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Physiological and metabolic bases of increased growth in the tomato ethylene-insensitive mutant Never ripe: extending ethylene signaling functions

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Abstract

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The tomato mutant Never ripe  ( Nr ), a loss-of-function for the ethylene receptor Sl ETR3, shows enhanced growth, associated with increased carbon assimilation and a rewiring of the central metabolism.

Abstract

Compelling evidence has demonstrated the importance of ethylene during tomato fruit development, yet its role on leaf central metabolism and plant growth remains elusive. Here, we performed a detailed characterization of Never ripe (Nr) tomato, a loss-of-function mutant for the ethylene receptor SlETR3, known for its fruits which never ripe. However, besides fruits, the Nr gene is also constitutively expressed in vegetative tissues. Nr mutant showed a growth enhancement during both the vegetative and reproductive stage, without an earlier onset of leaf senescence, with Nr plants exhibiting a higher number of leaves and an increased dry weight of leaves, stems, roots, and fruits. At metabolic level, Nr also plays a significant role with the mutant showing changes in carbon assimilation, carbohydrates turnover, and an exquisite reprogramming of a large number of metabolite levels. Notably, the expression of genes related to ethylene signaling and biosynthesis are not altered in Nr. We assess our results in the context of those previously published for tomato fruits and of current models of ethylene signal transduction, and conclude that ethylene insensitivity mediated by Nr impacts the whole central metabolism at vegetative stage, leading to increased growth rates.

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Acknowledgements

The authors would like to acknowledge Dr. Jim Giovannoni (Boyce Thompson Institute for Plant Research, Ithaca, New York, USA) for sharing seeds used in this work. This work was supported by funding from the National Council for Scientific and Technological Development (CNPq-Brazil, Grant 402511/2016-6 to WLA) and the FAPEMIG (Foundation for Research Assistance of the Minas Gerais State, Brazil, Grant APQ-01171-17 and RED-00053-16). We also thank the scholarships granted by the Brazilian Federal Agency for Support and Evaluation of Graduate Education (CAPES-Brazil—Finance Code 001) to VLN, AMP and LCC, and by the CNPq to CEAB. RS was supported by a Research Stimulus Grant (VICCI—Grant No: 14/S/819) funded by the Irish Department of Agriculture, Food and the Marine (DAFM). Research fellowships granted by CNPq-Brazil to DMR, ANN, AZ, and WLA are also gratefully acknowledged.

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Conception and design of the experiments: VLN and WLA. Performance of the experiments: VLN, AMP, ASP, VFS, LCC, and CEAB. Analysis of the data: VLN, RS, DMR, CC, AZ, ANN, and WLA. Contribution of reagents/materials/analysis tools: DMR, CC, AZ, ANN, and WLA. Writing of the manuscript: VLN, RS, DMR, AZ, ANN, and WLA.

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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 Neal Stewart.

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Nascimento, V.L., Pereira, A.M., Pereira, A.S. et al. Physiological and metabolic bases of increased growth in the tomato ethylene-insensitive mutant Never ripe: extending ethylene signaling functions. Plant Cell Rep 40, 1377–1393 (2021). https://doi.org/10.1007/s00299-020-02623-y

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  • DOI: https://doi.org/10.1007/s00299-020-02623-y

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