Promoter replacement of ANT1 induces anthocyanin accumulation and triggers the shade avoidance response through developmental, physiological and metabolic reprogramming in tomato

Abstract

The accumulation of anthocyanins is a well-known response to abiotic stresses in many plant species. However, the effects of anthocyanin accumulation on light absorbance and photosynthesis are unknown. Here, we addressed this question using a promoter replacement line of tomato constitutively expressing a MYB transcription factor (ANTHOCYANIN1, ANT1) that leads to anthocyanin accumulation. ANT1-overexpressing plants displayed traits associated with shade avoidance response: thinner leaves, lower seed germination rate, suppressed side branching, increased chlorophyll concentration, and lower photosynthesis rates than the wild type. Anthocyanin-rich leaves exhibited higher absorbance of light in the blue and red ends of the spectrum, while higher anthocyanin content in leaves provided photoprotection to high irradiance. Analyses of gene expression and primary metabolites content showed that anthocyanin accumulation produces a reconfiguration of transcriptional and metabolic networks that is consistent with, but not identical to those described for the shade avoidance response. Our results provide novel insights about how anthocyanins accumulation affects the trade-off between photoprotection and growth.

Acknowledgements

AZ was supported by a CAPES/Alexander von Humboldt Foundation Experienced Researcher Fellowship (88881.472837/2019-01) and Foundation for Research Assistance of the Minas Gerais State (FAPEMIG, Brazil, APQ-01942-22). FZ was supported by the Major Special Projects and Key R&D Projects in Yunnan Province (202102AE090020 and 202102AE090054). We thank Prof Lázaro E. P. Peres (University of São Paulo) and Prof Fábio M. DaMatta (Federal University of Viçosa) for valuable suggestions on early stages of the project.

Author contributions

JVAC, FZ carried out experiments and analyzed the data. SCVM, ANN and AZ helped to prepare materials and analysis tools. AZ, VB and ARF designed the experiments and wrote the paper with contributions from the other authors.

Data availability

All data supporting the findings of the present study are available within the paper and its supplementary material files.

Conflict of interest

No conflict of interest declared.

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