Environment-Dependent Switch between Two Immune Systems against Ralstonia solanacearum Infections in Pepper

Abstract

AbstractAlthough plant diseases generally cause more severe symptoms under conditions of high temperature and high humidity(HTHH), how plant respond to pathogen attack under this condition remains elusive.As an example, we herein comparatively studied pepper(Capsicum annuum) immunity against Ralstonia solanacearum under HTHH and ambient temperature by approaches of reverse genetics. We found that pepper respond to R.solanacearum infection by activating salicylic-acid- and jasmonic-acid-mediated immunity at ambient temperature. Under HTHH, However, it no longer activates JA-mediated immunity and activates only transient SA signaling at the early stage of R.solanacearum infection, but instead induces cytokinin mediated immunity.These two immune systems are positively regulated by CaWRKY40 via binding the WT-box and a novel W-box like (WL) box, respectively, in an environment-dependent manner: CaWRKY40 is activated upon R. solanacearum infection under HTHH, thereby upregulating ISOPENTENYLTRANSFERASE5(IPT5). The resulting cytokinin then works synergistically with CaWRKY40 in activating a subset of glutathione S-transferase genes via chromatin activation and WL-box binding, but prevent CaWRKY40 from activating ISOCHORISMATE SYNTHASE1 (ICS1) or SA-/JA-dependent pathogenesis-related genes by chromatin inactivation or by blocking WT-box binding.These results highlight the specific pepper immune response to R. solanacearum infection under HTHH and its synergistic activation by CaWRKY40 and cytokinins.