Root-to-shoot mobile mRNA CmoKARI1 promotes JA-Ile biosynthesis to confer chilling tolerance in grafted cucumbers.

Pumpkin rootstock is commonly used to graft cucurbit crops, improving their ability to withstand stress. While the significance of systemic signals from rootstocks to scions is recognized, the role of root-to-shoot transported mRNAs remains understudied. Cucumber plants often face growth and productivity limitations due to low temperatures. To shed light on the enhancement of chilling tolerance in grafted cucumber scions by pumpkin-derived mRNAs, we revisit the metabolomic and transcriptomic dataset from the cucumber/pumpkin heterograft under chilling condition. We identify pumpkin Ketol-acid reductoisomerase 1 (CmoKARI1) as the key mobile mRNA that specifically travels from pumpkin rootstock to cucumber scion upon early chilling stress. Overexpressing CmoKARI1 results in increased isoleucine level and chilling tolerance in both cucumber and Arabidopsis. The increased isoleucine is further used to synthesize JA-Ile conjugates, activating JA-Ile signaling and enabling heterografts to weather low temperatures. This study represents the instance of a unidirectional mobile mRNA triggered by specific environmental cues.