Compost tea enhances volatile content in tomato fruits via SlERF.E4-activated SlLOX expression

Abstract Aroma volatiles, essential for tomato fruit flavor, have been reported to accumulate more abundantly in fruits from plants cultivated with compost tea. However, the underlying molecular mechanisms by which compost tea regulates aroma volatile synthesis in tomato (Solanum lycopersicum L.) fruit remains elusive. Here, we found that compost tea treatment significantly increased the content of volatiles derived from fatty acids in tomato fruit. Transcriptional analysis revealed that compost tea treatment up-regulated the expression of linolenic acid metabolic pathway LOX genes (SlLOXD and SlLOXE). Furthermore, overexpression of SlLOXD and SlLOXE enhanced the volatiles in fruit, while compost tea treatment failed to increase volatiles content in loxd and loxe mutants. Interestingly, compost tea treatment increased the level of ACC, a precursor of ethylene. Treatment with an ethylene signaling inhibitor 1-methylcyclopropene (1-MCP) negated the aroma enhancement effect of compost tea on tomato fruits. SlERF.E4, a transcription factor responsive to ethylene signaling, was found to bind to the promoters of SlLOXD and SlLOXE. Overexpression of SlERF.E4 led to increased expression of SlLOXD and SlLOXE, as well as elevated fruit volatile content. Indeed, aroma enhancement in the SlERF.E4-overexpressed tomatoes was not affected by 1-MCP. These findings shed light on the molecular mechanisms underlying the improvement of flavor in organic fruits and provide valuable insights for the development of strategies in organic agriculture.