Variability of Hybrid Seed Failure in Wild Tomatoes (Solanum sect. Lycopersicon): Phenotypic and Molecular Signatures in the Developing Endosperm
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2017
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Doctoral Thesis
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Abstract
Seed development represents a critical stage for plant reproductive success. This dissertation focuses on phenotypic and molecular correlates of hybrid seed failure between closely-related species. Three main compartments comprise the angiosperm seed, each with different genomic make-up: the seed coat (maternal), the endosperm (2m:1p), and the embryo (1m:1p). The endosperm plays a central role in early seed development because it regulates embryo nutrient acquisition while synchronizing growth between seed compartments. Importantly, hybrid seed abortion is generally associated with an altered endosperm development. Moreover, genomic imprinting, i.e. parent-of-origin–dependent expression, is exceedingly rare in other plant tissues but widespread in the endosperm. Potential functional links between imprinting perturbation or -mismatch and seed abortion are predicted by evolutionary theory based on parental conflict, but have only begun to be elucidated at the molecular level. Wild tomatoes (Solanum sect. Lycopersicon) were chosen to compare seed development and gene expression in the endosperm of seeds from intraspecific and hybrid crosses, and to address the role of genomic imprinting in lineage divergence and hybrid seed failure. To this end, I used three tomato lineages with interesting hybrid seed phenotypes and patterns of genetic divergence: S. arcanum var marañón (A), S. chilense (C), and S. peruvianum (P). A large part of my study was based on laser-microdissected developing endosperm obtained from seeds of intra- and interspecific crosses and subsequent transcriptome sequencing.
In Chapter 1, I hypothesized that seed abortion in wild tomatoes is triggered by endosperm failure and that viable hybrid progenies, after seed germination, may reveal additional symptoms of hybrid incompatibility. Jointly with my collaborators, I provided a comprehensive morphological description of seed development in intra- and interspecific crosses. I found that the incidence of hybrid seed failure was variable among species combinations, with marked phenotypic asymmetries between reciprocal crosses with near- complete seed inviability. For the latter, circumstantial evidence pointed to endosperm proliferation defects being responsible for embryo arrest at early globular stages. The reciprocal C×A and A×C hybrid crosses yielded intermediate levels of viable seeds, from which we grew an F1 hybrid cohort showing some developmental abnormalities, interpreted as reflecting post-germination genetic incompatibilities.
Chapter 2 focuses on seeds from intraspecific crosses, i.e. those with normal seed development. My hypothesis was that genomic imprinting in the endosperm of normally developing seeds serves specific functions and is nonrandomly shared between recently diverged species. I found that the degree of overlap among imprinted genes across the three wild tomato lineages was significant, and higher for Paternally Expressed Genes (PEGs) than for Maternally Expressed Genes (MEGs). However, variation in imprinting status for many genes is suggestive of an evolutionarily fast turnover of imprinted expression. MEGs and PEGs appear to be associated with distinct functions, but I found evidence that they interact in functional and physical networks. In particular, I inferred that interactions between imprinted genes contribute to cell-cycle control. Candidate imprinted genes identified in this chapter should be representative of the typical imprinting landscape of wild tomato viable endosperm; they were used as a reference to compare parent-specific gene expression in within-lineage- and hybrid endosperms in Chapter 3.
Chapter 3 aimed at testing the hypothesis that hybrid seed failure involves imprinting perturbation and/or large gene expression changes in wild tomato hybrid endosperms. When compared to intraspecific endosperms, those from strongly abortive crosses were characterized by extensive gene expression perturbation together with increased maternal expression proportions. Two homogeneous groups of hybrid endosperms were separated by the largest expression differences in the whole dataset, congruent with either maternal-excess-like (P×A and P×C) or paternal-excess-like (A×P and C×P) endosperms at the phenotypic level. I found strong evidence for perturbations of parental dosage mechanisms in these abortive endosperms, particularly the widespread loss of imprinting status of candidate PEGs. Crosses yielding only partial seed abortion (A×C and C×A) had far fewer expression changes than strongly abortive endosperms and also retained the imprinted status of most candidate PEGs. I discuss the potential roles of parental conflict and coadaptation in driving expression perturbation in abortive endosperm. Finally, I hypothesize that different ‘genetic strengths’ evolved since lineage divergence and identify candidate genes, such as AGAMOUS-LIKE transcriptions factors, that may underlie this dosage-related phenomenon. Such genes may significantly contribute to postzygotic reproductive isolation between wild tomato lineages.
By revealing the widespread perturbation of imprinted expression in abortive hybrid endosperms, my project accrued molecular evidence for the fundamental role of parental dosage in successful seed development. As a collateral resource, it also provides a large number of candidate genes that are potentially useful for developmental and evolutionary biology and for plant breeding.
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Examiner: Widmer, Alex
Examiner : Städler, Thomas
Examiner : Parisod, Christian
Examiner : Tenaillon, Maud
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ETH Zurich
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Wild tomatoes; hybrid; endosperm; transcriptomics; seed; genomic imprinting; parental conflict
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03706 - Widmer, Alexander / Widmer, Alexander