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The gap in research on polyploidization between plants and vertebrates: model systems and strategic challenges
Sci. Bull. DOI 10.1007/s11434-015-0879-8
www.scibull.com www.springer.com/scp
Review
Life & Medical Sciences
The gap in research on polyploidization between plants and vertebrates: model systems and strategic challenges Jing Chai • Yuebo Su • Feng Huang • Shaojun Liu • Min Tao • Robert W. Murphy Jing Luo
•
Received: 23 July 2015 / Accepted: 10 August 2015 Ó Science China Press and Springer-Verlag Berlin Heidelberg 2015
Abstract Polyploidization via whole-genome duplications (WGD) is a common phenomenon in organisms. However, investigations into this phenomenon differ greatly between plants and animals. Recent research on polyploid plants illustrates the immediate changes that follow WGDs and the mechanisms behind in both genetic and epigenetic consequences. Unfortunately, equivalent questions remain to be explored in animals. Enlightened by botanical research, the study of polyploidization in vertebrates involves the identification of model animals and the establishment of strategies. Here we review and compare
the research on plants and vertebrates while considering intrageneric or intraspecific variation in genome size. Suitable research methods on recently established polyploidy systems could provide important clues for understanding what happens after WGDs in vertebrates. The approach yields insights into survival and the rarity of polyploidization in vertebrates. The species of Carassius and the allopolyploid system of goldfish 9 common carp hybridization appear to be suitable models for unraveling the evolution and adaptation of polyploid vertebrates. Keywords Polyploidization Recurrent WGD events Genome size variation Next-generation sequencing
Jing Chai and Yuebo Su have contributed equally to this work. J. Chai Y. Su F. Huang J. Luo (&) Laboratory of Conservation and Utilization of Bio-resources and Key Laboratory for Animal Genetic Diversity and Evolution of High Education in Yunnan Province, School of Life Sciences, Yunnan University, Kunming 650091, China e-mail: [email protected] J. Chai R. W. Murphy State Key Laboratory of Genetic Resources and Evolution and Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China J. Chai Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming 650000, China S. Liu M. Tao College of Life Sciences, Hunan Normal University, Changsha 410081, China R. W. Murphy Centre for Biodiversity and Conservation Biology, Royal Ontario Museum, 100 Queen’s Park, Toronto, ON M5S 2C6, Canada
Polyploidization via whole-genome duplication (WGD) involves the integration of more than two complete sets of chromosomes in a cell. It occurs in many eukaryotes [1, 2]. Two mechanisms can drive it: autopolyploidization, the duplication of a species’ own genome, and allopolyploidization, the doubling of chromosomes following interspecific hybridization [3, 4]. WGD may give rise to immediate genome doubling. Such duplications provide more genetic materials and yet create genomic redundancy [5]. Polyploidization occurs most commonly in angiosperms, of which at least 70 % species were thought to have experienced one or more WGD events in their history (Fig. 1) [6, 7]. In contrast, polyploidization is relatively rare in animals and it mainly occurs in some species of insects and a few vertebrates (Fig. 1) [8–10]. In this review, we discuss genetic and epigenetic events following polyploidization. We highlight challenges to investigating polyploidization, the differences between polyploidization of plants and animals, the possible explanations of why polyploidization rarely occurs in animals, and offer a
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Silurian Ordovician
Lycophytes
Tetrapods
Lobe-Fin fishes
Ray-Fin fishes
Acanthodians
Devonian
Seed plants
Carboniferous
Lycopsids
Permian
Progymnosperms
Jurassic
Jawless fishes Placoderms Shark and their relatives
Cretaceous
Triassic
Paleozoic
Fish and tetrapods
Tertiary
Pre-Lycopsids Zosterophylls Barinophytes Rhyniophytes Trimerophytes Monilophytes (Ferns)
Mesozoic
Cenozoic
Plants
Euphyllophytes
Cambrian
Gossypium
Arabidopsis
Goldfish (Carassius auratus red var.)
Fig. 1 Diversity of some plants, fishes and tetrapod groups according to the fossil record. The widths of colored columns indicate the relative number of species of plants and animals. The lower figures display representative angiosperms [11] and vertebrates that experienced wholegenome duplications. Adopted and modified from Murphy DC (http://www.devoniantimes.org) and Hegarty and Hiscock [11]
suitable model for investigating the phenomenon in the genomic era.
