Abstract

Systemin is a plant signal peptide hormone involved in the responses to wounding and insect damage in the Solanaceae family. It works in the same signaling pathway of jasmonic acid (JA) and enhances the expression of proteinase inhibitors. With the aim of studying a role for systemin in plant antiviral responses, a tomato (Solanum lycopersicum) transgenic line overexpressing the prosystemin cDNA, i.e. the systemin precursor, was inoculated with Cucumber mosaic virus (CMV) strain Fny supporting either a necrogenic or a non-necrogenic satellite RNA (satRNA) variant. Transgenic plants showed reduced susceptibility to both CMV/satRNA combinations. While symptoms of the non-necrogenic inoculum were completely suppressed, a delayed onset of lethal disease occurred in about half of plants challenged with the necrogenic inoculum. RT-qPCR analysis showed a correlation between the systemin-mediated reduced susceptibility and the JA biosynthetic and signaling pathways (e.g. transcriptional alteration of lipoxygenase D and proteinase inhibitor II). Moreover, transgenically overexpressed systemin modulated the expression of a selected set of receptor-like protein kinase (RLK) genes, including some playing a known role in plant innate immunity. A significant correlation was found between the expression profiles of some RLKs and the systemin-mediated reduced susceptibility to CMV/satRNA. These results show that systemin can increase plant defenses against CMV/satRNA through transcriptional reprogramming of diverse signaling pathways.

Highlights

  • Systemin is a plant signal peptide hormone involved in the wound response and insect damage in the Solanaceae family [1, 2]

  • In a previous transcriptomic analysis, prosystemin transcript resulted approximately three-fold overexpressed in tomato plants infected by Cucumber mosaic virus (CMV) in combination with 77-satellite RNA (satRNA) (i.e., FN), compared to mock-inoculated plants

  • Transgenic prosystemin overexpression reduces the susceptibility of tomato to CMV/satRNA

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Summary

Introduction

Systemin is a plant signal peptide hormone involved in the wound response and insect damage in the Solanaceae family [1, 2] This 18 amino acids peptide is released from the C-terminal. A role of systemin in plant antiviral responses was supported by a previous transcriptomic analysis showing a prosystemin overexpression in tomato plants infected by Cucumber mosaic virus (CMV) associated with a necrogenic variant of its satellite RNA (satRNA; Cillo F., unpublished). With the aim of elucidating the molecular mechanisms that may network the systemin signaling with antiviral defenses and necrosis development, we evaluated the prosystemin overexpression effects on the susceptibility of tomato to CMV/satRNA, and analyzed the transcriptomic changes on a set of stress hormone and receptor-like kinase (RLK) genes. Our data shed new light on the systemin-mediated defense network, and show functional implications for diverse molecular pathways of tomato-virus interaction

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