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The NtDEGP5 gene improves drought tolerance in tobacco (Nicotiana tabacum L.) by dampening plastid extracellular Ca2+ and flagellin signaling and thereby reducing ROS production

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Abstract

Tobacco is an essential cash crop, but drought has become a major factor in the decline of global tobacco production as a result of changes in the global climate. The HtrA protease is an oligomeric serine endopeptidase that responds to stress in plants. DEGP5 is a member of the gene family that encodes HtrA protease, which promotes plant adaptation to adversity. The aim of this study was to investigate the role and mechanism employed by the DEGP5 gene in response to drought stress in tobacco. NtDEGP5-overexpression lines were obtained by genetic transformation and the phenotypes and transcriptomes of NtDEGP5-overexpression lines and wild-type (K326) tobacco seedlings were compared under drought stress. The results demonstrated that plants overexpressing NtDEGP5 exhibited greater drought tolerance. The differentially expressed genes involved in the regulation of drought tolerance by DEGP5 were enriched in metabolic pathways, such as plant-pathogen interaction and glutathione metabolism, with the plant-pathogen interaction pathway having the most differentially expressed genes. An analysis of the plant-pathogen interaction pathway revealed that these genes contributed to the suppression of plastid extracellular Ca2+ signaling and flagellin signaling to inhibit reactive oxygen species production, and that lower levels of reactive oxygen species act as a signal to regulate the activation of the antioxidant system, further balancing the production and removal of reactive oxygen species in tobacco seedlings under drought stress. These findings suggest that the NtDEGP5 gene can enhance the drought tolerance of tobacco by regulating the homeostasis of reactive oxygen species by inhibiting extracellular plastids.

Key message

The NtDEGP5 gene in tobacco decreased ROS production by inhibiting intracellular transduction of plastid extracellular Ca2+ and flagellin signaling, thereby enhancing the mutant's drought resistance.

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Abbreviations

Pro:

Proline

MDA:

Malondialdehyde

SOD:

Superoxide dismutase

POD:

Peroxidase

CAT:

Catalase

H2O2 :

Hydrogen peroxide

O2· :

Superoxide anion

DEGs:

Differentially expressed genes

GO:

Gene ontology

KEGG:

Kyoto encyclopedia of genes and genomes

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Funding

National Natural Science Foundation of China (32060510), Guizhou Provincial Science and Technology Department ([2016] 5663), and Guizhou Provincial Tobacco Company (2022XM02).

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Contributions

CG: provided experimental design and wrote the original manuscript, writing-review, and editing. SYQ and JZL: performed the experiments and validation. DLL and MZJ: performed the methodology and validation. LRX provided experimental design, supervision, and manuscript revision.

Corresponding author

Correspondence to Renxiang Liu.

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The authors have not disclosed any competing interests.

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Chen, G., Shu, Y., Jian, Z. et al. The NtDEGP5 gene improves drought tolerance in tobacco (Nicotiana tabacum L.) by dampening plastid extracellular Ca2+ and flagellin signaling and thereby reducing ROS production. Plant Mol Biol 113, 265–278 (2023). https://doi.org/10.1007/s11103-023-01388-8

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  • DOI: https://doi.org/10.1007/s11103-023-01388-8

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