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BioMetals

, Volume 30, Issue 2, pp 185–200 | Cite as

Genome-wide exploration of silicon (Si) transporter genes, Lsi1 and Lsi2 in plants; insights into Si-accumulation status/capacity of plants

  • Recep Vatansever
  • Ibrahim Ilker Ozyigit
  • Ertugrul FilizEmail author
  • Nermin Gozukara
Article

Abstract

Silicon (Si) is a nonessential, beneficial micronutrient for plants. It increases the plant stress tolerance in relation to its accumulation capacity. In this work, root Si transporter genes were characterized in 17 different plants and inferred for their Si-accumulation status. A total of 62 Si transporter genes (31 Lsi1 and 31 Lsi2) were identified in studied plants. Lsi1s were 261–324 residues protein with a MIP family domain whereas Lsi2s were 472–547 residues with a citrate transporter family domain. Lsi1s possessed characteristic sequence features that can be employed as benchmark in prediction of Si-accumulation status/capacity of the plants. Silicic acid selectivity in Lsi1s was associated with two highly conserved NPA (Asn-Pro-Ala) motifs and a Gly-Ser-Gly-Arg (GSGR) ar/R filter. Two NPA regions were present in all Lsi1 members but some Ala substituted with Ser or Val. GSGR filter was only available in the proposed high and moderate Si accumulators. In phylogeny, Lsi1s formed three clusters as low, moderate and high Si accumulators based on tree topology and availability of GSGR filter. Low-accumulators contained filters WIGR, AIGR, FAAR, WVAR and AVAR, high-accumulators only with GSGR filter, and moderate-accumulators mostly with GSGR but some with A/CSGR filters. A positive correlation was also available between sequence homology and Si-accumulation status of the tested plants. Thus, availability of GSGR selectivity filter and sequence homology degree could be used as signatures in prediction of Si-accumulation status in experimentally uncharacterized plants. Moreover, interaction partner and expression profile analyses implicated the involvement of Si transporters in plant stress tolerance.

Keywords

ar/R Selectivity filter Accumulator Silicic acid Motifs Perturbation 

Supplementary material

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Supplementary material 1 (PDF 1233 kb)
10534_2017_9992_MOESM2_ESM.xlsx (18 kb)
Supplementary material 2 (XLSX 18 kb)

