, the broader impact of polyploidy on fish evolution and diversification remains poorly understood. Here, we investigate the association between polyploidy and diversification in several fish lineages: the sturgeons (Acipenseridae: Acipenseriformes), the botiid loaches (Botiidae: Cypriniformes), Cyprininae fishes (Cyprinidae: Cypriniformes) and the salmonids (Salmonidae: Salmoniformes). Using likelihood‐based evolutionary methodologies, we co‐estimate speciation and extinction rates associated with polyploid vs. diploid fish lineages. Family‐level analysis of Acipenseridae and Botiidae revealed no significant difference in diversification rates between polyploid and diploid relatives, while analysis of the subfamily Cyprininae revealed higher polyploid diversification. Additionally, order‐level analysis of the polyploid Salmoniformes and its diploid sister clade, the Esociformes, did not support a significantly different net diversification rate between the two groups. Taken together, our results suggest that polyploidy is generally not associated with decreased diversification in fish – a pattern that stands in contrast to that previously observed in plants. While there are notable differences in the time frame examined in the two studies, our results suggest that polyploidy is associated with different diversification patterns in these two major branches of the eukaryote tree of life.     

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.     

Species interactions and plant polyploidy

Polyploidy is a common mode of speciation that can have far‐reaching consequences for plant ecology and evolution. Because polyploidy can induce an array of phenotypic changes, there can be cascading effects on interactions with other species. These interactions, in turn, can have reciprocal effects on polyploid plants, potentially impacting their establishment and persistence. Although there is a wealth of information on the genetic and phenotypic effects of polyploidy, the study of species interactions in polyploid plants remains a comparatively young field. Here we reviewed the available evidence for how polyploidy may impact many types of species interactions that range from mutualism to antagonism. Specifically, we focused on three main questions: (1) Does polyploidy directly cause the formation of novel interactions not experienced by diploids, or does it create an opportunity for natural selection to then form novel interactions? (2) Does polyploidy cause consistent, predictable changes in species interactions vs. the evolution of idiosyncratic differences? (3) Does polyploidy lead to greater evolvability in species interactions? From the scarce evidence available, we found that novel interactions are rare but that polyploidy can induce changes in pollinator, herbivore, and pathogen interactions. Although further tests are needed, it is likely that selection following whole‐genome duplication is important in all types of species interaction and that there are circumstances in which polyploidy can enhance the evolvability of interactions with other species.     

植物多倍体研究的回顾与展望

多倍化是促进植物进化的重要力量。多倍体主要是通过未减数配子融合,体细胞染色体加倍以及多精受精三种方式起源的。其中,不减数配子是多倍体形成的主要机制。三倍体可能在四倍体的进化中起了重要作用。过去认为多倍体只能是进化的死胡同,现在发现很多多倍体类群都是多元起源的而不是单元起源的。当多倍体形成后,基因组中的重复基因大部分保持原有的功能,也有相当比例的基因发生基因沉默。多倍体通常表现出不存在于二倍体祖先的表型,并且超出了其祖先的分布范围,因为在多倍体中发生了很多基因表达的变化。主要从多倍体的起源、影响多倍体发生的因素及多倍体基因组的进化等方面回顾并展望多倍体的研究。     

Polyploidy and the evolution of domesticated plants

Polyploidy and domestication are common features of plant evolution. A number of selective advantages conferred by polyploidy appear relevant to domestication. Surprisingly, the correlation between the two has not previously been examined. Anderson (Plants, man and life. University of California Press, Berkeley, CA, 1969) asserted that we do not yet know exactly what percentage of cultivated plants and weeds are polyploid, but it must be high. Heiser (Seeds to civilization, the story of food, 2d ed., W. H. Freeman, San Francisco, CA, 1981) stated that a large number of the major food crops are polyploids, giving wheat, sugar cane, potatoes, sweet potatoes, and bananas as examples. In this study, the distribution of polyploidy in 244 crop species was compared to the estimates of polyploidy in their respective higher categories. The proportion of polyploidy in crop plants was considered in relation to taxonomic origin, habitat, and reproductive strategies of the crops. The study showed that the crop species were a random selection as far as ploidy level is concerned and that domestication did not appear to have favored polyploid over diploid genomes or vice versa. Vegetative, seed, and tree crops were statistically homogenous in their polyploid composition. The distribution of polyploidy in annual and perennial crops did not differ statistically. The data imply that polyploid genomic constitution neither facilitated nor hindered the ability of wild species for domestication.     