1 Intensive genetic and epigenetic changes in polyploidy lineages Following polyploidization or WGD, redundant genetic material causes genomic shock, which can result in genomic instabilities, chromosomal imbalances and regulatory incompatibilities that ultimately result in reproductive failure. These effects include random gene loss, accelerated mutations, chromosomal rearrangements and failed paring of homologous chromosomes [12, 13]. The increased gene content might also drive changes in cell architecture and regulatory networks. These phenomena can lead to genomic chaos displayed as dosage imbalances and abnormal expressions [3]. WGD might also give rise to irregularities of mitotic and meiotic activities, which are crucial for the stability of cells and the survival of zygotes [3, 14]. 1.1 Initial changes and potential drivers in newly formed polyploids Relative to polyploids that formed a few million years ago, those originating in the last few hundreds of years might be still ongoing genomic changes [15]. Newly formed
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polyploids undoubtedly experience fast and large-scale changes after genome doubling [12, 16, 17]. These changes involve genetic, epigenetic and some other levels that are important for survival. The tacking of these initial changes might yield insights into the potential mechanisms and drivers of survival. This requires choosing taxa that experienced a recent WGD. 1.2 Recently formed polyploid plants illustrate great genetic and epigenetic changes Since Hugo de Vires’ initial discovery of phenotypic variants breeding true or segregated in Oenothera lamarckiana, which later proved to be tetraploids [18], variation in chromosome numbers and its consequences has drawn much attention. Many polyploid plants have been discovered, and today they are bred for research and their economic value. Many naturally occurring or domesticated lineages have experienced recurrent WGD, and some involve differing levels of ploidy (Table 1). For example, wild chrysanthemum exists as diploids, allotetraploids, hexaploids and decaploids [19, 20]. Polyploid wild primrose consists of tetraploids (Primula malacoides, 2n = 4x = 36), hexaploids (P. incana, 2n = 6x = 54; P. scotica, 2n = 6x = 54), and even octoploids and decaploids [20, 21]. In some domesticated lineages, polyploid systems were established to increase production and
Sci. Bull. Table 1 Genus or species with multiple levels of ploidy in angiosperms and vertebrates Genus or species
Polyploidy level
Ploidy
References
Acipenser
Intrageneric level
A. ruthenus (2n = 4x = 120), A. gueldenstaedtii (2n = 8x = 240) and A. baerii (2n = 12x = 360)
[27, 28]
Carassius auratus
Intraspecific level
Tereaploid (2n = 4x = 100), hexaploid (2n = 6x = 150) and octoploid (2n = 8x = 200)
[29]
Carassius auratus gibelio Bufo
Intraspecific level Intrageneric level
Hexaploid (2n = 6x = 156 or 2n = 6x = 162) B. baturae (2n = 3x = 33), B. variabilis (2n = 2x = 22 or 2n = 3x = 33) and B. oblongus (2n = 4x = 44)
[30] [31]
Bufo viridis complex
Intraspecific level
Diploids, triploids and tetraploids
[32]
Gray treefrog complex
Intrageneric level
Hyla versicolor in Canada (2n = 4x = 48), H. chrysoscelis (2n = 2x = 24), H. arborea in France (2n = 2x = 24)
[33, 34]
Phyllomedusa burmeisteri treefrog group
Intrageneric level
Four diploids (P. bahiana, P. burmeisteri, P. distincta and P. iheringii) and one tetraploids (P. tetraploidea)
[35]
Aspidoscelis
Intrageneric level
Diploids (A. inornatus) and triploids (A. exsanguis)
[36, 37]
Darevskia
Intrageneric level
Diploids (D. Armeniaca and D. unisexualis) and triploids (D. middendorffiana)
[37]
Neobatrachus
Intrageneric level
Diploids (N. albipes) and tetraploids (N. aquilonius and N. centralis)
[37]
Silurana
Intrageneric level
Diploids (S. tropicalis) and tetraploids (S. epitropicalis)
[37]
Ambystoma
Intrageneric level
Diploids (A. mexicanum) and triploids (A. platineum, A. tremblayi, and A. texnumxlateraleare, 2n = 3x = 42)
[38, 39]
Dendranthema
Intrageneric level
D.dichrum (2n = 18 or 2n = 4x = 36), D. argrophyllum (2n = 6x = 54), D. naktongense (2n = 2x = 18 or 2n = 8x = 72) and D. mongolicum (2n = 18)
[40]
Allium tuberosum
Intraspecific level
Diploids (2n = 2x = 16), triploids (2n = 3x = 24) and tetraploids (2n = 4x = 32)
[41]
Manihot
Intrageneric level
Diploids (2n = 2x = 36), triploids (2n = 3x = 54) and tetraploids (2n = 4x = 72)
[42]
Tripsacum dactyloides
Intraspecific level
Diploids (2n = 2x = 36) and triploids (2n = 3x = 54)
[43]
tolerance of diseases. For example, common wheat (Triticum aestivum, 2n = 6x = 42) originated from hybridizing tetraploid Triticum turgidum (2n = 4x = 28) and diploid Aegilops tauschii (2n = 2x = 14) [22]. This crossing significantly increased grain yield or harvest index [23, 24]. Based on these systems, some nascent alternations and even hypotheses have been detected and put forward, among which the so-called genomic shock effects, such as gene loss, recombinations, mutations and large scale chromosome rearrangements, were clarified recently [12, 13, 17, 25, 26]. In the flowering plant Biscutella laevigata complex, genetic surveys within a large continuous population of tetraploids and diploids provided insights into different multilocus genotypes associated with particular ecological conditions [25]. Autotetraploid B. laevigata possess wide ecological tolerance due to having large phenotypic variation [26]. Representative studies on wellestablished polyploidy plants involve commercial crops. Cotton, genus Gossypium (Fig. 1), consists of 47 diploid species (2n = 2x = 26) and 5 tetraploid species (2n = 4x = 56). Based on next-generation sequencing, Flagel et al. [13] traced the signature of one or more episodes of non-reciprocal homoeologous recombination within 7 % of ‘‘A’’ and ‘‘D’’ genomes of allopolyploid cotton. Non-
reciprocal DNA exchanges were also well clarified by Paterson et al. [17] using comparative genomic data along with the evolution of repeated polyploidization and the rise spinnable cotton fibers. Liu et al. [12] detailed changes in the genetic architecture of polyploid genomes of Brassica. Comparisons of B. oleracea with its sister species B. rapa identified a series changes, including asymmetrical gene loss, different gene coretention in specific pathways, asymmetrical amplification of transposable elements and large scale of chromosomal rearrangement. Such genetic changes, which would happen continuously, could be retained only after survival. Changes in genomic architecture result in alterations of epigenetic gene expression. In cotton, changes in chromosome number via polyploidization may play an important role in controlling gene expression and provide new forms of epigenetic gene regulation [44]. Comparisons of gene expression in allohexaploid offspring of parents from different species documented extensive ‘‘transcriptome shock’’-like changes [45, 46]; WGD events in response to hybridization may have precluded widespread changes in expression within the first generation of hybrids. Analyses of cDNA-AFLPs from naturally occurring, established populations of diploid, autotetraploid and autohexaploid
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Helianthus decapetalus revealed that ploidy accounted for 6.6 % of the variation only [47]. Thus, gene expression was not strongly affected by genomic doubling in the long term [48]. Even at the level of DNA methylation, rapid changes in the triploid–allohexaploid system of Brassica—the ‘‘A’’, ‘‘B’’ and ‘‘C’’ genomes—displayed greater alterations of the A genome. The recovery of hemi-CCG methylation after genome doubling indicated an amelioration effect after WGD [49]. Thus, nascent short-term changes in levels of epigenetic and gene expression accompanied WGDs. Arabidopsis (Fig. 1) provides the best example of the integrated consequences of WGD. Diploids, triploids and autotetraploids [50] are phenotypically similar. Based on hybrid polyploid offspring of Arabidopsis [51], polyploidization via hybridization appeared to induce allelic interactions and epigenetic changes of homoeologous loci, which altered regulation networks by cis- and/or transfactors [51–53]. Non-additively expressed genes and loci were involved in various biological pathways, such as morphological and fitness traits, biomass, circadian clock and even flowering time [53–56]. Tolerance within Arabidopsis and the connected genetic variation provided important insights into the relationship between ploidy, evolution, and the genetic and epigenetic responses to dosage sensitivity [51]. Given the high proportion of polyploid plants in nature, the high frequency with which new polyploids are formed, and the existing hypotheses of the molecular mechanisms, plants probably offer the best model system for clarifying the nascent changes in naturally occurring or laboratory generated/synthetic systems. These changes might be involved in the forming and adapting of polyploids [57].
