Impact of SO2 on Arabidopsis thaliana transcriptome in wildtype and sulfite oxidase knockout plants analyzed by RNA deep sequencing

Hamisch D, Randewig D, Schliesky S, Bräutigam A, Weber APM, Geffers R, Herschbach C, Rennenberg H, Mendel RR, Hänsch R (2012)
New Phytologist 196(4): 1074-1085.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
OA 1.62 MB
Hamisch, Domenica; Randewig, Doerte; Schliesky, Simon; Bräutigam, AndreaUniBi ; Weber, Andreas P. M.; Geffers, Robert; Herschbach, Cornelia; Rennenberg, Heinz; Mendel, Ralf R.; Hänsch, Robert
Abstract / Bemerkung
High concentrations of sulfur dioxide (SO2) as an air pollutant, and its derivative sulfite, cause abiotic stress that can lead to cell death. It is currently unknown to what extent plant fumigation triggers specific transcriptional responses. To address this question, and to test the hypothesis that sulfite oxidase (SO) is acting in SO2 detoxification, we compared Arabidopsis wildtype (WT) and SO knockout lines (SO-KO) facing the impact of 600 nl l (1) SO2, using RNAseq to quantify absolute transcript abundances. These transcriptome data were correlated to sulfur metabolism-related enzyme activities and metabolites obtained from identical samples in a previous study. SO-KO plants exhibited remarkable and broad regulative responses at the mRNA level, especially in transcripts related to sulfur metabolism enzymes, but also in those related to stress response and senescence. Focusing on SO regulation, no alterations were detectable in the WT, whereas in SO-KO plants we found up-regulation of two splice variants of the SO gene, although this gene is not functional in this line. Our data provide evidence for the highly specific coregulation between SO and sulfur-related enzymes like APS reductase, and suggest two novel candidates for involvement in SO2 detoxification: an apoplastic peroxidase, and defensins as putative cysteine mass storages.
Arabidopsis knockout mutants; cluster analyses; gene ontology; RNA-deep-sequencing; SO2 fumigation; sulfate assimilation; sulfite; detoxification; sulfite oxidase (SO)
New Phytologist
Page URI


Hamisch D, Randewig D, Schliesky S, et al. Impact of SO2 on Arabidopsis thaliana transcriptome in wildtype and sulfite oxidase knockout plants analyzed by RNA deep sequencing. New Phytologist. 2012;196(4):1074-1085.
Hamisch, D., Randewig, D., Schliesky, S., Bräutigam, A., Weber, A. P. M., Geffers, R., Herschbach, C., et al. (2012). Impact of SO2 on Arabidopsis thaliana transcriptome in wildtype and sulfite oxidase knockout plants analyzed by RNA deep sequencing. New Phytologist, 196(4), 1074-1085. doi:10.1111/j.1469-8137.2012.04331.x
Hamisch, D., Randewig, D., Schliesky, S., Bräutigam, A., Weber, A. P. M., Geffers, R., Herschbach, C., Rennenberg, H., Mendel, R. R., and Hänsch, R. (2012). Impact of SO2 on Arabidopsis thaliana transcriptome in wildtype and sulfite oxidase knockout plants analyzed by RNA deep sequencing. New Phytologist 196, 1074-1085.
Hamisch, D., et al., 2012. Impact of SO2 on Arabidopsis thaliana transcriptome in wildtype and sulfite oxidase knockout plants analyzed by RNA deep sequencing. New Phytologist, 196(4), p 1074-1085.
D. Hamisch, et al., “Impact of SO2 on Arabidopsis thaliana transcriptome in wildtype and sulfite oxidase knockout plants analyzed by RNA deep sequencing”, New Phytologist, vol. 196, 2012, pp. 1074-1085.
Hamisch, D., Randewig, D., Schliesky, S., Bräutigam, A., Weber, A.P.M., Geffers, R., Herschbach, C., Rennenberg, H., Mendel, R.R., Hänsch, R.: Impact of SO2 on Arabidopsis thaliana transcriptome in wildtype and sulfite oxidase knockout plants analyzed by RNA deep sequencing. New Phytologist. 196, 1074-1085 (2012).
Hamisch, Domenica, Randewig, Doerte, Schliesky, Simon, Bräutigam, Andrea, Weber, Andreas P. M., Geffers, Robert, Herschbach, Cornelia, Rennenberg, Heinz, Mendel, Ralf R., and Hänsch, Robert. “Impact of SO2 on Arabidopsis thaliana transcriptome in wildtype and sulfite oxidase knockout plants analyzed by RNA deep sequencing”. New Phytologist 196.4 (2012): 1074-1085.
Alle Dateien verfügbar unter der/den folgenden Lizenz(en):
Copyright Statement:
Dieses Objekt ist durch das Urheberrecht und/oder verwandte Schutzrechte geschützt. [...]
Access Level
OA Open Access
Zuletzt Hochgeladen
MD5 Prüfsumme

