Abstract
Sulfate is an important macro nutrient for plant growth. Sulfate starvation negatively influences crop yield and plant performance. Systems analysis at the transcriptome and metabolome level of Arabidopsis thaliana exposed to sulfate deprivation recently provided further evidence that O-acetyl-L-serine (OAS) acts as a signal within plant sulfate deprivation response, but also under conditions when the sulfate status is not disturbed, such as reactive oxygen species (ROS ) accumulation, light to dark shifts or during the diurnal cycle. Here we compare the transcriptomes of roots and whole seedlings exposed to sulfate starvation with that of plants where OAS accumulation was induced by overexpression of a serine acetyltranferase gene (SERAT2;1). The results provide evidence for a sulfate-independent signalling role of OAS and for the modular response of plants to sulfate starvation.
Keywords
- Seed Storage Protein
- Sulfate Starvation
- Salicylic Acid Biosynthesis
- Brassinosteroid Signaling
- Modular Response
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Aarabi et al (2015) Chapter 13: OAS cluster genes: a tightly co-regulated network
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
Bogamuwa SP, Jang JC (2014) Tandem CCCH zinc finger proteins in plant growth, development and stress response. PCP 55:1367–1375
Caldana C, Degenkolbe T, Cuadros-Inostroza A, Klie S, Sulpice R, Leisse A, Steinhauser D, Fernie AR, Willmitzer L, Hannah MA (2011) High-density kinetic analysis of the metabolomic and transcriptomic response of Arabidopsis to eight environmental conditions. Plant J 67:869–884
Dominguez-Solis JR, He Z, Lima A, Ting J, Buchanan BB, Luan S (2009) A cyclophilin links redox and light signals to cysteine biosynthesis and stress responses in chloroplasts. Proc Natl Acad Sci U S A 106:1292–1292
Espinoza C, Degenkolbe T, Caldana C, Zuther E, Leisse A, Willmitzer L, Hincha DK, Hannah MA (2010) Interaction with diurnal and circadian regulation results in dynamic metabolic and transcriptional changes during cold acclimation in Arabidopsis. PLoS One 5(11):e14101. doi:10.1371/journal.pone.0014101
Falkenberg B, Witt I, Zanor MI, Steinhauser D, Mueller-Roeber B, Hesse H, Hoefgen R (2008) Transcription factors relevant to auxin signaling coordinate broad-spectrum metabolic shifts including sulphur metabolism. J Exp Bot 59:2831–2846
Gruber BD, Giehl RF, Friedel S, von Wirén N (2013) Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiol 163:161–179
Hoefgen R, Hesse H (2008) Sulfur and cysteine metabolism. In: Jez J (ed) Sulfur: a missing link between soils, crops and nutrition, vol 50. American Society of Agronomy, Madison, pp 83–104
Hopkins L, Parmar S, Blaszczyk A, Hesse H, Hoefgen R, Hawkesford MJ (2005) O-acetylserine and the regulation of expression of genes encoding components for sulfate uptake and assimilation in potato. Plant Physiol 13:433–440
Hubberten HM, Hesse H, Hoefgen R (2009) Lateral root growth in sulfur enriched patches. In: Sirko A, De Kok LJ, Haneklaus S, Hawkesford MJ, Rennenberg H, Saito K, Schnug E, Stulen I (eds) Sulfur metabolism in plants: regulatory aspects, significance of sulfur in the food chain, agriculture and the environment. Backhuys Publishers, Leiden, pp 105–108, Margraf Publishers, Weikersheim
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
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
Kinnersley AM, Turano FJ (2000) Gamma aminobutyric acid (GABA) and plant responses to stress. Crit Rev Plant Sci 19:479–509
Ko JH, Yang SH, Han KH (2006) Upregulation of an Arabidopsis RING-H2 gene, XERICO, confers drought tolerance through increased abscisic acid biosynthesis. Plant J 47:343–355
