Skip to main content
SpringerLink
Log in

Metabolomics reveals organ-specific metabolic rearrangements during early tomato seedling development

  • Original Article
  • Published:
Metabolomics Aims and scope Submit manuscript

Abstract

Tomato seedlings (Solanum lycopersicum cv. MoneyMaker), grown under strictly controlled conditions, have been used to study alterations occurring in secondary metabolite biosynthetic pathways following developmental and environmental perturbations. Robustness and reproducibility of the system were confirmed using detailed statistical analyses of the metabolome. LCMS profiling was applied using whole germinated seeds as well as cotyledons, hypocotyls and roots from 3 to 9 days old seedlings to generate relative levels of 433 metabolites, of which 62 were annotated. Initial focus was given to the polyphenol pathway and several additional mass signals have been putatively annotated using high mass resolution fragmentation. Clear organ and developmental stage—specific differences were observed. Seeds accumulated saponin-like compounds; roots accumulated mainly alkaloids; cotyledons contained mainly glycosylated flavonols and; hypocotyls contained mainly anthocyanins. For each organ, the developmental changes in metabolite profiles were described by using linear mixed models. Across three independent experiments, 85 % of the metabolites showed similar developmental trends. This tomato seedling system has given us valuable additional insights into the complexity of seedling secondary metabolism. How metabolic profiles reflect an interplay between depletion of stored molecules and de novo synthesis and how the overall picture for this important crop plant contrasts to e.g. Arabidopsis are emphasised.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aliferis, K. A., & Jabaji, S. (2012). Deciphering plant-pathogen interactions applying metabolomics: Principles and applications. Canadian Journal of Plant Pathology, 34, 29–33.

    Article  CAS  Google Scholar 

  • Allen, E., Moing, A., Ebbels, T. M., Maucourt, M., Tomos, A. D., Rolin, D., et al. (2010). Correlation Network Analysis reveals a sequential reorganization of metabolic and transcriptional states during germination and gene-metabolite relationships in developing seedlings of Arabidopsis. BMC Systems Biology, 4, 62.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ballester, A. R., Molthoff, J., de Vos, R., Hekkert, B. L., Orzaez, D., Fernandez-Moreno, J. P., et al. (2010). Biochemical and molecular analysis of pink tomatoes: Deregulated expression of the gene encoding transcription factor SlMYB12 leads to pink tomato fruit color. Plant Physiology, 152, 71–84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bolle, C. (2009). Phenotyping of Arabidopsis mutants for developmental effects of gene deletions plant signal transduction, vol. 479 (pp. 1–18). New York: Humana Press.

    Google Scholar 

  • Bovy, A., de Vos, R., Kemper, M., Schijlen, E., Pertejo, M. A., Muir, S., et al. (2002). High-flavonol tomatoes resulting from the heterologous expression of the maize transcription factor genes LC and C1. Plant Cell, 14, 2509–2526.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bovy, A. G., Gomez-Roldan, V., & Hall, R. D. (2010). Strategies to optimize the flavonoid content of tomato fruit. In V. Lattanzio (Ed.) Recent Advances in Polyphenol Research (vol 2, pp. 138–162).

  • Bovy, A., Schijlen, E., & Hall, R. D. (2007). Metabolic engineering of flavonoids in tomato (Solanum lycopersicum): The potential for metabolomics. Metabolomics, 3, 399–412.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Butelli, E., Titta, L., Giorgio, M., Mock, H. P., Matros, A., Peterek, S., et al. (2008). Enrichment of tomato fruit with health-promoting anthocyanins by expression of select transcription factors. Nature Biotechnology, 26, 1301–1308.

    Article  CAS  PubMed  Google Scholar 

  • Capanoglu, E., Beekwilder, J., Boyacioglu, D., Hall, R., & de Vos, R. (2008). Changes in antioxidant and metabolite profiles during production of tomato paste. Journal of Agriculture and Food Chemistry, 56, 964–973.