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。     

Small-molecule inducer of cancer cell polyploidy promotes apoptosis or senescence: Implications for therapy

Polyploidy results from deregulated cell division and has been considered an undesirable event leading to increased mutation rate and cancer development. However, polyploidy may also render cancer cells more vulnerable to chemotherapy. Here, we identify a small-molecule inducer of polyploidy, R1530, which interferes with tubulin polymerization and mitotic checkpoint function in cancer cells, leading to abortive mitosis, endoreduplication and polyploidy. In the presence of R1530, polyploid cancer cells underwent apoptosis or became senescent which translated into potent in vitro and in vivo efficacy. Normal proliferating cells were resistant to R1530-induced polyploidy thus supporting the rationale for cancer therapy by induced polyploidy. Mitotic checkpoint kinase BubR1 was found downregulated during R1530-induced exit from mitosis, a likely consequence of PLK4 inhibition. BubR1 knockdown in the presence of nocodazole induced an R1530-like phenotype, suggesting that BubR1 plays a key role in polyploidy induction by R1530 and could be exploited as a target for designing more specific polyploidy inducers.     

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 angiosperm diversification

Polyploidy has long been recognized as a major force in angiosperm evolution. Recent genomic investigations not only indicate that polyploidy is ubiquitous among angiosperms, but also suggest several ancient genome-doubling events. These include ancient whole genome duplication (WGD) events in basal angiosperm lineages, as well as a proposed paleohexaploid event that may have occurred close to the eudicot divergence. However, there is currently no evidence for WGD in Amborella, the putative sister species to other extant angiosperms. The question is no longer "What proportion of angiosperms are polyploid?", but "How many episodes of polyploidy characterize any given lineage?" New algorithms provide promise that ancestral genomes can be reconstructed for deep divergences (e.g., it may be possible to reconstruct the ancestral eudicot or even the ancestral angiosperm genome). Comparisons of diversification rates suggest that genome doubling may have led to a dramatic increase in species richness in several angiosperm lineages, including Poaceae, Solanaceae, Fabaceae, and Brassicaceae. However, additional genomic studies are needed to pinpoint the exact phylogenetic placement of the ancient polyploidy events within these lineages and to determine when novel genes resulting from polyploidy have enabled adaptive radiations.     

The more the better? The role of polyploidy in facilitating plant invasions

Background

Biological invasions are a major ecological and socio-economic problem in many parts of the world. Despite an explosion of research in recent decades, much remains to be understood about why some species become invasive whereas others do not. Recently, polyploidy (whole genome duplication) has been proposed as an important determinant of invasiveness in plants. Genome duplication has played a major role in plant evolution and can drastically alter a plant''s genetic make-up, morphology, physiology and ecology within only one or a few generations. This may allow some polyploids to succeed in strongly fluctuating environments and/or effectively colonize new habitats and, thus, increase their potential to be invasive.

Scope

We synthesize current knowledge on the importance of polyploidy for the invasion (i.e. spread) of introduced plants. We first aim to elucidate general mechanisms that are involved in the success of polyploid plants and translate this to that of plant invaders. Secondly, we provide an overview of ploidal levels in selected invasive alien plants and explain how ploidy might have contributed to their success.

Conclusions

Polyploidy can be an important factor in species invasion success through a combination of (1) ‘pre-adaptation’, whereby polyploid lineages are predisposed to conditions in the new range and, therefore, have higher survival rates and fitness in the earliest establishment phase; and (2) the possibility for subsequent adaptation due to a larger genetic diversity that may assist the ‘evolution of invasiveness’. Alternatively, polyploidization may play an important role by (3) restoring sexual reproduction following hybridization or, conversely, (4) asexual reproduction in the absence of suitable mates. We, therefore, encourage invasion biologists to incorporate assessments of ploidy in their studies of invasive alien species.     

