Jasmonic acid and salicylic acid transcriptionally regulate CuRe1 in cultivated tomato to activate resistance to parasitization by dodder Cuscuta australis

The parasitic dodder (Cuscuta, Convolvulaceae) species have wide ranges of hosts. However, some plants, including the cultivated tomato (Solanum lycopersicum), have different degrees of resistance to Cuscuta. The cultivated tomato plants activate a strong hypersensitive response (HR) where Cuscuta haustoria penetrate stems of cultivated tomato, but the underlying mechanisms by which the cultivated tomato perceives Cuscuta and activates resistance remain unclear. In this study, we show that the phytohormones jasmonic acid (JA) and salicylic acid (SA) in cultivated tomato stems were highly induced by Cuscuta australis parasitization. Genetic analyses and experiments of supplementation of JA or SA indicated that the JA and SA pathway not only are both required for activation of HR against Cuscuta parasitization but also function in non-HR-based resistance. The Cuscuta Receptor 1 (CuRe1), which is a leucine-rich repeat receptor-like protein, and suppressor of BAK1-interacting receptor kinase (SOBIR1) and SOBIR1-like, two adaptor kinases, are also important for HR-based and non-HR-based resistance. Importantly, we found that the JA and SA pathway both transcriptionally regulate CuRe1. However, in the cure1 mutants, JA and SA levels were still normally induced by C. australis parasitization. We propose a linear model that an unknown receptor perceives Cuscuta parasitization and thus triggers accumulation of JA and SA, which in turn induce the transcription of CuRe1, and CuRe1 and SOBIR1/SOBIR1-like thereby activate HR-based and non-HR-based resistance to Cuscuta. This study underscores the important roles of hormone signaling and resistance (R) genes in host plant-parasitic plant interactions.