Krueger S, Niehl A, Lopez-Martin MC, Steinhauser D, Donath A, Hildebrandt T, Romero LC, Hoefgen R, Gotor C, Hesse H (2009) Sub-cellular analysis of Arabidopsis serine acetyltransferase mutants: implications of compartmentation for cysteine biosynthesis. Plant Cell Environ 32:349–367
Krueger S, Donath A, Lopez-Martin MC, Hoefgen R, Gotor C, Hesse H (2010) Impact of sulfur starvation on cysteine biosynthesis in T-DNA mutants deficient for compartment-specific serine-acetyltransferase. Amino Acids 39:1029–1042
Lee BR, Huseby S, Koprivova A, Chételat A, Wirtz M, Mugford ST, Navid E, Brearley C, Saha S, Mithen R, Hell R, Farmer EE, Kopriva S (2012) Effects of fou8/fry1 mutation on sulfur metabolism: is decreased internal sulfate the trigger of sulfate starvation response? PLoS One 7:e39425
Lehmann M, Schwarzlaender M, Obata T, Sirikantaramas S, Burow M, Olsen CE, Tohge T, Fricker MD, Moller BL, Fernie AR, Sweetlove LJ, Laxa M (2009) The metabolic response of Arabidopsis roots to oxidative stress is distinct from that of heterotrophic cells in culture and highlights a complex relationship between the levels of transcripts, metabolites, and flux. Mol Plant 2:390–406
Lewandowska M, Wawrzynska A, Moniuszko G, Lukomska J, Zientara K, Piecho M, Hodurek P, Zhukov I, Liszewska F, Nikiforova V, Sirko A (2010) A contribution to identification of novel regulators of plant response to sulfur deficiency: characteristics of a tobacco gene UP9C, its protein product and the effects of UP9C silencing. Mol Plant 3:347–360
Li P, Ma S, Bohnert HJ (2008) Coexpression characteristics of trehalose-6-phosphate phosphatase subfamily genes reveal different functions in a network context. Physiol Plant 133:544–556
Lisso J, Schröder F, Müssig C (2013) EXO modifies sucrose and trehalose responses and connects the extracellular carbon status to growth. Front Plant Sci 4:219. doi:10.3389/fpls.2013.00219
Maris A, Kaewthai N, Eklöf JM, Miller JG, Brumer H, Fry SC, Verbelen JP, Vissenberg K (2011) Differences in enzymic properties of five recombinant xyloglucan endotransglucosylase/hydrolase (XTH) proteins of Arabidopsis thaliana. J Exp Bot 62:261–271
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
Minocha R, Majumdar R, Minocha SC (2014) Polyamines and abiotic stress in plants: a complex relationship. Front Plant Sci 5:175. doi:10.3389/fpls.2014.00175
Miyashita Y, Good AG (2008) Contribution of the GABA shunt to hypoxia-induced alanine accumulation in roots of Arabidopsis thaliana. Plant Cell Physiol 49:92–102
Nikiforova VJ, Freitag J, Kempa S, Adamik M, Hesse H, Hoefgen R (2003) Transcriptome analysis of sulphur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant J 33:633–650
Nikiforova VJ, Gakiere B, Kempa S, Adamik M, Willmitzer L, Hesse H, Hoefgen R (2004) Towards dissecting nutrient metabolism in plants: a systems biology case study on sulphur metabolism. J Exp Bot 55:1861–1870
Nikiforova VJ, Kopka J, Tolstikov V, Fieh O, Hopkins L, Hawkesford MJ, Hesse H, Hoefgen R (2005) Systems re-balancing of metabolism in response to sulfur deprivation, as revealed by metabolome analysis of Arabidopsis plants. Plant Physiol 138:304–318
Obayashi T, Kinoshita K, Nakai K, Shibaoka M, Hayashi S, Saeki M, Shibata D, Saito K, Ohta H (2007) ATTED-II: a database of co-expressed genes and cis-elements for identifying co-regulated gene groups in Arabidopsis. Nucleic Acids Res 35:D863–D869
Rashid A, Badhan A, Deyholos M, Kav N (2013) Proteomic profiling of the aleurone layer of mature Arabidopsis thaliana seed. Plant Mol Biol Rep 31:464–469