2 Ecological and adaptive effects of polyploidization Polyploidization can result in obvious phenotypic changes as well as alterations of fertility, hybrid vigor, apomixes and flowering time in plants [51]. These phenotypic traits might increase biomass, growth, vigor and occupancy of new ecological niches by developing new functions and phenotypes [3, 58–60]. Unlike its widespread occurrence in plants, polyploidization in animals is restricted to insects, fishes, amphibians and squamates (lizards and snakes). Several hypotheses attempt to explain why polyploidy is much rarer in animals than plants, and these usually involve barriers to sex determination, physiological and developmental constraints [61, 62], and genome shock or dramatic genomic restructuring [62]. For example, animals under XY sex determination require a single X chromosome in males but two in females. Thus, polyploids might not achieve a balance of gene expression in XX females and
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XY males [62]. Rapid genomic changes, including homoeologous recombination, loss of parental DNA fragments and formation of novel genes in first generations, resulted in dramatic genomic reconstruction in allotetraploid fish [63]. However, these explanations might not apply to all vertebrates because many other possible mechanisms exist, which remain to be explored. Further, we do not know which effect(s) explain the rarity of polyploidization in vertebrates [61]. Investigations into the initial changes of WGD within a suitable system may provide needed insights.
3 Challenges and difficulties for studying polyploidization Polyploid organisms, either plants or animals, offer many challenges for research due to redundant genetic components. Initial studies documented polyploidization based on cellular DNA content or karyology [18, 64]. Nowadays, other research goes beyond these borders [65]. Ex situ breeding documents changes in gene expression and regulation. Often polyploidization results in the ‘‘genomic shock’’ syndrome of plants. The doubling of genomes results in difficulties at the molecular level [66] because the larger the genome sets, the greater number of alleles within a species [2, 66]. Some traditional methods require large amounts of cloning to resolve abundant gene copies and alleles. This approach is labor intensive and requires much reagent. ‘‘Omic’’ research on redundant genomes is challenging because it is difficult to obtain well-assembled genomes. Analyses of transcriptomes and methylations are complicated because of identifying homologs and gene sets, and detailing patterns of expression and regulation. These factors explain the dearth of well-assembled polyploidy genomes [67, 68]. Unlike for plants, no model exists for animals. Hypothesis testing relies on indirect evidence, experimentation, which is limited, and mathematic modeling [69]. The genetic background of a well-established polyploid lineage will facilitate objective research on polyploidization.
4 Potential polyploid vertebrates for study model Although polyploidy is much rarer in animals than in plants, hundreds of insects and vertebrates are polyploids. In vertebrates, polyploidy is especially common in amphibians and fishes, and it also occurs in squamate reptiles, and even one mammal, which is a rat [2, 69–71]. Some recent lineages might have experienced recurrent genome doubling, and some of them may still be undergoing WGDs [72, 73].
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Within frogs, different numbers of chromosomes or genome sizes occur within genera and even species (Table 1). Female Bufo baturae (=Bufo pseodoraddei) can reproduce clonally and sexually simultaneously. This ability reflects underlying mechanisms that might shed much light on the processes that regulate vertebrate meiosis. These toads also offer interesting opportunities to compare evolutionary forces in recombining and non-recombining genomes within a species [31]. Gruber and Silva analyzed the chromosomes of Phyllomedusa distincta (2n = 2x = 26), P. tetraploidea (2n = 4x = 52) and their natural hybrid individuals (2n = 3x = 39). Analyses obtained some evidence for diploidization from tetraploids [74]. Species of Xenopus serve as models in developmental biology. Xenopus ruwenzoriensis (2n = 6x = 108) is a hexaploid, while X. vastitus (2n = 4x = 72) is a tetraploid [20]. Tetraploid X. laevis, which originated from diploid X. tropicalis, is an invasive species. It is extremely tolerant of severe environments and more resistant to disease than its diploid relative. It can produce triploids and gynogenetic diploids with chromosome numbers of 54 and 36, respectively. Triploids can be used for understanding important problems, such as the nucleo-cytoplasmic relationships in development or the differentiation of sex [75]. However, most research still centers on discoveries and hypotheses of polyploidy in vertebrates. No clear evidence explains what happened, how early lineages survived WGD and why polyploidization is much rarer in vertebrates than in plants. Teleosts are the largest group of vertebrates (Fig. 1) [76], and many species have experienced additional and recurrent full genome duplication. Among actinopterygians, the acipenserids (4.4–13.8 pg/N) and cyprinids (2.2–3.4 pg/N) reflect broad ranges of genome size and concomitant interspecific diversity in ploidy [77]. Chinook salmon (Oncorhynchus tshawytscha) has increased its number of chromosomes from diploid 68 to triploid 102 [78]. Rainbow trout (Salmo gairdneri) varies from having diploid 59 or 60 chromosomes to triploid with 89 or 90 chromosomes [79]. Johnson et al. [80] bred Chinook salmon using a paternal half-sibling mating design (62 females and 31 males) to test for dosage effects on the distribution and magnitude of phenotypic variation, narrow-sense heritability and maternal effects in fitness-related traits (survival, size at age, relative growth rate and serum lysozyme activity). Triploidization increased phenotypic variation for growth and survival traits, and this resulted in unpredicted performance and fitness outcomes. Similar to angiosperms, some recent WGDs might owe to hybridization. In the Tropidophoxinellus alburnoides complex of fishes, which has diploid (2n = 50) and triploid (2n = 3x = 75) forms, tetraploids may have been formed by the breeding of triploids [81]. The Cyprinini, which has a high frequency of polyploids, appears to have originated
