Aprile, Anna Maria (2023) Systemin and Prosystemin: novel benefits for sustainable protection of tomato crop. [Tesi di dottorato]

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Abstract

The variations in global climate have increased the attention of researchers worldwide, as these changes negatively affect agriculture by reducing crop productivity and food security. Climate change is a dynamic, complex system of alterations of environmental conditions that affect abiotic and biotic components of the world. It results in alteration in environmental conditions such as intensity of rainfall, soil salt concentration and temperature that lead to rise in new pests, weeds and pathogens. To overcome the impact of abiotic stressors, many strategies could be considered to support plant growth including the use of chemical induction of endogenous defense. Recent research suggests that chemical induction is a promising field in crop stress management because plants can be prepared (or primed) by chemical agents to increase their tolerance to various environmental stresses. To overcome pesticide drawbacks, growing interest has arisen in plant biotechnology towards the study of new molecules able to prevent, reduce or eradicate plant pests. In the current scenario, plant resistance inducers, acting by stimulating plant defense mechanisms, are seen as an eco-friendly and promising option to conventional pesticides, and their implementation in integrated pest management strategy is strongly encouraged. The tomato peptide Systemin (Sys) proved to be a very effective activator of plant defense in tomato, grapevine, and eggplant. It is an octadecapeptide proteolytically released, upon wounding and herbivore attack, from its precursor Prosystemin (ProSys). The interaction of Sys with its receptor activates the octadecanoid pathway and the production of Jasmonic Acid (JA), its derivatives and other molecules able to interfere with the colonization of fungal pathogens (e.g., the necrotrophic fungus Botrytis cinerea) or the growth and survival of insect pests (e.g., the noctuid moth Spodoptera littoralis). A novel approach to increase plant disease control is to combine different resistance inducers (e.g., chemical and/or biological). In chapter 1, we show that plant treatment with Trichoderma afroharzianum T22, one of the most widely used plant beneficial fungi in agriculture, and Sys confers protection against the fungal pathogen Fusarium oxysporum, and the insect pest Tuta absoluta. The observed defensive response was associated with an increase of JA and the expression of related genes and metabolites, and a decrease of Salicylic acid and its metabolites. Since plant responses to biotic and abiotic stress agents have some overlapping component, we investigated a possible role of Sys in plant protection from salt stress. We report that a soil drench of Sys solution increases salt stress tolerance by the upregulation of sodium transporters, and the enhancement of the cellular antioxidant power. Several evidences reported that the state of induced defense can be maintained through generations. In chapter 2, we show that Sys treatment induces a long-term stress memory since the progeny of treated plants showed reduced B. cinerea damages when attacked. Transcriptomic data of parental plants 24h post Sys treatments revealed an overlap of 768 differentially expressed genes (DEGs) with those of their progeny suggesting that Sys treatment induces a signal that is transmitted to progeny. Since stress memory can be programmed epigenetically, we investigated the epigenetic regulation of a subset of defense related DEGs common to both transcriptomic datasets, showing that the promoter region of PAL gene was enriched with an increased level of tri-methylation of lysine 4 on histone H3, a chromatin mark generally associated with gene activation. Sys was traditionally considered as the main actor of tomato resistance. Recent evidences suggest that ProSys is not only the precursor of Sys peptide but likely contribute itself to defense responses. Two different ProSys fragments, not including Sys, were used in bioassays to evaluate their biological activity. In chapter 3, we proved that both fragments were active at femtomolar concentration, being able to modulate the expression of defense-related genes and protect tomato plants against noctuid moth and a necrotrophic fungal pathogen. Interestingly, the biological activity of the two fragments is not overlapping for both and for Sys and does not show any toxicity on non-target organisms. The identification of these novel protein fragments may lead to a better understanding of ProSys defense mechanism. In addition, they represent novel tools to enhance plant stress resilience reducing the use of agrochemicals.

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