13 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

The mechanism of SO2 -induced stomatal closure differs from O3 and CO2 responses and is mediated by nonapoptotic cell death in guard cells.
Ooi L, Matsuura T, Munemasa S, Murata Y, Katsuhara M, Hirayama T, Mori IC., Plant Cell Environ 42(2), 2019
PMID: 30014483
Sulfite Reductase Co-suppression in Tobacco Reveals Detoxification Mechanisms and Downstream Responses Comparable to Sulfate Starvation.
Naumann M, Hubberten HM, Watanabe M, Hänsch R, Schöttler MA, Hoefgen R., Front Plant Sci 9(), 2018
PMID: 30374361
Toxicity of Melaleuca alternifolia essential oil to the mitochondrion and NAD+/NADH dehydrogenase in Tribolium confusum.
Liao M, Yang QQ, Xiao JJ, Huang Y, Zhou LJ, Hua RM, Cao HQ., PeerJ 6(), 2018
PMID: 30479882
Drought-Enhanced Xylem Sap Sulfate Closes Stomata by Affecting ALMT12 and Guard Cell ABA Synthesis.
Malcheska F, Ahmad A, Batool S, Müller HM, Ludwig-Müller J, Kreuzwieser J, Randewig D, Hänsch R, Mendel RR, Hell R, Wirtz M, Geiger D, Ache P, Hedrich R, Herschbach C, Rennenberg H., Plant Physiol 174(2), 2017
PMID: 28446637
miR398 and miR395 are involved in response to SO2 stress in Arabidopsis thaliana.
Li L, Yi H, Xue M, Yi M., Ecotoxicology 26(9), 2017
PMID: 28819808
Azolla domestication towards a biobased economy?
Brouwer P, Bräutigam A, Külahoglu C, Tazelaar AO, Kurz S, Nierop KG, van der Werf A, Weber AP, Schluepmann H., New Phytol 202(3), 2014
PMID: 24494738
Oxidation and reduction of sulfite contribute to susceptibility and detoxification of SO₂ in Populus� ×� canescens leaves
Randewig D, Hamisch D, Eiblmeier M, Boedecker C, Kreuzwieser J, Mendel RR, Hänsch R, Herschbach C, Rennenberg H., Trees (Berl West) 28(2), 2014
PMID: IND500740240
Impairment in Sulfite Reductase Leads to Early Leaf Senescence in Tomato Plants.
Yarmolinsky D, Brychkova G, Kurmanbayeva A, Bekturova A, Ventura Y, Khozin-Goldberg I, Eppel A, Fluhr R, Sagi M., Plant Physiol 165(4), 2014
PMID: 24987017
Is white clover able to switch to atmospheric sulphur sources when sulphate availability decreases?
Varin S, Lemauviel-Lavenant S, Cliquet JB., J Exp Bot 64(8), 2013
PMID: 23645868

54 References

Daten bereitgestellt von Europe PubMed Central.

