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Elevated carbon assimilation and metabolic reprogramming in tomato high pigment mutants support the increased production of pigments

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High pigment mutants in tomato (Solanum lycopersicum L.), a loss of function in the control of photomorphogenesis, with greater pigment production, show altered growth, greater photosynthesis, and a metabolic reprogramming.

Abstract

High pigment mutations cause plants to be extremely responsive to light and produce excessive pigmentation as well as fruits with high levels of health-beneficial nutrients. However, the association of these traits with changes in the physiology and metabolism of leaves remains poorly understood. Here, we performed a detailed morphophysiological and metabolic characterization of high pigment 1 (hp1) and high pigment 2 (hp2) mutants in tomato (Solanum lycopersicum L. ‘Micro-Tom’) plants under different sunlight conditions (natural light, 50% shading, and 80% shading). These mutants occur in the DDB1 (hp1) and DET1 (hp2) genes, which are related to the regulation of photomorphogenesis and chloroplast development. Our results demonstrate that these mutations delay plant growth and height, by affecting physiological and metabolic parameters at all stages of plant development. Although the mutants were characterized by higher net CO2 assimilation, lower stomatal limitation, and higher carboxylation rates, with anatomical changes that favour photosynthesis, we found that carbohydrate levels did not increase, indicating a change in the energy flow. Shading minimized the differences between mutants and the wild type or fully reversed them in the phenotype at the metabolic level. Our results indicate that the high levels of pigments in hp1 and hp2 mutants represent an additional energy cost for these plants and that extensive physiological and metabolic reprogramming occurs to support increased pigment biosynthesis.

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Acknowledgements

The authors would like to thank Professor Dr Lázaro E. P. Peres (Escola Superior de Agricultura Luiz de Queiroz -ESALQ/USP, Brazil) for sharing the seeds used in this work. This work was supported by funding from the Max Planck Society (to WLA), the National Council for Scientific and Technological Development (CNPq-Brazil), and the FAPEMIG (Foundation for Research Assistance of the Minas Gerais State, Brazil). We also thank the scholarships granted by the Brazilian Federal Agency for Support and Evaluation of Graduate Education (CAPES-Brazil) to AMP. Research fellowships granted by CNPq-Brazil to ANN and WLA are also gratefully acknowledged.

Funding

Funding was provided by "Fundação de Amparo à Pesquisa do Estado de Minas Gerais, Grant No. CRA-RED-00053-16" and the Max Planck Society, the National Council for Scientific and Technological Development (CNPq-Brazil), and by the Brazilian Federal Agency for Support and Evaluation of Graduate Education (CAPES-Brazil).

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Contributions

AMP and WLA conceived the original research plan; AMP and AOM performed the research with the support of JAC-A, VLN, VFS, LAO, and DBM; DBM, SCVM, and A.R.F. contributed new reagents/analytic tools; AMP, AOM, VLN, SCVM, AN-N, and WLA analysed the data and discussed the results; AMP, AOM, VLN, AN-N, and WLA wrote the article with contributions of all the authors.

Corresponding author

Correspondence to Wagner L. Araújo.

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The authors declare that there is no conflict of interest regarding the publication of this article.

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Communicated by Fumihiko Sato.

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Pereira, A.M., Martins, A.O., Batista-Silva, W. et al. Elevated carbon assimilation and metabolic reprogramming in tomato high pigment mutants support the increased production of pigments. Plant Cell Rep 41, 1907–1929 (2022). https://doi.org/10.1007/s00299-022-02900-y

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  • DOI: https://doi.org/10.1007/s00299-022-02900-y

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