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Impact of benzoic acid and 2,2’-methylenebis (6-tert-butyl-4-methylphenol) on the metabolome of flue-cured tobacco and rhizosphere microbial communities: implications for continuous cropping obstacles

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Abstract

Background and aims

This study examined the effects of benzoic acid (BA) and 2,2’-methylenebis (6-tert-butyl-4-methylphenol) (ME), compounds present in the root exudates of continuously cropped flue-cured tobacco, on the germination, seedling growth, and development of flue-cured tobacco. The primary objective of this study was to enhance the understanding of the underlying mechanisms of continuous cropping obstacles in flue-cured tobacco. Additionally, this study aimed to provide theoretical insights for managing continuous cropping obstacles not only in flue-cured tobacco but also in other plants.

Methods

The mechanisms governing the function of BA and ME were investigated by analyzing leaf transcriptomes and metabolomes and soil microbial communities.

Results

BA and ME significantly inhibited flue-cured tobacco seed germination, albeit with distinct concentration-dependent effects. Both compounds induced senescence and necrosis in tobacco leaves, primarily by suppressing seed germination and compromising the activity of the antioxidant system. Transcriptomic analysis revealed robust responses of photosynthesis and secondary metabolism to BA and ME, with a particular emphasis on flavonoid biosynthesis and alkaloid enrichment. Moreover, BA and ME significantly affected the richness and diversity of rhizosphere microorganisms, resulting in notable changes in microbial community structure and composition. Specifically, Actinobacteriota, Cyanobactreia, and Mucoromycot exhibited pronounced responses to flavonoid biosynthesis, particularly dihydromyricetin, while Proteobacteria, Cyanobacteria, and Mucoromycot strongly responded to alkaloid enrichment, especially with respect to tabersonine.

Conclusion

BA and ME induced senescence and necrosis in tobacco leaves, with dihydromyricetin in flavonoid biosynthesis and tabersonine in alkaloid enrichment having notable impacts on the rhizosphere microbial community of flue-cured tobacco.

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Data availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

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Funding

This research was supported by the Science and Technology Project in Yunnan Branch of China Tobacco Corporation (No. 2019530000241036) and the Scientific Research Fund Project of Yunnan Education Department of China (No. 2020Y0415).

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Authors and Affiliations

Authors

Contributions

Conceptualization, Yihong Pan and Jiayan Zhang; methodology, Xiaolong Zhang, Qiulian Peng, Yihong Pan, and Kun Huang; validation, Jiayan Zhang, Xiaolong Zhang and Guobin Deng; formal analysis, Xiaolong Zhang, Guobin Deng, Kun Huang, and Xinwei Ji; investigation, Qiulian Peng, Kun Huang, Xinwei Ji, and Lijuan Zhou; resources, Jiayan Zhang, Xiaolong Zhang, and Guobin Deng; data curation, Xiaolong Zhang, Qiulian Peng, Lijuan Zhou, Kun Huang and Xinwei Ji; writing—original draft preparation, Yihong Pan; writing—review and editing, Jiayan Zhang, Xiaolong Zhang, Guobin Deng and Yihong Pan; Visualization, Guobin Deng, Qiulian Peng, Kun Huang, Xinwei Ji and Lijuan Zhou; supervision, Jiayan Zhang, Guobin Deng and Xiaolong Zhang; project administration, Jiayan Zhang, Xiaolong Zhang and Guobin Deng; funding acquisition, Jiayan Zhang, Qiulian Peng, Xiaolong Zhang and Guobin Deng. All authors have approved this final version of the manuscript for submission.

Corresponding authors

Correspondence to Guobin Deng, Xiaolong Zhang or Jiayan Zhang.

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Competing interests

The authors have no relevant financial or non-financial interests to disclose.

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Responsible Editor: Elizabeth M Baggs.

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Pan, Y., Peng, Q., Huang, K. et al. Impact of benzoic acid and 2,2’-methylenebis (6-tert-butyl-4-methylphenol) on the metabolome of flue-cured tobacco and rhizosphere microbial communities: implications for continuous cropping obstacles. Plant Soil 495, 137–155 (2024). https://doi.org/10.1007/s11104-023-06332-9

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  • DOI: https://doi.org/10.1007/s11104-023-06332-9

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