References

  1. Ashraf MA, Morshed MM, Ahammad AS, Morshed MN (2013) Computational study of silicon transporter protein in rice and wheat. Int J Comput Bioinform Silico Model 2:199–205Google Scholar
  2. Bernsel A, Viklund H, Falk J, Lindahl E, von Heijne G, Elofsson A (2008) Prediction of membrane-protein topology from first principles. Proc Natl Acad Sci 105:7177–7181CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bienert G, Chaumont F (2011) Plant aquaporins: roles in water homeostasis, nutrition, and signaling processes. In: Geisler M, Venema K (eds) Transporters and pumps in plant signaling processes. Springer, Berlin, pp 3–36CrossRefGoogle Scholar
  4. Brodersen P, Petersen M, Bjørn Nielsen H et al (2006) Arabidopsis MAP kinase 4 regulates salicylic acid-and jasmonic acid/ethylene-dependent responses via EDS1 and PAD4. Plant J 47:532–546CrossRefPubMedGoogle Scholar
  5. Chiba Y, Mitani N, Yamaji N, Ma JF (2009) HvLsi1 is a silicon influx transporter in barley. Plant J 57:810–818CrossRefPubMedGoogle Scholar
  6. DeLano WL (2002) The PyMOL molecular graphics system. DeLano Scientific, San CarlosGoogle Scholar
  7. Dundas J, Ouyang Z, Tseng J, Binkowski A, Turpaz Y, Liang J (2006) CASTp: computed atlas of surface topography of proteins with structural and topographical mapping of functionally annotated residues. Nucl Acids Res 34:W116–W118CrossRefPubMedPubMedCentralGoogle Scholar
  8. Eastmond PJ, Li Y, Graham IA (2003) Is trehalose-6-phosphate a regulator of sugar metabolism in plants? J Exp Bot 54:533–537CrossRefPubMedGoogle Scholar
  9. Facchini PJ, Bird DA, St-Pierre B (2004) Can Arabidopsis make complex alkaloids? Trends Plant Sci 9:116–122CrossRefPubMedGoogle Scholar
  10. Fauteux F, Rémus-Borel W, Menzies JG, Bélanger RR (2005) Silicon and plant disease resistance against pathogenic fungi. FEMS Microbiol Lett 249:1–6CrossRefPubMedGoogle Scholar
  11. Feng J, Shi Q, Wang X, Wei M, Yang F, Xu H (2010) Silicon supplementation ameliorated the inhibition of photosynthesis and nitrate metabolism by cadmium (Cd) toxicity in Cucumis sativus L. Sci Hortic Amst 123:521–530CrossRefGoogle Scholar
  12. Forrest KL, Bhave M (2007) Major intrinsic proteins (MIPs) in plants: a complex gene family with major impacts on plant phenotype. Func Integr Genom 7:263–289CrossRefGoogle Scholar
  13. Franceschini A, Szklarczyk D, Frankild S et al (2013) STRING v9. 1: protein-protein interaction networks, with increased coverage and integration. Nucl Acids Res 41:D808–D815CrossRefPubMedGoogle Scholar
  14. Fu D, Libson A, Miercke LJ, Weitzman C, Nollert P, Krucinski J, Stroud RM (2000) Structure of a glycerol conducting channel and the basis for its selectivity. Science 290:481–486CrossRefPubMedGoogle Scholar
  15. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD et al (2005) Protein identification and analysis tools on the ExPASy server. In: Walker JM (ed) The proteomics protocols handbook. Humana, Louisville, pp 571–607CrossRefGoogle Scholar
  16. Geourjon C, Deleage G (1995) SOPMA: significant improvements in protein secondary structure prediction by consensus prediction from multiple alignments. Comput Appl Biosci 11:681–684PubMedGoogle Scholar
  17. Goodstein DM, Shu S, Howson R et al (2012) Phytozome: a comparative platform for green plant genomics. Nucl Acids Res 40:D1178–D1186CrossRefPubMedGoogle Scholar
  18. Guo AY, Zhu QH, Chen X, Luo JC (2007) [GSDS: a gene structure display server]. Yi chuan = Hereditas/Zhongguo yi chuan xue hui bian ji 29:1023–1026CrossRefGoogle Scholar
  19. Harries WE, Akhavan D, Miercke LJ, Khademi S, Stroud RM (2004) The channel architecture of aquaporin 0 at a 2.2 Å resolution. Proc Natl Acad Sci 101:14045–14050CrossRefPubMedPubMedCentralGoogle Scholar
  20. Hruz T, Laule O, Szabo G et al (2008) Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinform 2008:420747CrossRefGoogle Scholar
  21. Ilan B, Tajkhorshid E, Schulten K, Voth GA (2004) The mechanism of proton exclusion in aquaporin channels. Proteins 55:223–228CrossRefPubMedGoogle Scholar
  22. Jia-Wen WU, Yu SHI, Yong-Xing ZHU, Yi-Chao WA, Hai-Jun GO (2013) Mechanisms of enhanced heavy metal tolerance in plants by silicon: a review. Pedosphere 23:815–825CrossRefGoogle Scholar
  23. Kelley LA, Sternberg MJ (2009) Protein structure prediction on the web: a case study using the Phyre server. Nat Protoc 4:363–371CrossRefPubMedGoogle Scholar
  24. Kim YH, Khan AL, Kim DH et al (2014) Silicon mitigates heavy metal stress by regulating P-type heavy metal ATPases, Oryza sativa low silicon genes, and endogenous phytohormones. BMC Plant Biol 14:13CrossRefPubMedPubMedCentralGoogle Scholar
  25. Kliebenstein DJ (2012) Plant defense compounds: systems approaches to metabolic analysis. Annu Rev Phytopathol 50:155–173CrossRefPubMedGoogle Scholar
  26. Krogh A, Larsson B, Von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580CrossRefPubMedGoogle Scholar
  27. Lovell SC, Davis IW, Arendall WB et al (2003) Structure validation by Cα geometry: ϕ, ψ and Cβ deviation. Proteins 50:437–450CrossRefPubMedGoogle Scholar
  28. Lunn JE, Delorge I, Figueroa CM, Van Dijck P, Stitt M (2014) Trehalose metabolism in plants. Plant J 79:544–567CrossRefPubMedGoogle Scholar
