Di Serio, Ermanno (2025) Epigenetic Mechanisms Underlying Phenotypic Plasticity in Vitis vinifera. [Tesi di dottorato]

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Abstract

Phenotypic plasticity is the ability of the same genotype to express different phenotypes in response to environmental cues. It represents the main mechanism by which plants, as sessile organisms, are able to thrive despite their limited capacity to modify their surroundings. However, due to its complex nature, the molecular mechanisms underlying this phenomenon are still largely unknown. In recent years, transcriptomic studies have revealed that environmental plasticity is often accompanied by extensive changes in gene expression, highlighting the dynamic nature of plant regulatory networks. Increasing evidence suggests that epigenetic mechanisms may play a key role in mediating phenotypic plasticity, as they enable plants to change gene expression without changes in DNA sequence. Epigenetic modifications include histone modifications, DNA methylation and the activity of small non-coding RNAs, all of which may be induced by both endogenous and/or external stimuli. Therefore, understanding how transcriptional and epigenetic processes interact represents a crucial step toward elucidating the molecular basis of phenotypic plasticity. Grapevine (Vitis vinifera L.) is one of the most widely cultivated perennial crops in the world and is known for its remarkable phenotypic plasticity. Indeed, grape berries display distinct morphological and biochemical characteristics depending on the environmental conditions in which the plants are grown, a concept commonly referred to as “terroir.” Moreover, the perennial woody growth of grapevine and its non-climacteric fruit ripening make this species a valuable model for studying both transcriptional and epigenetic mechanisms in plants. In this thesis, we employed different Next-Generation Sequencing (NGS) techniques to investigate the transcriptional and epigenetic regulation of gene expression in grape berries at ripe stage of two grapevine varieties, Aglianico and Cabernet Sauvignon, grown in three different areas of southern Italy (Sicily, Campania and Molise). The first part of the work focused on the berry transcriptome and on how the genotype and the environment influenced the gene expression of the two varieties (chapter 2). The results revealed that the transcriptome of Cabernet Sauvignon was more stable across the growing environments, whereas Aglianico exhibited a higher degree of plasticity. These transcriptional differences provided the foundation for investigating the regulatory mechanisms underlying such plasticity. In the second part of the work, we investigated the epigenetic mechanisms regulating gene expression by exploring two different layers of epigenetic regulation: small RNAs post-transcriptional silencing (chapter 3) and DNA methylation (chapter 4). Both analyses revealed that Cabernet Sauvignon maintained a more stable epigenetic landscape across environments, while Aglianico exhibited higher variability in DNA methylation and small RNA expression across sites, and we proposed that such differences may partially explain the contrasting transcriptional plasticity observed between the two cultivars. In addition, WGCNA analyses allowed us to identify modules of genes and modules of small RNAs correlated to climatic parameters and biochemical traits that play crucial roles in the final aroma of the wine. Finally, by integrating the results of the three analyses, we identified in Aglianico several target genes of differentially expressed small RNAs (DESs) and several differentially methylated genes (DMGs) involved in secondary metabolites accumulation, such as anthocyanins and polyphenols. Taken collectively, these findings contribute to our knowledge of the molecular basis of genotype × environment interactions in grapevine and elucidate cultivar- and site-dependent transcriptional and epigenetic patterns linked to environmental variability and fruit composition. Overall, the results may provide a beneficial platform for future studies aimed at detection of molecular correlates of environmental adaptation and fruit quality, with apparent ramifications for viticulture and breeding with dynamic climate

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