The basis for different sensitivities of photosynthesis to SO2 in two cultivars of pea
Alscher, Journal of Experimental Botany 38(), 1987
Studies on the tolerance to sulphur dioxide of grass populations in polluted areas. I. Identification of tolerant populations
Ayazloo, The New Phytologist 88(), 1981
A stress-inducible sulphotransferase sulphonates salicylic acid and confers pathogen resistance in Arabidopsis.
Baek D, Pathange P, Chung JS, Jiang J, Gao L, Oikawa A, Hirai MY, Saito K, Pare PW, Shi H., Plant Cell Environ. 33(8), 2010
PMID: 20374532
Response of plants to sulphur dioxide
Bell, Nature 284(), 1980
Peroxidase-dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance.
Bindschedler LV, Dewdney J, Blee KA, Stone JM, Asai T, Plotnikov J, Denoux C, Hayes T, Gerrish C, Davies DR, Ausubel FM, Bolwell GP., Plant J. 47(6), 2006
PMID: 16889645
Sulfite oxidase protects plants against sulfur dioxide toxicity.
Brychkova G, Xia Z, Yang G, Yesbergenova Z, Zhang Z, Davydov O, Fluhr R, Sagi M., Plant J. 50(4), 2007
PMID: 17425719
Elevated glutathione biosynthetic capacity in the chloroplasts of transgenic tobacco plants paradoxically causes increased oxidative stress
Creissen G, Firmin J, Fryer M, Kular B, Leyland N, Reynolds H, Pastori G, Wellburn F, Baker N, Wellburn A, Mullineaux P., Plant Cell 11(7), 1999
PMID: 10402429
Regulation of sulfate uptake and assimilation--the same or not the same?
Davidian JC, Kopriva S., Mol Plant 3(2), 2010
PMID: 20139159

De, 1990

De, Plant Ecophysiology 6(), 2007
Identification and biochemical characterization of Arabidopsis thaliana sulfite oxidase. A new player in plant sulfur metabolism.
Eilers T, Schwarz G, Brinkmann H, Witt C, Richter T, Nieder J, Koch B, Hille R, Hansch R, Mendel RR., J. Biol. Chem. 276(50), 2001
PMID: 11598126

Filner, 1984
The plant glutathione transferase gene family: genomic structure, functions, expression and evolution
Frova, Physiologia Plantarum 119(), 2003
Cytosolic γ-glutamyl peptidases process glutathione conjugates in the biosynthesis of glucosinolates and camalexin in Arabidopsis.
Geu-Flores F, Moldrup ME, Bottcher C, Olsen CE, Scheel D, Halkier BA., Plant Cell 23(6), 2011
PMID: 21712415
Plant sulfite oxidase as novel producer of H2O2: combination of enzyme catalysis with a subsequent non-enzymatic reaction step.
Hansch R, Lang C, Riebeseel E, Lindigkeit R, Gessler A, Rennenberg H, Mendel RR., J. Biol. Chem. 281(10), 2006
PMID: 16407262
Sulfite oxidation in plant peroxisomes.
Hansch R, Mendel RR., Photosyn. Res. 86(3), 2005
PMID: 16307306
Transporter gene families in plants: the sulphate transporter gene family-redundancy or specialization?
Hawkesford, Physiologia Plantarum 117(), 2003
Action of SO2 on plants and metabolic detoxification of SO2
Heber, International Review of Cytology - A Survey of Cell Biology 177(), 1998
A new picture of cell wall protein dynamics in elongating cells of Arabidopsis thaliana: confirmed actors and newcomers.
Irshad M, Canut H, Borderies G, Pont-Lezica R, Jamet E., BMC Plant Biol. 8(), 2008
PMID: 18796151
Identification of novel Arabidopsis thaliana genes which are induced by high levels of boron
Kasajima, Plant Biotechnology 24(), 2007
Vacuolar sulfate transporters are essential determinants controlling internal distribution of sulfate in Arabidopsis.
Kataoka T, Watanabe-Takahashi A, Hayashi N, Ohnishi M, Mimura T, Buchner P, Hawkesford MJ, Yamaya T, Takahashi H., Plant Cell 16(10), 2004
PMID: 15367713
Uptake and metabolism of sulphur dioxide by Arabidopsis thaliana.
Kooij TAWvander, Kok LJde, Haneklaus S, Schnug E., New Phytol. 135(1), 1997
PMID: IND20702005
Recombinant expression, affinity purification and functional characterization of scots pine defensin 1
Kovaleva, Applied Microbiology and Biotechnology 89(), 2010
Sulphite oxidase as key enzyme for protecting plants against sulphur dioxide.
Lang C, Popko J, Wirtz M, Hell R, Herschbach C, Kreuzwieser J, Rennenberg H, Mendel RR, Hansch R., Plant Cell Environ. 30(4), 2007
PMID: 17324231
Strong cellular preference in the expression of a housekeeping gene of Arabidopsis thaliana encoding S-adenosylmethionine synthetase.
Peleman J, Boerjan W, Engler G, Seurinck J, Botterman J, Alliotte T, Van Montagu M, Inze D., Plant Cell 1(1), 1989
PMID: 2535470

