Virus-induced drought tolerance presents a fascinating facet of biotic-abiotic interaction in plants, yet its molecular intricacies remain unclear. Our study shows that cowpea mild mottle virus (CPMMV) infection enhances drought tolerance in common bean (Phaseolus vulgaris) plants through a virus-derived small interfering RNA (vsiRNA)-activated autophagy pathway. Specifically, a 21-bp vsiRNA originating from the CPMMV Triple Gene Block1 (TGB1) gene targeted the 5' untranslated region (UTR) of the host Teosinte branched 1, Cycloidea, Proliferating Cell Factor (TCP) transcription factor gene PvTCP2, independent of the known role of TGB1 as an RNA silencing suppressor. This targeting attenuated the expression of PvTCP2, which encodes a transcriptional repressor, and in turn upregulated the core autophagy-related gene (ATG) PvATG8c, leading to activated autophagy activity surpassing the level induced by drought or CPMMV infection alone. The downstream EARLY RESPONSIVE TO DEHYDRATION (ERD) effector PvERD15 is a homologue of Arabidopsis thaliana AtERD15, which positively regulates stomatal aperture. PvERD15 was degraded in PvATG8c-mediated autophagy. Therefore, we establish a TGB1-PvTCP2-PvATG8c-PvERD15 module as a trans-kingdom fine-tuning mechanism that contributes to virus-induced drought tolerance in plant-drought-virus interactions.

Grafting technology can improve the yield and quality of crops. In this study, we investigated the effects of grafting on watermelon using transcriptomic and metabolomic analysis. A total of 216 differentially accumulated metabolites (DAMs) were identified between pumpkin-grafted watermelon and self-grafted watermelon. KO (Kyoto Encyclopedia of Genes and Genomes Orthology) analysis revealed that the DAMs were mainly enriched in the flavone and flavonol biosynthesis pathway. In addition, high levels of phloretin and citric acid were found in pumpkin-grafted watermelon, which contributes to fruit quality. Meanwhile, compounds such as olivetol and ferulaldehyde, which confer a bitter taste, were downregulated in pumpkin-grafted watermelon. The transcriptome data indicated that the differentially expressed genes (DEGs) identified in the pulp were enriched in fructose and mannose metabolism, biosynthesis of secondary metabolites, and flavone and flavonol biosynthesis pathways. Moreover, genes related to the microtubule, cell wall, and fiber were highly expressed in the stem of pumpkin-grafted watermelon, suggesting that grafting could change the structure of the stem and improve the quality of watermelon fruit. Our study provides a comprehensive picture of the transcriptional and metabolic profile of watermelon induced by grafting, which furthers our understanding of the molecular mechanisms involved in improving watermelon fruit quality by grafting.

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.