    Article  CAS  Google Scholar 

  • Carli, P., Arima, S., Fogliano, V., Tardella, L., Frusciante, L., & Ercolano, M. R. (2009). Use of network analysis to capture key traits affecting tomato organoleptic quality. Journal of Experimental Botany, 60, 3379–3386.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carrari, F., Baxter, C., Usadel, B., Urbanczyk-Wochniak, E., Zanor, M. I., Nunes-Nesi, A., et al. (2006). Integrated analysis of metabolite and transcript levels reveals the metabolic shifts that underlie tomato fruit development and highlight regulatory aspects of metabolic network behavior. Plant Physiology, 142, 1380–1396.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, M., & Thelen, J. J. (2010). The plastid isoform of triose phosphate isomerase is required for the postgerminative transition from heterotrophic to autotrophic growth in Arabidopsis. The Plant Cell Online, 22, 77–90.

    Article  Google Scholar 

  • Cook, D., Fowler, S., Fiehn, O., & Thomashow, M. F. (2004). A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. Proc Natl Acad Sci USA, 101, 15243–15248.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De-la-Cruz Chacon, I., Riley-Saldana, C., & Gonzalez-Esquinca, A. (2012). Secondary metabolites during early development in plants. Phytochemistry Reviews, 12, 47–64.

    Article  Google Scholar 

  • Dixon, R. A., Achnine, L., Kota, P., Liu, C.-J., Reddy, M. S. S., & Wang, L. (2002). The phenylpropanoid pathway and plant defence—a genomics perspective. Molecular Plant Pathology, 3, 371–390.

    Article  CAS  PubMed  Google Scholar 

  • Fabre, J., Dauzat, M., Negre, V., Wuyts, N., Tireau, A., Gennari, E., et al. (2011). PHENOPSIS DB: An information system for Arabidopsis thaliana phenotypic data in an environmental context. BMC Plant Biology, 11, 77.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ferreres, F., Taveira, M., Pereira, D. M., Valentao, P., & Andrade, P. B. (2010). Tomato (Lycopersicon esculentum) seeds: New flavonols and cytotoxic effect. Journal of Agricultural and Food Chemistry, 58, 2854–2861.

    Article  CAS  PubMed  Google Scholar 

  • Gomez, C., Terrier, N., Torregrosa, L., Vialet, S., Fournier-Level, A., Verries, C., et al. (2009). Grapevine MATE-type proteins act as vacuolar H+-dependent acylated anthocyanin transporters. Plant Physiology, 150, 402–415.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gómez-Romero, M., Segura-Carretero, A., & Fernández-Gutiérrez, A. (2010). Metabolite profiling and quantification of phenolic compounds in methanol extracts of tomato fruit. Phytochemistry, 71, 1848–1864.

    Article  PubMed  Google Scholar 

  • Guo, J., & Wang, M.-H. (2010). Ultraviolet A-specific induction of anthocyanin biosynthesis and PAL expression in tomato (Solanum lycopersicum L.). Plant Growth Regulation, 62, 1–8.

    Article  CAS  Google Scholar 

  • Gupta, V., Mathur, S., Solanke, A. U., Sharma, M. K., Kumar, R., Vyas, S., et al. (2009). Genome analysis and genetic enhancement of tomato. Critical Reviews in Biotechnology, 29, 152–181.

    Article  CAS  PubMed  Google Scholar 

  • Huang, L. D., & Backhouse, D. (2005). Induction of defence responses in roots and mesocotyls of sorghum seedlings by inoculation with Fusarium thapsinum and F. proliferatum, wounding and light. Journal of Phytopathology, 153, 522–529.

    Article  Google Scholar 

  • Iijima, Y., Nakamura, Y., Ogata, Y., Ki, Tanaka, Sakurai, N., Suda, K., et al. (2008). Metabolite annotations based on the integration of mass spectral information. The Plant Journal, 54, 949–962.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • International V. (2011). GenStat for Windows. In Edition, VSN International, Hemel Hempstead, UK, p GenStat.co.uk.

  • Itkin, M., Rogachev, I., Alkan, N., Rosenberg, T., Malitsky, S., Masini, L., et al. (2011). Glycoalkaloid metabolism1 is required for steroidal alkaloid glycosylation and prevention of phytotoxicity in tomato. Plant Cell, 23, 4507–4525.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keurentjes, J. J. B., Angenent, G. C., Dicke, M., Santos, V. A. P. M. D., Molenaar, J., van der Putten, W. H., et al. (2011). Redefining plant systems biology: From cell to ecosystem. Trends in Plant Science, 16, 183–190.

