Phloem unloading in cultivated melon fruits follows an apoplasmic pathway during enlargement and ripening

Abstract Melon (Cucumis melo L.) has a long history of cultivation worldwide. During cultivation, domestication, and selection breeding, the sugar content of mature melon fruits has been significantly increased. Compared with unsweet melon and wild melon, rapid sucrose accumulation can occur in the middle and late stages of sweet melon fruit development. The phloem unloading pathway during the evolution and development of melon fruit has not been identified and analyzed. In this study, the phloem unloading pathway and the function of related sugar transporters in cultivated and wild melon fruits were analyzed by CFDA [5(6)-carbofluorescein diacetate] and esculin tracing, cytological pathway observation, qRT–PCR, and gene function analysis, etc. Results show that the phloem unloading pathway of wild melon fruit is largely symplastic, whereas the phloem unloading pathway of cultivated melon fruit shifts from symplastic to apoplasmic during development. According to a fruit grafting experiment, the fruit sink accumulates sugars independently. Correlation analysis showed that the expression amounts of several sucrose transporter genes were positively correlated with the sucrose content of melon fruit. Furthermore, CmSWEET10 was proved to be a sucrose transporter located on the plasma membrane of the phloem and highly expressed in the premature stage of sweet melon fruits, which means it may be involved in phloem apoplast unloading and sucrose accumulation in sweet melon fruits. Finally, we summarize a functional model of related enzymes and sugar transporters involved in the apoplast unloading of sweet melon fruits during enlargement and sucrose accumulation.