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Genome-wide identification and cadmium induced expression profiling of sulfate transporter (SULTR) genes in sorghum (Sorghum bicolor L.)

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Abstract

Sulfur is an essential element for all living organisms. Plants can convert inorganic sulfur into organic sulfur compounds by complex enzymatic steps. In this study, we conducted a genome-wide analysis of sulfate transporter genes (SULTRs) in the sorghum (Sorghum bicolor) genome and examined expression profiles of SbSULTR genes under 200 µM cadmium (Cd) exposure. As a result of sorghum genome analysis, 11 SULTR genes were identified, including SbSULTR1;1, SbSULTR1;2, SbSULTR1;3, SbSULTR2;1, SbSULTR2;2, SbSULTR3;1, SbSULTR3;2, SbSULTR3;3, SbSULTR3;4, SbSULTR3;5, and SbSULTR4. Given names are based on phylogeny and chromosomal locations. Except SbSULTR4, all SbSULTR proteins contained Sulfate_transp (PF00916), STAS (PF01740) domains and 12 trans-membrane domains. Phylogenetic analysis revealed that four major groups were identified such as SULTR1, 2, 3, and 4 groups and SULTR4 group was separated to other SULTR groups. In promotor sequences of SbSULTR genes, many diverse cis-acting elements were found mainly related with physiological processes such as light, stress and hormone responsiveness. The expression profiles of SbSULTR genes showed that SULTR1;2, 1;3, 3;3, and 3;5 genes up-regulated in root, while expression level of SULTR4 decreased under 200 µM Cd exposure. The predicted 3D structures of SULTR proteins showed some conformational changes, suggesting functional diversities of SbSULTRs. Finally, results of this study may contribute towards understanding SbSULTR genes and their regulations and roles in Cd stress in sorghum.

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References

  • Anjum NA, Gill R, Kaushik M, Hasanuzzaman M, Pereira E, Ahmad I et al (2015) ATP-sulfurylase, sulfur-compounds, and plant stress tolerance. Front Plant Sci 6:210

    PubMed  PubMed Central  Google Scholar 

  • Bae SH, Han HW, Moon J (2015) Functional analysis of the molecular interactions of TATA box-containing genes and essential genes. PLoS ONE 10:e0120848

    Article  PubMed  PubMed Central  Google Scholar 

  • Bailey TL, Johnson J, Grant CE, Noble WS (2015) The MEME suite. Nucleic Acids Res 43(W1):39–49

    Article  Google Scholar 

  • Ballaré CL (2014) Light regulation of plant defense. Annu Rev Plant Biol 65:335–363

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Buchner P, Parmar S, Kriegel A, Carpentier M, Hawkesford MJ (2010) The sulfate transporter family in wheat: tissue-specific gene expression in relation to nutrition. Mol Plant 3:374–389

    Article  CAS  PubMed  Google Scholar 

  • Cao MJ, Wang Z, Wirtz M, Hell R, Oliver DJ, Xiang CB (2013) SULTR3; 1 is a chloroplast localized sulfate transporter in Arabidopsis thaliana. Plant J 73:607–616

    Article  CAS  PubMed  Google Scholar 

  • Cao MJ, Wang Z, Zhao Q, Mao JL, Speiser A, Wirtz M et al (2014) Sulfate availability affects ABA levels and germination response to ABA and salt stress in Arabidopsis thaliana. Plant J 77:604–615

    Article  CAS  PubMed  Google Scholar 

  • Capaldi FR, Gratão PL, Reis AR, Lima LW, Azevedo RA (2015) Sulfur metabolism and stress defense responses in plants. Trop Plant Biol 8:60–73

    Article  CAS  Google Scholar 

  • Casieri L, Gallardo K, Wipf D (2012) Transcriptional response of Medicago truncatula sulphate transporters to arbuscular mycorrhizal symbiosis with and without sulphur stress. Planta 235:1431–1447

    Article  CAS  PubMed  Google Scholar 

  • Chan KX, Wirtz M, Phua SY, Estavillo GM, Pogson BJ (2013) Balancing metabolites in drought: the sulfur assimilation conundrum. Trends Plant Sci 18:18–29

    Article  CAS  PubMed  Google Scholar 

  • Dillon SL, Shapter FM, Henry RJ, Cordeiro G, Izquierdo L, Lee LS (2007) Domestication to crop improvement: genetic resources for Sorghum and Saccharum (Andropogoneae). Ann Bot 100:975–989

    Article  PubMed  PubMed Central  Google Scholar 

  • Feng S, Martinez C, Gusmaroli G, Wang Y, Zhou J, Wang F et al (2008) Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451(7177):475–479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferri A, Lancilli C, Maghrebi M, Lucchini G, Sacchi GA, Nocito FF (2017) The sulfate supply maximizing Arabidopsis shoot growth is higher under long-than short-term exposure to cadmium. Front Plant Sci 8:854

    Article  PubMed  PubMed Central  Google Scholar 

  • Flores-Cáceres ML, Hattab S, Hattab S, Boussetta H, Banni M, Hernández LE (2015) Specific mechanisms of tolerance to copper and cadmium are compromised by a limited concentration of glutathione in alfalfa plants. Plant Sci 233:165–173