Rouached H, Secco D, Arpat B, Poirier Y (2011) The transcription factor PHR1 plays a key role inthe regulation of sulfate shoot-to-root flux upon phosphate starvation in Arabidopsis. BMC Plant Biol 11:19. doi:10.1186/1471-2229-11-19
Saito K (2000) Regulation of sulfate transport and synthesis of sulfur-containing amino acids. Curr Opin Plant Biol 3:188–195
Sakakibara H, Takei K, Hirose N (2006) Interactions between nitrogen and cytokinin in the regulation of metabolism and development. TiPS 11:440–448
Sasaki-Sekimoto Y, Jikumaru Y, Obayashi T, Saito H, Masuda S, Kamiya Y, Ohta H, Shirasu K (2013) Basic helix-loop-helix transcription factors JASMONATE-ASSOCIATED MYC2-LIKE1 (JAM1), JAM2, and JAM3 are negative regulators of jasmonate responses in Arabidopsis. Plant Physiol 163:291–304
Schröder F, Lisso J, Lange P, Müssig C (2009) The extracellular EXO protein mediates cell expansion in Arabidopsis leaves. BMC Plant Biol. doi:10.1186/1471-2229-9-20
Stamm P, Kumar PP (2013) Auxin and gibberellin responsive Arabidopsis SMALL AUXIN UP RNA36 regulates hypocotyl elongation in the light. Plant Cell Rep 32:759–769
Tahir J, Watanabe M, Jing HC, Hunter DA, Tohge T, Nunes-Nesi A, Brotman Y, Fernie AR, Hoefgen R, Dijkwel PP (2013) Activation of R-mediated innate immunity and disease susceptibility is affected by mutations in a cytosolic O-acetylserine (thiol) lyase in Arabidopsis. Plant J 73:118–130
Vandesteene L, López-Galvis L, Vanneste K, Feil R, Maere S, Lammens W, Rolland F, Lunn JE, Avonce N, Beeckman T, Van Dijck P (2012) Expansive evolution of the trehalose-6-phosphate phosphatase gene family in Arabidopsis. Plant Physiol 160:884–896
Wan D, Li R, Zou B, Zhang X, Cong J, Wang R, Xia Y, Li G (2012) Calmodulin-binding protein CBP60g is a positive regulator of both disease resistance and drought tolerance in Arabidopsis. Plant Cell Rep 31:1269–1281
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
Watanabe M, Hubberten HM, Hoefgen R (2012) Plant response to mineral ion availability: transcriptome responses to sulfate, selenium and iron. In: De Kok LJ, Tausz M, Hawkesford MJ, Hoefgen R, McManus MT, Norton RM, Rennenberg H, Saito K, Schnug E, Tabe L (eds) Sulfur metabolism in plants, Proceedings of the International Sulfur Workshop. Springer, Netherlands, pp 123–134
Watanabe M, Balazadeh S, Tohge T, Erban A, Giavalisco P, Kopka J, Mueller-Roeber B, Fernie AR, Hoefgen R (2013) Comprehensive dissection of spatio-temporal metabolic shifts in primary, secondary and lipid metabolism during developmental senescence in Arabidopsis thaliana. Plant Physiol 162:1290–1310
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 (ZG), Switzerland, pp 205–228
Acknowledgements
We thank Sarah J Whitcomb for discussion and help with preparing the manuscript. We thank the Max Planck Society for financial contribution. Additional funding was received for HMH by the DFG grant HO1916/3-2, for FA by the Ministry of Science, Research and Technology of Iran and for EH by the EU – ITN grant 264296 (acronym: BIONUT).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2015 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Hubberten, HM., Watanabe, M., Bielecka, M., Heyneke, E., Aarabi, F., Hoefgen, R. (2015). More Than a Substrate: The O-Acetylserine Responsive Transcriptome. In: De Kok, L., Hawkesford, M., Rennenberg, H., Saito, K., Schnug, E. (eds) Molecular Physiology and Ecophysiology of Sulfur. Proceedings of the International Plant Sulfur Workshop. Springer, Cham. https://doi.org/10.1007/978-3-319-20137-5_14
Download citation
DOI: https://doi.org/10.1007/978-3-319-20137-5_14
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-20136-8
Online ISBN: 978-3-319-20137-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)