from an allopolyploidization event 12–20 Ma [72]. Within this lineage, the natural Carassius auratus species complex consists of tetraploid, hexaploid and even octaploid individuals owing to repeated allopolyploidization and autopolyploidization [73]. The high frequency of hexaploid C. auratus in highly polluted Lake Dianchi [73] suggests that these fishes might constitute an ideal system for unraveling the relationship between polyploidization and adaptation to extreme environments. One of the best model vertebrates for studying polyploidization is the hybrid system of goldfish (C. auratus red var., Fig. 1) as the maternal parent (100 chromosomes) 9 common carp (Cyprinus carpio) as the paternal parent (also 100 chromosomes). The first two generations of hybrids consist of tetraploids (F1, F2, 2n = 4x = 100) followed in subsequent generations by octaploid offspring (F3–F23, 2n = 8x = 200). Post-hybridization WGD has been established for 30 years only [82, 83]. Transcriptomic analyses revealed that the initial changes were mainly deleterious, although some offspring survived their genomic abnormalities (Liu et al. unpublished data). This system might be suitable for exploring the effects of hybridization and polyploidization. Natural and ex situ breeding systems indicate that the C. auratus species complex are genomically plastic; they can double their genome and hybridize with other species. Thus, the newly formed polyploids should lend themselves to the study of dosage compensation in autopolyploidy and allopolyploidy. Table 1 lists taxa with intrageneric and intraspecific variation in levels of ploidy. These systems may have experienced recurrent and recent WGDs. WGDs within natural and synthetic young lineages indicate that polyploidization still occurs in vertebrates. Such fishes constitute ideal systems for unveiling the consequences of intergenomic interactions in hybridized and doubled vertebrate genomes. Botanical investigations yield many intriguing hypotheses that may explain some of the drivers of the system. In contrast, most studies of polyploidy vertebrates still focus on the discovery of the phenomenon. Unlike for plants, little is known about the mechanisms of survival and adaptation in animals largely due to challenges of choosing and breeding species suitable for effective research. Lineages that experienced recurrent WGD events will likely serve best.
5 Polyploid vertebrate models and investigation strategies A suitable strategy is paramount for studying polyploidization as is a well-assembled and annotated genome to facilitate epigenetic and network analyses. Next-generation sequencing technologies allow studying polyploidization. For example, it is possible to obtain a
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doubled-haploid genome from one individual within autopolyploid or allopolyploid systems, which deceases the difficulties of ab initio assembly. These approaches are a breakthrough for gathering and analyzing large datasets characterized by high levels of genetic heterozygosity, as occurs in polyploids [67, 84]. Only a few species, especially in animals, can reproduce gynogenetic offspring asexually with a decreased-alleles genome. Before sequencing, it is necessary to identify an organism or lineage that experienced a recent WGD. Anthropogenic breeding, such as occurs in Arabidopsis, cotton and Brassica, and involves various levels of ploidy, may constitute the best models for studying the immediate changes that occur after WGD and the potential drivers of change, because their polyploid genomes are smaller than those of most of vertebrates [16, 51, 85, 86]. Natural systems in vertebrates, such as cyprinid fishes and Xenopus, may yield insights into the nascent changes following WGD at genetic and epigenetic levels [73, 75, 87–89]. Polyploidization and its subsequent effects, such as repetitive regions, greater number of paralogs, elevated heterozygosity in allopolyploidization, might result in highly fragmented assemblies [90]. Recent strategies for sequencing and assembly can handle such complexities (Fig. 2). On the one hand, longer read lengths facilitate polyploid genome sequencing. Single-molecule, real-time sequencing technology (SMRT) of Pacific Bioscience improves the read length, which can markedly improve genome assembly in cases of high GC content via gap filling and repeat resolution [91–93]. However, this technology still requires next-generation sequencing data and associated algorithms for correcting errors and improving operational efficiency; these constraints may explain why it
is widely used in bacterial research only [94]. The strategy of using sub-genome sequencing via long-range mate pairs and long-read data, with the assistance of a bacteria artificial chromosome library, and even isolated chromosome arm sequencing, can greatly reduce such complexities [68, 90, 95]. On the other hand, a myriad of repeat sequences and multiple gene copies complicate assembly of enlarged genomes. However, recent improved algorithms may help to solve the above problem to some extent [95–99]. Similarities of changes and drivers of polyploidization between plants and animals await to be explored. The hypotheses and drivers in botanical systems [16, 51, 85, 86] can serve to guide strategies for investigating polyploidization in animals. Cyprinid fishes of the Carassius auratus complex are an ideal system for studying polyploidization in vertebrates. We expect that the genome of C. auratus will greatly facilitate explorations into genetic, epigenetic, expression and regulation network changes in both natural and synthetic polyploids. Eventually, effective research strategies could yield important clues into the crucial changes in newly formed polyploid vertebrates. We expect that the initial changes and the differences between plants and vertebrates might lead to an understanding of the consequences of WGD, and how polyploid vertebrates adapt in natural or extreme environments (Fig. 2). Acknowledgments This work was supported by the National Natural Science Foundation of China (91331105, 31360514), Laboratory of Conservation and Utilization of Bio-resources and Key Laboratory for Animal Genetic Diversity and Evolution of High Education in Yunnan Province, and State Key Laboratory of Genetic Resources and Evolution and Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences. Conflict of interest of interest.
