Arabidopsis alkaline ceramidase ACER functions in defense against insect herbivory

Plant sphingolipids are important membrane components and bioactive molecules in development and defense responses. However, the function of sphingolipids in plant defense, especially against herbivores, is not fully understood. Here, we report that Spodoptera exigua feeding affects sphingolipid metabolism in Arabidopsis, resulting in increased levels of sphingoid long-chain bases, ceramides, and hydroxyceramides. Insect-induced ceramide and hydroxyceramide accumulation is dependent on the jasmonate signaling pathway. Loss of the Arabidopsis alkaline ceramidase ACER increases ceramides and decreases long-chain base levels in plants; in this work, we found that loss of ACER enhances plant resistance to S. exigua and improves response to mechanical wounding. Moreover, acer-1 mutants exhibited more severe root-growth inhibition and higher anthocyanin accumulation than wild-type plants in response to methyl jasmonate treatment, indicating that loss of ACER increases sensitivity to jasmonate and that ACER functions in jasmonate-mediated root growth and secondary metabolism. Transcript levels of ACER were also negatively regulated by jasmonates, and this process involves the transcription factor MYC2. Thus, our findings reveal that ACER is involved in mediating jasmonate-related plant growth and defense and that jasmonates function in regulating the expression of ACER. Herbivore feeding affects Arabidopsis sphingolipid metabolism; alkaline ceramidase is regulated by the jasmonate pathway and its loss enhances plant resistance to Spodoptera exiguaand improves response to wounding and exogenous jasmonate.

Automated summary

Plant sphingolipids play important roles in membrane composition and defense responses. This study reveals that feeding by Spodoptera exigua affects sphingolipid metabolism in Arabidopsis, leading to increased levels of certain sphingolipids. The accumulation of these sphingolipids is dependent on the jasmonate signaling pathway. Loss of the alkaline ceramidase ACER enhances plant resistance to S. exigua and improves response to mechanical wounding and exogenous jasmonate, indicating the involvement of ACER in jasmonate-mediated plant defense and growth.