The significance of cysteine synthesis for acclimation to high light conditions

Speiser A, Haberland S, Watanabe M, Wirtz M, Dietz K-J, Saito K, Hell R (2015)
Frontiers in Plant Science 5: 776.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
Download
Es wurden keine Dateien hochgeladen. Nur Publikationsnachweis!
Autor*in
Speiser, Anna; Haberland, Stefan; Watanabe, Mutsumi; Wirtz, Markus; Dietz, Karl-JosefUniBi; Saito, Kazuki; Hell, Rüdiger
Abstract / Bemerkung
Situations of excess light intensity are known to result in the emergence of reactive oxygen species that originate from the electron transport chain in chloroplasts. The redox state of glutathione and its biosynthesis contribute importantly to the plant's response to this stress. In this study we analyzed the significance of cysteine synthesis for long-term acclimation to high light conditions in Arabidopsis thaliana. Emphasis was put on the rate-limiting step of cysteine synthesis, the formation of the precursor O-acetylserine (OAS) that is catalyzed by serine acetyltransferase (SERAT). Wild type Arabidopsis plants responded to the high light condition (800 mu mol m(-2) s(-1) for 10 days) with synthesis of photo-protective anthocyanins, induction of total SERAT activity and elevated glutathione levels when compared to the control condition (100 mu mol m(-2) s(-1)). The role of cysteine synthesis in chloroplasts was probed in mutant plants lacking the chloroplast isoform SERAT2;1 (serat2;1) and two knock-out alleles of CYP20-3, a positive interactor of SERAT in the chloroplast. Acclimation to high light resulted in a smaller growth enhancement than wild type in the serat2;1 and cyp20-3 mutants, less induction of total SERAT activity and OAS levels but similar cysteine and glutathione concentrations. Expression analysis revealed no increase in mRNA of the chloroplast SERAT2;1 encoding SERAT2;1 gene but up to 4.4-fold elevated SERAT2;2 mRNA levels for the mitochondrial SE RAT isoform. Thus, lack of chloroplast SERAT2;1 activity or its activation by CYP20-3 prevents the full growth response to high light conditions, but the enhanced demand for glutathione is likely mediated by synthesis of OAS in the mitochondria. In conclusion, cysteine synthesis in the chloroplast is important for performance but is dispensable for survival under long-term exposure to high light and can be partially complemented by cysteine synthesis in mitochondria.
Stichworte
glutathione; mitochondria; SERAT; high light stress; chloroplasts; CYP20-3
Erscheinungsjahr
2015
Zeitschriftentitel
Frontiers in Plant Science
Band
5
Art.-Nr.
776
ISSN
1664-462X
Page URI
https://pub.uni-bielefeld.de/record/2720078

Zitieren

Speiser A, Haberland S, Watanabe M, et al. The significance of cysteine synthesis for acclimation to high light conditions. Frontiers in Plant Science. 2015;5: 776.
Speiser, A., Haberland, S., Watanabe, M., Wirtz, M., Dietz, K. - J., Saito, K., & Hell, R. (2015). The significance of cysteine synthesis for acclimation to high light conditions. Frontiers in Plant Science, 5, 776. doi:10.3389/fpls.2014.00776
Speiser, Anna, Haberland, Stefan, Watanabe, Mutsumi, Wirtz, Markus, Dietz, Karl-Josef, Saito, Kazuki, and Hell, Rüdiger. 2015. “The significance of cysteine synthesis for acclimation to high light conditions”. Frontiers in Plant Science 5: 776.
Speiser, A., Haberland, S., Watanabe, M., Wirtz, M., Dietz, K. - J., Saito, K., and Hell, R. (2015). The significance of cysteine synthesis for acclimation to high light conditions. Frontiers in Plant Science 5:776.
Speiser, A., et al., 2015. The significance of cysteine synthesis for acclimation to high light conditions. Frontiers in Plant Science, 5: 776.
A. Speiser, et al., “The significance of cysteine synthesis for acclimation to high light conditions”, Frontiers in Plant Science, vol. 5, 2015, : 776.
Speiser, A., Haberland, S., Watanabe, M., Wirtz, M., Dietz, K.-J., Saito, K., Hell, R.: The significance of cysteine synthesis for acclimation to high light conditions. Frontiers in Plant Science. 5, : 776 (2015).
Speiser, Anna, Haberland, Stefan, Watanabe, Mutsumi, Wirtz, Markus, Dietz, Karl-Josef, Saito, Kazuki, and Hell, Rüdiger. “The significance of cysteine synthesis for acclimation to high light conditions”. Frontiers in Plant Science 5 (2015): 776.