Ex situ polyploid
Natural polyploid
Model systems e. g.: Arabidopsis, cotton, Brassica in angiosperm; Carassius auratus complex in vertebrate
Genetic changes
Expression, regulation networks
Epigenetic changes
Survival and adaptation in Natural/servere environment Fig. 2 Botanical strategies for studying polyploidy vertebrates
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The authors declare that they have no conflict
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Review
Life & Medical Sciences
The gap in research on polyploidization between plants and vertebrates: model systems and strategic challenges Jing Chai • Yuebo Su • Feng Huang • Shaojun Liu • Min Tao • Robert W. Murphy Jing Luo
•
Received: 23 July 2015 / Accepted: 10 August 2015 Ó Science China Press and Springer-Verlag Berlin Heidelberg 2015
Abstract Polyploidization via whole-genome duplications (WGD) is a common phenomenon in organisms. However, investigations into this phenomenon differ greatly between plants and animals. Recent research on polyploid plants illustrates the immediate changes that follow WGDs and the mechanisms behind in both genetic and epigenetic consequences. Unfortunately, equivalent questions remain to be explored in animals. Enlightened by botanical research, the study of polyploidization in vertebrates involves the identification of model animals and the establishment of strategies. Here we review and compare
the research on plants and vertebrates while considering intrageneric or intraspecific variation in genome size. Suitable research methods on recently established polyploidy systems could provide important clues for understanding what happens after WGDs in vertebrates. The approach yields insights into survival and the rarity of polyploidization in vertebrates. The species of Carassius and the allopolyploid system of goldfish 9 common carp hybridization appear to be suitable models for unraveling the evolution and adaptation of polyploid vertebrates. Keywords Polyploidization Recurrent WGD events Genome size variation Next-generation sequencing
Jing Chai and Yuebo Su have contributed equally to this work. J. Chai Y. Su F. Huang J. Luo (&) Laboratory of Conservation and Utilization of Bio-resources and Key Laboratory for Animal Genetic Diversity and Evolution of High Education in Yunnan Province, School of Life Sciences, Yunnan University, Kunming 650091, China e-mail: [email protected] J. Chai R. W. Murphy State Key Laboratory of Genetic Resources and Evolution and Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China J. Chai Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming 650000, China S. Liu M. Tao College of Life Sciences, Hunan Normal University, Changsha 410081, China R. W. Murphy Centre for Biodiversity and Conservation Biology, Royal Ontario Museum, 100 Queen’s Park, Toronto, ON M5S 2C6, Canada
Polyploidization via whole-genome duplication (WGD) involves the integration of more than two complete sets of chromosomes in a cell. It occurs in many eukaryotes [1, 2]. Two mechanisms can drive it: autopolyploidization, the duplication of a species’ own genome, and allopolyploidization, the doubling of chromosomes following interspecific hybridization [3, 4]. WGD may give rise to immediate genome doubling. Such duplications provide more genetic materials and yet create genomic redundancy [5]. Polyploidization occurs most commonly in angiosperms, of which at least 70 % species were thought to have experienced one or more WGD events in their history (Fig. 1) [6, 7]. In contrast, polyploidization is relatively rare in animals and it mainly occurs in some species of insects and a few vertebrates (Fig. 1) [8–10]. In this review, we discuss genetic and epigenetic events following polyploidization. We highlight challenges to investigating polyploidization, the differences between polyploidization of plants and animals, the possible explanations of why polyploidization rarely occurs in animals, and offer a
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Silurian Ordovician
Lycophytes
Tetrapods
Lobe-Fin fishes
Ray-Fin fishes
Acanthodians
Devonian
Seed plants
Carboniferous
Lycopsids
Permian
Progymnosperms
Jurassic
Jawless fishes Placoderms Shark and their relatives
Cretaceous
Triassic
Paleozoic
Fish and tetrapods
Tertiary
Pre-Lycopsids Zosterophylls Barinophytes Rhyniophytes Trimerophytes Monilophytes (Ferns)
Mesozoic
Cenozoic
Plants
Euphyllophytes
Cambrian
Gossypium
Arabidopsis
Goldfish (Carassius auratus red var.)
Fig. 1 Diversity of some plants, fishes and tetrapod groups according to the fossil record. The widths of colored columns indicate the relative number of species of plants and animals. The lower figures display representative angiosperms [11] and vertebrates that experienced wholegenome duplications. Adopted and modified from Murphy DC (http://www.devoniantimes.org) and Hegarty and Hiscock [11]
suitable model for investigating the phenomenon in the genomic era.
1 Intensive genetic and epigenetic changes in polyploidy lineages Following polyploidization or WGD, redundant genetic material causes genomic shock, which can result in genomic instabilities, chromosomal imbalances and regulatory incompatibilities that ultimately result in reproductive failure. These effects include random gene loss, accelerated mutations, chromosomal rearrangements and failed paring of homologous chromosomes [12, 13]. The increased gene content might also drive changes in cell architecture and regulatory networks. These phenomena can lead to genomic chaos displayed as dosage imbalances and abnormal expressions [3]. WGD might also give rise to irregularities of mitotic and meiotic activities, which are crucial for the stability of cells and the survival of zygotes [3, 14]. 1.1 Initial changes and potential drivers in newly formed polyploids Relative to polyploids that formed a few million years ago, those originating in the last few hundreds of years might be still ongoing genomic changes [15]. Newly formed
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polyploids undoubtedly experience fast and large-scale changes after genome doubling [12, 16, 17]. These changes involve genetic, epigenetic and some other levels that are important for survival. The tacking of these initial changes might yield insights into the potential mechanisms and drivers of survival. This requires choosing taxa that experienced a recent WGD. 1.2 Recently formed polyploid plants illustrate great genetic and epigenetic changes Since Hugo de Vires’ initial discovery of phenotypic variants breeding true or segregated in Oenothera lamarckiana, which later proved to be tetraploids [18], variation in chromosome numbers and its consequences has drawn much attention. Many polyploid plants have been discovered, and today they are bred for research and their economic value. Many naturally occurring or domesticated lineages have experienced recurrent WGD, and some involve differing levels of ploidy (Table 1). For example, wild chrysanthemum exists as diploids, allotetraploids, hexaploids and decaploids [19, 20]. Polyploid wild primrose consists of tetraploids (Primula malacoides, 2n = 4x = 36), hexaploids (P. incana, 2n = 6x = 54; P. scotica, 2n = 6x = 54), and even octoploids and decaploids [20, 21]. In some domesticated lineages, polyploid systems were established to increase production and
