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Re-assessing Systems Biology Approaches on Analyzing Sulfate Metabolism

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Part of the book series: Proceedings of the International Plant Sulfur Workshop ((PIPSW))

Abstract

Mainly driven by the availability of the first Arabidopsis genome sequence in 2000 a rapid development of high throughput analytical techniques were developed and termed transcriptomics. This development was quickly followed by developing metabolite-profiling technologies, metabolomics. The ever-growing data bases made the development of new biostatistical and bioinformatics tools necessary. These ‘omics’ approaches were also applied to analyze the response of plants towards sulfate deprivation with the aim to gain a more complete, holistic view on plant metabolism and its control in response to varied nutrient supply. Early results though already providing novel results and fostering new routes of investigation were hampered by the incomplete annotation of the genes of the Arabidopsis genome. In recent years this informational gap was largely filled. Thus, we revisit here one old data set obtained at the infancy of ‘omics’ research and indicate novel conclusions possible when re-assessing these data as well as indicate new possibilities of continued analyses.

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References

  • Aarabi F, Kusajima M, Tohge T, Konishi T, Gigolashvili T, Takamune M, Sasazaki Y, Watanabe M, Nakashita H, Fernie AR, Saito K, Takahashi H, Hubberten HM, Hoefgen R, Maruyama-Nakashita A (2016) Sulfur deficiency-induced repressor proteins optimize glucosinolate biosynthesis in plants. Sci Adv 2:e1601087

    Article  PubMed  PubMed Central  Google Scholar 

  • Bielecka M, Watanabe M, Morcuende R, Scheible WR, Hawkesford MJ, Hesse H, Hoefgen R (2015) Transcriptome and metabolome analysis of plant sulfate starvation and resupply provides novel information on transcriptional regulation of metabolism associated with sulfur, nitrogen and phosphorus nutritional responses in Arabidopsis. Front Plant Sci 5:805

    Article  PubMed  PubMed Central  Google Scholar 

  • Falkenberg B, Witt I, Zanor MI, Steinhauser D, Mueller-Roeber B, Hesse H, Hoefgen R (2008) Transcription factors relevant to auxin signalling coordinate broad-spectrum metabolic shifts including sulphur metabolism. J Exp Bot 59:2831–2846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernie AR, Trethewey RN, Krotzky AJ, Willmitzer L (2004) Metabolite profiling: from diagnostics to systems biology. Nat Rev Mol Cell Biol 5:763–769

    Article  CAS  PubMed  Google Scholar 

  • Fiehn O, Kopka J, Dörmann P, Altmann T, Trethewey RN, Willmitzer L (2000) Metabolite profiling for plant functional genomics. Nat Biotechnol 18:1157–1161

    Article  CAS  PubMed  Google Scholar 

  • Forieri I, Sticht C, Reichelt M, Gretz N, Hawkesford MJ, Malagoli M, Wirtz M, Hell R (2017) System analysis of metabolism and the transcriptome in Arabidopsis thaliana roots reveals differential co-regulation upon iron, sulfur and potassium deficiency. Plant Cell Environ 40:95–107

    Article  CAS  PubMed  Google Scholar 

  • Gutierrez L, Mongelard G, Floková K, Pacurar DI, Novák O, Staswick P, Kowalczyk M, Pacurar M, Demailly H, Geiss G, Bellini C (2012) Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis. Plant Cell 24:2515–2527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hagen JB (2000) The origins of bioinformatics. Nat Rev Genet 1:231–236

    Article  CAS  PubMed  Google Scholar 

  • Hirai MY, Fujiwara T, Awazuhara M, Kimura T, Noji M, Saito K (2003) Global expression profiling of sulfur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-L-serine as a general regulator of gene expression in response to sulfur nutrition. Plant J 33:651–663

    Article  CAS  PubMed  Google Scholar 

  • Hirai MY, Yano M, Goodenowe DB, Kanaya S, Kimura T, Awazuhara M, Arita M, Fujiwara T, Saito K (2004) Integration of transcriptomics and metabolomics for understanding of global responses to nutritional stresses in Arabidopsis thaliana. Proc Natl Acad Sci USA 101(27):10205–10210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirai MY, Klein M, Fujikawa Y, Yano M, Goodenowe DB, Yamazaki Y, Kanaya S, Nakamura Y, Kitayama M, Suzuki H, Sakurai N, Shibata D, Tokuhisa J, Reichelt M, Gershenzon J, Papenbrock J, Saito K (2005) Elucidation of gene-to-gene and metabolite-to-gene networks in arabidopsis by integration of metabolomics and transcriptomics. J Biol Chem 280:25590–25595

    Article  CAS  PubMed  Google Scholar 

  • Hoefgen R, Nikiforova VJ (2008) Metabolomics integrated with transcriptomics: assessing systems response to sulfur-deficiency stress. Physiol Plant 132:190–198

    Article  CAS  PubMed  Google Scholar 

  • Hubberten HM, Klie S, Caldana C, Degenkolbe T, Willmitzer L, Hoefgen R (2012a) Additional role of O-acetylserine as a sulfur status-independent regulator during plant growth. Plant J 70:666–677

    Article  CAS  PubMed  Google Scholar 

  • Hubberten HM, Drozd A, Tran BV, Hesse H, Hoefgen R (2012b) Local and systemic regulation of sulfur homeostasis in roots of Arabidopsis thaliana. Plant J 72:625–635