    Article  PubMed  Google Scholar 

  • Gallardo K, Courty PE, Le Signor C, Wipf D, Vernoud V (2014) Sulfate transporters in the plant’s response to drought and salinity: regulation and possible functions. Front Plant Sci 5:580

    Article  PubMed  PubMed Central  Google Scholar 

  • Gasteiger E, Hoogland C, Gattiker A, Duvaud SE, Wilkins MR, Appel RD et al (2005) Protein identification and analysis tools on the ExPASy server. Humana Press, New York, pp 571–607

    Google Scholar 

  • Gigolashvili T, Kopriva S (2014) Transporters in plant sulfur metabolism. Front Plant Sci 5:442

    Article  PubMed  PubMed Central  Google Scholar 

  • Gläser K, Kanawati B, Kubo T, Schmitt-Kopplin P, Grill E (2014) Exploring the Arabidopsis sulfur metabolome. Plant J 77:31–45

    Article  PubMed  Google Scholar 

  • Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J et al (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:1178–1186

    Article  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp 41:95–98

    CAS  Google Scholar 

  • Hernández LE, Sobrino-Plata J, Montero-Palmero MB, Carrasco-Gil S, Flores-Cáceres ML, Ortega-Villasante C et al (2015) Contribution of glutathione to the control of cellular redox homeostasis under toxic metal and metalloid stress. J Exp Bot 66(10):2901–2911

    Article  PubMed  Google Scholar 

  • Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2014) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297

    Article  PubMed  PubMed Central  Google Scholar 

  • Iqbal A, Sadia B, Khan AI, Awan FS, Kainth RA, Sadaqat HA (2010) Biodiversity in the sorghum (Sorghum bicolor L. Moench) germplasm of Pakistan. Genet Mol Res 9(2):756–764

    Article  CAS  PubMed  Google Scholar 

  • Jiao Y, Lau OS, Deng XW (2007) Light-regulated transcriptional networks in higher plants. Nat Rev Genet 8(3):217–230

    Article  CAS  PubMed  Google Scholar 

  • Johnson SM, Lim FL, Finkler A, Fromm H, Slabas AR, Knight MR (2014) Transcriptomic analysis of Sorghum bicolor responding to combined heat and drought stress. BMC Genom 15(1):456

    Article  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  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJ (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10(6):845–858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan MIR, Nazir F, Asgher M, Per TS, Khan NA (2015) Selenium and sulfur influence ethylene formation and alleviate cadmium-induced oxidative stress by improving proline and glutathione production in wheat. J Plant Physiol 173:9–18

    Article  CAS  PubMed  Google Scholar 

  • Khan MIR, Iqbal N, Masood A, Mobin M, Anjum NA, Khan NA (2016) Modulation and significance of nitrogen and sulfur metabolism in cadmium challenged plants. Plant Growth Regul 78(1):1–11

    Article  CAS  Google Scholar 

  • Kopriva S, Mugford SG, Matthewman C, Koprivova A (2009) Plant sulfate assimilation genes: redundancy versus specialization. Plant Cell Rep 28:1769–1780

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kozuka T, Kobayashi J, Horiguchi G, Demura T, Sakakibara H, Tsukaya H et al (2010) Involvement of auxin and brassinosteroid in the regulation of petiole elongation under the shade. Plant Physiol 153(4):1608–1618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Asif MA, Chakrabarty D, Tripathi RD, Trivedi PK (2011) Differential expression and alternative splicing of rice sulphate transporter family members regulate sulphur status during plant growth, development and stress conditions. Funct Integr Genom 11:259–273

    Article  CAS  Google Scholar 

  • Laloum T, De Mita S, Gamas P, Baudin M, Niebel A (2013) CCAAT-box binding transcription factors in plants: y so many? Trends Plant Sci 18:157–166

    Article  CAS  PubMed  Google Scholar 

  • Lancilli C, Giacomini B, Lucchini G, Davidian JC, Cocucci M, Sacchi GA et al (2014) Cadmium exposure and sulfate limitation reveal differences in the transcriptional control of three sulfate transporter (Sultr1; 2) genes in Brassica juncea. BMC Plant Biol 14(1):132

    Article  PubMed  PubMed Central  Google Scholar 

  • Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y et al (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30(1):325–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Z, Wakao S, Fischer BB, Niyogi KK (2009) Sensing and responding to excess light. Annu Rev Plant Biol 60:239–260

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Wu FH, Li JX, Chen J, Wang GH, Wang WH et al (2016) Glutathione homeostasis and Cd tolerance in the Arabidopsis sultr1; 1-sultr1; 2 double mutant with limiting sulfate supply. Plant Cell Rep 35(2):397–413

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Method 25(4):402–408

    Article  CAS  Google Scholar 

  • Lovell SC, Davis IW, Arendall WB, de Bakker PI, Word JM, Prisant MG et al (2003) Structure validation by Cα geometry: ϕ, ψ and Cβ deviation. Proteins 50(3):437–450

