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  • Review Article
  • Published:

Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species

Nature Reviews Genetics volume 8, pages 382–393 (2007)Cite this article

Key Points

  • Post-zygotic genetic incompatibility can ensue when hybridization brings together gene products that no longer function properly together in the same genome, thus reducing gene flow among incompatible genotypes.

  • In plants, numerous forms of postzygotic genetic incompatibilities exist, including hybrid sterility, cytoplasmic male sterility and hybrid necrosis or weakness.

  • Hybrid necrosis is a common type of incompatibility found in F1 progeny of many crosses within species and between species, which suggests it could be a model for understanding factors that are important at various stages in the processes of genetic differentiation, and perhaps speciation.

  • Classical and newly described cases of hybrid necrosis generally involve two-locus interactions that are similar to Dobzhansky–Muller interactions. The observation that hybrid necrosis is characterized by a recurring suite of characteristics that are similar to phenotypes associated with oxidative stress, such as yellowing, wilting, cell death and tissue necrosis, in multiple taxa, indicates a common underlying mechanism might be responsible.

  • Hybrid necrosis has been described many times during the past 80 years; one common theme that has emerged is a strong association between hybrid necrosis and selection for disease resistance, which suggest that causal alleles might evolve repeatedly in response to common external pressures, such as host–pathogen conflict.

  • In one case of mild autonecrosis, the causal genes have been identified; one is a disease-resistance (R) gene, implicating this diverse and rapidly evolving class of genes in plant hybrid incompatibility, and suggesting that hybrid necrosis is akin to an autoimmune response.

  • Other types of hybrid failure that are due to F1 weakness in plants might be caused by factors as varied as stresses in the physical environment, hormonal aberrations and genome-integrated viruses.

  • Identifying the evolutionary pressures that contribute to divergence or genetic incompatibility remains an important goal with implications for speciation, and hybrid necrosis, given its prevalence in the plant kingdom, could provide a particularly good model for understanding such processes.

Abstract

Ecological factors, hybrid sterility and differences in ploidy levels are well known for contributing to gene-flow barriers in plants. Another common postzygotic incompatibility, hybrid necrosis, has received comparatively little attention in the evolutionary genetics literature. Hybrid necrosis is associated with a suite of phenotypic characteristics that are similar to those elicited in response to various environmental stresses, including pathogen attack. The genetic architecture is generally simple, and complies with the Bateson–Dobzhansky–Muller model for hybrid incompatibility between species. We survey the extensive literature on this topic and present the hypothesis that hybrid necrosis can result from autoimmunity, perhaps as a pleiotropic effect of evolution of genes that are involved in pathogen response.

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Figure 1: Genetic differentiation in populations.
Figure 2: Wheat hybrid necrosis and the rise of Ne2.

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Acknowledgements

We thank L. Yant and three anonymous reviewers for helpful comments on the manuscript, and B. Dilkes, S. Hedrick and several members of our department for thoughtful discussions. The authors are funded by a Ruth Kirschstein NRSA postdoctoral fellowship to K.B., a Gottfried–Wilhelm–Leibniz Award of the German Research Foundation (DFG) to D.W., and the Max Planck Society. D.W. is a Director of the Max Planck Institute.

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  1. Department of Molecular Biology, Max Planck Institute for Developmental Biology, Spemanstrasse 37–39, Tübingen, 72076, Germany

    Kirsten Bomblies & Detlef Weigel

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Glossary

Prezygotic barriers

Gene-flow barriers or incompatibilities that act to prevent successful fertilization.

Postzygotic barriers

Gene-flow barriers or incompatibilities that act after successful fertilization and formation of a zygote, in either the first or subsequent hybrid generations.

Homeologous

Refers to loci (or entire chromosomes) that are duplicated as a result of a genome duplication event (polyploidy).

Amphidiploid

A species or strain with a doubled genome complement, with the components (subgenomes) originating from different parents.

Subgenome

One of two (or more) full genome complements found in an amphidiploid, recognizable as separate from other genome complements.

Hypersensitive response

A cell-death response that is elicited during pathogen response activation in plants to limit the ability of pathogens to spread through living tissue.

Episome

A DNA element that is capable of replication within a host cell independently of the nuclear genome; for example, replicated viral genome copies that are generated after an integrated copy in the host genome is activated.

Skin strength

The degree to which organs are able to acquire nutrients and other resources from other parts of the plant.

Reinforcement

The strengthening of earlier-acting barriers (for example, prezygotic) as a result of selection against hybrids that are adversely affected at a later stage (for example, postzygotic).

Autonecrosis

The spontaneous appearance of lesions that are similar to those involved in pathogen response, in the absence of pathogen attack.

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Bomblies, K., Weigel, D. Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species. Nat Rev Genet 8, 382–393 (2007). https://doi.org/10.1038/nrg2082

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