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

The parasitic dodder (<i>Cuscuta</i>, Convolvulaceae) species have wide ranges of hosts. However, some plants, including the cultivated tomato (<i>Solanum lycopersicum</i>), have different degrees of resistance to <i>Cuscuta</i>. The cultivated tomato plants activate a strong hypersensitive response (HR) where <i>Cuscuta</i> haustoria penetrate stems of cultivated tomato, but the underlying mechanisms by which the cultivated tomato perceives <i>Cuscuta</i> 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 <i>Cuscuta australis</i> 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 <i>Cuscuta</i> 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 <i>CuRe1</i>. However, in the <i>cure1</i> mutants, JA and SA levels were still normally induced by <i>C. australis</i> parasitization. We propose a linear model that an unknown receptor perceives <i>Cuscuta</i> parasitization and thus triggers accumulation of JA and SA, which in turn induce the transcription of <i>CuRe1</i>, and CuRe1 and SOBIR1/SOBIR1-like thereby activate HR-based and non-HR-based resistance to <i>Cuscuta</i>. This study underscores the important roles of hormone signaling and <i>resistance</i> (<i>R</i>) genes in host plant-parasitic plant interactions.