    Article  CAS  PubMed  Google Scholar 

  • Kim, J. K., Bamba, T., Harada, K., Fukusaki, E., & Kobayashi, A. (2007). Time-course metabolic profiling in Arabidopsis thaliana cell cultures after salt stress treatment. Journal of Experimental Botany, 58, 415–424.

    Article  CAS  PubMed  Google Scholar 

  • Lawson, D. R., Green, T. P., Haynes, L. W., & Miller, A. R. (1997). Nuclear magnetic resonance spectroscopy and mass spectrometry of solanidine, leptinidine, and acetylleptinidine. Steroidal alkaloids from Solanum chacoense bitter. Journal of Agricultural and Food Chemistry, 45, 4122–4126.

    Article  CAS  Google Scholar 

  • Lommen, A. (2009). MetAlign: Interface-driven, versatile metabolomics tool for hyphenated full-scan mass spectrometry data preprocessing. Analytical Chemistry, 81, 3079–3086.

    Article  CAS  PubMed  Google Scholar 

  • McCulloch, C. E., Searle, S. R., & Neuhaus, J. M. (2008). Generalized, linear and mixed models. Hoboken, NJ: Wiley.

    Google Scholar 

  • Milkowski, C., & Strack, D. (2010). Sinapate esters in brassicaceous plants: Biochemistry, molecular biology, evolution and metabolic engineering. Planta, 232, 19–35.

    Article  CAS  PubMed  Google Scholar 

  • Moco, S., Bino, R. J., Vorst, O., Verhoeven, H. A., de Groot, J., van Beek, T. A., et al. (2006). A liquid chromatography-mass spectrometry-based metabolome database for tomato. Plant Physiology, 141, 1205–1218.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moco, S., Capanoglu, E., Tikunov, Y., Bino, R. J., Boyacioglu, D., Hall, R. D., et al. (2007). Tissue specialization at the metabolite level is perceived during the development of tomato fruit. Journal of Experimental Botany, 58, 4131–4146.

    Article  CAS  PubMed  Google Scholar 

  • Offen, W., Martinez-Fleites, C., Yang, M., Kiat-Lim, E., Davis, B. G., Tarling, C. A., et al. (2006). Structure of a flavonoid glucosyltransferase reveals the basis for plant natural product modification. EMBO Journal, 25, 1396–1405.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Osorio, S., Alba, R., Damasceno, C. M., Lopez-Casado, G., Lohse, M., Zanor, M. I., et al. (2011). 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. Plant Physiology, 157, 405–425.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ozfidan, C., Turkan, I., Sekmen, A. H., & Seckin, B. (2013). Time course analysis of ABA and non-ionic osmotic stress-induced changes in water status, chlorophyll fluorescence and osmotic adjustment in Arabidopsis thaliana wild-type (Columbia) and ABA-deficient mutant (aba2). Environmental and Experimental Botany, 86, 44–51.

  • Peel, G. J., Pang, Y., Modolo, L. V., & Dixon, R. A. (2009). The LAP1 MYB transcription factor orchestrates anthocyanidin biosynthesis and glycosylation in Medicago. Plant Journal, 59, 136–149.

    Article  CAS  PubMed  Google Scholar 

  • Rohrmann, J., Tohge, T., Alba, R., Osorio, S., Caldana, C., McQuinn, R., et al. (2011). Combined transcription factor profiling, microarray analysis and metabolite profiling reveals the transcriptional control of metabolic shifts occurring during tomato fruit development. Plant Journal, 68, 999–1013.

    Article  CAS  PubMed  Google Scholar 

  • Saito, K., Yonekura-Sakakibara, K., Nakabayashi, R., Higashi, Y., Yamazaki, M., Tohge, T., et al. (2013). The flavonoid biosynthetic pathway in Arabidopsis: Structural and genetic diversity. Plant Physiology and Biochemistry, 72, 21–34.

    Article  CAS  PubMed  Google Scholar 

  • Sato, S., Arita, M., Soga, T., Nishioka, T., & Tomita, M. (2008). Time-resolved metabolomics reveals metabolic modulation in rice foliage. BMC Systems Biology, 2, 51.

