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Seasonal and cell type specific expression of sulfate transporters in the phloem of Populus reveals tree specific characteristics for SO4 2− storage and mobilization

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Abstract

The storage and mobilization of nutrients in wood and bark tissues is a typical feature of trees. Sulfur can be stored as sulfate, which is transported from source to sink tissues through the phloem. In the present study two transcripts encoding sulfate transporters (SULTR) were identified in the phloem of grey poplar (Populus tremula × P. alba). Their cell-specific expression was analyzed throughout poplar in source tissues, such as mature leaves, and in sink tissues, such as the wood and bark of the stem, roots and the shoot apex. PtaSULTR1;1 mRNA was detected in companion cells of the transport phloem, in the phloem of high-order leaf veins and in fine roots. PtaSULTR3;3a mRNA was found exclusively in the transport phloem and here in both, companion cells and sieve elements. Both sulfate transporter transcripts were located in xylem parenchyma cells indicating a role for PtaSULTR1;1 and PtaSULTR3;3a in xylem unloading. Changes in mRNA abundance of these and of the sulfate transporters PtaSULTR4;1 and PtaSULTR4;2 were analyzed over an entire growing season. The expression of PtaSULTR3;3a and of the putative vacuolar efflux transporter PtaSULTR4;2 correlated negatively with the sulfate content in the bark. Furthermore, the expression pattern of both PtaSULTR3;3a and PtaSULTR4;2 correlated significantly with temperature and day length. Thus both SULTRs seem to be involved in mobilization of sulfate during spring: PtaSULTR4;2 mediating efflux from the vacuole and PtaSULTR3;3a mediating loading into the transport phloem. In contrast, the abundance of PtaSULTR1;1 and PtaSULTR4;1 transcripts was not affected by environmental changes throughout the whole season. The transcript abundance of all tested sulfate transporters in leaves was independent of weather conditions. However, PtaSULTR1;1 abundance correlated negatively with sulfate content in leaves, supporting its function in phloem loading. Taken together, these findings indicate a transcriptional regulation of sulfate distribution in poplar trees.

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References

  • Adiputra IGK, Anderson JW (1995) Effect of sulfur nutrition on redistribution of sulfur in vegetative barely. Physiol Plant 95:643–650

    Article  CAS  Google Scholar 

  • Aravind L, Koonin EV (2000) The STAS domain a link between anion transporters and antisigma-factor antagonists. Curr Biol 10:53–55

    Article  Google Scholar 

  • Arend M, Weisenseel MH, Brummer M, Osswald W, Fromm J (2002) Seasonal changes of plasmamembrane H+-ATPase and endogenous ion current during cambial growth in poplar plants. Plant Physiol 129:1651–1663

    Article  CAS  PubMed  Google Scholar 

  • Bell CI, Cram WJ, Clarkson DT (1994) Compartmental analysis of 35SO4 2− exchange kinetics in roots and leaves of a tropical legume Macroptilium atropurpureum cv. Siratro. J Exp Bot 45:879–886

    Article  Google Scholar 

  • Biddulph SF (1956) Visual indications of 35S and 32P translocation in the phloem. Am J Bot 43:143–148

    Article  CAS  Google Scholar 

  • Brunner AM, Yakovlev IA, Strauss SH (2004) Validating internal controls for quantitative plant gene expression studies. BMC Plant Biol 4:14

    Article  PubMed  Google Scholar 

  • Buchner P, Takahashi H, Hawkesford M (2004a) Plant sulfate transporters: co-ordination of uptake, intracellular and long distance transport. J Exp Bot 55:1765–1773

    Article  CAS  PubMed  Google Scholar 

  • Buchner P, Stuiver EE, Westerman S, Wirtz M, Hell R, Hawkesford MJ, De Kok LJ (2004b) Regulation of sulfate uptake and expression of sulphate transporter genes in Brassica oleracea as affected by atmospheric H2S and pedospheric sulphate nutrition. Plant Physiol 136:3396–3408