7 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Sulfate-Induced Stomata Closure Requires the Canonical ABA Signal Transduction Machinery.
Rajab H, Khan MS, Malagoli M, Hell R, Wirtz M., Plants (Basel) 8(1), 2019
PMID: 30654485
Peroxiredoxins and Redox Signaling in Plants.
Liebthal M, Maynard D, Dietz KJ., Antioxid Redox Signal 28(7), 2018
PMID: 28594234
Sulfur Partitioning between Glutathione and Protein Synthesis Determines Plant Growth.
Speiser A, Silbermann M, Dong Y, Haberland S, Uslu VV, Wang S, Bangash SAK, Reichelt M, Meyer AJ, Wirtz M, Hell R., Plant Physiol 177(3), 2018
PMID: 29752309
The redox-sensitive module of cyclophilin 20-3, 2-cysteine peroxiredoxin and cysteine synthase integrates sulfur metabolism and oxylipin signaling in the high light acclimation response.
Müller SM, Wang S, Telman W, Liebthal M, Schnitzer H, Viehhauser A, Sticht C, Delatorre C, Wirtz M, Hell R, Dietz KJ., Plant J 91(6), 2017
PMID: 28644561

61 References

Daten bereitgestellt von Europe PubMed Central.

Functional complementation of anthocyanin sequestration in the vacuole by widely divergent glutathione S-transferases.
Alfenito MR, Souer E, Goodman CD, Buell R, Mol J, Koes R, Walbot V., Plant Cell 10(7), 1998
PMID: 9668133
Kinetics of retrograde signalling initiation in the high light response of Arabidopsis thaliana.
Alsharafa K, Vogel MO, Oelze ML, Moore M, Stingl N, Konig K, Friedman H, Mueller MJ, Dietz KJ., Philos. Trans. R. Soc. Lond., B, Biol. Sci. 369(1640), 2014
PMID: 24591725
Too much of a good thing: light can be bad for photosynthesis.
Barber J, Andersson B., Trends Biochem. Sci. 17(2), 1992
PMID: 1566330
Photosynthetic adaptation to length of day is dependent on S-sulfocysteine synthase activity in the thylakoid lumen.
Bermudez MA, Galmes J, Moreno I, Mullineaux PM, Gotor C, Romero LC., Plant Physiol. 160(1), 2012
PMID: 22829322
Low abundance does not mean less importance in cysteine metabolism.
Gotor C, Alvarez C, Bermudez MA, Moreno I, Garcia I, Romero LC., Plant Signal Behav 5(8), 2010
PMID: 20699647
Function of ROC4 in the efficient repair of photodamaged photosystem II in Arabidopsis.
Cai W, Ma J, Guo J, Zhang L., Photochem. Photobiol. 84(6), 2008
PMID: 19067955
Environmental significance of anthocyanins in plant stress responses
Chalker-Scott L.., 1999
Balancing metabolites in drought: the sulfur assimilation conundrum.
Chan KX, Wirtz M, Phua SY, Estavillo GM, Pogson BJ., Trends Plant Sci. 18(1), 2012
PMID: 23040678
A cyclophilin links redox and light signals to cysteine biosynthesis and stress responses in chloroplasts.
Dominguez-Solis JR, He Z, Lima A, Ting J, Buchanan BB, Luan S., Proc. Natl. Acad. Sci. U.S.A. 105(42), 2008
PMID: 18845687
A simple and rapid method for the preparation of plant genomic DNA for PCR analysis.
Edwards K, Johnstone C, Thompson C., Nucleic Acids Res. 19(6), 1991
PMID: 2030957
Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health.
Edwards R, Dixon DP, Walbot V., Trends Plant Sci. 5(5), 2000
PMID: 10785664
Photorespiratory metabolism: genes, mutants, energetics, and redox signaling.
Foyer CH, Bloom AJ, Queval G, Noctor G., Annu Rev Plant Biol 60(), 2009
PMID: 19575589
Ascorbate and glutathione: the heart of the redox hub.
Foyer CH, Noctor G., Plant Physiol. 155(1), 2011
PMID: 21205630
Imaging of photo-oxidative stress responses in leaves.
Fryer MJ, Oxborough K, Mullineaux PM, Baker NR., J. Exp. Bot. 53(372), 2002
PMID: 11997373
Characterization and Measurement of Anthocyanins by UV-Visible Spectroscopy
Giusti M., Wrolstad R.., 2001
Negative regulation of anthocyanin biosynthesis in Arabidopsis by a miR156-targeted SPL transcription factor.
Gou JY, Felippes FF, Liu CJ, Weigel D, Wang JW., Plant Cell 23(4), 2011
PMID: 21487097
