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.

Acknowledgements

We thank Professor Huaisong Wang (Chinese Academy of Agricultural Sciences) for providing melon seeds and thank Professor Chunlong Li (Huazhong Agricultural University) for providing yeast strain CSY4000. We thank Muhammad Mohsin Kaleem for his critical reading and editing of the manuscript. We also thank Jianbo Cao and Limin He (Huazhong Agricultural University) for transmission electron microscope support. This work was supported by the National Natural Science Foundation of China (31972435), the National Key Research and Development Program of China (2019YFD1000300), the Fundamental Research Funds for the Central Universities (2662018QD062), and the China Agriculture Research System of MOF and MORA (CARS-25).

Author contributions

J.C., Y.Z., and Z.B. conceived and designed the experiments. Y.Z. performed most of the experiments and analyzed the data. K.L. identified the functional characteristics and subcellular localization of SWEET protein. D.Y., P.Z., and J.C. performed the CFDA and tracing experiment. S.W. measured the sugar content. Z.W. and Y.Z. performed the qRT–PCR. Y.Z. and J.G. conducted the fruit grafting experiment. Y.Z. prepared the figures and tables and wrote the first draft of the manuscript with assistance from S.W. J.C. revised the manuscript and figures.

Data availability

Relevant data can be found within the paper and its supporting materials. All data from this study are available from the corresponding author upon reasonable request.

Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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