The advantages and disadvantages of being polyploid

Key Points

  • The occurrence and behaviour of polyploids — organisms that inherit multiple complete sets of chromosomes — has been studied for nearly a century. Recently, the footprints of ancestral polyploidy have been detected in many eukaryotic genomes, indicating that polyploidization and diploidization can be cyclical.

  • Understanding the effect of polyploidization on gene diversification and genome evolution requires an understanding of the mechanisms that lead to the formation and establishment of polyploidy. The possible incentives and constraints on polyploid formation are discussed.

  • There are three obvious advantages of becoming polyploid: heterosis, gene redundancy (a result of gene duplication) and asexual reproduction. Heterosis causes polyploids to be more vigorous than their diploid progenitors, whereas gene redundancy shields polyploids from the deleterious effect of mutations. Asexual reproduction, for which the mechanistic connection to polyploidy is unclear, enables polyploids to reproduce in the absence of sexual mates.

  • There are several disadvantages, documented or conjectured, of polyploidy. They include the potentially disrupting effects of nuclear and cell enlargement, the propensity of polyploid mitosis and meiosis to produce aneuploid cells, and the epigenetic instability that results in transgressive (non-additive) gene regulation.

  • The amount of experimental evidence that addresses these problems varies considerably. In particular, recent data on gene regulation in polyploids provide interesting but still incomplete information on the genetic responses that are involved in polyploidy and on the role of epigenetic remodelling.

  • Transcriptional remodelling in polyploids has two causes. The first is the interaction of diverged parental genomes that are reunited in the allopolyploid; this interaction has both genetic and epigenetic effects. The second, less characterized causal mechanism is genome duplication.

  • Triploidy and aneuploidy are unstable states that often lead to or result from the more stable polyploidy states such as tetraploidy. Both conditions can have potentially disruptive effects on genome regulation, some of which might result from meiotically unpaired DNA.

Abstract

Polyploids — organisms that have multiple sets of chromosomes — are common in certain plant and animal taxa, and can be surprisingly stable. The evidence that has emerged from genome analyses also indicates that many other eukaryotic genomes have a polyploid ancestry, suggesting that both humans and most other eukaryotes have either benefited from or endured polyploidy. Studies of polyploids soon after their formation have revealed genetic and epigenetic interactions between redundant genes. These interactions can be related to the phenotypes and evolutionary fates of polyploids. Here, I consider the advantages and challenges of polyploidy, and its evolutionary potential.

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Figure 1: Evolutionary alternation of diploidy and polyploidy.
Figure 2: Polyploid formation and ensuing meiotic and mitotic irregularities.
Figure 3: Contrasting patterns of inheritance in diploids and polyploids.
Figure 4: Ploidy-dependent paramutation.

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Acknowledgements

I wish to thank three anonymous reviewers for their suggestions. I also gratefully acknowledge funding by the National Science Foundation Plant Genome Program.

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DATABASES

Entrez Gene

sucrose synthase

Grain Genes

pairing homeologous 1

Swiss-Prot

p53

FURTHER INFORMATION

Functional Genomics of Plant Polyploids

General polyploidy portal

Luca Comai's homepage

Glossary

NEOPOLYPLOID

A polyploid that has been produced by artificially inducing chromosome doubling.

DIPLOIDIZATION

Gradual conversion from polyploidy to diploidy through genetic changes that differentiate duplicated loci.

SUBFUNCTIONALIZATION

Retention by duplicated genes of different components of the original common function.

NEOFUNCTIONALIZATION

Acquisition of novel function by a duplicated gene.

EPIGENETIC

A mitotically stable change in gene expression that depends not on a change in DNA sequence, but on covalent modifications of DNA or chromatin proteins such as histones.

HETEROSIS

The increase in performance displayed by hybrids compared with their inbred parents. Because performance can be a subjective trait (for example, age of reproduction), a more precise definition is non-additive inheritance in which a trait in the F1 transgresses both parental values.

DYSGENESIS

Sterility or other deleterious trait of an F1 hybrid that results from incompatibilities between parental genomes.

ALLOPOLYPLOID

A polyploid that is generated through hybridization and thus combines different types of chromosome sets; by contrast, an autopolyploid arises through the multiplication of the same chromosome set.

HOMEOLOGOUS

Duplicated genes or chromosomes that are derived from different parental species and are related by ancestry.

MULTIVALENT

Meiotic association of more than two chromosomes, resulting in synapsis and recombination between partners.

ANEUPLOIDY

The property of having a chromosome number that is not an exact multiple of X.

CENTROSOME

The microtubule-organizing centre that divides to organize the two poles of the mitotic spindle and directs assembly of the cytoskeleton, so controlling cell division, motility and shape.

INBREEDING DEPRESSION

The loss of vigour and fitness that is observed when genome-wide heterozygosity is decreased by inbreeding.

GENOTOXICITY

The action of chemical, physical and biological agents that damage DNA.

ENDOREDUPLICATION

Successive rounds of DNA replication without cytokinesis.

ENDOPOLYPLOIDY

The property of cells in certain developmental stages of an organism of having more chromatid sets or, less frequently, more chromosome sets than the germ line.

APOMICTIC

Species that produce embryos from maternal tissues, bypassing normal meiosis and sexual fusion of egg and sperm.

SEGREGATION DISTORTION

Departure from the expected gametic ratio of alleles that is observed in the progeny of a cross, usually caused by preferential loss of certain chromosomes during gametogenesis (meiotic drive) or by selection on gametes and zygotes.

PLASTICITY

The ability of the same genotype to change and adapt its phenotype in response to different environmental conditions.

EUPLOID

An organism or cell that has a balanced set of chromosomes.

B CHROMOSOMES

Supernumerary chromosomes that differ from the normal complement by being dispensable, often heterochromatic and exhibiting unusual meiotic behaviour.

ACCESSION

A strain of a species, usually classified from the geographical site of isolation. In the Arabidopsis genus it is also known as an ecotype.

HAPLOTYPE

Allelic composition over a contiguous chromosome stretch.

GENOMIC SHOCK

The concomitant and widespread misregulation and activation of suppressed heterochromatic elements, leading to genomic remodelling.

ENDOSPERM

A fertilization-derived, triploid nutritive tissue that is found in the seeds of flowering plants.

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Comai, L. The advantages and disadvantages of being polyploid. Nat Rev Genet 6, 836–846 (2005). https://doi.org/10.1038/nrg1711

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