The ups and downs of genome size evolution in polyploid species of Nicotiana (Solanaceae)

BACKGROUND: In studies looking at individual polyploid species, the most common patterns of genomic change are that either genome size in the polyploid is additive (i.e. the sum of parental genome donors) or there is evidence of genome downsizing. Reports showing an increase in genome size are rare. In a large-scale analysis of 3008 species, genome downsizing was shown to be a widespread biological response to polyploidy. Polyploidy in the genus Nicotiana (Solanaceae) is common with approx. 40 % of the approx. 75 species being allotetraploid. Recent advances in understanding phylogenetic relationships of Nicotiana species and dating polyploid formation enable a temporal dimension to be added to the analysis of genome size evolution in these polyploids. METHODS: Genome sizes were measured in 18 species of Nicotiana (nine diploids and nine polyploids) ranging in age from <200,000 years to approx. 4.5 Myr old, to determine the direction and extent of genome size change following polyploidy. These data were combined with data from genomic in situ hybridization and increasing amounts of information on sequence composition in Nicotiana to provide insights into the molecular basis of genome size changes. KEY RESULTS AND CONCLUSIONS: By comparing the expected genome size of the polyploid (based on summing the genome size of species identified as either a parent or most closely related to the diploid progenitors) with the observed genome size, four polyploids showed genome downsizing and five showed increases. There was no discernable pattern in the direction of genome size change with age of polyploids, although with increasing age the amount of genome size change increased. In older polyploids (approx. 4.5 million years old) the increase in genome size was associated with loss of detectable genomic in situ hybridization signal, whereas some hybridization signal was still detected in species exhibiting genome downsizing. The possible significance of these results is discussed.     

From polyploidy to aneuploidy, genome instability and cancer

Polyploidy is a frequent phenomenon in the eukaryotic world, but the biological properties of polyploid cells are not well understood. During evolution, polyploidy is thought to be an important mechanism that contributes to speciation. Polyploid, usually non-dividing, cells are formed during development in otherwise diploid organisms. A growing amount of evidence indicates that polyploid cells also arise during a variety of pathological conditions. Genetic instability in these cells might provide a route to aneuploidy and thereby contribute to the development of cancer.     

Polyploidy: an evolutionary and ecological force in stressful times

Polyploidy has been hypothesized to be both an evolutionary dead-end and a source for evolutionary innovation and species diversification. Although polyploid organisms, especially plants, abound, the apparent nonrandom long-term establishment of genome duplications suggests a link with environmental conditions. Whole-genome duplications seem to correlate with periods of extinction or global change, while polyploids often thrive in harsh or disturbed environments. Evidence is also accumulating that biotic interactions, for instance, with pathogens or mutualists, affect polyploids differently than nonpolyploids. Here, we review recent findings and insights on the effect of both abiotic and biotic stress on polyploids versus nonpolyploids and propose that stress response in general is an important and even determining factor in the establishment and success of polyploidy.     

Polyploidy in fungi: evolution after whole-genome duplication

Polyploidy is a major evolutionary process in eukaryotes-particularly in plants and, to a less extent, in animals, wherein several past and recent whole-genome duplication events have been described. Surprisingly, the incidence of polyploidy in other eukaryote kingdoms, particularly within fungi, remained largely disregarded by the scientific community working on the evolutionary consequences of polyploidy. Recent studies have significantly increased our knowledge of the occurrence and evolutionary significance of fungal polyploidy. The ecological, structural and functional consequences of polyploidy in fungi are reviewed here and compared with the knowledge acquired with conventional plant and animal models. In particular, the genus Saccharomyces emerges as a relevant model for polyploid studies, in addition to plant and animal models.     