    Article  CAS  PubMed  Google Scholar 

  • Carpaneto A, Geiger D, Bamberg E, Sauer NM, Fromm J, Hedrich R (2005) Phloem-localized, proton-coupled sucrose carrier ZmSUT1 mediates sucrose efflux under the control of the sucrose gradient and the proton motive force. J Biol Chem 280:21437–21443

    Article  CAS  PubMed  Google Scholar 

  • Cnops G, Neyt P, Raes J, Petrarulo M, Nelissen H, Malenica N, Luschnig C, Tietz O, Ditengou F, Palme K, Azmi A, Prinsen E, van Lijsebettens M (2006) The TORNADO1 and TORNADO2 genes function in several patterning processes during early leaf development in Arabidopsis thaliana. Plant Cell 18:852–866

    Article  CAS  PubMed  Google Scholar 

  • Decourteix M, Alves G, Brunel N, Améglio T, Guilliot A, Lemoine R, Péter G, Sakr S (2006) JrSUT1, a putative xylem sucrose transporter, could mediate sucrose influx into xylem parenchyma cells and be up-regulated by freeze-thaw cycles over the autumn-winter period in walnut tree (Juglans regia L.). Plant Cell Environ 29:36–47

    Article  CAS  PubMed  Google Scholar 

  • Deeken R, Ache P, Kajahn I, Klinkenberg J, Bringmann G, Hedrich R (2008) Identification of Arabidopsis thaliana RNAs provides a search criterion for phloem-based transcripts hidden in complex datasets of microarray experiments. Plant J 55:746–759

    Article  CAS  PubMed  Google Scholar 

  • Dickson RE (1991) Assimilate distribution and storage. In: Raghavendra AS (ed) Physiology of trees. Wiley, New York, pp 51–85

    Google Scholar 

  • Doering-Saad C, Newbury HJ, Couldridge CE, Bale JS, Pritchard J (2006) A phloem-enriched cDNA library from Ricinus: insights into phloem function. J Exp Bot 57:3183–3193

    Article  CAS  PubMed  Google Scholar 

  • Emanuelsson O, Nielsen H, von Heijne G (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Prot Sci 8:978–984

    Article  CAS  Google Scholar 

  • Frachisse J-M, Thomine S, Colcombet J, Guern J, Barbier-Brygoo H (1999) Sulfate is both a substrate and an activator of the voltage-dependent anion channel of Arabidopsis hypocotyl cells. Plant Physiol 121:253–261

    Article  CAS  PubMed  Google Scholar 

  • Fritz E (1980) Microautoradiographic localization of assimilates in phloem: problems and new method. Ber Dtsch Bot Ges 93:109–121

    Google Scholar 

  • Hartmann T, Mult S, Suter M, Rennenberg H, Herschbach C (2000) Leaf age-dependent differences in sulfur assimilation and allocation in poplar (Populus tremula × P. alba) leaves. J Exp Bot 51:1077–1088

    Article  CAS  PubMed  Google Scholar 

  • Hawkesford MJ (2003) Transporter gene families in plants: the sulfate transporter gene family—redundancy or specialization? Physiol Plant 117:155–163

    Article  CAS  Google Scholar 

  • Hawkesford MJ, Davidian J-C, Grignon C (1993) Sulfate/proton cotransport in plasma-membrane vesicles isolated from roots of Brassica napus L.: increased transport in membranes isolated from sulfur starves plants. Planta 190:297–304

    Article  CAS  Google Scholar 

  • Heiss S, Schäfer HJ, Haag-Kerwer A, Rausch T (1999) Cloning sulfur assimilation genes of Brassica juncea L.: cadmium differentially affects the expression of putative low-affinity sulphate transporter and isoforms of ATP sulphurylase and APS reductase. Plant Mol Biol 39:847–857

    Article  CAS  PubMed  Google Scholar 

  • Herschbach C (2003) Whole plant regulation of sulfur nutrition of deciduous trees—influences of the environment. Plant Biol 5:233–244

    Article  CAS  Google Scholar 

  • Herschbach C, Rennenberg H (1996) Storage and remobilization of sulfur in beech trees (Fagus sylvatica). Physiol Plant 98:125–132

