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Genomic and epigenetic insights into the molecular bases of heterosis

Nature Reviews Genetics volume 14, pages 471–482 (2013)Cite this article

Subjects

Key Points

  • Century-old genetic models are limited in their ability to explain the molecular bases of heterosis.

  • Transcriptomic, proteomic, metabolic and epigenomic studies provide new insights into parental genomic interactions, leading to regulatory and network changes and heterosis.

  • Genetic and epigenetic reprogramming of individual genes, regulatory factors and their associated networks in hybrids promotes growth, stress tolerance and fitness.

  • Key regulators can be manipulated using biochemical and transgenic approaches to alter biological networks and heterosis.

  • Although heterosis is most extensively studied in plants, the principles uncovered in plants are likely to apply more broadly across organisms.

Abstract

Heterosis, also known as hybrid vigour, is widespread in plants and animals, but the molecular bases for this phenomenon remain elusive. Recent studies in hybrids and allopolyploids using transcriptomic, proteomic, metabolomic, epigenomic and systems biology approaches have provided new insights. Emerging genomic and epigenetic perspectives suggest that heterosis arises from allelic interactions between parental genomes, leading to altered programming of genes that promote the growth, stress tolerance and fitness of hybrids. For example, epigenetic modifications of key regulatory genes in hybrids and allopolyploids can alter complex regulatory networks of physiology and metabolism, thus modulating biomass and leading to heterosis. The conceptual advances could help to improve plant and animal productivity through the manipulation of heterosis.

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Figure 1: Heterosis and additive and non-additive gene expression.
Figure 2: Growth vigour in plant hybrids.
Figure 3: Molecular changes at epigenetic, genomic, proteomic and metabolic levels lead to heterosis traits.
Figure 4: A regulatory network of the circadian clock in Arabidopsis thaliana
Figure 5: Models for altered clock gene expression.
Figure 6: A model for small RNAs in the allelic expression of genes and transposable elements in hybrids and allopolyploids.

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Acknowledgements

I am grateful to former and current members of the Laboratory of Polyploidy, Heterosis and Epigenetics for their contributions to this work. I apologize for omitting or glossing over some relevant studies owing to the space limitation. Funding for the research is provided by the US National Science Foundation (grants IOS1238048, IOS1025947 and MCB1110857), the US National Institutes of Health (grant GM067015), the Cotton Incorporated (grant 07161) and the National Natural Science Foundation of China (grant No. 31290213).

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  1. Institute for Cellular and Molecular Biology and Center for Computational Biology and Bioinformatics, The University of Texas at Austin, Austin, 78712, Texas, USA

    Z. Jeffrey Chen

  2. National Laboratory of Plant Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing, 210095, China

    Z. Jeffrey Chen

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Glossary

Allopolyploid

An organism or individual that contains two or more sets of genetically distinct chromosomes, usually through hybridization between different species. A disomic allopolyploid (also known as amphidiploid) is a type of allopolyploid in which bivalents form within each chromosome set.

Heterosis

(Also known as hybrid vigour). When hybrids display increased levels of growth, survival or fitness relative to their parents.

Apomixis

A phenomenon that transmits genes and genomes from only one parent (usually the female) to the offspring.

Dominance

A scenario in which the phenotype of alleles displays fully when they are present in the heterozygous or heterokaryotic state.

Overdominance

(Also known as monohybrid heterosis). The phenomenon of heterozygotes having a more extreme phenotype than either homozygote.

Heterozygote advantage

When the heterozygote genotype has a higher relative fitness than either the homozygote dominant or homozygote recessive genotype.

Epistasis

Non-reciprocal interactions between non-allelic genes, which cannot be easily explained by quantitative genetic models.

Pseudo-dominance

A phenomenon of overdominance that is associated with the complementation of two or more linked dominant and recessive alleles in repulsion, in which the dominant and recessive alleles are located on opposite homologues of the two genes, acting as overdominance.

Quantitative trait locus

(QTL). A genetic locus that contributes to variation in quantitative phenotypes. The effects may also vary under certain environmental conditions.

Autopolyploids

Polyploids created by the multiplication of one basic set of chromosomes (usually within the same species).

Parent-of-origin effects

Phenomena whereby the expression of a gene is dependent on the parental origin. This is usually synonymous to imprinting but could be different from imprinting in cases in which the parent-of-origin effect can be caused by cytoplasmic–nuclear gene interactions (known as maternal effects) in plants, whereas imprinting occurs between two alleles in the nucleus with the same maternal parent.

Homoeologous

Chromosomes or genes in the related species that are derived from the same ancestor and coexist in an allopolyploid.

Circadian period

The time for the completion of an oscillation cycle from one peak to the next or from one trough to the next, which is usually 24 hours.

Circadian amplitude

The difference between the level of a peak (or trough) and the mean value of a wave. For symmetrical waves, the amplitude is half the value of the range of oscillation.

Photoperiod

A light–dark cycle in a given day. Long-day plants, such as Arabidopsis thaliana and wheat, respond to lengthening days and they flower in spring. Short-day plants, such as rice and maize, respond to shortening days and flower in late summer or autumn.

Paramutation

An epigenetic phenomenon discovered in maize in which one allele influences the expression of another allele at the same locus when the two alleles are combined in a heterozygote.

Small interfering RNAs

(siRNAs). A class of 20–25 nucleotide-long small RNAs that repress gene expression or induce epigenetic processes. They are normally derived from transposable elements and repetitive DNA.

MicroRNAs

(miRNAs). A class of 21–23 nucleotide-long small RNAs that have functions in transcriptional and post-transcriptional regulation of gene expression, usually through mRNA degradation or translational repression through complementarity with the target transcripts.

Trans-acting siRNAs

(ta-siRNAs). A class of small RNAs that are generated from target mRNAs, in a process triggered by specific microRNAs (miRNAs), thus leading to a series of consecutive 21-nucleotide small interfering RNAs (siRNAs), called 'phasing'. These secondary siRNAs can act in trans to regulate their target transcripts through mRNA degradation.

RNA-directed DNA methylation

(RdDM). An epigenetic process to establish DNA methylation through the biogenesis of siRNAs that guide the methylation of homologous loci. The process is known as de novo DNA methylation and is predominately found in plants and fungi.

Genome shock

The release of genome-wide chromatin constraints of gene expression, including the activation of transposons in response to environmental changes and genomic hybridization. The term was first used by Barbara McClintock in 1984.

Imprinting

Expression of only the maternal or paternal allele of a gene in the offspring; it is an epigenetic phenomenon involving DNA methylation, chromatin modifications and non-coding RNAs.

Genome-wide association studies

(GWASs). Examinations of many common genetic variants (usually SNPs in linkage disequilibrium) of different individuals to test if any variant is associated with a phenotypic trait.

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Chen, Z. Genomic and epigenetic insights into the molecular bases of heterosis. Nat Rev Genet 14, 471–482 (2013). https://doi.org/10.1038/nrg3503

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