Chromosome studies in southern species of Mimosa (Fabaceae,Mimosoideae) and their taxonomic and evolutionary inferences

In this work, chromosome numbers and karyotype parameters of 36 taxa of the genus Mimosa were studied, especially from the southern South America center of diversification. Results support that x = 13 is the basic chromosome number in the genus. Polyploidy is very frequent, ca. 56 % of the total of the studied species here are polyploid, confirming that polyploids are more frequent at higher latitudes. The most common ploidy levels found are 2x and 4x, but some species studied exhibit 6x and 8x. In different groups, several ploidy levels were found. Parameters of chromosome size show statistically significant differences between close species, and asymmetry index A ₂ exhibited low variation between them. It is possible to infer variations of chromosome size between diploids and tetraploids and between basal and derived taxa. The present studies confirm or reveal polyploidy in several groups of South America which are highly diversified in the southernmost area of distribution of the genus, such as sect. Batocaulon ser. Stipellares and sect. Calothamnos. Our data are discussed in a taxonomic context, making inferences about the origin of some polyploid taxa. Polyploidy could be an important phenomenon that increases the morphologic diversity and specific richness in southern South America. On basis of our data, it is possible to hypothesize hybridization between same-ploidy level or different ploidy level taxa. As already shown in the literature, our results confirm the importance of the polyploidy in the speciation of the genus.     

A role for polyploidy in the tumorigenicity of Pim-1-expressing human prostate and mammary epithelial cells

Background

Polyploidy is a prominent feature of many human cancers, and it has long been hypothesized that polyploidy may contribute to tumorigenesis by promoting genomic instability. In this study, we investigated whether polyploidy per se induced by a relevant oncogene can promote genomic instability and tumorigenicity in human epithelial cells.

Principal Findings

When the oncogenic serine-threonine kinase Pim-1 is overexpressed in immortalized, non-tumorigenic human prostate and mammary epithelial cells, these cells gradually converted to polyploidy and became tumorigenic. To assess the contribution of polyploidy to tumorigenicity, we obtained sorted, matched populations of diploid and polyploid cells expressing equivalent levels of the Pim-1 protein. Spectral karyotyping revealed evidence of emerging numerical and structural chromosomal abnormalities in polyploid cells, supporting the proposition that polyploidy promotes chromosomal instability. Polyploid cells displayed an intact p53/p21 pathway, indicating that the viability of polyploid cells in this system is not dependent on the inactivation of the p53 signaling pathway. Remarkably, only the sorted polyploid cells were tumorigenic in vitro and in vivo.

Conclusions

Our results support the notion that polyploidy can promote chromosomal instability and the initiation of tumorigenesis in human epithelial cells.     

Novel patterns of gene expression in polyploid plants

Genome doubling, or polyploidy, is a major factor accounting for duplicate genes found in most eukaryotic genomes. Polyploidy has considerable effects on duplicate gene expression, including silencing and up- or downregulation of one of the duplicated genes. These changes can arise with the onset of polyploidization or within several generations after polyploid formation and they can have epigenetic causal factors. Many expression alterations are organ-specific. Specific genes can be independently and repeatedly silenced during polyploidization, whereas patterns for other genes appear to be more stochastic. Three recent reports have provided intriguing new insights into the patterns, timing and mechanisms of gene expression changes that accompany polyploidy in plants.     

Perspectives on polyploidy in plants – ancient and neo

It is timely to re-examine the phenomenon of polyploidy in plants. Indeed, the power of modern molecular technology to provide new insights, and the impetus of genomics, make polyploidy a fit, fashionable and futuristic topic for review. Some historical perspective is essential to understand the meaning of the terms, to recognize what is already known and what is dogma, and to frame incisive questions for future research. Polyploidy is important because life on earth is predominantly a polyploid phenomenon. Moreover, civilization is mainly powered by polyploid food – notably cereal endosperm. Ongoing uncertainty about the origin of triploid endosperm epitomizes our ignorance about somatic polyploidy. New molecular information makes it timely to reconsider how to identity polyploids and what is a polyploid state. A functional definition in terms of a minimal genome may be helpful. Genes are known that can raise or lower ploidy level. Molecular studies can test if, contrary to dogma, the relationship between diploids and polyploids is a dynamic two-way system. We still need to understand the mechanisms and roles of key genes controlling ploidy level and disomic inheritance. New evidence for genome duplications should be compared with old ideas about cryptopolyploidy, and new views of meiosis should not ignore premeiotic genome separation. In practice, new knowledge about polyploidy will be most useful only when it reliably predicts which crops can be usefully improved as stable autopolyploids and which genomes combined to create successful new allopolyloids.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 411–423.     

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.