Fumonisin B1–Induced Cell Death in Arabidopsis Protoplasts Requires Jasmonate-, Ethylene-, and Salicylate-Dependent Signaling Pathways

Abstract

We have established an Arabidopsis protoplast model system to study plant cell death signaling. The fungal toxin fumonisin B1 (FB1) induces apoptosis-like programmed cell death (PCD) in wild-type protoplasts. FB1, however, only marginally affects the viability of protoplasts isolated from transgenic NahG plants, in which salicylic acid (SA) is metabolically degraded; from pad4-1 mutant plants, in which an SA amplification mechanism is thought to be impaired; or from jar1-1 or etr1-1 mutant plants, which are insensitive to jasmonate (JA) or ethylene (ET), respectively. FB1 susceptibility of wild-type protoplasts decreases in the dark, as does the cellular content of phenylalanine ammonia-lyase, a light-inducible enzyme involved in SA biosynthesis. Interestingly, however, FB1-induced PCD does not require the SA signal transmitter NPR1, given that npr1-1 protoplasts display wild-type FB1 susceptibility. Arabidopsis cpr1-1 , cpr6-1 , and acd2-2 protoplasts, in which the SA signaling pathway is constitutively activated, exhibit increased susceptibility to FB1. The cpr6-1 and acd2-2 mutants also constitutively express the JA and ET signaling pathways, but only the acd2-2 protoplasts undergo PCD in the absence of FB1. These results demonstrate that FB1 killing of Arabidopsis is light dependent and requires SA-, JA-, and ET-mediated signaling pathways as well as one or more unidentified factors activated by FB1 and the acd2-2 mutation. INTRODUCTIONPlant cell death is often the consequence of plant-pathogen interactions in both compatible and incompatible relationships (Greenberg, 1997). A notable example is localized cell collapse, called the hypersensitive response (HR), which is induced rapidly in a resistant plant at the infection site of an avirulent pathogen (Staskawicz et al., 1995; Bent, 1996; Dangl et al., 1996; Hammond-Kosack and Jones, 1996). Hypersensitive cell death, which is distinct from necrosis caused by metabolic toxins or severe trauma, is genetically programmed (programmed cell death [PCD]) and requires active host cell metabolism Morel and Dangl, 1997;Pennell and Lamb, 1997; Gilchrist, 1998; Gray and Johal, 1998; Heath, 1998;Richberg et al., 1998). In fact, plant cells undergoing the HR display several molecular and morphological markers characteristic of animal apoptosis (a specialized form of PCD), including systematic DNA degradation and formation of apoptotic-like bodies, which suggests that the terminal steps in PCD are well conserved in animals and plants (Levine et al., 1996;Ryerson and Heath, 1996; Wang et al., 1996). It remains to be determined, however, whether the signal transduction mechanisms leading to the onset of PCD are also equally conserved between the two kingdoms.Salicylic acid (SA) is the best-characterized signaling molecule in plant defense responses (Ryals et al., 1996; Delaney, 1997; Durner et al., 1997). Application of exogenous SA or SA analogs activates the expression of a variety of pathogenesis-related ( PR ) genes and enhances resistance to a variety of pathogens (W...

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