  29. Lux A, Luxová M, Hattori T, Inanaga S, Sugimoto Y (2002) Silicification in sorghum (Sorghum bicolor) cultivars with different drought tolerance. Physiol Plant 115:87–92CrossRefPubMedGoogle Scholar
  30. Ma JF (2004) Role of silicon in enhancing the resistance of plants to biotic and abiotic stresses. Soil Sci Plant Nutr 50:11–18CrossRefGoogle Scholar
  31. Ma JF (2010) Si transporters in higher plant. In: Jhon PT, Bienert PG (eds) MIPs and their role in the exchange of materials. Landes Bioscience, Austin, pp 99–109CrossRefGoogle Scholar
  32. Ma JF, Yamaji N (2006) Silicon uptake and accumulation in higher plants. Trends Plant Sci 11:392–397CrossRefPubMedGoogle Scholar
  33. Ma JF, Yamaji N (2008) Functions and transport of silicon in plants. Cell Mol Life Sci 65:3049–3057CrossRefPubMedGoogle Scholar
  34. Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S, Katsuhara M, Ishiguro M, Murata Y, Yano M (2006) A silicon transporter in rice. Nature 440:688–691CrossRefPubMedGoogle Scholar
  35. Ma JF, Yamaji N, Mitani N, Kazunori T, Konishi S, Fujiwara T, Katsuhara M, Yano M (2007) An efflux transporter of silicon in rice. Nature 448:209–212CrossRefPubMedGoogle Scholar
  36. Marchler-Bauer A, Lu S, Anderson JB et al (2011) CDD: a conserved domain database for the functional annotation of proteins. Nucl Acids Res 39:D225–D229CrossRefPubMedGoogle Scholar
  37. Mitani N, Yamaji N, Ma JF (2008) Characterization of substrate specificity of a rice silicon transporter, Lsi1. Pflüger Arch Eur J Phy 456:679–686CrossRefGoogle Scholar
  38. Mitani N, Chiba Y, Yamaji N, Ma JF (2009a) Identification and characterization of maize and barley Lsi2-like silicon efflux transporters reveals a distinct silicon uptake system from that in rice. Plant Cell 21:2133–2142CrossRefPubMedPubMedCentralGoogle Scholar
  39. Mitani N, Yamaji N, Ma JF (2009b) Identification of maize silicon influx transporters. Plant Cell Physiol 50:5–12CrossRefPubMedGoogle Scholar
  40. Mitani N, Yamaji N, Ago Y, Iwasaki K, Ma JF (2011) Isolation and functional characterization of an influx silicon transporter in two pumpkin cultivars contrasting in silicon accumulation. Plant J 66:231–240CrossRefPubMedGoogle Scholar
  41. Mitani-Ueno N, Yamaji N, Zhao FJ, Ma JF (2011) The aromatic/arginine selectivity filter of NIP aquaporins plays a critical role in substrate selectivity for silicon, boron, and arsenic. J Exp Bot 62:4391–4398CrossRefPubMedPubMedCentralGoogle Scholar
  42. Mithöfer A, Boland W (2012) Plant defense against herbivores: chemical aspects. Annu Rev Plant Biol 63:431–450CrossRefPubMedGoogle Scholar
  43. Montpetit J, Vivancos J, Mitani-Ueno N et al (2012) Cloning, functional characterization and heterologous expression of TaLsi1, a wheat silicon transporter gene. Plant Mol Biol 79:35–46CrossRefPubMedGoogle Scholar
  44. Romiti M (2010) Entrez nucleotide and entrez protein FAQs. Gene 1:270Google Scholar
  45. Smoot ME, Ono K, Ruscheinski J, Wang PL, Ideker T (2011) Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 27:431–432CrossRefPubMedGoogle Scholar
  46. Sonnhammer EL, Eddy SR, Durbin R (1997) Pfam: a comprehensive database of protein domain families based on seed alignments. Proteins 28:405–420CrossRefPubMedGoogle Scholar
  47. Sui H, Han BG, Lee JK, Walian P, Jap BK (2001) Structural basis of water-specific transport through the AQP1 water channel. Nature 414:872–878CrossRefPubMedGoogle Scholar
  48. Tamai K, Ma JF (2003) Characterization of silicon uptake by rice roots. New Phytol 158:431–436CrossRefGoogle Scholar
  49. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  50. 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. Nucl Acids Res 22:4673–4680CrossRefPubMedPubMedCentralGoogle Scholar
  51. Timothy TL, Bodén BM, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucl Acids Res 37:202–208CrossRefGoogle Scholar
  52. Wallace IS, Roberts DM (2004) Homology modeling of representative subfamilies of Arabidopsis major intrinsic proteins. Classification based on the aromatic/arginine selectivity filter. Plant Physiol 135:1059–1068CrossRefPubMedPubMedCentralGoogle Scholar
  53. Wu B, Beitz E (2007) Aquaporins with selectivity for unconventional permeants. Cell Mol Life Sci 64:2413–2421CrossRefPubMedGoogle Scholar
  54. Yu CS, Chen YC, Lu CH, Hwang JK (2006) Prediction of protein subcellular localization. Proteins 64:643–651CrossRefPubMedGoogle Scholar
  55. Zhang C, Wang L, Nie Q, Zhang W, Zhang F (2008) Long-term effects of exogenous silicon on cadmium translocation and toxicity in rice (Oryza sativa L.). Environ Exp Bot 62:300–307CrossRefGoogle Scholar
  56. Zhu Y, Gong H (2014) Beneficial effects of silicon on salt and drought tolerance in plants. Agron Sustain Dev 34:455–472CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Recep Vatansever
    • 1
  • Ibrahim Ilker Ozyigit
    • 1
  • Ertugrul Filiz
    • 2
    Email author
  • Nermin Gozukara
    • 3
  1. 1.Department of Biology, Faculty of Science and ArtsMarmara UniversityIstanbulTurkey
  2. 2.Department of Crop and Animal Production, Cilimli Vocational SchoolDuzce UniversityDuzceTurkey
  3. 3.Department of Molecular Biology and Genetics, Faculty of ScienceIstanbul UniversityIstanbulTurkey

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