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Overexpression of oilseed rape trehalose-6-phosphate synthesis gene BnaC02.TPS8 confers sensitivity to low nitrogen and high sucrose-induced anthocyanin accumulation in Arabidopsis

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Main conclusion

Overexpression of BnaC02.TPS8 increased low N and high sucrose-induced anthocyanin accumulation.

Abstract

Anthocyanin plays a crucial role in safeguarding photosynthetic tissues against high light, UV radiation, and oxidative stress. Their accumulation is triggered by low nitrogen (N) stress and elevated sucrose levels in Arabidopsis. Trehalose-6-phosphate (T6P) serves as a pivotal signaling molecule, sensing sucrose availability, and carbon (C) metabolism. However, the mechanisms governing the regulation of T6P synthase (TPS) genes responsible for anthocyanin accumulation under conditions of low N and high sucrose remain elusive. In a previous study, we demonstrated the positive impact of a cytoplasm-localized class II TPS protein ‘BnaC02.TPS8’ on photosynthesis and seed yield improvement in Brassica napus. The present research delves into the biological role of BnaC02.TPS8 in response to low N and high sucrose. Ectopic overexpression of BnaC02.TPS8 in Arabidopsis seedlings resulted in elevated shoot T6P levels under N-sufficient conditions, as well as an increased carbon-to-nitrogen (C/N) ratio, sucrose accumulation, and starch storage under low N conditions. Overexpression of BnaC02.TPS8 in Arabidopsis heightened sensitivity to low N stress and high sucrose levels, accompanied by increased anthocyanin accumulation and upregulation of genes involved in flavonoid biosynthesis and regulation. Metabolic profiling revealed increased levels of intermediate products of carbon metabolism, as well as anthocyanin and flavonoid derivatives in BnaC02.TPS8-overexpressing Arabidopsis plants under low N conditions. Furthermore, yeast two-hybrid (Y2H) and bimolecular fluorescence complementation (BiFC) analyses demonstrated that BnaC02.TPS8 interacts with both BnaC08.TPS9 and BnaA01.TPS10. These findings contribute to our understanding of how TPS8-mediated anthocyanin accumulation is modulated under low N and high sucrose conditions.

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Data availability

The raw RNA-seq data are deposited in the Gene Expression Omnibus (GEO) database under accession number GSE77396 at the National Center for Biotechnology Information (NCBI). All other data generated in this study are included in this manuscript and its supplementary information.

Abbreviations

BiFC:

Bimolecular fluorescence complementation

C:

Carbon

C/N:

Carbon-to-nitrogen ratio

DFR:

Dihydroflavonol reductase

F3'H:

Flavonoid 3′-hydroxylase

N:

Nitrogen

T6P:

Trehalose-6-phosphate

TPS8:

Trehalose-6-phosphate synthase8

Y2H:

Yeast two-hybrid

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Acknowledgements

This work was supported by the National Nature Science Foundation of China (Grant Nos. 32301885 and 32172662). Pan Yuan gratefully acknowledges financial support from the China Scholarship Council to Reading University for joint doctoral student education. The authors thank Prof. Junpei Takano (Osaka Metropolitan University) for providing us the vectors for the BiFC system. The authors owe thank Qi Li, Limei Zhang, Shu Zhu, Huan He at the public laboratory platform of the College of Resources and Environment, Huazhong Agricultural University, for their help with experimental test. The authors thank Wuhan Greensword Creation Technology Co. Ltd. for their technical support for T6P concentration analysis.

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PY and LS conceived and designed the study. PY, MZY, and HJL performed experiments and analyzed the data. PY, JPH, HC, GDD, SLW, FSX, CW, DFH, and LS wrote the manuscript. All authors have reviewed and approved the final manuscript.

Corresponding author

Correspondence to Lei Shi.

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The authors declare no competing interests.

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Communicated by Dorothea Bartels.

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Yuan, P., Yu, M., Liu, H. et al. Overexpression of oilseed rape trehalose-6-phosphate synthesis gene BnaC02.TPS8 confers sensitivity to low nitrogen and high sucrose-induced anthocyanin accumulation in Arabidopsis. Planta 259, 122 (2024). https://doi.org/10.1007/s00425-024-04404-3

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  • DOI: https://doi.org/10.1007/s00425-024-04404-3

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