Abstract
Crosses between the wild tomato species Solanum peruvianum and Solanum chilense result in hybrid seed failure (HSF), characterized by endosperm misdevelopment and embryo arrest. We previously showed that genomic imprinting, the parent-of-origin–dependent expression of alleles, is perturbed in the hybrid endosperm, with many of the normally paternally expressed genes losing their imprinted status. Here, we report transcriptome-based analyses of gene and small RNA (sRNA) expression levels. We identified 2,295 genes and 387 sRNA clusters as differentially expressed when comparing reciprocal hybrid seed to seeds and endosperms from the two within-species crosses. Our analyses uncovered a pattern of overdominance in endosperm gene expression in both hybrid cross directions, in marked contrast to the patterns of sRNA expression in whole seeds. Intriguingly, patterns of increased gene expression resemble the previously reported increased maternal expression proportions in hybrid endosperms. We identified physical clusters of sRNAs; differentially expressed sRNAs exhibit reduced transcript abundance in hybrid seeds of both cross directions. Moreover, sRNAs map to genes coding for key proteins involved in epigenetic regulation of gene expression, suggesting a regulatory feedback mechanism. We describe examples of genes that appear to be targets of sRNA-mediated gene silencing; in these cases, reduced sRNA abundance is concomitant with increased gene expression in hybrid seeds. Our analyses also show that S. peruvianum dominance impacts gene and sRNA expression in hybrid seeds. Overall, our study indicates roles for sRNA-mediated epigenetic regulation in HSF between closely related wild tomato species.
Highlights
The establishment of reproductive barriers between diverging lineages is a basic component of the speciation process and of major interest in evolutionary biology (Coyne and Orr 2004)
The 24-nt small RNAs (sRNAs) category was the prevalent type among the 57,711 clusters identified within 2.5 Kb of annotated genes, whereas 21-22-nt sRNAs and miRNAs accounted for only 10% of the total identified sRNA clusters
The pattern of whole-seed sRNA differential expression is in stark contrast to the increase in gene expression we found among differentially expressed (DE) genes in hybrid endosperms
Summary
The establishment of reproductive barriers between diverging lineages is a basic component of the speciation process and of major interest in evolutionary biology (Coyne and Orr 2004). Transgressive and complementary hybrid seed phenotypes are common and thought to reveal different levels of parental conflict between lineages (Lu et al 2012; Haig 2013; Rebernig et al 2015; Florez-Rueda, Paris, et al.2016). These observations have led to the hypothesis that parent-of-origin–dependent allelic expression (i.e. genomic imprinting) might be causally involved in HSF. While occurring in the embryo, genomic imprinting is prevalent in the endosperm and critical for proper seed development (Berger 2003)
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