    Article  CAS  PubMed  Google Scholar 

  • McAtee P, Karim S, Schaffer RJ, David K (2013) A dynamic interplay between phytohormones is required for fruit development, maturation, and ripening. Front Plant Sci 4:79

    Article  PubMed  PubMed Central  Google Scholar 

  • Mera R, Torres E, Abalde J (2014) Sulphate, more than a nutrient, protects the microalga Chlamydomonas moewusii from cadmium toxicity. Aquat Toxicol 148:92–103

    Article  CAS  PubMed  Google Scholar 

  • Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H et al (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457(7229):551–556

    Article  CAS  PubMed  Google Scholar 

  • Pozo MJ, López-Ráez JA, Azcón-Aguilar C, García-Garrido JM (2015) Phytohormones as integrators of environmental signals in the regulation of mycorrhizal symbioses. New Phytol 205(4):1431–1436

    Article  CAS  PubMed  Google Scholar 

  • Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C et al (2012) The Pfam protein families database. Nucleic Acids Res 40:D290–D301. https://doi.org/10.1093/nar/gkr1065

    Article  CAS  PubMed  Google Scholar 

  • Reddy PS, Reddy DS, Sivasakthi K, Bhatnagar-Mathur P, Vadez V, Sharma KK (2016) Evaluation of sorghum [Sorghum bicolor (L.)] reference genes in various tissues and under abiotic stress conditions for quantitative real-time PCR data normalization. Front Plant Sci 7:529

    Google Scholar 

  • Rouached H, Wirtz M, Alary R, Hell R, Arpat AB, Davidian JC et al (2008) Differential regulation of the expression of two high-affinity sulfate transporters, SULTR1.1 and SULTR1. 2, in Arabidopsis. Plant Physiol 147:897–911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seo PJ, Mas P (2015) Stressing the role of the plant circadian clock. Trends Plant Sci 20(4):230–237

    Article  CAS  PubMed  Google Scholar 

  • Sghayar S, Ferri A, Lancilli C, Lucchini G, Abruzzese A, Porrini M et al (2015) Analysis of cadmium translocation, partitioning and tolerance in six barley (Hordeum vulgare L) cultivars as a function of thiol metabolism. Biol Fertil Soils 51(3):311–320

    Article  CAS  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 29:475–486

    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  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Takahashi H, Kopriva S, Giordano M, Saito K, Hell R (2011) Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu Rev Plant Biol 62:157–184

    Article  CAS  PubMed  Google Scholar 

  • Takahashi H, Buchner P, Yoshimoto N, Hawkesford MJ, Shiu SH (2012) Evolutionary relationships and functional diversity of plant sulfate transporters. Front Plant Sci 2:119

    Article  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tombuloglu H, Filiz E, Aydın M, Koc I (2017) Genome-wide identification and expression analysis of sulphate transporter (SULTR) genes under sulfur deficiency in Brachypodium distachyon. J Plant Biochem Biotechnol 26(3):263–273

    Article  CAS  Google Scholar 

  • Tsirigos KD, Peters C, Shu N, Käll L, Elofsson A (2015) The TOPCONS web server for consensus prediction of membrane protein topology and signal peptides. Nucleic Acids Res 3(W1):W401–W407

    Article  Google Scholar 

  • Vatansever R, Koc I, Ozyigit II, Sen U, Uras ME, Anjum NA et al (2016) Genome-wide identification and expression analysis of sulfate transporter (SULTR) genes in potato (Solanum tuberosum L.). Planta 244(6):1167–1183

    Article  CAS  PubMed  Google Scholar 

  • Wolfe D, Dudek S, Ritchie MD, Pendergrass SA (2013) Visualizing genomic information across chromosomes with PhenoGram. BioData Mining 6(1):18

    Article  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi C, Takimoto Y, Ohkama-Ohtsu N, Hokura A, Shinano T, Nakamura T et al (2016) Effects of cadmium treatment on the uptake and translocation of sulfate in Arabidopsis thaliana. Plant Cell Physiol 57(11):2353–2366

    Article  CAS  PubMed  Google Scholar 

  • Yi H, Ravilious GE, Galant A, Krishnan HB, Jez JM (2010) From sulfur to homoglutathione: thiol metabolism in soybean. Amino Acids 39:963–978

    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  PubMed Central  Google Scholar 

  • Yu CS, Chen YC, Lu CH, Hwang JK (2006) Prediction of protein subcellular localization. Proteins 64(3):643–651

    Article  CAS  PubMed  Google Scholar 

  • Zuber H, Davidian JC, Aubert G, Aimé D, Belghazi M, Lugan R et al (2010) The seed composition of Arabidopsis mutants for the group 3 sulfate transporters indicates a role in sulfate translocation within developing seeds. Plant Physiol 154:913–926

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Correspondence to M. Aydın Akbudak or Ertugrul Filiz.

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Akbudak, M.A., Filiz, E. & Kontbay, K. Genome-wide identification and cadmium induced expression profiling of sulfate transporter (SULTR) genes in sorghum (Sorghum bicolor L.). Biometals 31, 91–105 (2018). https://doi.org/10.1007/s10534-017-0071-5

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