Do anthocyanins function as antioxidants in leaves? Imaging of HO in red and green leaves after mechanical injury
Gould K., McKelvie J., Markham K.., 2002
Mitochondrial serine acetyltransferase functions as a pacemaker of cysteine synthesis in plant cells.
Haas FH, Heeg C, Queiroz R, Bauer A, Wirtz M, Hell R., Plant Physiol. 148(2), 2008
PMID: 18753283
The serine acetyltransferase gene family in Arabidopsis thaliana and the regulation of its expression by cadmium.
Howarth JR, Dominguez-Solis JR, Gutierrez-Alcala G, Wray JL, Romero LC, Gotor C., Plant Mol. Biol. 51(4), 2003
PMID: 12650624
Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes.
Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P., Adv Bioinformatics 2008(), 2008
PMID: 19956698
Sulfite reductase defines a newly discovered bottleneck for assimilatory sulfate reduction and is essential for growth and development in Arabidopsis thaliana.
Khan MS, Haas FH, Samami AA, Gholami AM, Bauer A, Fellenberg K, Reichelt M, Hansch R, Mendel RR, Meyer AJ, Wirtz M, Hell R., Plant Cell 22(4), 2010
PMID: 20424176
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.
Lehmann M, Schwarzlander M, Obata T, Sirikantaramas S, Burow M, Olsen CE, Tohge T, Fricker MD, Moller BL, Fernie AR, Sweetlove LJ, Laxa M., Mol Plant 2(3), 2008
PMID: 19825624
Cloning and characterization of chloroplast and cytosolic forms of cyclophilin from Arabidopsis thaliana.
Lippuner V, Chou IT, Scott SV, Ettinger WF, Theg SM, Gasser CS., J. Biol. Chem. 269(11), 1994
PMID: 8132503
The NADPH-dependent thioredoxin system constitutes a functional backup for cytosolic glutathione reductase in Arabidopsis.
Marty L, Siala W, Schwarzlander M, Fricker MD, Wirtz M, Sweetlove LJ, Meyer Y, Meyer AJ, Reichheld JP, Hell R., Proc. Natl. Acad. Sci. U.S.A. 106(22), 2009
PMID: 19451637
Evidence for posttranscriptional activation of gamma-glutamylcysteine synthetase during plant stress responses.
May MJ, Vernoux T, Sanchez-Fernandez R, Van Montagu M, Inze D., Proc. Natl. Acad. Sci. U.S.A. 95(20), 1998
PMID: 9751788
Glutathione homeostasis and redox-regulation by sulfhydryl groups.
Meyer AJ, Hell R., Photosyn. Res. 86(3), 2005
PMID: 16315075
Chloroplast cyclophilin is a target protein of thioredoxin. Thiol modulation of the peptidyl-prolyl cis-trans isomerase activity.
Motohashi K, Koyama F, Nakanishi Y, Ueoka-Nakanishi H, Hisabori T., J. Biol. Chem. 278(34), 2003
PMID: 12923164
ASCORBATE AND GLUTATHIONE: Keeping Active Oxygen Under Control.
Noctor G, Foyer CH., Annu. Rev. Plant Physiol. Plant Mol. Biol. 49(), 1998
PMID: 15012235
Glutathione in plants: an integrated overview.
Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, Queval G, Foyer CH., Plant Cell Environ. 35(2), 2011
PMID: 21777251
Glutathione.
Noctor G, Queval G, Mhamdi A, Chaouch S, Foyer CH., Arabidopsis Book 9(), 2011
PMID: 22303267
Cyclophilin 20-3 relays a 12-oxo-phytodienoic acid signal during stress responsive regulation of cellular redox homeostasis.
Park SW, Li W, Viehhauser A, He B, Kim S, Nilsson AK, Andersson MX, Kittle JD, Ambavaram MM, Luan S, Esker AR, Tholl D, Cimini D, Ellerstrom M, Coaker G, Mitchell TK, Pereira A, Dietz KJ, Lawrence CB., Proc. Natl. Acad. Sci. U.S.A. 110(23), 2013
PMID: 23671085
The oligomeric stromal proteome of Arabidopsis thaliana chloroplasts.
Peltier JB, Cai Y, Sun Q, Zabrouskov V, Giacomelli L, Rudella A, Ytterberg AJ, Rutschow H, van Wijk KJ., Mol. Cell Proteomics 5(1), 2005
PMID: 16207701
The Arabidopsis cyclophilin gene family.
Romano PG, Horton P, Gray JE., Plant Physiol. 134(4), 2004
PMID: 15051864
A mutation affecting ASCORBATE PEROXIDASE 2 gene expression reveals a link between responses to high light and drought tolerance.
Rossel JB, Walter PB, Hendrickson L, Chow WS, Poole A, Mullineaux PM, Pogson BJ., Plant Cell Environ. 29(2), 2006
PMID: 17080642