    Article  CAS  Google Scholar 

  • Herschbach C, Rennenberg H (2001a) Significance of phloem-translocated organic sulfur compounds for the regulation of sulfur nutrition. Prog Bot 62:177–193

    CAS  Google Scholar 

  • Herschbach C, Rennenberg H (2001b) Sulfur nutrition of deciduous trees. Naturwissenschaften 88:25–36

    Article  CAS  PubMed  Google Scholar 

  • Herschbach C, van der Zalm E, Schneider A, Jouanin L, De Kok LJ, Rennenberg H (2000) Regulation of sulfur nutrition in wild-type and transgenic poplar over-expressing γ-glutamylcysteine synthetase in the cytosol as affected by atmospheric H2S. Plant Physiol 124:461–473

    Article  CAS  PubMed  Google Scholar 

  • Hopkins L, Parmar S, Bouranis DL, Howarth JR, Hawkesford MJ (2004) Coordinated expression of sulphate uptake and components of the sulphate assimilatory pathway in maize. Plant Biol 6:408–414

    Article  CAS  PubMed  Google Scholar 

  • Jansson S, Douglas CJ (2007) Populus: a model system for plant biology. Annu Rev Plant Biol 58:435–458

    Article  CAS  PubMed  Google Scholar 

  • Jones DT, Taylor WR, Thorton JM (1994) A model recognition approach to the prediction of all-helical membrane-protein structure and topology. Biochemistry 33:3038–3049

    Article  CAS  PubMed  Google Scholar 

  • Kataoka T, Hayashi N, Yamaya T, Takahashi H (2004a) Root-to-shoot transport of sulfate in Arabidopsis. Evidence for the role of SULTR3;5 as a component of low-affinity sulfate transport system in the root vasculature. Plant Physiol 136:4198–4204

    Article  CAS  PubMed  Google Scholar 

  • Kataoka T, Watanabe-Takahashi A, Hayashi N, Ohnishi M, Mimura T, Buchner P, Hawkesford MJ, Yamaya T, Takahashi H (2004b) Vacuolar sulfate transporters are essential determinants controlling internal distribution of sulfate in Arabidopsis. Plant Cell 16:2693–2704

    Article  CAS  PubMed  Google Scholar 

  • Kehr J, Buhtz A (2008) Long distance transport and movement of RNA through the phloem. J Exp Bot 59:85–92

    Article  CAS  PubMed  Google Scholar 

  • Kolosova N, Miller B, Ralph S, Ellis BE, Douglas C, Ritland K, Bohlmann J (2004) Isolation of high-quality RNA from gymnosperm and angiosperm trees. Biotechniques 36:821–824

    CAS  PubMed  Google Scholar 

  • Kopriva S, Koprivova A (2004) Plant adenine 5′-phosphosulfate reductase: the past, the present, and the future. J Exp Bot 55:1775–1783

    Article  CAS  PubMed  Google Scholar 

  • Kopriva S, Jones S, Koprivova A, Suter M, von Ballmoos P, Brander K, Flückiger J, Brunold C (2001) Influence of chilling stress on the intercellular distribution of assimilatory sulfate reduction and thiols in Zea mays. Plant Biol 3:24–31

    Article  CAS  Google Scholar 

  • Koralewska A, Buchner P, Stuiver CEE, Posthumus FS, Kopriva S, Hawkesford MJ, De Kok LJ (2009) Expression and activity of sulphate transporters and APS reductase in crly kale in response to sulphate deprivation and re-supply. J Plant Physiol 166:168–179

    Article  CAS  PubMed  Google Scholar 

  • Kühn C, Franceschi VR, Schulz A, Lemoine R, Frommer WB (1997) Macromolecular trafficking indicated by locatization and turnover of sucrose transporters in enucleated sieve elements. Science 275:1298–1300

    Article  PubMed  Google Scholar 

  • Lass B, Ullrich-Eberius CI (1984) Evidence for proton/sulfate cotransport and its kinetics in Lemna gibba G1. Planta 161:53–60

