Incidence and developmental timing of endosperm failure in post-zygotic isolation between wild tomato lineages

Background and AimsDefective hybrid seed development in angiosperms might mediate the rapid establishment of intrinsic post-zygotic isolation between closely related species. Extensive crosses within and among three lineages of wild tomatoes (Solanum section Lycopersicon) were performed to address the incidence, developmental timing and histological manifestations of hybrid seed failure. These lineages encompass different, yet fairly recent, divergence times and both allopatric and partially sympatric pairs.MethodsMature seeds were scored visually 2 months after hand pollinations, and viable-looking seeds were assessed for germination success. Using histological sections from early-developing seeds from a sub-set of crosses, the growth of three major seed compartments (endosperm, embryo and seed coat) was measured at critical developmental stages up to 21 d after pollination, with a focus on the timing and histological manifestations of endosperm misdevelopment in abortive hybrid seeds.Key ResultsFor two of three interspecific combinations including the most closely related pair that was also studied histologically, almost all mature seeds appeared ‘flat’ and proved inviable; histological analyses revealed impaired endosperm proliferation at early globular embryo stages, concomitant with embryo arrest and seed abortion in both cross directions. The third interspecific combination yielded a mixture of flat, inviable and plump, viable seeds; many of the latter germinated and exhibited near-normal juvenile phenotypes or, in some instances, hybrid necrosis and impaired growth.ConclusionsThe overall results suggest that near-complete hybrid seed failure can evolve fairly rapidly and without apparent divergence in reproductive phenology/biology. While the evidence accrued here is largely circumstantial, early-acting disruptions of normal endosperm development are most probably the common cause of seed failure regardless of the type of endosperm (nuclear or cellular)

Differences in effective ploidy as drivers of genome-wide endosperm expression asymmetries and seed failure in wild tomato hybrids

Endosperm misdevelopment leading to hybrid seed failure is a common cause of postzygotic isolation in angiosperms and is observed in both interploidy and homoploid crosses between closely related lineages. Moreover, parental dosage is critical for successful endosperm and seed development, typically requiring a ratio of two maternal to one paternal genome(s) in within-species crosses. The recently revived concept of 'effective ploidy' can largely explain the outcome of experimental crosses that (partly) ameliorate hybrid seed failure by manipulating the actual ploidy in one of the parents. However, genome-wide expression perturbations concomitant with levels of hybrid seed failure have yet to be reported. The tomato clade (Solanum section Lycopersicon), encompassing closely related diploids with partial-to-complete hybrid seed failure and diverse mating systems, provides outstanding opportunities to study these issues. Here we compared replicated endosperm transcriptomes from six crosses within and among three wild tomato lineages. Strikingly, both strongly inviable hybrid crosses displayed conspicuous, asymmetric expression perturbations with strong signatures of cross direction. In particular, Solanum peruvianum, the species inferred to have evolved higher effective ploidy than the other two, drove hybrid expression landscapes in both maternal and paternal roles. This global expression divergence was mirrored in functionally important gene families such as transcription factors and E3 ubiquitin ligases, and revealed differences in cell-cycle tuning between lineages that match phenotypic differences in developing endosperm and mature seed size between reciprocal crosses. Our work initiates the exploration of links between parental conflict, genomic imprinting, expression dosage and hybrid seed failure in flowering plants

A revival of effective ploidy: the asymmetry of parental roles in endosperm-based hybridization barriers

Interest in understanding hybrid seed failure (HSF) has mushroomed, both in terms of identifying underlying molecular processes and their evolutionary drivers. We review phenotypic and molecular advances with a focus on the ‘effective ploidy’ concept, witnessing a recent revival after long obscurity. Endosperm misdevelopment has now been shown to underlie HSF in many inter-specific, homoploid crosses. The consistent asymmetries in seed size and developmental trajectories likely reflect parental divergence in key, dosage-sensitive processes. Transcriptomic and epigenomic studies reveal genome-wide, polarized expression perturbations and shifts in parental expression proportions, consistent with small-RNA imbalances between parental roles. Among-species differences in levels of parental conflict over resource allocation enjoy strong support in explaining why differences in effective ploidy may evolve.ISSN:1369-5266ISSN:1879-035

Differences in Effective Ploidy Drive Genome-Wide Endosperm Expression Polarization and Seed Failure in Wild Tomato Hybrids

ISSN:1943-263

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

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

Population Genomics of the “Arcanum” Species Group in Wild Tomatoes: Evidence for Separate Origins of Two Self-Compatible Lineages

Given their diverse mating systems and recent divergence, wild tomatoes (Solanum section Lycopersicon) have become an attractive model system to study ecological divergence, the build-up of reproductive barriers, and the causes and consequences of the breakdown of self-incompatibility. Here we report on a lesser-studied group of species known as the “Arcanum” group, comprising the nominal species Solanum arcanum, Solanum chmielewskii, and Solanum neorickii. The latter two taxa are self-compatible but are thought to self-fertilize at different rates, given their distinct manifestations of the morphological “selfing syndrome.” Based on experimental crossings and transcriptome sequencing of a total of 39 different genotypes from as many accessions representing each species’ geographic range, we provide compelling evidence for deep genealogical divisions within S. arcanum; only the self-incompatible lineage known as “var. marañón” has close genealogical ties to the two self-compatible species. Moreover, there is evidence under multiple inference schemes for different geographic subsets of S. arcanum var. marañón being closest to S. chmielewskii and S. neorickii, respectively. To broadly characterize the population-genomic consequences of these recent mating-system transitions and their associated speciation events, we fit demographic models indicating strong reductions in effective population size, congruent with reduced nucleotide and S-locus diversity in the two independently derived self-compatible species.ISSN:1664-462

Incidence and developmental timing of endosperm failure in post-zygotic isolation between wild tomato lineages

Abstract Background and Aims Defective hybrid seed development in angiosperms might mediate the rapid establishment of intrinsic post-zygotic isolation between closely related species. Extensive crosses within and among three lineages of wild tomatoes (Solanum section Lycopersicon) were performed to address the incidence, developmental timing and histological manifestations of hybrid seed failure. These lineages encompass different, yet fairly recent, divergence times and both allopatric and partially sympatric pairs. Methods Mature seeds were scored visually 2 months after hand pollinations, and viable-looking seeds were assessed for germination success. Using histological sections from early-developing seeds from a sub-set of crosses, the growth of three major seed compartments (endosperm, embryo and seed coat) was measured at critical developmental stages up to 21 d after pollination, with a focus on the timing and histological manifestations of endosperm misdevelopment in abortive hybrid seeds. Key Results For two of three interspecific combinations including the most closely related pair that was also studied histologically, almost all mature seeds appeared ‘flat' and proved inviable; histological analyses revealed impaired endosperm proliferation at early globular embryo stages, concomitant with embryo arrest and seed abortion in both cross directions. The third interspecific combination yielded a mixture of flat, inviable and plump, viable seeds; many of the latter germinated and exhibited near-normal juvenile phenotypes or, in some instances, hybrid necrosis and impaired growth. Conclusions The overall results suggest that near-complete hybrid seed failure can evolve fairly rapidly and without apparent divergence in reproductive phenology/biology. While the evidence accrued here is largely circumstantial, early-acting disruptions of normal endosperm development are most probably the common cause of seed failure regardless of the type of endosperm (nuclear or cellular)