Prosystemin Overexpression in Tomato Enhances Resistance to Different Biotic Stresses by Activating Genes of Multiple Signaling Pathways

Abstract

Systemin is a signal peptide that promotes the response to wounding and herbivore attack in tomato. This 18-amino acid peptide is released from a larger precursor, prosystemin. To study the role of systemin as a modulator of defense signaling, we generated tomato (Solanum lycopersicum) transgenic plants that overexpress the prosystemin cDNA. We carried out a transcriptomic analysis comparing two different transgenic events with the untransformed control. The Gene Ontology categories of the 503 differentially expressed genes indicated that several biological functions were affected. Systemin promotes the expression of an array of defense genes that are dependent on different signaling pathways and it downregulates genes connected with carbon fixation and carbohydrate metabolism. These alterations present a degree of overlap with the response programs that are classically associated to pathogen defense or abiotic stress protection, implying that end products of the systemin signaling pathway may be more diverse than expected. We show also that the observed transcriptional modifications have a relevant functional outcome, since transgenic lines were more resistant against very different biotic stressors such as aphids (Macrosiphum euphorbiae), phytopathogenic fungi (Botrytis cinerea and Alternaria alternata) and phytophagous larvae (Spodoptera littoralis). Our work demonstrated that in tomato the modulation of a single gene is sufficient to provide a wide resistance against stress by boosting endogenous defense pathways. Overall, the data provided evidence that the systemin peptide might serve as DAMP signal in tomato, acting as a broad indicator of tissue integrity.Electronic supplementary materialThe online version of this article (doi:10.1007/s11105-014-0834-x) contains supplementary material, which is available to authorized users.

Prosystemin, a prohormone that modulates plant defense barriers, is an intrinsically disordered protein

“…These multiple functions appear to be strictly correlated with the IDP nature of LEA that work as a hub interacting with multiple partners . Similarly, the disordered nature of Prosys may promote selective binding of several partners as well as integrate signals from multiple stress agents supporting the hypothesis that Prosys has a biological function other than being an intermediate in the synthesis of Sys. Interestingly, as reported for genes encoding IDPs or disordered domains that originated by duplication and module exchange, Prosys gene is thought to be originated through duplication and elongation events …”

“…In tomato, these events are triggered by a peptide hormone named Systemin (Sys) . The signaling molecule is an octadecapeptide intensely investigated over the years which, upon wounding, is released from the C‐terminal region of a larger pro‐hormone of 200 amino acids called Prosystemin (Prosys) by means of a molecular mechanism still unknown …”

“…Conversely, plants expressing Prosys cDNA in anti‐sense orientation showed a nearly complete suppression of PIs production upon wounding associated with a reduced capacity to limit the feeding damage by Manduca sexta larvae . The constitutive production of Prosys in tomato plants resulted in an increased resistance not only against chewing larvae but also against phytopathogenic fungi and aphids . Moreover, transgenic plants showed indirect defenses reinforced, being more attractive towards parasitoids and predators of their insect pests and show an increased plant resistance to saline stress .…”

The expression of the tomato prosystemin in tobacco induces alterations irrespective of its functional domain

“…Furthermore, differences between MZ119 and the two PRO8 lines were present only for the GST gene. Pin II was overexpressed in both types of transgenic lines, although at a level that is much lower than in tomato plants overexpressing the prosystemin (Coppola et al 2015). The relative quantification of the expression level of tobacco hydroxyproline-rich glycopeptides HypSys I and II showed an overexpression in both types of transgenic lines.…”

Tomato tolerance to abiotic stress: a review of most often engineered target sequences

“…This eighteenth-amino-acid-long molecule was isolated from tomato leaves, where it is synthesized as a protein precursor-prosystemin (Coppola et al 2015). Grafting experiments showed that, in tomato plants containing prosystemin transgene (transformed rootstock), a systemic signal responsible for production of high content of proteinase inhibitor in undamaged leaves (nontransformed scion) was present (McGurl et al 1994).…”