Mobile transcriptome profiling reveals pumpkin-derived CmoHSP83 and CmoCAT2 mRNAs enhancing salt tolerance in grafted cucumber

Abstract

Grafting cucumber onto salt-tolerant pumpkin rootstocks is widely used to alleviate salt stress, yet the contribution of long-distance mRNA signaling to rootstock-conferred salt tolerance remains unclear. In this study, using reciprocal cucumber/pumpkin heterografts with SNP-resolved tracking, we demonstrate that salt stress rewires long-distance mRNA trafficking. Salinity imposes a pronounced directional bias, favouring mRNA export from the tolerant pumpkin to the sensitive cucumber while limiting reverse flux, irrespective of graft configuration. This identifies directional RNA mobility as an emergent property of salt stress adaptation. Among pumpkin-derived mobile transcripts, CmoHSP83 and CmoCAT2 were strongly enriched in cucumber scions and selected for functional validation. Their long-distance mobility was confirmed using transgenic hairy-root systems, species-specific RT–PCR, SNP-informed Hi-TOM sequencing, and GUS assays. Rootstock overexpression of either gene enhanced salt tolerance in grafted cucumber, accompanied by reduced ROS accumulation and improved Na +/K+ homeostasis. Collectively, these findings establish mobile mRNAs as functional long-distance signals in rootstock–scion communication under salinity and provide mechanistic insights into pumpkin rootstock-conferred systemic salt adaptation in grafted cucumber.