Fungal pathogen: A game changer for insect herbivore in sequential attack on tomato

Abstract

Plants have several means of coping with biotic stress, which involves physiological, cellular and molecular mechanisms. The interplay of two principal phytohormonal pathways, Jasmonic acid (JA) and Salicylic acid (SA) play a crucial role in transmitting stress-induced signals throughout the plant. However, the interplay of these hormonal pathways is not clear when plants encounter biotic agents that trigger antagonistic hormonal signals. To address this, we conducted biochemical and gene expression studies on tomato, Solanum lycopersicum plants, exposed to insect alone (IA), fungus alone (FA), or sequential dual stress with fungi followed by insect (FI) and insect followed by fungi (IF), with untreated control. We also assessed the performance of late-arriving conspecific herbivore on these plant sets. The total phenol, and non-tannin phenols content in IF and FI plants showed similar increase or decrease as FA and IA plants, respectively. Gene expression analysis revealed that JA-related genes (MYC2) were dominant in FI plants, while SA-related genes (PR1) were upregulated in IF plants. Moreover, late-arriving herbivores showed significantly decreased relative growth rate, efficiency of conversion of ingested food (ECI) and digested food (ECD) when feeding on FA and IF plants, indicating that sequential treatments substantially induce plant responses. However, herbivory did not affect the late-arriving conspecific herbivore. Thus, biochemical responses and hormonal interplay of the plant are influenced by both sequence as well as the duration of the biotic stress. Furthermore, while the late-arriving conspecific herbivore is negatively affected by the presence of a pathogen, it remains unaffected by previous herbivory.