    Article  PubMed  PubMed Central  Google Scholar 

  • Schmidt, A., Li, C., Shi, F., Jones, A. D., & Pichersky, E. (2011). Polymethylated myricetin in trichomes of the wild tomato species Solanum habrochaites and characterization of trichome-specific 3′/5′- and 7/4′-myricetin O-methyltransferases. Plant Physiology, 155, 1999–2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Self, S. G., & Liang, K. Y. (1987). Properties of maximum likelihood estimators and likelihood ratio tests under nonstandard conditions. Journal of the American Statistical Association, 82, 605–610.

    Article  Google Scholar 

  • Shirley, B. W. (1996). Flavonoid biosynthesis: ‘New’ functions for an ‘old’ pathway. Trends in Plant Science, 1, 377–382.

    Google Scholar 

  • Slimestad, R., Fossen, T., & Verheul, M. J. (2008). The flavonoids of tomatoes. Journal of Agricultural and Food Chemistry, 56, 2436–2441.

    Article  CAS  PubMed  Google Scholar 

  • Strack, D., Gross, W., Wray, V., & Grotjahn, L. (1987). Enzymic synthesis of caffeoylglucaric acid from chlorogenic acid and glucaric acid by a protein preparation from tomato cotyledons. Plant Physiology, 83, 475–478.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sumner, L., Amberg, A., Barrett, D., Beale, M., Beger, R., Daykin, C., et al. (2007). Proposed minimum reporting standards for chemical analysis. Metabolomics, 3, 211–221.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tikunov, Y. M., de Vos, R. C. H., Paramas, A. M. G., Hall, R. D., & Bovy, A. G. (2010). A role for differential glycoconjugation in the emission of phenylpropanoid volatiles from tomato fruit discovered using a metabolic data fusion approach. Plant Physiology, 152, 55–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tikunov, Y. M., Laptenok, S., Hall, R. D., Bovy, A., & de Vos, R. C. H. (2012). MSClust: A tool for unsupervised mass spectra extraction of chromatography-mass spectrometry ion-wise aligned data. Metabolomics, 8, 714–718.

    Article  CAS  PubMed  Google Scholar 

  • Tohge, T., Nishiyama, Y., Hirai, M. Y., Yano, M., Nakajima, J., Awazuhara, M., et al. (2005). Functional genomics by integrated analysis of metabolome and transcriptome of Arabidopsis plants over-expressing an MYB transcription factor. Plant Journal, 42, 218–235.

    Article  CAS  PubMed  Google Scholar 

  • Tomato Genome, C. (2012). The tomato genome sequence provides insights into fleshy fruit evolution. Nature, 485, 635–641.

    Article  Google Scholar 

  • Vallverdu-Queralt, A., Jauregui, O., Medina-Remon, A., Andres-Lacueva, C., & Lamuela-Raventos, R. M. (2010). Improved characterization of tomato polyphenols using liquid chromatography/electrospray ionization linear ion trap quadrupole Orbitrap mass spectrometry and liquid chromatography/electrospray ionization tandem mass spectrometry. Rapid Communications in Mass Spectrometry, 24, 2986–2992.

    Article  CAS  PubMed  Google Scholar 

  • van der Hooft, J. J. J., Mihaleva, V., de Vos, R. C. H., Bino, R. J., & Vervoort, J. (2011). A strategy for fast structural elucidation of metabolites in small volume plant extracts using automated MS-guided LC-MS-SPE-NMR. Magnetic Resonance in Chemistry, 49, S55–S60.

    Article  CAS  PubMed  Google Scholar 

  • van der Hooft, J., Vervoort, J., Bino, R., & de Vos, R. (2012). Spectral trees as a robust annotation tool in LC–MS based metabolomics. Metabolomics, 8, 691–703.

    Article  Google Scholar 

  • Weitbrecht, K., Muller, K., & Leubner-Metzger, G. (2011). First off the mark: Early seed germination. Journal of Experimental Botany, 62, 3289–3309.

    Article  CAS  PubMed  Google Scholar 

  • Yamanaka, T., Vincken, J. P., Zuilhof, H., Legger, A., Takada, N., & Gruppen, H. (2009). C22 isomerization in alpha-tomatine-to-esculeoside A conversion during tomato ripening is driven by C27 hydroxylation of triterpenoidal skeleton. Journal of Agricultural and Food Chemistry, 57, 3786–3791.

