Paper · 2006 · PLANT PHYSIOLOGY

Integrated Analysis of Metabolite and Transcript Levels Reveals the Metabolic Shifts That Underlie Tomato Fruit Development and Highlight Regulatory Aspects of Metabolic Network Behavior

Fernando Carrari; Charles Baxter; Björn Usadel; et al.

9
claims
18
verbatim quotes
490
citations
4
research areas
✓
Open access

Abstract

Tomato (Solanum lycopersicum) is a well-studied model of fleshy fruit development and ripening. Tomato fruit development is well understood from a hormonal-regulatory perspective, and developmental changes in pigment and cell wall metabolism are also well characterized. However, more general aspects of metabolic change during fruit development have not been studied despite the importance of metabolism in the context of final composition of the ripe fruit. In this study, we quantified the abundance of a broad range of metabolites by gas chromatography-mass spectrometry, analyzed a number of the principal metabolic fluxes, and in parallel analyzed transcriptomic changes during tomato fruit development. Metabolic profiling revealed pronounced shifts in the abundance of metabolites of both primary and secondary metabolism during development. The metabolite changes were reflected in the flux analysis that revealed a general decrease in metabolic activity during ripening. However, there were several distinct patterns of metabolite profile, and statistical analysis demonstrated that metabolites in the same (or closely related) pathways changed in abundance in a coordinated manner, indicating a tight regulation of metabolic activity. The metabolite data alone allowed investigations of likely routes through the metabolic network, and, as an example, we analyze the operational feasibility of different pathways of ascorbate synthesis. When combined with the transcriptomic data, several aspects of the regulation of metabolism during fruit ripening were revealed. First, it was apparent that transcript abundance was less strictly coordinated by functional group than metabolite abundance, suggesting that posttranslational mechanisms dominate metabolic regulation. Nevertheless, there were some correlations between specific transcripts and metabolites, and several novel associations were identified that could provide potential targets for manipulation of fruit compositional traits. Finally, there was a strong relationship between ripening-associated transcripts and specific metabolite groups, such as TCA-cycle organic acids and sugar phosphates, underlining the importance of the respective metabolic pathways during fruit development.

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Claims 9

Observationobservedoriginal resultmeasured

Claim · model-written summary

Primary and secondary metabolite abundances shifted during tomato fruit development.

Organ / stage
fruite1
Outcome
abundance of metabolites of both primary and secondary metabolisme0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“Metabolic profiling revealed pronounced shifts in the abundance of metabolites of both primary and secondary metabolism during development”

✓ located verbatim in the source · abstract, characters 710–848 · show in text ↑
e1

“Tomato fruit development”

✓ located verbatim in the source · abstract, characters 96–120 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Overall metabolic activity decreased during tomato fruit ripening.

Organ / stage
fruite1
Outcome
metabolic activitye0
Direction
decreasee0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“flux analysis that revealed a general decrease in metabolic activity during ripening”

✓ located verbatim in the source · abstract, characters 895–979 · show in text ↑
e1

“Tomato fruit development”

✓ located verbatim in the source · abstract, characters 96–120 · show in text ↑
Associationobservedoriginal resultmeasured

Claim · model-written summary

Metabolites in the same or related pathways changed abundance in a coordinated manner.

Organ / stage
fruite1
Outcome
abundancee0
Direction
changede0
Qualifier
in a coordinated mannere0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“metabolites in the same (or closely related) pathways changed in abundance in a coordinated manner”

✓ located verbatim in the source · abstract, characters 1093–1191 · show in text ↑
e1

“Tomato fruit development”

✓ located verbatim in the source · abstract, characters 96–120 · show in text ↑
Method / resourceobservedoriginal resultmeasured

Claim · model-written summary

Metabolite data alone permitted investigation of likely routes through the tomato metabolic network.

Outcome
investigations of likely routes through the metabolic networke0
Comparator
metabolite data alonee0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“The metabolite data alone allowed investigations of likely routes through the metabolic network”

✓ located verbatim in the source · abstract, characters 1246–1341 · show in text ↑
e1

“Tomato fruit development”

✓ located verbatim in the source · abstract, characters 96–120 · show in text ↑
Associationobservedoriginal resultmeasured

Claim · model-written summary

Tomato fruit transcript abundance was less coordinated by functional group than metabolite abundance.

Organ / stage
fruite1
Outcome
transcript abundancee0
Direction
less strictly coordinatede0
Comparator
metabolite abundancee0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“transcript abundance was less strictly coordinated by functional group than metabolite abundance”

✓ located verbatim in the source · abstract, characters 1605–1701 · show in text ↑
e1

“Tomato fruit development”

✓ located verbatim in the source · abstract, characters 96–120 · show in text ↑
Associationobservedoriginal resultmeasured

Claim · model-written summary

Specific tomato transcripts and metabolites were correlated.

Organ / stage
fruite1
Outcome
correlations between specific transcripts and metabolitese0

Not reportedDirection

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“there were some correlations between specific transcripts and metabolites”

✓ located verbatim in the source · abstract, characters 1793–1866 · show in text ↑
e1

“Tomato fruit development”

✓ located verbatim in the source · abstract, characters 96–120 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Novel associations between transcripts and metabolites were identified as potential fruit composition targets.

Organ / stage
fruite1
Outcome
novel associationse0
Qualifier
could provide potential targets for manipulation of fruit compositional traitse0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“several novel associations were identified that could provide potential targets for manipulation of fruit compositional traits”

✓ located verbatim in the source · abstract, characters 1872–1998 · show in text ↑
e1

“Tomato fruit development”

✓ located verbatim in the source · abstract, characters 96–120 · show in text ↑
Associationobservedoriginal resultmeasured

Claim · model-written summary

Ripening associated transcripts were strongly related to TCA cycle organic acids and sugar phosphates.

Organ / stage
fruite1
Outcome
strong relationship between ripening-associated transcripts and specific metabolite groupse0

Not reportedDirection

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“there was a strong relationship between ripening-associated transcripts and specific metabolite groups, such as TCA-cycle organic acids and sugar phosphates”

✓ located verbatim in the source · abstract, characters 2009–2165 · show in text ↑
e1

“Tomato fruit development”

✓ located verbatim in the source · abstract, characters 96–120 · show in text ↑
Mechanismauthor interpretationoriginal resultmeasured

Claim · model-written summary

The weaker transcript coordination suggested that posttranslational mechanisms dominate tomato metabolic regulation.

Outcome
metabolic regulatione0
Qualifier
posttranslational mechanismse0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“suggesting that posttranslational mechanisms dominate metabolic regulation”

✓ located verbatim in the source · abstract, characters 1703–1777 · show in text ↑
e1

“Tomato fruit development”

✓ located verbatim in the source · abstract, characters 96–120 · show in text ↑