Integrated transcriptomic and metabolic analysis reveal the mechanism controlling cucumber-pumpkin grafting compatibility.

Background: The most widely used rootstock of cucumber grafting is pumpkin (Cucurbita moschata). The main task of pumpkin rootstock breeding is to evaluate its compatibility with cucumber scions. One of the main factors affecting grafting compatibility is the rootstock bleeding sap, which affects the wound healing of graft junction.

Results: We evaluated the grafting affinity of 30 pumpkin rootstocks, which were F1 hybrids derived from 56 breeding lines, by grafting them with the cucumber scion FH8. Correlation analysis of grafting compatibility with phenotypic traits of rootstock seedlings, grafted plants, and biochemical characteristics of rootstock bleeding sap highlighted the positive role of soluble solids content and the negative role of the absorbance of bleeding sapsmeasured at multiple wavelengths (from 280 nm to 700 nm). Bleeding saps from three rootstocks (RS50, RS83, and RS55) with different grafting compatibility were assayed by ultra-performance liquid chromatography-tandem mass spectrometry (UPLC-MS/MS). The predominant content in bleeding saps was amino acids. Compared with self-rooted-grafting, intergeneric grafting caused changes in the pathways associated with "abiotic stress responses", "ribosome" and "plant hormone signal transduction" in integrated transcriptomic and metabolic analysis. When compared with the bleeding sap of RS50 (BS-RS50) with low grafting compatibility, BS-RS55 with high grafting compatibility contained much lower content of flavonoids such as nicotiflorin, lonicerin, isoquercitrin and isovitexin. A similar difference profile of these flavonoids was not observed in cucumber scions, although flavonoid pathway was also affected by grafting in scions.

Conclusion: Pumpkin rootstocks show a big variation in grafting compatibility with cucumbers scions, which at least partially depends on the nutrients (bleeding saps) transported from rootstocks to scions. Flavonoids play a negative role in pumpkin-cucumber grafting compatibility.