Genomic Imprinting in the Endosperm Is Systematically Perturbed in Abortive Hybrid Tomato Seeds

Abstract

Hybrid seed failure represents an important postzygotic barrier to interbreeding among species of wild tomatoes (Solanum section Lycopersicon) and other flowering plants. We studied genome-wide changes associated with hybrid seed abortion in the closely related Solanum peruvianum and S. chilense where hybrid crosses yield high proportions of inviable seeds due to endosperm failure and arrested embryo development. Based on differences of seed size in reciprocal hybrid crosses and developmental evidence implicating endosperm failure, we hypothesized that perturbed genomic imprinting is involved in this strong postzygotic barrier. Consequently, we surveyed the transcriptomes of developing endosperms from intra- and inter-specific crosses using tissues isolated by laser-assisted microdissection. We implemented a novel approach to estimate parent-of-origin–specific expression using both homozygous and heterozygous nucleotide differences between parental individuals and identified candidate imprinted genes. Importantly, we uncovered systematic shifts of “normal” (intraspecific) maternal:paternal transcript proportions in hybrid endosperms; the average maternal proportion of gene expression increased in both crossing directions but was stronger with S. peruvianum in the maternal role. These genome-wide shifts almost entirely eliminated paternally expressed imprinted genes in S. peruvianum hybrid endosperm but also affected maternally expressed imprinted genes and all other assessed genes. These profound, systematic changes in parental expression proportions suggest that core processes of transcriptional regulation are functionally compromised in hybrid endosperm and contribute to hybrid seed failure.

Endosperm-based hybridization barriers explain the pattern of gene flow between Arabidopsis lyrata and Arabidopsis arenosa in Central Europe

“…The presence of distinct incompatibility loci in A. arenosa populations suggests a recent intraspecific diversification of those loci and therefore a fast evolving genetic basis of hybrid incompatibility, similar to that proposed for other species (38,44,45). Genomic imprinting, the epigenetic phenomenon by which genes are expressed in a parent-of-origin manner, has been causally linked to endosperm-based hybridization barriers and is disturbed in interspecific hybrid seeds (24,(46)(47)(48). Moreover, genomic imprinting has been shown to vary among populations of the same species (49,50).…”

“…To this end, deregulated imprinted genes underpin endosperm-based hybridization barriers (46)(47)(48), and are thus likely to form the molecular basis of the EBN. Consistent with this idea, Solanum species with different EBNs exhibit different genomic imprinting patterns (48). Additional studies are needed to determine whether this difference not only correlates with but is indeed causative for the EBN.…”

Selfish X chromosomes and speciation

“…There is growing evidence for a role for imprinted genes in hybrid inviability in both mammals and seed plants (e.g., Brekke & Good, ; Brekke, Henry, & Good, ; Burkart‐Waco, Ngo, Lieberman, & Comai, ; Florez‐Rueda et al., ; Garner, Kenney, Fishman, & Sweigart, ; Josefsson, Dilkes, & Comai, ; Loschiavo, Nguyen, Duselis, & Vrana, ; Vrana et al., ), and dysregulation of imprinted genes caused by trans effects has been suggested as a possible source of this incompatibility (Wolf, Oakey, & Feil, ). Intriguingly for the X‐autosome conflict hypothesis, Vrana et al.…”

Wild tomato endosperm transcriptomes reveal common roles of genomic imprinting in both nuclear and cellular endosperm

“…The kin conflict theory further predicts that imprinting will evolve under strong selective constraints in outcrossing lineages with high levels of multiple paternity, while such constraints might be relaxed under long‐term inbreeding (Brandvain and Haig, ). To our knowledge, genomic imprinting in the endosperm has been studied in representatives of four angiosperm families (Brassicaceae, Poaceae, Solanaceae and Euphorbiaceae), including: (i) (mainly) inbreeding species such as A. thaliana (Wolff et al ., ; Pignatta et al ., ), Capsella rubella (Hatorangan et al ., ) and rice (Yuan et al ., ); and (ii) (mainly) outcrossing species such as Arabidopsis lyrata (Klosinska et al ., ), maize (Zhang et al ., ), Sorghum bicolor (Zhang et al ., ), Solanum peruvianum (Florez‐Rueda et al ., ) and castor bean (Xu et al ., ). While seed phenotypes of homoploid crosses between closely‐related species with different mating systems are consistent with predictions of the kin conflict theory, they have hitherto not been associated with specific imprinting patterns (Rebernig et al ., ; Lafon‐Placette et al ., ).…”