    Article  CAS  PubMed  Google Scholar 

  • Yao, M., Tweddell, R., & Désilets, H. (2002). Effect of two vesicular-arbuscular mycorrhizal fungi on the growth of micropropagated potato plantlets and on the extent of disease caused by Rhizoctonia solani. Mycorrhiza, 12, 235–242.

    Article  CAS  PubMed  Google Scholar 

  • Yonekura-Sakakibara, K., Tohge, T., Matsuda, F., Nakabayashi, R., Takayama, H., Niida, R., et al. (2008). Comprehensive flavonol profiling and transcriptome coexpression analysis leading to decoding gene-metabolite correlations in Arabidopsis. The Plant Cell Online, 20, 2160–2176.

    Article  CAS  Google Scholar 

  • Yonekura-Sakakibara, K., Tohge, T., Niida, R., & Saito, K. (2007). Identification of a flavonol 7-O-rhamnosyltransferase gene determining flavonoid pattern in Arabidopsis by transcriptome coexpression analysis and reverse genetics. Journal of Biological Chemistry, 282, 14932–14941.

    Article  CAS  PubMed  Google Scholar 

  • Zhao, J., & Dixon, R. A. (2010). The ‘ins’ and ‘outs’ of flavonoid transport. Trends in Plant Science, 15, 72–80.

    Article  CAS  PubMed  Google Scholar 

  • Zhou, B., Li, Y., Xu, Z., Yan, H., Homma, S., & Kawabata, S. (2007). Ultraviolet A-specific induction of anthocyanin biosynthesis in the swollen hypocotyls of turnip (Brassica rapa). Journal of Experimental Botany, 58, 1771–1781.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was funded by Netherlands Consortium for Systems Biology, Centre for BioSystems Genomics and Netherlands Metabolomics Centre, members of the Netherlands Genomics Initiative/Netherlands Organization for Scientific Research.

Conflict of interest

The authors have declared that no competing interests exist.

Author information

Author notes

  1. Maria Victoria Gomez Roldan

    Present address: URGV - Crop Genomics, INRA Functional Genomics, CP5708, 2 rue Gaston Crémieux, 91000, Evry, France

Authors and Affiliations

  1. Netherlands Consortium for Systems Biology, Amsterdam, The Netherlands

    Maria Victoria Gomez Roldan, Laura Astola, Marian Groenenboom, Arnaud Bovy, Jaap Molenaar, Fred van Eeuwijk & Robert D. Hall

  2. Plant Research International, PO Box 16, 6700 AA, Wageningen, The Netherlands

    Maria Victoria Gomez Roldan, Ric C. H. de Vos, Henri van de Geest, Arnaud Bovy & Robert D. Hall

  3. Biometris, Wageningen University and Research Centre, Droevendaalsesteeg 1, Wageningen, The Netherlands

    Bas Engel, Pieter Vereijken, Laura Astola, Marian Groenenboom, Jaap Molenaar & Fred van Eeuwijk

  4. Netherlands Metabolomics Centre, Einsteinweg 55, 2333 CC, Leiden, The Netherlands

    Ric C. H. de Vos & Robert D. Hall

  5. Centre for Biosystems Genomics, P.O. Box 98, 6700 AB, Wageningen, The Netherlands

    Ric C. H. de Vos, Henri van de Geest, Arnaud Bovy, Fred van Eeuwijk & Robert D. Hall

Authors
  1. Maria Victoria Gomez Roldan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bas Engel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ric C. H. de Vos
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pieter Vereijken
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Laura Astola
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Marian Groenenboom
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Henri van de Geest
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Arnaud Bovy
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jaap Molenaar
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Fred van Eeuwijk
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Robert D. Hall
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maria Victoria Gomez Roldan.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 617 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Roldan, M.V.G., Engel, B., de Vos, R.C.H. et al. Metabolomics reveals organ-specific metabolic rearrangements during early tomato seedling development. Metabolomics 10, 958–974 (2014). https://doi.org/10.1007/s11306-014-0625-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11306-014-0625-2

Keywords

Search

Navigation