Rootstock-Scion Exchanging mRNAs Participate in Watermelon Fruit Quality Improvement

Grafting significantly enhances plant quality, including stress resistance and fruit quality. We previously found that grafting watermelon onto pumpkin can alter the metabolite content, but the involvement of mobile RNA was unclear. Here, we established and comprehensively analyzed mobile mRNA (mb-mRNA) profiles, transcriptomes, and metabolomes between the rootstock (pumpkin) and scion (watermelon). A total of 834 mobile RNAs were identified in the pulp and stem of pumpkin-grafted watermelon. GO (Gene Ontology) and KO (Kyoto Encyclopedia of Genes and Genomes Orthology) analyses revealed photosynthesis- and carbon fixation-related mobile RNAs (e.g., Photosystem II D2, P700 chlorophyll a apoprotein) in the watermelon pulp and cell division-related mobile RNAs in the stem. Additionally, transcription factors like MADS and DNAJ exhibited mobility. The secondary structure prediction of the MADS-box transcription factor (CmoCh20G002790) showed multiple loop structures (e.g., internal and hairpin loops) related to its mobility. An integrated analysis of transcript and metabolite profiles indicated that photosynthesis-related products are regulated not only by the scion's own RNA but also by mb-mRNA synthesized by the rootstock. This research advances our understanding of grafting's molecular mechanisms and provides insights for improving crop quality and sustainability in agriculture.