Effect of the biosynthesis of the volatile compound phenylacetaldehyde on chloroplast modifications in tea (Camellia sinensis) plants

Abstract

Plant volatile compounds have important physiological and ecological functions. Phenylacetaldehyde (PAld), a volatile phenylpropanoid/benzenoid, accumulates in the leaves of tea (Camellia sinensis) plants grown under continuous shading. This study was conducted to determine whether PAld production is correlated with light and to elucidate the physiological functions of PAld in tea plants. Specifically, the upstream mechanism modulating PAld biosynthesis in tea plants under different light conditions as well as the effects of PAld on chloroplast/chlorophyll were investigated. The biosynthesis of PAld was inhibited under light, whereas it was induced in darkness. The structural gene encoding aromatic amino acid aminotransferase 1 (CsAAAT1) was expressed at a high level in darkness, consistent with its importance for PAld accumulation. Additionally, the results of a transcriptional activation assay and an electrophoretic mobility shift assay indicated CsAAAT1 expression was slightly activated by phytochrome-interacting factor 3-2 (CsPIF3-2), which is a light-responsive transcription factor. Furthermore, PAld might promote the excitation of chlorophyll in dark-treated chloroplasts and mediate electron energy transfer in cells. However, the accumulated PAld can degrade chloroplasts and chlorophyll, with potentially detrimental effects on photosynthesis. Moreover, PAld biosynthesis is inhibited in tea leaves by red and blue light, thereby decreasing the adverse effects of PAld on chloroplasts during daytime. In conclusion, the regulated biosynthesis of PAld in tea plants under light and in darkness leads to chloroplast modifications. The results of this study have expanded our understanding of the biosynthesis and functions of volatile phenylpropanoids/benzenoids in tea leaves.

Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (31902074), the Guangdong Basic and Applied Basic Research Foundation (2020A1515010539), the Young Elite Scientists Sponsorship Program by China Association for Science and Technology (2020QNRC001), the Youth Innovation Promotion Association of Chinese Academy of Sciences (2022351), the Basic Frontier Science Research Program of Chinese Academy of Sciences (ZDBS-LY-SM032), the Guangdong Provincial Special Fund for Modern Agriculture Industry Technology Innovation Teams (2023KJ120), and Guangdong Provincial Department of Science and Technology Rural Science and Technology Commissioner Project (KTP20210351). We thank Dr Yuhua Yang and Dr Chen Zhu at the South China Botanical Garden, Chinese Academy of Sciences for the revision of electrophoretic mobility shift assay and analysis of cis-element in the promoter of the gene, respectively.

Author contributions

Z.Y. conceived the experiments. L.Z., X.Z., X.F., Y.H., D.G., and F.D. conducted the experiments. X.H. gave instructive comments on the experiments. L.Z., X.Z., X.F., and Z.Y. analyzed the results. L.Z., X.Z., and Z.Y. wrote the manuscript. All authors reviewed the manuscript.

Data availability

All relevant data are provided within the paper and its supplementary files. All sequencing data have been uploaded to the National Genomics Data Center (NGDC) under the accession number PRJCA011336.

Conflict of interest

None declared.

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