Sorbitol mediates age-dependent changes in apple plant growth strategy through gibberellin signaling

Abstract

Plants experience various age-dependent changes during juvenile to adult vegetative phase. However, the regulatory mechanisms orchestrating the changes remain largely unknown in apple (Malus domestica ). This study showed that tissue-cultured apple plants at juvenile, transition, and adult phase exhibit age-dependent changes in their plant growth, photosynthetic performance, hormone levels, and carbon distribution. Moreover, this study identified an age-dependent gene, sorbitol dehydrogenase (MdSDH1 ), a key enzyme for sorbitol catabolism, highly expressed in the juvenile phase in apple. Silencing MdSDH1 in apple significantly decreased the plant growth and GA3 levels. However, exogenous GA3 rescued the reduced plant growth phenotype of TRV- MdSDH1. Biochemical analysis revealed that MdSPL1 interacts with MdWRKY24 and synergistically enhance the repression of MdSPL1 and MdWRKY24 on MdSDH1, thereby promoting sorbitol accumulation during vegetative phase change. Exogenous sorbitol application indicated that sorbitol promotes the transcription of MdSPL1 and MdWRKY24. Notably, MdSPL1-MdWRKY24 module functions as key repressor to regulate GA-responsive gene, Gibberellic Acid-Stimulated Arabidopsis (MdGASA1 ) expression, thereby leading to a shift from the quick to the slow-growth strategy. These results reveal the pivotal role of sorbitol in controlling apple plant growth, thereby improving our understanding of vegetative phase change in apple.

Acknowledgements

We thank Prof. Jing Zhang (Horticulture Science Research Center, Northwest A&F University, Yangling, China) for the technical support. This work was supported by the National Key Research and Development Program of China (2023YFD2301000), the Earmarked Fund for the China Agriculture Research System (CARS-27), the Key S&T Special Projects of Shaanxi Province (2020zdzx03-01-02), and the Chinese Universities Scientific Fund (2452023067). We would like to thank MogoEdit (https://www.mogoedit.com) for its English editing during the preparation of this manuscript.

Author contributions

X.J. and F.M conceived and designed the experiments. C.L., X.J., S.X., Y.Q., and Z.Z performed the research. F.W., T.G., Y.J., X.L., and C.Y. analysed the data. X.J. and F.M wrote the paper. All authors approved this manuscript.

Data availability

The authors confirm that all experimental data are available and accessible via the main text and/or the supplemental data. Accession numbers: MdSDH1 (MD00G1005700), MdSPL1 (MD03G1230600), MdWRKY24 (MD11G1059400), MdGASA1 (MD02G1132400).

Conflict of interest statement

The authors declare no conflict of interest.

Supplementary data

Supplementary data is available at Horticulture Research online.

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