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Enrichment of two important metabolites d-galacturonic acid and d-glucuronic acid inhibits MdHb1-mediated fruit softening in apple

Nature Plants volume 11, pages 891–908 (2025)Cite this article

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Abstract

In apples, fruit firmness is a crucial quality trait influencing fruit storability, transportability, shelf life and consumer preference. However, the genetic network underlying this trait remains unclear. Therefore, the present study investigated the changes in apple fruit at different stages of postharvest storage using a combination of transcriptomic and metabolomic analyses. With prolonged storage, we detected a significant increase in two metabolites, d-galacturonic acid (d-GalUA) and d-glucuronic acid (d-GlcA), which are associated with a key class 1 non-symbiotic haemoglobin (MdHb1). We innovatively found that MdHb1 regulates fruit softening by catalysing the conversion from protopectin to water-soluble pectin. Biochemical analysis demonstrated that MdMYB2/MdNAC14/MdNTL9 transcription factors directly bind to the MdHb1 promoter to activate its transcriptional expression and promote fruit softening. Further injection experiments in apple fruit and histological as well as transmission electron microscopy analyses of the fruit samples revealed that d-GalUA and d-GlcA reduce the transcription of MdHb1, or through the MdMYB2/MdNAC14/MdNTL9-MdHb1 regulatory module, thereby delaying fruit softening. Our study provides novel insights into the role of two important metabolites, d-GalUA and d-GlcA, in the regulation of MdHb1-mediated fruit softening in apples.

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Fig. 1: Texture of Malus pumila ‘Starking Delicious’ apple fruit during postharvest storage.
Fig. 2: Changes in gene expression and metabolism in apple fruit during postharvest storage.
Fig. 3: MdHb1 promotes apple fruit softening.
Fig. 4: MdMYB2, MdNAC14 and MdNTL9 bind to the MdHb1 promoter and activate its transcription.
Fig. 5: MdMYB2, MdNAC14 and MdNTL9 function upstream of MdHb1 and promote apple fruit softening.
Fig. 6: d-Galacturonic acid inhibits fruit softening.
Fig. 7: d-Galacturonic acid and d-glucuronic acid inhibit the expression of MdMYB2, MdNAC14, MdNTL9 and MdHb1.
Fig. 8: A proposed model indicating that d-GalUA/d-GlcA-mediated MdMYB2/MdNAC14/MdNTL9-MdHb1 module regulates fruit softening.

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Data availability

All data generated or analysed during this study are provided in this published article and its supplementary data files. Sequence data from this article can be found in the Genome Database for Rosaceae (https://www.rosaceae.org/) under accession numbers MdHb1 (MD00G1018700), MdMYB2 (MD16G1228600), MdNAC14 (MD01G1094400), MdNTL9 (MD01G1093700) and MdHSF24 (MD02G1171800). Transcriptome sequencing data are available under accession number PRJNA1124641. Identified metabolites were annotated using the KEGG Compound database (http://www.kegg.jp/kegg/compound/), and annotated metabolites were then mapped to the KEGG Pathway database (http://www.kegg.jp/kegg/pathway.html). Additional data related to this study are available from the corresponding author upon request. All biological materials used in this study are available from the corresponding author on reasonable request. Source data are provided with this paper.

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Acknowledgements

This work was supported by grants from the National Key Research and Development Program of China (2022YFD2100100, 2023YFD2301000), the National Natural Science Foundation of China (32122080) and the Key Research and Development Program of Shandong Province (2023CXGC010709), the Taishan Scholar Project Special Funds of China (Grant No. tsqnz20231206), and the China Postdoctoral Science Foundation (2023M742152).

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  1. These authors contributed equally: Yu-Wen Zhao, Ting-Ting Zhao, Quan Sun, Xiao-Long Liu.

Authors and Affiliations

  1. National Research Center for Apple Engineering and Technology; Shandong Collaborative Innovation Center of Fruit and Vegetable Quality and Efficient Production; College of Horticulture Science and Engineering, Shandong Agricultural University, Tai’an, Shandong, China

    Yu-Wen Zhao, Ting-Ting Zhao, Quan Sun, Xiao-Long Liu, Xiao-Yu Huang, Wan-Kun Li, Chu-Kun Wang, Wen-Yan Wang, Chang-Ning Ma, Xue-Sen Chen & Da-Gang Hu

  2. Shandong Institute of Pomology, Key Laboratory for Fruit Biotechnology Breeding of Shandong, Tai’an, Shandong, China

    Lin-Guang Li & Hai-Bo Wang

  3. Department of Horticulture, Agriculture College, Shihezi University, Shihezi, China

    Ying Xiang

  4. Section of Horticulture, School of Integrative Plant Science, Cornell University, Ithaca, NY, USA

    Lailiang Cheng

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Contributions

D.-G.H. conceived and designed the study. Y.-W.Z., T.-T.Z., Q.S. and X.-L.L. performed the experiments. X.-Y.H., L.-G.L., H.-B.W., W.-K.L., C.-K.W., W.-Y.W., Y.X., C.-N.M., X.-S.C. and L.C. analysed the data. D.-G.H., Y.-W.Z., T.-T.Z., Q.S. and X.-L.L. wrote the paper. All authors discussed the results and commented on the manuscript.

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Correspondence to Da-Gang Hu.

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Supplementary Appendix 1. Gene expression profiles of apple fruits at 0,15, and 45 days after harvest. Appendix 2. The abundance of metabolites in apple fruits at 0,15, and 45 days after harvest.

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Zhao, YW., Zhao, TT., Sun, Q. et al. Enrichment of two important metabolites d-galacturonic acid and d-glucuronic acid inhibits MdHb1-mediated fruit softening in apple. Nat. Plants 11, 891–908 (2025). https://doi.org/10.1038/s41477-025-01964-4

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