Systems biology of tomato fruit development: combined transcript, protein, and metabolite analysis of tomato transcription factor (nor, rin) and ethylene receptor (Nr) mutants reveals novel regulatory interactions.

Sonia Osorio,Takayuki Tohge,James J Giovannoni,Alisdair R Fernie,Zhangjun Fei,Marc Lohse,Maria Inés Zanor,Björn Usadel,Cynthia M.B Damasceno,Jocelyn K.C Rose,Gloria Lopez-Casado,Rob Alba

doi:10.1104/pp.111.175463

Sonia Osorio, Takayuki Tohge + Show 10 more

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https://doi.org/10.1104/pp.111.175463

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Abstract

Tomato (Solanum lycopersicum) is an established model to study fleshy fruit development and ripening. Tomato ripening is regulated independently and cooperatively by ethylene and transcription factors, including nonripening (NOR) and ripening-inhibitor (RIN). Mutations of NOR, RIN, and the ethylene receptor Never-ripe (Nr), which block ethylene perception and inhibit ripening, have proven to be great tools for advancing our understanding of the developmental programs regulating ripening. In this study, we present systems analysis of nor, rin, and Nr at the transcriptomic, proteomic, and metabolomic levels during development and ripening. Metabolic profiling marked shifts in the abundance of metabolites of primary metabolism, which lead to decreases in metabolic activity during ripening. When combined with transcriptomic and proteomic data, several aspects of the regulation of metabolism during ripening were revealed. First, correlations between the expression levels of a transcript and the abundance of its corresponding protein were infrequently observed during early ripening, suggesting that posttranscriptional regulatory mechanisms play an important role in these stages; however, this correlation was much greater in later stages. Second, we observed very strong correlation between ripening-associated transcripts and specific metabolite groups, such as organic acids, sugars, and cell wall-related metabolites, underlining the importance of these metabolic pathways during fruit ripening. These results further revealed multiple ethylene-associated events during tomato ripening, providing new insights into the molecular biology of ethylene-mediated ripening regulatory networks.

Highlights

Tomato (Solanum lycopersicum) is an established model to study fleshy fruit development and ripening
The Gr gene is suggested to interact with components of the fruit-specific ethylene response (Barry and Giovannoni, 2006), while the Nr mutation has been characterized as an ERS-like ethylene receptor that is impaired in the ability to bind ethylene (Lanahan et al, 1994)
Transcriptional analysis was carried out using the tomato cDNA microarray (TOM1; Alba et al, 2005), microarray-containing ESTs, proteomic data were obtained using isobaric tag labeling, and metabolomics data were obtained by gas chromatography-mass spectrometry (GC-MS) according to Carrari et al (2006)

Summary

Introduction

Tomato (Solanum lycopersicum) is an established model to study fleshy fruit development and ripening. We observed very strong correlation between ripening-associated transcripts and specific metabolite groups, such as organic acids, sugars, and cell wall-related metabolites, underlining the importance of these metabolic pathways during fruit ripening These results further revealed multiple ethylene-associated events during tomato ripening, providing new insights into the molecular biology of ethylene-mediated ripening regulatory networks. We have examined three dominant ripening mutants of tomato, nor, rin, and Nr, along the developmental and ripening periods at the transcriptomic, proteomic, and metabolomic levels in order to further extend the analysis carried out by Alba et al (2005) Use of these specific mutants helps define transcriptional activity as transcriptionally regulated and ethylene response subtranscriptomes. The combined results are discussed in the context of current models of ripening and development

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