Pfanz, 1990
Mesophyll Resistances to SO(2) Fluxes into Leaves.
Pfanz H, Martinoia E, Lange OL, Heber U., Plant Physiol. 85(4), 1987
PMID: 16665832

Pfanz, 1991
Sulfite oxidase controls sulfur metabolism under SO2 exposure in Arabidopsis thaliana.
Randewig D, Hamisch D, Herschbach C, Eiblmeier M, Gehl C, Jurgeleit J, Skerra J, Mendel RR, Rennenberg H, Hansch R., Plant Cell Environ. 35(1), 2011
PMID: 21895698
The fate of excess sulfur in higher plants
Rennenberg, Annual Review of Plant Physiology and Plant Molecular Biology 35(), 1984
An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics.
Rosso MG, Li Y, Strizhov N, Reiss B, Dekker K, Weisshaar B., Plant Mol. Biol. 53(1-2), 2003
PMID: 14756321
Purification and identification of a Ca(2+)-pectate binding peroxidase from Arabidopsis leaves.
Shah K, Penel C, Gagnon J, Dunand C., Phytochemistry 65(3), 2004
PMID: 14751301
Alternative splicing--when two's a crowd.
Smith CW., Cell 123(1), 2005
PMID: 16213205
Buthionine sulfoximine (BSO)-mediated improvement in cultured embryo quality in vitro entails changes in ascorbate metabolism, meristem development and embryo maturation.
Stasolla C, Belmonte MF, Tahir M, Elhiti M, Khamiss K, Joosen R, Maliepaard C, Sharpe A, Gjetvaj B, Boutilier K., Planta 228(2), 2008
PMID: 18458948
Plant defensins: defense, development and application
Stotz, Plant Signaling and Behavior 4(), 2009
Glutathione as an antioxidant and regulatory molecule in plants under abiotic stress conditions
Szalai, Journal of Plant Growth Regulation 28(), 2009
Acid precipitation and forest vegetation
Tamm, Water, Air, and Soil Pollution 7(), 1977
Plant defensins.
Thomma BP, Cammue BP, Thevissen K., Planta 216(2), 2002
PMID: 12447532
Flux control of sulphate assimilation in Arabidopsis thaliana: adenosine 5'-phosphosulphate reductase is more susceptible than ATP sulphurylase to negative control by thiols.
Vauclare P, Kopriva S, Fell D, Suter M, Sticher L, von Ballmoos P, Krahenbuhl U, den Camp RO, Brunold C., Plant J. 31(6), 2002
PMID: 12220264
Recruitment of glutathione into the nucleus during cell proliferation adjusts whole-cell redox homeostasis in Arabidopsis thaliana and lowers the oxidative defence shield.
Vivancos PD, Dong Y, Ziegler K, Markovic J, Pallardo FV, Pellny TK, Verrier PJ, Foyer CH., Plant J. 64(5), 2010
PMID: 21105929
DEGseq: an R package for identifying differentially expressed genes from RNA-seq data.
Wang L, Feng Z, Wang X, Wang X, Zhang X., Bioinformatics 26(1), 2009
PMID: 19855105
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
Three Arabidopsis genes encoding proteins with differential activities for cysteine synthase and beta-cyanoalanine synthase
Yamaguchi, Plant and Cell Physiology 41(), 2000


Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®


PMID: 23025405
PubMed | Europe PMC

Suchen in

Google Scholar