    Article  CAS  Google Scholar 

  • Le Hir R, Beneteau J, Bellini C, Vilaine F, Dinant S (2008) Gene expression profiling: keys for investigating phloem functions. Trends Plant Sci 13:273–280

    Article  CAS  PubMed  Google Scholar 

  • Lough TJ, Lucas WJ (2006) Integrative plant biology: role of phloem long-distance macromolecular trafficking. Annu Rev Plant Biol 57:203–232

    Article  CAS  PubMed  Google Scholar 

  • Martin MN, Tarczynski MC, Shen B, Leustek T (2005) The role of 5′-adenylylsulfate reductase in controlling sulfate reduction in plants. Photosynth Res 86:309–329

    Article  CAS  PubMed  Google Scholar 

  • Nicot N, Hausman JF, Hoffmann L, Evers D (2005) Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. J Exp Bot 56:2907–2914

    Article  CAS  PubMed  Google Scholar 

  • Nocito FF, Lancilli C, Crema B, Fourcroy P, Davidian J-C, Sacchi GA (2006) Heavy metal stress and sulfate uptake in maize roots. Plant Physiol 141:1138–1148

    Article  CAS  PubMed  Google Scholar 

  • Noctor G, Strohm M, Jouanin L, Kunert K-J, Foyer CH, Rennenberg H (1996) Synthesis of glutathione in leaves of transgenic poplar overexpression γ-glutamylcysteine synthetase. Plant Physiol 112:1071–1078

    CAS  PubMed  Google Scholar 

  • Omid A, Keilin T, Glass A, Leshkowitz D, Wolf S (2007) Characterisation of phloem-sap transcription profile in melon plants. J Exp Bot 58:3645–3656

    Article  CAS  PubMed  Google Scholar 

  • Pearson WR (2000) Flexible sequence similarity searching with the FASTA3 program package. Methods Mol Biol 132:185–219

    CAS  PubMed  Google Scholar 

  • Persson B, Argos P (1994) Prediction of transmembrane segments in proteins utilizing multiple sequence alignments. J Mol Biol 237:182–192

    Article  CAS  PubMed  Google Scholar 

  • Rennenberg H, Herschbach C, Harberer K, Kopriva S (2007) Sulfur metabolism in plants: are trees different? Plant Biol 9:620–637

    Article  CAS  PubMed  Google Scholar 

  • Roberts SK (2006) Plasma membrane anion channels in higher plants and their putative functions in roots. New Phytol 169:647–666

    Article  PubMed  Google Scholar 

  • Rouached H, Berthomieu P, El Kassis E, Cathala N, Catherinot V, Labesse G, Davidian JC, Fourcroy P (2005) Structural and functional analysis of the C-terminal STAS (sulfate transporter and anti-sigma antagonist) domain of the Arabidopsis thaliana sulfate transporter SULTR1.2. J Biol Chem 280:15976–15983

    Article  CAS  PubMed  Google Scholar 

  • Rouached H, Wirtz M, Alary R, Hell R, Arpat AB, Davidian J-C, Fourcroy P, Berthomieu P (2008) Differentialregulation of the expression of two high-affinity sulphate transporters, SULTR1.1 and SULTR1.2, in Arabidopsis. Plant Physiol 147:897–911

    Article  CAS  PubMed  Google Scholar 

  • Saito K (2004) Sulfur assimilatory metabolism. The long and smelling road. Plant Physiol 136:2443–2450

    Article  CAS  PubMed  Google Scholar 

  • Sanderson J (1981) Modified development to improve the performance of AR-10 stripping emulsions for use the more energetic isotopes. J Microsc 124:177–182

    CAS  PubMed  Google Scholar 

  • Scheerer U, Haensch R, Mendel R, Kopriva S, Rennenberg H, Herschbach C (2009) Sulphur flux through the sulphate assimilation pathway is differently controlled by adenosine 5′-phosphosulphate reductase under stress and in transgenic poplar plants overexpressing γ-ECS, SO or APR. J Exp Bot. doi:10.1093/jxb/erp327

