Integrated multi-omics investigation revealed the importance of phenylpropanoid metabolism in the defense response of Lilium regale Wilson to fusarium wilt

Abstract

Lilies (genus Lilium) play a significant role in the global cut-flower industry, but they are highly susceptible to fusarium wilt caused by Fusarium oxysporum. However, Lilium regale, a wild lily species, exhibits remarkable resistance to F. oxysporum. To investigate the quantitative resistance of L. regale to fusarium wilt, a comprehensive multi-omics analysis was conducted. Upon inoculation with F. oxysporum, L. regale roots showed a significant accumulation of phenylpropane metabolites, including lignin precursors, flavonoids, and hydroxycinnamic acids. These findings were consistent with the upregulated expression of phenylpropanoid biosynthesis-related genes encoding various enzymes, as revealed by transcriptomics and proteomics analyses. Furthermore, metabolomics and proteomics data demonstrated differential activation of monoterpenoid and isoquinoline alkaloid biosynthesis. Colorimetry and high-performance liquid chromatography analyses revealed significantly higher levels of total flavonoids, lignin, ferulic acid, phlorizin, and quercetin contents in L. regale scales compared with susceptible lily ‘Siberia’ scales during F. oxysporum infection. These phenylpropanes exhibited inhibitory effects on F. oxysporum growth and suppressed the expression of pathogenicity-related genes. Transcriptional regulatory network analysis suggested that ethylene-responsive transcription factors (ERFs) may positively regulate phenylpropanoid biosynthesis. Therefore, LrERF4 was cloned and transiently overexpressed in the fusarium wilt-susceptible Oriental hybrid lily ‘Siberia’. The overexpression of LrERF4 resulted in increased levels of total flavonoids, lignin, ferulic acid, phlorizin, and quercetin, while the silencing of LrERF4 in L. regale through RNAi had the opposite effect. In conclusion, phenylpropanoid metabolism plays a crucial role in the defense response of L. regale against fusarium wilt, with LrERF4 acting as a positive regulator of phenylpropane biosynthesis.

Acknowledgements

The National Natural Sciences Foundation of China (grant 31760586) supported this research.

Author contributions

D.J. contributed to the conduct of the investigation, the meticulous curation of the data, formal analysis, the creation of visualizations, and writing the original draft. C.X.L. and G.Y. contributed to the conduct of the investigation and the creation of visualizations. Q.Y. contributed to the methodology and data curation. L.D.Q. contributed to the methodology, the conduct of the investigation, reviewed the writing, performed editing, and supervised validation of the study.

Data availability statement

The original transcriptome data can be obtained from NCBI under accession number PRJNA1094676 (https://www.ncbi.nlm.nih.gov/sra/PRJNA1094676). The original proteome data can be found in ProteomeXchange with number PXD051239 (https://proteomecentral.proteomexchange.org/cgi/GetDataset?ID=PXD051239). The original metabolome data can be obtained in OMIX with number OMIX006147 (https://ngdc.cncb.ac.cn/omix/release/OMIX006147).

Conflict of interests

The authors have no conflict of interest to declare.

Supplementary information

Supplementary data are available at Horticulture Research online.

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