Grafting with pumpkin rootstock is commonly used not only to improve the quality of cucumber fruits but also to confer biotic or abiotic stress tolerance. However, the molecular mechanism of the response of grafted cucumbers to drought stress and the possible roles of mobile mRNAs in improving stress tolerance have remained obscure. Hence, we conducted transcriptome sequencing and combined it with morphophysiological experiments to compare the response of homografts (cucumber as scion and rootstock) and heterografts (cucumber as scion and pumpkin as rootstock) to drought stress. After applying drought stress, homografts and heterografts expressed 2960 and 3088 genes, respectively, in response to the stress. The differentially expressed genes identified in heterografts under drought stress were categorized into different stress-responsive groups, such as carbohydrate metabolism (involved in osmotic adjustment by sugar accumulation), lipid and cell wall metabolism (involved in cell membrane integrity by a reduction in lipid peroxidation), redox homeostasis (increased antioxidant enzyme activities), phytohormone (increased abscisic acid content), protein kinases, and transcription factors, using MapMan software. Earlier and greater H₂O₂ accumulation in xylem below the graft union was accompanied by leaf abscisic acid accumulation in heterografts in response to drought stress. Greater leaf abscisic acid helped heterografted cucumbers to sense and respond to drought stress earlier than homografts. The timely response of heterografts to drought stress led to the maintenance of higher water content in the leaves even in the late stage of drought stress. The mobile mRNAs identified in heterografts were mostly related to photosynthesis, which would be the possible reason for improved chlorophyll content and maximum photochemical efficiency of photosystem II (Fv/Fm). The existence of some stress-responsive pumpkin (rootstock) mRNAs in cucumber (scion), such as heat shock protein (HSP70, a well-known stress-responsive gene), led to higher proline accumulation than in homografts. Expression of mobile and immobile stress-responsive mRNAs and timely response of heterografts to drought stress could improve drought tolerance in pumpkin-rooted plants.

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