    Google Scholar 

  • Schrader J, Moyle R, Bhalerao R, Hertzberg M, Lundeberg J, Nilsson P, Bhalerao RP (2004) Cambial meristem dormancy in trees involves extensive remodelling of the transcriptome. Plant J 40:173–187

    Article  CAS  PubMed  Google Scholar 

  • Schulte M, Herschbach C, Rennenberg H (1998) Interactive effects of elevated atmospheric CO2, mycorrhization and drought on long-distance transport of reduced sulfur in young pedunculate oak trees (Quercus robur L.). Plant Cell Environ 21:917–926

    Article  CAS  Google Scholar 

  • Shibagaki N, Grossman AR (2004) Probing the function of STAS domains of the Arabidopsis sulfate transporters. J Biol Chem 279:30791–30799

    Article  CAS  PubMed  Google Scholar 

  • Shibagaki N, Grossman AR (2006) The role of the STAS domain in the function and biogenesis of a sulfate transporter as probed by random mutagenesis. J Biol Chem 281:22964–22973

    Article  CAS  PubMed  Google Scholar 

  • Shibagaki N, Rose A, McDermott JP, Fujiwara T, Hayashi H, Yoneyama T, Davies JP (2002) Selenate-resistant mutants of Arabidopsis thaliana identify Sultr1;2 a sulfate transporter required for efficient transport of sulfate into roots. Plant J 29:475–489

    Article  CAS  PubMed  Google Scholar 

  • Smith IK, Lang AL (1988) Translocation of sulfate in soybean (Glycine max L. Merr). Plant Physiol 86:798–802

    Article  CAS  PubMed  Google Scholar 

  • Smith FW, Ealing PM, Hawkesford MJ, Clarkson DT (1995) Plant members of a family of sulfate transporters reveal functional subtypes. Proc Natl Acad Sci USA 92:9373–9377

    Article  CAS  PubMed  Google Scholar 

  • Smith FW, Hawkesford MJ, Ealing PM, Clarkson DT, Vanden Berg PJ, Belcher AR, Warrilow GS (1997) Regulation of a cDNA from barley roots encoding a high affinity sulfate transporter. Plant J 12:875–884

    Article  CAS  PubMed  Google Scholar 

  • Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43

    Article  CAS  PubMed  Google Scholar 

  • Strohm M, Jouanin L, Kunert KJ, Pruvost C, Polle A, Foyer C, Rennenberg H (1995) Regulation of GSH synthesis in leaves of transgenic poplar (Populus tremula × P. alba) overexpressing GSH synthetase. Plant J 7:141–145

    Article  CAS  Google Scholar 

  • Takahashi H, Yamazaki M, Sasakura N, Watanabe A, Leustek T, Engler JA, Engler G, van Montagu M, Saito K (1997) Regulation of sulfur assimilation in higher plants: a sulfate transporter induced in sulfate-starved roots plays a central role in Arabidopsis thaliana. Proc Natl Acad Sci USA 94:11102–11107

    Article  CAS  PubMed  Google Scholar 

  • Takahashi H, Watanabe-Takahashi A, Smith FW, Blake-Kalff M, Hawkesford MJ, Saito K (2000) The roles of three functional sulfate transporters involved in uptake and translocation of sulfate in Arabidopsis thaliana. Plant J 23:171–182

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Tatusova TA, Madden TL (1999) BLAST 2 Sequences, a new tool for comparing protein and nucleotide sequences. FEMS 174:247–250

    Article  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  Google Scholar 

  • Tomatsu H, Takano J, Takahashi H, Watanabe-Takahashi A, Shibagaki N, Fujiwara T (2007) An Arabidopsis thaliana high-affinity molybdate transporter required for efficient uptake of molybdate from soil. Proc Natl Acad Sci USA 104:18807–18812

    Article  CAS  PubMed  Google Scholar 

  • Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Dejardin A, Depamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjarvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leple JC, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouze P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai CJ, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, Van de Peer Y, Rokhsar D (2006) The genome of black cottonwood, Populus trichocarpa (Torr & Gray). Science 131:1596–1604