Sambrook J., Fritsch E., Maniatis T.., 1989
ROS and redox signalling in the response of plants to abiotic stress.
Suzuki N, Koussevitzky S, Mittler R, Miller G., Plant Cell Environ. 35(2), 2011
PMID: 21486305
Light intensity-dependent retrograde signalling in higher plants.
Szechynska-Hebda M, Karpinski S., J. Plant Physiol. 170(17), 2013
PMID: 23850030
Genome-wide analysis of hydrogen peroxide-regulated gene expression in Arabidopsis reveals a high light-induced transcriptional cluster involved in anthocyanin biosynthesis.
Vanderauwera S, Zimmermann P, Rombauts S, Vandenabeele S, Langebartels C, Gruissem W, Inze D, Van Breusegem F., Plant Physiol. 139(2), 2005
PMID: 16183842
The cyclophilins.
Wang P, Heitman J., Genome Biol. 6(7), 2005
PMID: 15998457
Physiological roles of the beta-substituted alanine synthase gene family in Arabidopsis.
Watanabe M, Kusano M, Oikawa A, Fukushima A, Noji M, Saito K., Plant Physiol. 146(1), 2007
PMID: 18024555
Comparative genomics and reverse genetics analysis reveal indispensable functions of the serine acetyltransferase gene family in Arabidopsis.
Watanabe M, Mochida K, Kato T, Tabata S, Yoshimoto N, Noji M, Saito K., Plant Cell 20(9), 2008
PMID: 18776059
Mitochondrial cysteine synthase complex regulates O-acetylserine biosynthesis in plants.
Wirtz M, Beard KF, Lee CP, Boltz A, Schwarzlander M, Fuchs C, Meyer AJ, Heeg C, Sweetlove LJ, Ratcliffe RG, Hell R., J. Biol. Chem. 287(33), 2012
PMID: 22730323
Structure and function of the hetero-oligomeric cysteine synthase complex in plants.
Wirtz M, Birke H, Heeg C, Muller C, Hosp F, Throm C, Konig S, Feldman-Salit A, Rippe K, Petersen G, Wade RC, Rybin V, Scheffzek K, Hell R., J. Biol. Chem. 285(43), 2010
PMID: 20720017
The biological functions of glutathione revisited in arabidopsis transgenic plants with altered glutathione levels.
Xiang C, Werner BL, Christensen EM, Oliver DJ., Plant Physiol. 126(2), 2001
PMID: 11402187
Protective effect of supplemental anthocyanins on Arabidopsis leaves under high light
Zeng XQ, Chow WS, Su LJ, Peng XX, Peng CL., Physiol Plant 138(2), 2010
PMID: IND44310578
Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®
Quellen

PMID: 25653656
PubMed | Europe PMC

Suchen in

Google Scholar