The fungi effector VmRnt2 from Valsa mali modulates host transcription factor to suppress immunity in apple

Abstract

Apple Valsa canker (AVC), a disease instigated by Valsa mali (syn. Cytospora mali), poses a significant global threat to apple cultivation. Throughout its infection process, V. mali introduces an array of effector proteins into the host cells aimed at undermining the host immune defenses. The exact molecular mechanisms through which these effectors manipulate host transcription factors (TFs) to promote pathogenesis are not fully understood. This study identifies a ribonuclease T2-like effector, VmRnt2, that notably inhibits INF1-triggered cell death, chitin-induced reactive oxygen species bursts, and callose deposition. Knockout of the VmRnt2 gene markedly reduced the virulence of V. mali, without impacting fungal growth or spore production. Conversely, heterologous expression of VmRnt2 in Nicotiana benthamiana and apple markedly enhanced susceptibility to infections by Sclerotinia sclerotiorum and V. mali, respectively, highlighting its pivotal role in facilitating pathogenicity. VmRnt2 was found to interact specifically with an apple TF, MdMYB44, which belongs to the myeloblastosis (MYB) family of proteins. Further functional assays revealed that overexpression of MdMYB44 in apple enhances resistance to V. mali. Additionally, MdMYB44 was shown to bind specifically to the promoter of the defense-related gene MdPR1A, subsequently activating its transcription. Importantly, during V. mali infection, VmRnt2 disrupts the DNA-binding activity of MdMYB44. Collectively, our results elucidate how V. mali employs VmRnt2 to compromise MdMYB44-mediated immune regulation, thereby facilitating the pathogen’s colonization of apple trees.

Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (Grant No. 32330089) and Shenzhen Science and Technology Innovation Program (JCYJ20220530161405012).

Author contributions

L.X. and L.H. conceived the project and designed the research. H.L., P.D., X.G., S.C., and Q.Z. performed the experiments and analyzed data. Q.Z. and S.C. gave suggestion for this research. H.L. and P.D. wrote the manuscript. All authors reviewed and approved the manuscript for publication.

Data availability

All relevant data can be found within the published article and its supporting material.

Conflicts of interest statement

The authors declare no conflicts of interest.

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