Why Polyploidy is Rarer in Animals Than in Plants

Müller, Hj.

doi:10.1086/280047

Cited by 234 publications

(128 citation statements)

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“…(4,6) The relative paucity of polyploidy in animals is attributed to the delicate schemes of sex determination and animal development, which are disrupted by polyploidization. (7,8) Therefore, polyploid animals rarely exist. (9) Moreover, aneuploid and polyploid cells in animals and human are often associated with malignant cell proliferation or carcinogenesis.…”

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confidence: 99%

Mechanisms of genomic rearrangements and gene expression changes in plant polyploids

2006

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SummaryPolyploidy is produced by multiplication of a single genome (autopolyploid) or combination of two or more divergent genomes (allopolyploid). The available data obtained from the study of synthetic (newly created or human-made) plant allopolyploids have documented dynamic and stochastic changes in genomic organization and gene expression, including sequence elimination, inter-chromosomal exchanges, cytosine methylation, gene repression, novel activation, genetic dominance, subfunctionalization and transposon activation. The underlying mechanisms for these alterations are poorly understood. To promote a better understanding of genomic and gene expression changes in polyploidy, we briefly review origins and forms of polyploidy and summarize what has been learned from genome-wide gene expression analyses in newly synthesized autoand allopolyploids. We show transcriptome divergence between the progenitors and in the newly formed allopolyploids. We propose models for transcriptional regulation, chromatin modification and RNA-mediated pathways in establishing locus-specific expression of orthologous and homoeologous genes during allopolyploid formation and evolution. Polyploidy and its formsPolyploidy occurs throughout the evolutionary history of all eukaryotes, (1,2) predominately in flowering plants (3,4) including many important agricultural crops. (5) Compared to plants, polyploidy occurs rarely in animals, but clearly exists in some invertebrates (e.g. insects) and vertebrates (e.g. fish, amphibians and reptiles). (4,6) The relative paucity of polyploidy in animals is attributed to the delicate schemes of sex determination and animal development, which are disrupted by polyploidization. (7,8) Therefore, polyploid animals rarely exist. (9) Moreover, aneuploid and polyploid cells in animals and human are often associated with malignant cell proliferation or carcinogenesis. (10) However, endopolyploidy (somatic polyploid cells within a diploid individual) appears to be a physiological response to developmental changes in plants and some animals, (11,12) indicating plasticity of plant and animal genomes. In the post-sequencing era, polyploidy is proving to be a fascinating and challenging field of plant biology, stimulating many research advances and insightful reviews. (2,13 -24) Here we attempt to update the views using genomic-scale results and provide new mechanistic insights.Historically, Winkler (1916) introduced the term polyploidy, (25) and Winge (1917) called attention to the general importance of polyploidy in the evolution of angiosperms. (26) At that time, research in polyploidy was somewhat limited by the plant and animal materials that were available in nature. In 1937, Blakeslee and Avery induced polyploidy in plants using colchicine, a chemical inhibitor of mitotic cell divisions. (27) The technique has been successfully used to induce chromosome doubling in meristemic cells of diploids and interspecific hybrids. Doubling a single 'diploid' genome results in an autotetraploid, while doubling c...

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Mechanisms of genomic rearrangements and gene expression changes in plant polyploids

2006

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“…White (1973) favors the view that the prevalence of obligatory cross-fertilization is the principal barrier to bisexual polyploidy in animals. Bisexual polyploidy is unknown in amniote vertebrates, being precluded perhaps by the existence of well-developed chromosomal mechanisms of sex determination (Muller, 1925;Ohno, 1970;Jackson, 1976), but it has been a factor in the evolution of fishes and amphibians. Among amphibians, 12 bisexual polyploid species of anurans representing five families have been identified (Bogart and Tandy, 1976).…”

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EVOLUTIONARY GENETICS OF DIPLOID—TETRAPLOID SPECIES OF TREEFROGS OF THE GENUS HYLA

Ralin

Selander

1979

Evolution

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“…If this correlation also holds for polyploids as our data support, the strongly female-biased recombination documented here for B. baturae and B. pewzowi suggests maintenance of the initial male heterogamety during polyploidization events. This point obviously deserves further investigation, given that sex chromosomes and sex-determination systems have been seen as major obstacles to polyploidization (Muller, 1925;Orr, 1990).…”

Section: Bac212mentioning

confidence: 99%

“…Similarly, assuming sex-determination systems to be conserved during polyploidization, then sex-determining genes with functional X and Y alleles should localize on the paternal LG 1 in both B. baturae and B. pewzowi. Given that sex-determination systems have been proposed to constitute major barriers to polyploidization in animals (Muller, 1925;Otto and Whitton, 2000), the reorganization of sex chromosomes that may follow polyploidization is an important issue, which deserves further investigation by sequence analyses of paternal subgenomes in polyploid species from the B. viridis radiation. Very strong mtDNA similarity in the D-loop (Stöck et al, 2006 and our still unpublished data) suggests a single maternal origin of alltriploid B. baturae sampled here in two isolated high mountain valleys in the Karakoram.…”

Section: Bac212mentioning

confidence: 99%

“…Polyploidy is much rarer in animals than in plants (Otto and Whitton, 2000), a pattern attributed by Muller (1925) to the disruption of sex determination in gonochoristic animals. Nevertheless, polyploidization has been documented across a wide range of animal taxa, including turbellarians, annelids, mollusks, insects and crustaceans (Gregory and Mable, 2005), teleost fishes (Schultz, 1980;Le Comber and Smith, 2004), reptiles (Gregory and Mable, 2005), and amphibians (Bogart, 1980).…”

Section: Introductionmentioning

confidence: 99%

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Origin and genome evolution of polyploid green toads in Central Asia: evidence from microsatellite markers

Betto‐Colliard¹,

Sermier²,

Litvinchuk³

et al. 2014

Heredity

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Polyploidization, which is expected to trigger major genomic reorganizations, occurs much less commonly in animals than in plants, possibly because of constraints imposed by sex-determination systems. We investigated the origins and consequences of allopolyploidization in Palearctic green toads (Bufo viridis subgroup) from Central Asia, with three ploidy levels and different modes of genome transmission (sexual versus clonal), to (i) establish a topology for the reticulate phylogeny in a species-rich radiation involving several closely related lineages and (ii) explore processes of genomic reorganization that may follow polyploidization. Sibship analyses based on 30 cross-amplifying microsatellite markers substantiated the maternal origins and revealed the paternal origins and relationships of subgenomes in allopolyploids. Analyses of the synteny of linkage groups identified three markers affected by translocation events, which occurred only within the paternally inherited subgenomes of allopolyploid toads and exclusively affected the linkage group that determines sex in several diploid species of the green toad radiation. Recombination rates did not differ between diploid and polyploid toad species, and were overall much reduced in males, independent of linkage group and ploidy levels. Clonally transmitted subgenomes in allotriploid toads provided support for strong genetic drift, presumably resulting from recombination arrest. The Palearctic green toad radiation seems to offer unique opportunities to investigate the consequences of polyploidization and clonal transmission on the dynamics of genomes in vertebrates.

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Why Polyploidy is Rarer in Animals Than in Plants

Cited by 234 publications

References 0 publications

Mechanisms of genomic rearrangements and gene expression changes in plant polyploids

Mechanisms of genomic rearrangements and gene expression changes in plant polyploids

EVOLUTIONARY GENETICS OF DIPLOID—TETRAPLOID SPECIES OF TREEFROGS OF THE GENUS HYLA

Origin and genome evolution of polyploid green toads in Central Asia: evidence from microsatellite markers

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