Sci. Bull. Table 1 Genus or species with multiple levels of ploidy in angiosperms and vertebrates Genus or species
Polyploidy level
Ploidy
References
Acipenser
Intrageneric level
A. ruthenus (2n = 4x = 120), A. gueldenstaedtii (2n = 8x = 240) and A. baerii (2n = 12x = 360)
[27, 28]
Carassius auratus
Intraspecific level
Tereaploid (2n = 4x = 100), hexaploid (2n = 6x = 150) and octoploid (2n = 8x = 200)
[29]
Carassius auratus gibelio Bufo
Intraspecific level Intrageneric level
Hexaploid (2n = 6x = 156 or 2n = 6x = 162) B. baturae (2n = 3x = 33), B. variabilis (2n = 2x = 22 or 2n = 3x = 33) and B. oblongus (2n = 4x = 44)
[30] [31]
Bufo viridis complex
Intraspecific level
Diploids, triploids and tetraploids
[32]
Gray treefrog complex
Intrageneric level
Hyla versicolor in Canada (2n = 4x = 48), H. chrysoscelis (2n = 2x = 24), H. arborea in France (2n = 2x = 24)
[33, 34]
Phyllomedusa burmeisteri treefrog group
Intrageneric level
Four diploids (P. bahiana, P. burmeisteri, P. distincta and P. iheringii) and one tetraploids (P. tetraploidea)
[35]
Aspidoscelis
Intrageneric level
Diploids (A. inornatus) and triploids (A. exsanguis)
[36, 37]
Darevskia
Intrageneric level
Diploids (D. Armeniaca and D. unisexualis) and triploids (D. middendorffiana)
[37]
Neobatrachus
Intrageneric level
Diploids (N. albipes) and tetraploids (N. aquilonius and N. centralis)
[37]
Silurana
Intrageneric level
Diploids (S. tropicalis) and tetraploids (S. epitropicalis)
[37]
Ambystoma
Intrageneric level
Diploids (A. mexicanum) and triploids (A. platineum, A. tremblayi, and A. texnumxlateraleare, 2n = 3x = 42)
[38, 39]
Dendranthema
Intrageneric level
D.dichrum (2n = 18 or 2n = 4x = 36), D. argrophyllum (2n = 6x = 54), D. naktongense (2n = 2x = 18 or 2n = 8x = 72) and D. mongolicum (2n = 18)
[40]
Allium tuberosum
Intraspecific level
Diploids (2n = 2x = 16), triploids (2n = 3x = 24) and tetraploids (2n = 4x = 32)
[41]
Manihot
Intrageneric level
Diploids (2n = 2x = 36), triploids (2n = 3x = 54) and tetraploids (2n = 4x = 72)
[42]
Tripsacum dactyloides
Intraspecific level
Diploids (2n = 2x = 36) and triploids (2n = 3x = 54)
[43]
tolerance of diseases. For example, common wheat (Triticum aestivum, 2n = 6x = 42) originated from hybridizing tetraploid Triticum turgidum (2n = 4x = 28) and diploid Aegilops tauschii (2n = 2x = 14) [22]. This crossing significantly increased grain yield or harvest index [23, 24]. Based on these systems, some nascent alternations and even hypotheses have been detected and put forward, among which the so-called genomic shock effects, such as gene loss, recombinations, mutations and large scale chromosome rearrangements, were clarified recently [12, 13, 17, 25, 26]. In the flowering plant Biscutella laevigata complex, genetic surveys within a large continuous population of tetraploids and diploids provided insights into different multilocus genotypes associated with particular ecological conditions [25]. Autotetraploid B. laevigata possess wide ecological tolerance due to having large phenotypic variation [26]. Representative studies on wellestablished polyploidy plants involve commercial crops. Cotton, genus Gossypium (Fig. 1), consists of 47 diploid species (2n = 2x = 26) and 5 tetraploid species (2n = 4x = 56). Based on next-generation sequencing, Flagel et al. [13] traced the signature of one or more episodes of non-reciprocal homoeologous recombination within 7 % of ‘‘A’’ and ‘‘D’’ genomes of allopolyploid cotton. Non-
reciprocal DNA exchanges were also well clarified by Paterson et al. [17] using comparative genomic data along with the evolution of repeated polyploidization and the rise spinnable cotton fibers. Liu et al. [12] detailed changes in the genetic architecture of polyploid genomes of Brassica. Comparisons of B. oleracea with its sister species B. rapa identified a series changes, including asymmetrical gene loss, different gene coretention in specific pathways, asymmetrical amplification of transposable elements and large scale of chromosomal rearrangement. Such genetic changes, which would happen continuously, could be retained only after survival. Changes in genomic architecture result in alterations of epigenetic gene expression. In cotton, changes in chromosome number via polyploidization may play an important role in controlling gene expression and provide new forms of epigenetic gene regulation [44]. Comparisons of gene expression in allohexaploid offspring of parents from different species documented extensive ‘‘transcriptome shock’’-like changes [45, 46]; WGD events in response to hybridization may have precluded widespread changes in expression within the first generation of hybrids. Analyses of cDNA-AFLPs from naturally occurring, established populations of diploid, autotetraploid and autohexaploid
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Helianthus decapetalus revealed that ploidy accounted for 6.6 % of the variation only [47]. Thus, gene expression was not strongly affected by genomic doubling in the long term [48]. Even at the level of DNA methylation, rapid changes in the triploid–allohexaploid system of Brassica—the ‘‘A’’, ‘‘B’’ and ‘‘C’’ genomes—displayed greater alterations of the A genome. The recovery of hemi-CCG methylation after genome doubling indicated an amelioration effect after WGD [49]. Thus, nascent short-term changes in levels of epigenetic and gene expression accompanied WGDs. Arabidopsis (Fig. 1) provides the best example of the integrated consequences of WGD. Diploids, triploids and autotetraploids [50] are phenotypically similar. Based on hybrid polyploid offspring of Arabidopsis [51], polyploidization via hybridization appeared to induce allelic interactions and epigenetic changes of homoeologous loci, which altered regulation networks by cis- and/or transfactors [51–53]. Non-additively expressed genes and loci were involved in various biological pathways, such as morphological and fitness traits, biomass, circadian clock and even flowering time [53–56]. Tolerance within Arabidopsis and the connected genetic variation provided important insights into the relationship between ploidy, evolution, and the genetic and epigenetic responses to dosage sensitivity [51]. Given the high proportion of polyploid plants in nature, the high frequency with which new polyploids are formed, and the existing hypotheses of the molecular mechanisms, plants probably offer the best model system for clarifying the nascent changes in naturally occurring or laboratory generated/synthetic systems. These changes might be involved in the forming and adapting of polyploids [57].
