A putative E3 ubiquitin ligase substrate receptor degrades transcription factor SmNAC to enhance bacterial wilt resistance in eggplant

Abstract

Bacterial wilt caused by Ralstonia solanacearum is a severe soil-borne disease globally, limiting the production in Solanaceae plants. SmNAC negatively regulated eggplant resistance to Bacterial wilt (BW) though restraining salicylic acid (SA) biosynthesis. However, other mechanisms through which SmNAC regulates BW resistance remain unknown. Here, we identified an interaction factor, SmDDA1b, encoding a substrate receptor for E3 ubiquitin ligase, from the eggplant cDNA library using SmNAC as bait. SmDDA1b expression was promoted by R. solanacearum inoculation and exogenous SA treatment. The virus-induced gene silencing of the SmDDA1b suppressed the BW resistance of eggplants; SmDDA1b overexpression enhanced the BW resistance of tomato plants. SmDDA1b positively regulates BW resistance by inhibiting the spread of R. solanacearum within plants. The SA content and the SA biosynthesis gene ICS1 and signaling pathway genes decreased in the SmDDA1b-silenced plants but increased in SmDDA1b-overexpression plants. Moreover, SmDDB1 protein showed interaction with SmCUL4 and SmDDA1b and protein degradation experiments indicated that SmDDA1b reduced SmNAC protein levels through proteasome degradation. Furthermore, SmNAC could directly bind the SmDDA1b promoter and repress its transcription. Thus, SmDDA1b is a novel regulator functioning in BW resistance of solanaceous crops via the SmNAC-mediated SA pathway. Those results also revealed a negative feedback loop between SmDDA1b and SmNAC controlling BW resistance.

Acknowledgements

We thank Chuhao Li (South China Agricultural University) for his help in drawing figures and Lianhui Zhang (South China Agricultural University) for providing the GMI1000 strain.

This research was funded by the Key R&D Projects in Guang-dong Province (2022B0202080003), the Key Project of Guangzhou (202103000085), the seed industry revitalization project of Guang-dong (2022NPY00026), Fruit and Vegetable Industry System Inno-vation Team Project of Guangdong (2021KJ110), and the National Natural Science Foundation of China (31672156).

Author contributions

S.Y., Y.W., and B.Y. performed the research; B.C., Z.Q., and J.L. designed the research; C.C., Y.G., and Z.Z. provided new reagents; and S.Y., Y.W., Z.Q., and B.C. wrote the manuscript.

Data availability

All relevant data generated or analysed are included in the manuscript and the supporting materials.

Conflict of interest statement

The authors have no conflicts of interest.

Accession numbers

The GenBank/Sol Genomics Network (SGN) accession numbers of the sequences reported in this paper are as follows: SmNAC, KM435267; SmDDA1b, MZ736671; DDB1, SMEL_002g158220.1.01; CUL4, SMEL_002g157970.1.01; ICS1, SMEL_006g263050.1.01; SmEDS1, SMEL_006g263300.1.01; SmGluA, SMEL_001g150160.1.01; SmNPR1, SMEL _000g071090.1.01; SmSGT1, SMEL_006g251310.1.01; SmPAD4, SMEL_002g157190.1.01; SmTGA, SMEL_010g361040.1.01; SlICS1, NM_001247865.2; SlEDS1, NM_001320249.1; SlGluA, M80604.1; SlNPR1, NM_001247633.1; SlTGA NM_001324613.1; SlSGT1, EF011105.1; SlPAD4, XM_004231563.4.

Supplementary data

Supplementary data is available at Horticulture Research online.

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