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Florez-Rueda, A. M.

Publications and source records attributed to Florez-Rueda, A. M..

5 recordsLinked to original sources

Trans-allelic Epigenetic Dominance Disrupts Hybrid Endosperm Development in Wild Tomatoes

Background and AimsHybrid seed failure (HSF) is a common reproductive barrier in flowering plants, but how divergence in so-called effective ploidy translates into genome-wide allelic imbalance in hybrid endosperm remains unresolved. Using wild tomatoes (Solanum sect. Lycopersicon) as our model system, we test whether parent-of-origin expression shifts in hybrids are consistent with simple dosage effects or instead reflect lineage-specific trans regulation. MethodsUsing reciprocal interspecific crosses, we quantified parent-of-origin (allele-specific) expression in developing endosperm and analyzed patterns of differential parent-of-origin expression (DPE) across cross contexts. Guided by strong patterns in parental expression, we further classified DPE genes into four functional classes defined by their relationship to Solanum peruvianum (Per). This exercise captured distinct modes of trans-allelic regulation and guided functional interpretation. Key ResultsParental expression proportions are strongly asymmetric in hybrids, with the most pronounced and repeatable shifts occurring in crosses involving Per. These shifts recur across reciprocal contexts and include elevated maternal proportions even in crosses phenotypically classified as paternal-excess-like, arguing against a dosage-only model. Instead, we observed cross-consistent, coordinated DPE patterns corresponding to trans-acting dominance associated with Per. Functional enrichment of Per-associated DPE highlights chromatin regulation, including DNA methylation/RdDM- and chromatin remodeling-related factors, and Polycomb-linked regulators, implicating disruption of chromatin-based repression in hybrid endosperm. Concurrently, Per-associated activation of auxin- and cell-cycle regulatory pathways in non-Per alleles suggests mis-timed hormone-dependent developmental transitions that can destabilize proliferation-cellularization programs. ConclusionsOur findings support a model of trans-allelic epigenetic dominance in which Per-associated regulatory inputs reshape allelic expression landscapes in hybrid endosperm largely independent of parental origin. This provides a mechanistic link between effective ploidy divergence, genome-wide transcriptional imbalance, and HSF, and motivates reciprocal hybrid studies that integrate expression with chromatin-state and accessibility profiling.

plant biology↗

Genomic imprinting in an early-diverging angiosperm reveals ancient mechanisms for seed initiation in flowering plants

The evolution of the seed habit marks a pivotal innovation of the spermatophytes. Angiosperms further refined this trait by coupling the development of seed accessory structures to fertilization, optimizing resource allocation. Here, we demonstrate that post-fertilization auxin production is an evolutionarily conserved mechanism for seed initiation in angiosperms. We also provide evidence that this pathway likely emerged from a switch from maternal to paternal control after the divergence of angiosperms from their gymnosperm ancestors. Our study thus brings new insights into the evolutionary origins of the endosperm, which was a determining feature for the rapid rise to dominance of flowering plants.

plant biology↗

Comparative transcriptomics of seed nourishing tissues: uncovering conserved and divergent pathways in seed plants

The evolutionary and ecological success of spermatophytes is intrinsically linked to the seed habit, which provides a protective environment for the initial development of the new generation. This environment includes an ephemeral nourishing tissue that supports embryo growth. In gymnosperms this tissue originates from the asexual proliferation of the maternal megagametophyte, while in angiosperms it is a product of fertilization, and is called the endosperm. The emergence of these nourishing tissues is of profound evolutionary value, and they are also food staples for most of the worlds population. Here, using Orthofinder to infer orthologue genes among novel and previously published datasets, we provide a comparative transcriptomic analysis of seed nourishing tissues from representative species of all main angiosperm clades, including those of early diverging basal angiosperms, and a gymnosperm representative. Our results show that, although the structure and composition of seed nourishing tissues has seen significant divergence along evolution, there are signatures that are conserved throughout the phylogeny. Conversely, we identified processes that are specific to species within the clades studied, and thus illustrate their functional divergence. With this, we aimed to provide a foundation for future studies on the evolutionary history of seed nourishing structures, as well as a resource for gene discovery in new functional studies. Significance StatementWithin seeds a specialized structure is responsible for nourishing the embryo during its development. These nourishing tissues are also important sources of staple foods and feed. Here, we provide novel gene expression datasets of nourishing tissues of early diverging angiosperms, and use this information for a meta-analysis to identify pathways conserved, or divergent, throughout evolution. Thus, we aim to provide a resource for gene discovery for seed biology studies.

plant biology↗

Endosperm and seed transcriptomes reveal possible roles for small RNA pathways in wild tomato hybrid seed failure

Crosses between the wild tomato species Solanum peruvianum and S. 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 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 expression levels. We identified 2,295 genes and 468 small RNAs (sRNAs) as differentially expressed (DE) 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 cross directions, in marked contrast to the patterns of sRNA expression in whole seeds. Intriguingly, patterns of increased gene expression resembled the previously reported increased maternal expression proportions in hybrid endosperms. We identified physical clusters of sRNAs; DE sRNAs exhibited reduced levels of expression in hybrid seeds from both cross directions. Moreover, sRNAs mapped to genes coding for key proteins involved in epigenetic regulation of gene expression, suggesting a regulatory feedback mechanism. We describe examples of genes that are targets of sRNA-mediated gene silencing; in these cases, reduced sRNA expression was 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.

plant biology↗

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.

genetics↗