2 Ecological and adaptive effects of polyploidization Polyploidization can result in obvious phenotypic changes as well as alterations of fertility, hybrid vigor, apomixes and flowering time in plants [51]. These phenotypic traits might increase biomass, growth, vigor and occupancy of new ecological niches by developing new functions and phenotypes [3, 58–60]. Unlike its widespread occurrence in plants, polyploidization in animals is restricted to insects, fishes, amphibians and squamates (lizards and snakes). Several hypotheses attempt to explain why polyploidy is much rarer in animals than plants, and these usually involve barriers to sex determination, physiological and developmental constraints [61, 62], and genome shock or dramatic genomic restructuring [62]. For example, animals under XY sex determination require a single X chromosome in males but two in females. Thus, polyploids might not achieve a balance of gene expression in XX females and
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XY males [62]. Rapid genomic changes, including homoeologous recombination, loss of parental DNA fragments and formation of novel genes in first generations, resulted in dramatic genomic reconstruction in allotetraploid fish [63]. However, these explanations might not apply to all vertebrates because many other possible mechanisms exist, which remain to be explored. Further, we do not know which effect(s) explain the rarity of polyploidization in vertebrates [61]. Investigations into the initial changes of WGD within a suitable system may provide needed insights.
3 Challenges and difficulties for studying polyploidization Polyploid organisms, either plants or animals, offer many challenges for research due to redundant genetic components. Initial studies documented polyploidization based on cellular DNA content or karyology [18, 64]. Nowadays, other research goes beyond these borders [65]. Ex situ breeding documents changes in gene expression and regulation. Often polyploidization results in the ‘‘genomic shock’’ syndrome of plants. The doubling of genomes results in difficulties at the molecular level [66] because the larger the genome sets, the greater number of alleles within a species [2, 66]. Some traditional methods require large amounts of cloning to resolve abundant gene copies and alleles. This approach is labor intensive and requires much reagent. ‘‘Omic’’ research on redundant genomes is challenging because it is difficult to obtain well-assembled genomes. Analyses of transcriptomes and methylations are complicated because of identifying homologs and gene sets, and detailing patterns of expression and regulation. These factors explain the dearth of well-assembled polyploidy genomes [67, 68]. Unlike for plants, no model exists for animals. Hypothesis testing relies on indirect evidence, experimentation, which is limited, and mathematic modeling [69]. The genetic background of a well-established polyploid lineage will facilitate objective research on polyploidization.
4 Potential polyploid vertebrates for study model Although polyploidy is much rarer in animals than in plants, hundreds of insects and vertebrates are polyploids. In vertebrates, polyploidy is especially common in amphibians and fishes, and it also occurs in squamate reptiles, and even one mammal, which is a rat [2, 69–71]. Some recent lineages might have experienced recurrent genome doubling, and some of them may still be undergoing WGDs [72, 73].
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Within frogs, different numbers of chromosomes or genome sizes occur within genera and even species (Table 1). Female Bufo baturae (=Bufo pseodoraddei) can reproduce clonally and sexually simultaneously. This ability reflects underlying mechanisms that might shed much light on the processes that regulate vertebrate meiosis. These toads also offer interesting opportunities to compare evolutionary forces in recombining and non-recombining genomes within a species [31]. Gruber and Silva analyzed the chromosomes of Phyllomedusa distincta (2n = 2x = 26), P. tetraploidea (2n = 4x = 52) and their natural hybrid individuals (2n = 3x = 39). Analyses obtained some evidence for diploidization from tetraploids [74]. Species of Xenopus serve as models in developmental biology. Xenopus ruwenzoriensis (2n = 6x = 108) is a hexaploid, while X. vastitus (2n = 4x = 72) is a tetraploid [20]. Tetraploid X. laevis, which originated from diploid X. tropicalis, is an invasive species. It is extremely tolerant of severe environments and more resistant to disease than its diploid relative. It can produce triploids and gynogenetic diploids with chromosome numbers of 54 and 36, respectively. Triploids can be used for understanding important problems, such as the nucleo-cytoplasmic relationships in development or the differentiation of sex [75]. However, most research still centers on discoveries and hypotheses of polyploidy in vertebrates. No clear evidence explains what happened, how early lineages survived WGD and why polyploidization is much rarer in vertebrates than in plants. Teleosts are the largest group of vertebrates (Fig. 1) [76], and many species have experienced additional and recurrent full genome duplication. Among actinopterygians, the acipenserids (4.4–13.8 pg/N) and cyprinids (2.2–3.4 pg/N) reflect broad ranges of genome size and concomitant interspecific diversity in ploidy [77]. Chinook salmon (Oncorhynchus tshawytscha) has increased its number of chromosomes from diploid 68 to triploid 102 [78]. Rainbow trout (Salmo gairdneri) varies from having diploid 59 or 60 chromosomes to triploid with 89 or 90 chromosomes [79]. Johnson et al. [80] bred Chinook salmon using a paternal half-sibling mating design (62 females and 31 males) to test for dosage effects on the distribution and magnitude of phenotypic variation, narrow-sense heritability and maternal effects in fitness-related traits (survival, size at age, relative growth rate and serum lysozyme activity). Triploidization increased phenotypic variation for growth and survival traits, and this resulted in unpredicted performance and fitness outcomes. Similar to angiosperms, some recent WGDs might owe to hybridization. In the Tropidophoxinellus alburnoides complex of fishes, which has diploid (2n = 50) and triploid (2n = 3x = 75) forms, tetraploids may have been formed by the breeding of triploids [81]. The Cyprinini, which has a high frequency of polyploids, appears to have originated
