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

Roth, Morgane; Florez-Rueda, Ana M; Griesser, Stephan; Paris, Margot; Städler, Thomas

doi:10.1093/aob/mcx133

Cited by 49 publications

(94 citation statements)

References 68 publications

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“…By generating RNA‐Seq data from developing endosperm in replicated reciprocal crosses, we assessed genomic imprinting in the three wild tomato lineages A , C and P . To maximize power to assess PSE, the parental combinations were chosen based on high inter‐individual molecular polymorphism as well as high seed viability (Roth et al ., ). Biological variation was taken into consideration by using three clonal replicates for each cross, resulting in a total of 18 endosperm samples.…”

Section: Resultsmentioning

confidence: 99%

“…Thus, further investigations are needed to explore patterns of sequence evolution in MEGs and PEGs, for example by repeating such analyses with more individuals and more IGs, preferentially in outcrossing species where IGs are expected to evolve under stronger parental conflict (Brandvain and Haig, ; Haig, ). Data on endosperm growth and seed size in interspecific crosses between these three lineages suggest that lineage P experienced higher levels of parental conflict compared with both A and C (Roth et al ., ), consistent with its higher level of nucleotide diversity (Städler et al ., ; Tellier et al ., ; Beddows et al ., ). Interestingly, we found that conserved IGs tend to have a higher expression in lineage P compared with both A and C (Figure ), possibly reflecting higher levels of parental conflict and mirroring observations in A. lyrata – A. thaliana comparisons (Klosinska et al ., ).…”

Section: Discussionmentioning

confidence: 98%

“…Interestingly, we found that conserved IGs tend to have a higher expression in lineage P compared with both A and C (Figure ), possibly reflecting higher levels of parental conflict and mirroring observations in A. lyrata – A. thaliana comparisons (Klosinska et al ., ). Whether directly or indirectly, such expression differences might be involved in the molecular underpinnings of hybrid seed failure observed between these wild tomato lineages (Florez‐Rueda et al ., ; Roth et al ., ).…”

Section: Discussionmentioning

confidence: 98%

“…marañón ( A ), Solanum chilense ( C ) and S. peruvianum ( P ). These lineages are morphologically and ecologically well differentiated (Rick and Lamm, ; Rick, ; Peralta et al ., ), and are reproductively isolated from each other to varying degrees by endosperm‐based hybrid seed failure, causing partial to near‐complete seed abortion (Roth et al ., ). Using estimates of maternal expression proportions for between 7730 and 13 198 genes per lineage, our study characterizes genomic imprinting and probes the level of imprinting divergence between the three closely related wild tomato lineages.…”

Section: Introductionmentioning

confidence: 97%

“…Wild tomatoes (Solanum section Lycopersicon) provide an excellent model system to study the incidence, evolution and consequences of imprinting in the endosperm; they diverged fairly recently (~2.5 Mya; Pease et al ., ), harbor a diversity of mating systems and exhibit various degrees of post‐zygotic isolation mediated by endosperm‐based hybrid seed failure (Baek et al ., ; Roth et al ., ). Unlike all other taxa that have been the focus of studies on endosperm genomic imprinting, Solanum is characterized by a cellular‐ rather than a nuclear‐type endosperm during early development.…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2018

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Genomic imprinting is a conspicuous feature of the endosperm, a triploid tissue nurturing the embryo and synchronizing angiosperm seed development. An unknown subset of imprinted genes (IGs) is critical for successful seed development and should have highly conserved functions. Recent genome-wide studies have found limited conservation of IGs among distantly related species, but there is a paucity of data from closely related lineages. Moreover, most studies focused on model plants with nuclear endosperm development, and comparisons with properties of IGs in cellular-type endosperm development are lacking. Using laser-assisted microdissection, we characterized parent-specific expression in the cellular endosperm of three wild tomato lineages (Solanum section Lycopersicon). We identified 1025 candidate IGs and 167 with putative homologs previously identified as imprinted in distantly related taxa with nuclear-type endosperm. Forty-two maternally expressed genes (MEGs) and 17 paternally expressed genes (PEGs) exhibited conserved imprinting status across all three lineages, but differences in power to assess imprinted expression imply that the actual degree of conservation might be higher than that directly estimated (20.7% for PEGs and 10.4% for MEGs). Regardless, the level of shared imprinting status was higher for PEGs than for MEGs, indicating dissimilar evolutionary trajectories. Expression-level data suggest distinct epigenetic modulation of MEGs and PEGs, and gene ontology analyses revealed MEGs and PEGs to be enriched for different functions. Importantly, our data provide evidence that MEGs and PEGs interact in modulating both gene expression and the endosperm cell cycle, and uncovered conserved cellular functions of IGs uniting taxa with cellular- and nuclear-type endosperm.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 98%

