Epigenetic mechanisms of postzygotic reproductive isolation in plants
Introduction
Reproductive isolation (RI), defined as the absence or the restriction of gene flow between two populations, allows the conservation of their genetic and phenotypic distinctiveness in geographical proximity and consequently, is a requirement for speciation [1, 2]. RI can be initiated by different mechanisms and can be classified depending on whether it occurs before or after fertilization, named prezygotic or postzygotic RI, respectively [2]. The former can result from different pollinators, flowering periods or pollen–pistil incompatibility, while the latter affects hybrid viability or fertility and more generally, fitness.
Factors that build up postzygotic RI can be extrinsic or intrinsic. While the first depends on the environment, the latter does not (for details see [2]). In both cases, the Bateson–Dobzhansky–Muller (BDM) model explains postzygotic RI as a consequence of negative epistatic interactions between alleles that, while harmless in their native genomic context, have independently evolved in each parental lineage [3]. The identification of hybrid incompatibility genes in several species provided substantial support for this model [2]. Classically it has been viewed that BDM incompatibilities evolve as an incidental by-product of species adaptation to different ecological niches [4]. However, new findings suggest that the evolution of hybrid incompatibility is not necessarily a consequence of adaptation; instead, hybrid incompatibility is often a consequence of the evolution of neutral or selfish genetic changes that cause compensatory alterations at interacting loci [5]. Selfish genetic elements like transposable elements (TEs) are the cause for a phenomenon described as ‘genomic shock’ [6], which manifests in extensive genome and transcriptome changes as a consequence of the merging of two distinct genomes and that can create the basis for negative epistatic interactions and hybrid dysfunction [7, 8]. TE silencing in plants is mediated by small RNAs (sRNAs) and sRNA-directed DNA methylation (RdDM) in addition to DNA methylation maintenance [9], placing both pathways in the focus of research directed to understand the origins of hybrid incompatibility [8]. In this review, we highlight the latest advances and the future challenges to assess the role of epigenetic pathways in establishing postzygotic RI in plants.
Section snippets
Epigenetic processes in the endosperm establish a barrier to hybrid seed survival
In angiosperm seeds, embryo and endosperm are the products of two independent fertilization events. The development of the former is highly dependent on the latter. Most angiosperms follow a nuclear-type of endosperm development, where the endosperm initially develops as a syncytium and cellularization is triggered after a defined number of mitotic cycles [10]. Endosperm cellularization is a crucial developmental transition, which in case of failure triggers embryo arrest [11, 12, 13]. It has
Epigenetic effects on hybrid fitness
The role of epigenetic mechanisms in building hybridization barriers is not restricted to the endosperm, but may play a substantial role in reducing hybrid fitness [39••]. From described cases to date, two scenarios emerge to explain the effect of epigenetics on hybrid fitness: firstly, parental alleles can interact epigenetically via trans interactions. Thus, when meeting in the hybrid genome, an epigenetically silenced locus of one of the parents will trigger, via RdDM, the silencing of a
Conclusions
It is becoming evident that epigenome incompatibilities are a significant factor contributing to postzygotic hybrid barriers and it remains an exciting future challenge to fully elucidate the basis of this phenomenon and to explore the evolutionary consequences. As outlined above, hybrid incompatibility is often associated with deregulated sRNA levels and transcriptional activation of TEs. Whether or not hybrid barriers are a consequence of TE transposition or rather a consequence of
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgement
This research was supported by a European Research Council Starting Independent Researcher grant (to C.K.).
References (50)
- et al.
Big roles for small RNAs in polyploidy, hybrid vigor, and hybrid incompatibility
Curr Opin Plant Biol
(2012) Endosperm: the crossroad of seed development
Curr Opin Plant Biol
(2003)- et al.
Dosage-dependent deregulation of an AGAMOUS-LIKE gene cluster contributes to interspecific incompatibility
Curr Biol
(2009) - et al.
Epigenetic mechanisms in the endosperm and their consequences for the evolution of flowering plants
Biochim Biophys Acta
(2011) - et al.
Epigenetic mechanisms underlying genomic imprinting in plants
Annu Rev Plant Biol
(2012) - et al.
Whole-genome sequencing of multiple Arabidopsis thaliana populations
Nat Genet
(2011) - et al.
Maternal siRNAs as regulators of parental genome imbalance and gene expression in endosperm of Arabidopsis seeds
Proc Natl Acad Sci U S A
(2012) - et al.
Allele-specific DNA methylation analyses associated with siRNAs in Arabidopsis hybrids
Sci China Life Sci
(2014) What is a species, and what is not?
Philos Sci
(1996)- et al.
Genomics and the origin of species
Nat Rev Genet
(2014)
Speciation
Genetics and ecological speciation
Proc Natl Acad Sci U S A
The molecular evolutionary basis of species formation
Nat Rev Genet
The significance of responses of the genome to challenge
Science
Epigenetic, transposon and small RNA determinants of hybrid dysfunctions
Heredity
Establishing, maintaining and modifying DNA methylation patterns in plants and animals
Nat Rev Genet
Parent-of-origin effects on seed development in Arabidopsis thaliana
Development
ENDOSPERM DEFECTIVE1 is a novel microtubule-associated protein essential for seed development in Arabidopsis
Plant Cell
Endosperm cellularization defines an important developmental transition for embryo
Development
The transport of sugars to developing embryos is not via the bulk endosperm in oilseed rape seeds
Plant Physiol
Studies in British Primulas. X. Seed incompatibility in intraspecific and interspecific crosses at diploid and tetraploid levels
New Phytol
Dissection of two major components of the post-zygotic hybridization barrier in rice endosperm
Plant J
Generation of interspecific hybrids of Trifolium using embryo rescue techniques
Production of interspecific hybrids in ornamental plants
Unidirectional hybridization and reproductive barriers between two heterostylous primrose species in north-west Yunnan, China
Ann Bot
Cited by (35)
Evolution of epigenetic mechanisms in animals and their role in speciation
2017, Handbook of Epigenetics: The New Molecular and Medical GeneticsOrigination and Establishment of a Trigenic Reproductive Isolation System in Rice
2016, Molecular PlantACL and HAT1 form a nuclear module to acetylate histone H4K5 and promote cell proliferation
2023, Nature CommunicationsEnforcement of Postzygotic Species Boundaries in the Fungal Kingdom
2022, Microbiology and Molecular Biology ReviewsEpigenetics and reproductive isolation: a commentary on Westram et al., 2022
2022, Journal of Evolutionary Biology