    Article  Google Scholar 

  • Van Bel AJE (2003) The phloem, a miracle of ingenuity. Plant Cell Environ 26:125–149

    Article  Google Scholar 

  • Van Bel AJE, Kempers R (1990) Symplastically isolation of the sieve element-companion cell complex in the phloem of Ricinus communis and Salix alba stems. Planta 183:69–76

    Google Scholar 

  • Van Bel AJE, Ehlers K, Knoblauch M (2002) Sieve elements caught in the act. Trends Plant Sci 7:126–132

    Article  PubMed  Google Scholar 

  • Vidmar JJ, Schjoerring JK, Touraine B, Glass ADM (1999) Regulation of the hvst1 gene encoding a high-affinity sulfate transporter from Hordeum vulgare. Plant Mol Biol 40:883–892

    Article  CAS  PubMed  Google Scholar 

  • Vidmar JJ, Tagmount A, Cathala N, Tourain B, Davidian J-V (2000) Cloning and characterization of a root specific high-affinity sulfate transporter from Arabidopsis thaliana. FEBS Lett 475:65–69

    Article  CAS  PubMed  Google Scholar 

  • Williams LE, Lemoine R, Sauer N (2000) Sugar transporters in higher plants—a diversity of roles and complex regulation. Trends Plant Sci 5:283–290

    Article  CAS  PubMed  Google Scholar 

  • Wissel K, Pettersson F, Berglund A, Jansson S (2003) What affects mRNA levels in leaves of field-grown aspen? A study of developmental and environmental influences. Plant Physiol 133:1190–1197

    Article  CAS  PubMed  Google Scholar 

  • Yoshimoto N, Takahashi H, Smith FW, Yamaya T, Saito K (2002) Two distinct high-affinity sulfate transporters with different inducibilities mediate uptake of sulfate in Arabidopsis roots. Plant J 29:465–473

    Article  CAS  PubMed  Google Scholar 

  • Yoshimoto N, Inoue E, Saito K, Yamaya T, Takahashi H (2003) Phloem-localizing sulfate transporter, Sultr1;3, mediates re-distribution of sulfur from source to sink organs in Arabidopsis. Plant Physiol 131:1511–1517

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was financial supported by the Deutsche Forschungsgemeinschaft (DFG) under the contract numbers HE 3003/2 & 3. The Excellence Initiative of the German Federal and State Governments (EXC 294), SFB 592 and the Landesstiftung are gratefully acknowledged. The authors thank Simone Sikora and Katja Rapp for technical assistance and Dr. William Teale to improve language.

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  1. Chair of Tree Physiology, Institute of Forest Botany and Tree Physiology, Albert-Ludwigs-University Freiburg, Georges-Köhler-Allee 053/054, 79110, Freiburg, Germany

    Jasmin Dürr, Susanne Mult, Henning Wildhagen, Heinz Rennenberg & Cornelia Herschbach

  2. Biology and Microbiology Department, South Dakota State University, Northern Plains Biostress (SNP, 251B), Brookings, SD, 57007, USA

    Heike Bücking

  3. Institute of Biology II, Faculty of Biology, Albert-Ludwigs-Universiy Freiburg, Schänzlestrasse 1, 79104, Freiburg, Germany

    Klaus Palme & Franck Ditengou

  4. Centre for Biological Signaling Studies, Albert-Ludwigs-University Freiburg, Albertstrasse 19, 79104, Freiburg, Germany

    Klaus Palme & Franck Ditengou

  5. Freiburg Institute of Advanced Sciences, Albert-Ludwigs-University Freiburg, Albertstrasse 19, 79104, Freiburg, Germany

    Klaus Palme

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Dürr, J., Bücking, H., Mult, S. et al. Seasonal and cell type specific expression of sulfate transporters in the phloem of Populus reveals tree specific characteristics for SO4 2− storage and mobilization. Plant Mol Biol 72, 499–517 (2010). https://doi.org/10.1007/s11103-009-9587-6

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