Transcriptomic and genetic approaches reveal that low-light-induced disease susceptibility is related to cellular oxidative stress in tomato

Abstract

The impact of low light intensities on plant disease outbreaks represents a major challenge for global crop security, as it frequently results in significant yield losses. However, the underlying mechanisms of the effect of low light on plant defense are still poorly understood. Here, using an RNA-seq approach, we found that the susceptibility of tomato to Pseudomonas syringae pv. tomato DC3000 (Pst DC3000) under low light was associated with the oxidation–reduction process. Low light conditions exacerbated Pst DC3000-induced reactive oxygen species (ROS) accumulation and protein oxidation. Analysis of gene expression and enzyme activity of ascorbate peroxidase 2 (APX2) and other antioxidant enzymes revealed that these defense responses were significantly induced by Pst DC3000 inoculation under normal light, whereas these genes and their associated enzyme activities were not responsive to pathogen inoculation under low light. Additionally, the reduced ascorbate to dehydroascorbate (AsA/DHA) ratio was lower under low light compared with normal light conditions upon Pst DC3000 inoculation. Furthermore, the apx2 mutants generated by a CRISPR-Cas9 gene-editing approach were more susceptible to Pst DC3000 under low light conditions. Notably, this increased susceptibility could be significantly reduced by exogenous AsA treatment. Collectively, our findings suggest that low-light-induced disease susceptibility is associated with increased cellular oxidative stress in tomato plants. This study sheds light on the intricate relationship between light conditions, oxidative stress, and plant defense responses, and may pave the way for improved crop protection strategies in low light environments.

Acknowledgements

This work was supported by the National Natural Science Foundation of China (32172650) and the Key Research and Development Program of Zhejiang Province (2021C02040).

Author contributions

K.S. conceived the research; Q.L., J.W., and K.S. designed the experiments; Q.L., P.W., X.L., J.L., C.W., H.F., S.D., and S.S. performed the research and analyzed the data; and Q.L., J.W., and K.S. wrote the article with contributions from other authors.

Data availability

The data used to support the findings of this study are included within the article and the supporting information file. RNA-seq datasets can be accessed in the SRA database (https://www.ncbi.nlm.nih.gov/sra/PRJNA990324) under record number PRJNA990324. Sequence data from this article can be found in the Sol Genomics Network (http://solgenomics.net/) under the following accession numbers: APX2, Solyc06g005150, APX6, Solyc11g018550, SOD2, Solyc02g021140, SOD5, Solyc06g048410, POD8, Solyc07g042440, POD107, Solyc04g071900, CAT5, Solyc12g094620, CAT4, Solyc04g082460, SlACTIN, Solyc03g078400.

Conflict of interests

The authors declare that they have no conflict of interest.

Supplementary information

Supplementary data is available at Horticulture Research online.

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