from an allopolyploidization event 12–20 Ma [72]. Within this lineage, the natural Carassius auratus species complex consists of tetraploid, hexaploid and even octaploid individuals owing to repeated allopolyploidization and autopolyploidization [73]. The high frequency of hexaploid C. auratus in highly polluted Lake Dianchi [73] suggests that these fishes might constitute an ideal system for unraveling the relationship between polyploidization and adaptation to extreme environments. One of the best model vertebrates for studying polyploidization is the hybrid system of goldfish (C. auratus red var., Fig. 1) as the maternal parent (100 chromosomes) 9 common carp (Cyprinus carpio) as the paternal parent (also 100 chromosomes). The first two generations of hybrids consist of tetraploids (F1, F2, 2n = 4x = 100) followed in subsequent generations by octaploid offspring (F3–F23, 2n = 8x = 200). Post-hybridization WGD has been established for 30 years only [82, 83]. Transcriptomic analyses revealed that the initial changes were mainly deleterious, although some offspring survived their genomic abnormalities (Liu et al. unpublished data). This system might be suitable for exploring the effects of hybridization and polyploidization. Natural and ex situ breeding systems indicate that the C. auratus species complex are genomically plastic; they can double their genome and hybridize with other species. Thus, the newly formed polyploids should lend themselves to the study of dosage compensation in autopolyploidy and allopolyploidy. Table 1 lists taxa with intrageneric and intraspecific variation in levels of ploidy. These systems may have experienced recurrent and recent WGDs. WGDs within natural and synthetic young lineages indicate that polyploidization still occurs in vertebrates. Such fishes constitute ideal systems for unveiling the consequences of intergenomic interactions in hybridized and doubled vertebrate genomes. Botanical investigations yield many intriguing hypotheses that may explain some of the drivers of the system. In contrast, most studies of polyploidy vertebrates still focus on the discovery of the phenomenon. Unlike for plants, little is known about the mechanisms of survival and adaptation in animals largely due to challenges of choosing and breeding species suitable for effective research. Lineages that experienced recurrent WGD events will likely serve best.
5 Polyploid vertebrate models and investigation strategies A suitable strategy is paramount for studying polyploidization as is a well-assembled and annotated genome to facilitate epigenetic and network analyses. Next-generation sequencing technologies allow studying polyploidization. For example, it is possible to obtain a
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doubled-haploid genome from one individual within autopolyploid or allopolyploid systems, which deceases the difficulties of ab initio assembly. These approaches are a breakthrough for gathering and analyzing large datasets characterized by high levels of genetic heterozygosity, as occurs in polyploids [67, 84]. Only a few species, especially in animals, can reproduce gynogenetic offspring asexually with a decreased-alleles genome. Before sequencing, it is necessary to identify an organism or lineage that experienced a recent WGD. Anthropogenic breeding, such as occurs in Arabidopsis, cotton and Brassica, and involves various levels of ploidy, may constitute the best models for studying the immediate changes that occur after WGD and the potential drivers of change, because their polyploid genomes are smaller than those of most of vertebrates [16, 51, 85, 86]. Natural systems in vertebrates, such as cyprinid fishes and Xenopus, may yield insights into the nascent changes following WGD at genetic and epigenetic levels [73, 75, 87–89]. Polyploidization and its subsequent effects, such as repetitive regions, greater number of paralogs, elevated heterozygosity in allopolyploidization, might result in highly fragmented assemblies [90]. Recent strategies for sequencing and assembly can handle such complexities (Fig. 2). On the one hand, longer read lengths facilitate polyploid genome sequencing. Single-molecule, real-time sequencing technology (SMRT) of Pacific Bioscience improves the read length, which can markedly improve genome assembly in cases of high GC content via gap filling and repeat resolution [91–93]. However, this technology still requires next-generation sequencing data and associated algorithms for correcting errors and improving operational efficiency; these constraints may explain why it
is widely used in bacterial research only [94]. The strategy of using sub-genome sequencing via long-range mate pairs and long-read data, with the assistance of a bacteria artificial chromosome library, and even isolated chromosome arm sequencing, can greatly reduce such complexities [68, 90, 95]. On the other hand, a myriad of repeat sequences and multiple gene copies complicate assembly of enlarged genomes. However, recent improved algorithms may help to solve the above problem to some extent [95–99]. Similarities of changes and drivers of polyploidization between plants and animals await to be explored. The hypotheses and drivers in botanical systems [16, 51, 85, 86] can serve to guide strategies for investigating polyploidization in animals. Cyprinid fishes of the Carassius auratus complex are an ideal system for studying polyploidization in vertebrates. We expect that the genome of C. auratus will greatly facilitate explorations into genetic, epigenetic, expression and regulation network changes in both natural and synthetic polyploids. Eventually, effective research strategies could yield important clues into the crucial changes in newly formed polyploid vertebrates. We expect that the initial changes and the differences between plants and vertebrates might lead to an understanding of the consequences of WGD, and how polyploid vertebrates adapt in natural or extreme environments (Fig. 2). Acknowledgments This work was supported by the National Natural Science Foundation of China (91331105, 31360514), Laboratory of Conservation and Utilization of Bio-resources and Key Laboratory for Animal Genetic Diversity and Evolution of High Education in Yunnan Province, and State Key Laboratory of Genetic Resources and Evolution and Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences. Conflict of interest of interest.
Ex situ polyploid
Natural polyploid
Model systems e. g.: Arabidopsis, cotton, Brassica in angiosperm; Carassius auratus complex in vertebrate
Genetic changes
Expression, regulation networks
Epigenetic changes
Survival and adaptation in Natural/servere environment Fig. 2 Botanical strategies for studying polyploidy vertebrates
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The authors declare that they have no conflict
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