    Article  CAS  PubMed  Google Scholar 

  • Malek B, van der Graaff E, Schneitz K, Keller B (2002) The Arabidopsis male-sterile mutant dde2-2 is defective in the ALLENE OXIDE SYNTHASE gene encoding one of the key enzymes of the jasmonic acid biosynthesis pathway. Planta 216:187–192

    Article  Google Scholar 

  • Maruyama-Nakashita A, Inoue E, Watanabe-Takahashi A, Yamaya T, Takahashi H (2003) Transcriptome profiling of sulfur-responsive genes in Arabidopsis reveals global effects of sulfur nutrition on multiple metabolic pathways. Plant Physiol 132:597–605

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maruyama-Nakashita A, Nakamura Y, Yamaya T, Takahashi H (2004) Regulation of high-affinity sulphate transporters in plants: towards systematic analysis of sulphur signalling and regulation. J Exp Bot 55:1843–1849

    Article  CAS  PubMed  Google Scholar 

  • Maruyama-Nakashita A, Nakamura Y, Tohge T, Saito K, Takahashi H (2006) Arabidopsis SLIM1 is a central transcriptional regulator of plant sulfur response and metabolism. Plant Cell 18:3235–3251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nikiforova V, Freitag J, Kempa S, Adamik M, Hesse H, Hoefgen R (2003) Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant J 33:633–650

    Article  CAS  PubMed  Google Scholar 

  • Nikiforova V, Gakière B, Kempa S, Adamik M, Willmitze L, Hesse H, Hoefgen R (2004) Towards dissecting nutrient metabolism in plants: a systems biology case study on sulfur metabolism. J Exp Bot 55:1861–1870

    Article  CAS  PubMed  Google Scholar 

  • Nikiforova VJ, Kopka J, Tolstikov V, Fiehn O, Hopkins L, Hawkesford MJ, Hesse H, Hoefgen R (2005a) Systems rebalancing of metabolism in response to sulfur deprivation, as revealed by metabolome analysis of Arabidopsis plants. Plant Physiol 138:304–318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nikiforova VJ, Daub CO, Hesse H, Willmitzer L, Hoefgen R (2005b) Integrative gene-metabolite network with implemented causality deciphers informational fluxes of sulphur stress response. J Exp Bot 56:1887–1896

    Article  CAS  PubMed  Google Scholar 

  • Roessner U, Luedemann A, Brust D, Fiehn O, Linke T, Willmitzer L, Fernie AR (2001) Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell 13:11–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sasaki-Sekimoto Y, Taki N, Obayashi T, Aono M, Matsumoto F, Sakurai N, Suzuki H, Hirai MY, Noji M, Saito K, Masuda T, Takamiya K, Shibata D, Ohta H (2005) Coordinated activation of metabolic pathways for antioxidants and defence compounds by jasmonates and their roles in stress tolerance in Arabidopsis. Plant J 44:653–668

    Article  CAS  PubMed  Google Scholar 

  • Sirko A, Wawrzyńska A, Rodríguez MC, Sęktas P (2015) The family of LSU-like proteins. Front Plant Sci 5:774

    Article  PubMed  PubMed Central  Google Scholar 

  • Watanabe M, Hubberten HM, Saito K, Hoefgen R (2010) General regulatory patterns of plant mineral nutrient depletion as revealed by serat quadruple mutants disturbed in cysteine synthesis. Mol Plant 3:438–466

    Article  CAS  PubMed  Google Scholar 

  • Watanabe M, Balazadeh S, Tohge T, Erban A, Giavalisco P, Kopka J, Mueller-Roeber B, Fernie AR, Hoefgen R (2013) Comprehensive dissection of spatiotemporal metabolic shifts in primary, secondary, and lipid metabolism during developmental senescence in Arabidopsis. Plant Physiol 162:1290–1310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wen R, Wang S, Xiang D, Venglat P, Shi X, Zang Y, Datla R, Xiao W, Wang H (2014) UBC13, an E2 enzyme for Lys63-linked ubiquitination, functions in root development by affecting auxin signaling and Aux/IAA protein stability. Plant J 80:424–436

    Article  CAS  PubMed  Google Scholar 

  • Whitcomb SJ, Heyneke E, Aarabi F, Watanabe M, Hoefgen R (2014) Mineral nutrient depletion affects plant development and crop yield. In: Hawkesford MJ, Kopriva S, De Kok LJ (eds) Nutrient use efficiency in plants: concepts and approaches. Springer, Cham, pp 205–228

    Google Scholar 

  • Wulff-Zottele C, Gatzke N, Kopka J, Orellana A, Hoefgen R, Fisahn J, Hesse H (2010) Photosynthesis and metabolism interact during acclimation of Arabidopsis thaliana to high irradiance and sulphur depletion. Plant Cell Environ 33:1974–1988

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank the Max Planck Society (MPG) for funding.

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Correspondence to Rainer Hoefgen .

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Hoefgen, R., Watanabe, M. (2017). Re-assessing Systems Biology Approaches on Analyzing Sulfate Metabolism. In: De Kok, L., Hawkesford, M., Haneklaus, S., Schnug, E. (eds) Sulfur Metabolism in Higher Plants - Fundamental, Environmental and Agricultural Aspects. Proceedings of the International Plant Sulfur Workshop. Springer, Cham. https://doi.org/10.1007/978-3-319-56526-2_12

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