Section: Discussionmentioning

confidence: 98%

Section: Introductionmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 99%

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

et al. 2018

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The role of hybrid seed inviability in angiosperm speciation

Coughlan

2023

American J of Botany

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Understanding which reproductive barriers contribute to speciation is essential to understanding the diversity of life on earth. Several contemporary examples of strong hybrid seed inviability (HSI) between recently diverged species suggest that HSI may play a fundamental role in plant speciation. Yet, a broader synthesis of HSI is needed to clarify its role in diversification. Here, I review the incidence and evolution of HSI. Hybrid seed inviability is common and evolves rapidly, suggesting that it may play an important role early in speciation. The developmental mechanisms that underlie HSI involve similar developmental trajectories in endosperm, even between evolutionarily deeply diverged incidents of HSI. In hybrid endosperm, HSI is often accompanied by whole‐scale gene misexpression, including misexpression of imprinted genes which have a key role in endosperm development. I explore how an evolutionary perspective can clarify the repeated and rapid evolution of HSI. In particular, I evaluate the evidence for conflict between maternal and paternal interests in resource allocation to offspring (i.e., parental conflict). I highlight that parental conflict theory generates explicit predictions regarding the expected hybrid phenotypes and genes responsible for HSI. While much phenotypic evidence supports a role of parental conflict in the evolution of HSI, an understanding of the underlying molecular mechanisms of this barrier is essential to test parental conflict theory. Lastly, I explore what factors may influence the strength of parental conflict in natural plant populations as an explanation for why rates of HSI may differ between plant groups and the consequences of strong HSI in secondary contact.

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Biosystematic studies on the status of Solanum chilense

Raduski

Igić

2021

American J of Botany

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Common taxonomic practices, which condition species' descriptions on diagnostic morphological traits, may systematically lump outcrossing species and unduly split selfing species. Specifically, higher effective population sizes and genetic diversity of obligate outcrossers are expected to result less reliable phenotypic diagnoses. Wild tomatoes, members of Solanum sect. Lycopersicum, are commonly used as a source of exotic germplasm for improvement of the cultivated tomato, and are increasingly employed in basic research. Although the section experienced significant early work, which continues presently, the taxonomic status of many wild species has undergone a number of significant revisions and remains uncertain. Species in this section vary in their breeding systems, notably the expression of self-incompatibility, which determines individual propensity for outcrossing METHODS: Here, we examine the taxonomic status of obligately outcrossing Chilean wild tomato (Solanum chilense) using reduced-representation sequencing (RAD-seq), a range of phylogenetic and population genetic analyses, as well as analyses of crossing and morphological data. RESULTS: Overall, each of our analyses provides a considerable weight of evidence that the Pacific coastal populations and Andean inland populations of the currently described Solanum chilense represent separately evolving populations, and conceal at least one undescribed cryptic species. CONCLUSIONS: Despite its vast economic importance, Solanum sect. Lycopersicon still exhibits considerable taxonomic instability. A pattern of under-recognition of outcrossing species may be common, not only in tomatoes, but across flowering plants. We discuss the possible causes and implications of this observation, with a focus on macroevolutionary inference.

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

Cited by 49 publications

References 68 publications

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

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

The role of hybrid seed inviability in angiosperm speciation

Biosystematic studies on the status of Solanum chilense

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