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Harnessing lipids
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Grapevine (Vitis vinifera L.) is one of the most extensively cultivated plants worldwide. However, the majority of Vitis vinifera cultivars used in the wine industry exhibit high susceptibility to diseases such as grapevine downy mildew, which is caused by the obligate biotrophic oomycete, Plasmopara viticola. To control this disease, viticulturers often resort to the preventive use of phytochemicals throughout the growing season, leading to significant economic and environmental costs. It is crucial that farmers, governments, and consumers collaborate to promote more sustainable agriculture practices, minimizing excessive pesticide use. Understanding the molecular processes underlying plant tolerance or susceptibility to diseases is fundamental to achieve this goal.
Lipids play a critical role in grapevine defence mechanisms. In response to pathogens, plants can alter the ratio of saturated to unsaturated fatty acids in membrane lipids, adjusting its fluidity to optimize cellular processes such as protein transport and signal transduction. This modulation of membrane fluidity is crucial for activating defence mechanisms, including the production of antimicrobial compounds and the initiation of signalling cascades. Beyond physical alterations, cellular membranes serve as reservoirs of precursors of signalling compounds, such as jasmonic acid. Jasmonic acid, derived from the polyunsaturated fatty acid, α-linolenic acid, acts as a plant hormone regulating the expression of defence-related genes and triggering various physiological responses, such as stomatal closure, synthesis of antimicrobial compounds, and activation of physical defences like callose deposition.
In addition to the understanding of their essential roles in plant defence mechanisms, lipid profiling has demonstrated a broad range of potential applications. It has proven to be a robust chemotaxonomic tool, allowing the distinction between grapevines genotypes with different degrees of susceptibility and tolerance to Plasmopara viticola. Given the significant value of lipids, this thesis aims to deepen the understanding of lipid signalling mechanisms in grapevine response to Plasmopara viticola and leverage this knowledge to utilize lipids and lipid-derived molecules to promote a more sustainable viticulture (CHAPTER I).
To fill the gaps regarding the involvement of lipids in grapevine defence mechanisms, were evaluated the fatty acid metabolism of grapevine leaves in response to Plasmopara viticola (CHAPTERS II and III). Lipid signalling events were evaluated by examining the modulations during the establishment of the incompatible interaction between grapevine and Plasmopara viticola using V. vinifera cv. Regent, a hybrid with high disease tolerance (CHAPTER II). Within the initial hours of grapevine-Plasmopara viticola interaction, there was significant fatty acid desaturation, resulting in the accumulation of polyunsaturated fatty acids, particularly α-linolenic acid. Concurrently, at the molecular level, the up-regulation of fatty acid desaturases coding genes, responsible for the formation of these polyunsaturated fatty acids, was observed. To further understand the involvement of lipids in grapevine defence mechanisms against downy mildew, were evaluated the lipid modulation in three cultivars with varying degrees of susceptibility and tolerance to P. viticola: cv. Chardonnay (susceptible), Regent (tolerant, with the Rpv3-1 resistance locus), and cv. Sauvignac (resistant, with Rpv12 and Rpv3-1 loci in pyramid) (CHAPTER III). These three cultivars were inoculated with a highly resistant isolate of Plasmopara viticola, NW-10/16, capable of surpass the grapevines tolerance traits. Regent exhibited specific modulation of genes associated with lipid signalling and fatty acids unsaturation, possibly linked to the Rpv3 locus. In contrast, the Sauvignac genotype, which carries the Rpv12 locus dominantly, may activate alternative defence pathways instead of lipid signalling.
In CHAPTERS IV and V, the use of lipid-derived molecules as potential immune priming agents in grapevine was evaluated. In Trincadeira, a disease susceptible cultivar, eicosapentaenoic acid (EPA) and jasmonic acid were used as elicitors. EPA is a fatty acid absent in higher plants but specific to pathogens such as Plasmopara viticola, whereas, jasmonic acid is an endogenous phytohormone of the plant. During the first 72 hours postelicitation, the treatment with EPA and jasmonic acid stimulated grapevine immunity by altering lipid metabolism and increasing the expression of several genes involved in defence and secondary metabolism (CHAPTER IV). After inoculation with Plasmopara viticola, preelicited grapevines triggered the induction of defence gene expression, activated secondary metabolism leading to the accumulation of phytoalexins, lead to fatty acids production and exhibited a higher abundance of lipid metabolites predominantly associated with lipidsignalling pathways (CHAPTER V). In both experiments, EPA stood out as a promising elicitor by promoting a more robust and long-lasting defence mechanism, compared to jasmonic acid.
Each chapter of this thesis was written as a scientific article, each with its own abstract, introduction, materials and methods, results and discussion, conclusion, acknowledgments, and references. The results obtained in this PhD thesis reaffirm the importance of lipidmediated signalling inherent to grapevine defence mechanisms against diseases. Understanding lipid-mediated signalling mechanisms paves the way for utilizing these molecules and their derivatives as powerful tools in promoting sustainable viticulture, highlighting their promise as agents in pest control.
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Vitis vinifera Downy mildew Lipids Elicitors Míldio Lípidos Eliciadores