MdVQ17 negatively regulates apple resistance to Glomerella leaf spot by promoting MdWRKY17-mediated salicylic acid degradation and pectin lyase activity

Abstract

Glomerella leaf spot (GLS) is a fungal disease caused by Colletotrichum fructicola, which severely restricts the yield and quality of apples. Valine-glutamine (VQ) proteins are transcriptional regulators involved in the regulation of plant growth and stress responses. However, little is known about the role of VQ proteins in the biotic stress response in apple. Here, a VQ gene, MdVQ17, that was highly induced by C. fructicola infection was identified. Overexpression of MdVQ17 in apple increased susceptibility to C. fructicola and significantly reduced the salicylic acid content and β-1,3-glucanase and chitinase activities. Based on yeast two-hybrid screening, MdWRKY17, which promotes susceptibility to C. fructicola, was identified as an MdVQ17-interacting protein. Co-expression of MdVQ17 can promote the binding and transcriptional activation activity of MdWRKY17 on the promoter of Downy Mildew Resistant 6 (MdDMR6), thereby promoting MdWRKY17-mediated salicylic acid degradation. Based on DNA affinity purification sequencing, the pectin lyase-encoding gene MdPL-like was identified as a direct target of MdWRKY17. MdWRKY17 can directly bind to the promoter of MdPL-like and activate its transcription, and the binding and activation of MdWRKY17 on the MdPL-like promoter were significantly enhanced by MdVQ17 co-expression. Functional identification showed that MdPL-like promoted pectin lyase activity and susceptibility to C. fructicola. In sum, these results demonstrate that the MdVQ17-MdWRKY17 module mediates the response to C. fructicola infection by regulating salicylic acid accumulation and pectin lyase activity. Our findings provide novel insights into the mechanisms by which the VQ-WRKY complex modulates plant pathogen defense responses.

Acknowledgements

We thank Prof. Zhihong Zhang (Shenyang Agricultural University) for providing the GL-3 apple plants. We also thank Prof. Jing Zhang and Ms Beibei He of the Horticulture Science Research Center, NWAFU, for their technical support in this work. This work was supported by the Postdoctoral Fellowship Program of CPSF (GZC20232160), the Postdoctoral Research Project of Shaanxi Province (2023BSHYDZZ72), the Key S&T Special Projects of Shaanxi Province (2020zdzx03-01-02), and the China Agriculture Research System of MOF and MARA (CARS-27).

Author contributions

D.D., J.Y., K.M., and F.M. conceived the project and wrote the manuscript. D.D., R.Y., Q.D., M.S., and J.H. conducted the experiments.

Data availability

The sequencing information presented in this paper is available on the Apple Genome Database (https://iris.angers.inra.fr/gddh13/) as follows: MdVQ17 (MDP0000856686), MdWRKY17 (MD12G1181000), MdDMR6 (MD10G1053200), and MdPL-like (MD00G1117900). All data in this study are provided in the article and its supplementary materials.

Conflict of interest statement

The authors declare that there is no conflict of interest.

Supplementary data

Supplementary data are available at Horticulture Research online.

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