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Identification and functional characterization of silicon transporters in soybean using comparative genomics of major intrinsic proteins in Arabidopsis and rice

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Abstract

Silicon (Si) confers several benefits to many plant species when absorbed as silicic acid through nodulin 26-like intrinsic proteins (NIPs). The NIPs belong to major intrinsic protein (MIP) family, members of which form channels with high selectivity to control transport of water and different solutes. Here, comparative genomic analysis of the MIPs was performed to investigate the presence of Si transporter MIPs in soybean. Thorough analysis of phylogeny, gene organization, transcriptome profiling and protein modeling was performed to characterize MIPs in rice, Arabidopsis and soybean. Based on several attributes, two putative Si transporter genes, GmNIP2-1 and GmNIP2-2, were identified, characterized and cloned from soybean. Expression of both genes was detected in shoot and root tissues, and decreased as Si increased. The protein encoded by GmNIP2-2 showed functionality for Si transport when expressed in Xenopus oocytes, thus confirming the genetic capability of soybean to absorb the element. Comparative analysis of MIPs in plants provides opportunities to decipher gene evolution, functionality and selectivity of nutrient uptake mechanisms. Exploitation of this strategy has helped to uncover unique features of MIPs in soybean. The identification and functional characterization of Si transporters can be exploited to optimize the benefits that plants can derive from Si absorption.

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References

  • Arsenault-Labrecque G, Menzies JG, Bélanger RR (2012) Effect of silicon absorption on soybean resistance to Phakopsora pachyrhizi in different cultivars. Plant Dis 96(1):37–42

    Article  CAS  Google Scholar 

  • Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34(Suppl 2):W369–W373

    Article  PubMed  CAS  Google Scholar 

  • Bernsel A, Viklund H, Hennerdal A, Elofsson A (2009) TOPCONS: consensus prediction of membrane protein topology. Nucleic Acids Res 37(Suppl 2):W465–W468

    Article  PubMed  CAS  Google Scholar 

  • Bienert GP, Bienert MD, Jahn TP, Boutry M, Chaumont F (2011) Solanaceae XIPs are plasma membrane aquaporins that facilitate the transport of many uncharged substrates. Plant J 66(2):306–317

    Article  PubMed  CAS  Google Scholar 

  • Caron L, Rousseau F, Gagnon E, Isenring P (2000) Cloning and functional characterization of a cation Cl cotransporter-interacting protein. J Biol Chem 275(41):32027–32036

    Article  PubMed  CAS  Google Scholar 

  • de Hoon MJ, Imoto S, Nolan J, Miyano S (2004) Open source clustering software. Bioinformatics 20(9):1453–1454

    Article  PubMed  Google Scholar 

  • Dean RM, Rivers RL, Zeidel ML, Roberts DM (1999) Purification and functional reconstitution of soybean nodulin 26. An aquaporin with water and glycerol transport properties. Biochemistry 38(1):347–353

    Article  PubMed  CAS  Google Scholar 

  • Deren CW (2001) Plant genotype, silicon concentration, and silicon-related responses. Stud Plant Sci 8:149–158

    Article  CAS  Google Scholar 

  • Epstein E (1994) The anomaly of silicon in plant biology. Proc Natl Acad Sci USA 91:11–17

    Article  PubMed  CAS  Google Scholar 

  • Fauteux F, Rémus-Borel W, Menzies JG, Bélanger RR (2005) Silicon and plant disease resistance against pathogenic fungi. FEMS Microbiol Lett 249(1):1–6

    Article  PubMed  CAS  Google Scholar 

  • Fortin MG, Morrison NA, Verma DP (1987) Nodulin 26, a peribacteroid membrane nodulin is expressed independently of the development of the peribacteroid compartment. Nucleic Acids Res 15(2):813–824

    Article  PubMed  CAS  Google Scholar 

  • Fouquet R, Léon C, Ollat N, Barrieu F (2008) Identification of grapevine aquaporins and expression analysis in developing berries. Plant Cell Rep 27(9):1541–1550

    Article  PubMed  CAS  Google Scholar 

  • Froger A, Thomas D, Delamarche C, Tallur B (1998) Prediction of functional residues in water channels and related proteins. Protein Sci 7(6):1458–1468

    Article  PubMed  CAS  Google Scholar 

  • Gattolin S, Sorieul M, Frigerio L (2011) Mapping of tonoplast intrinsic proteins in maturing and germinating Arabidopsis seeds reveals dual localization of embryonic TIPs to the tonoplast and plasma membrane. Mol Plant 4(1):180–189

    Article  PubMed  CAS  Google Scholar 

  • Giovannetti M, Balestrini R, Volpe V, Guether M, Straub D, Costa A, Ludewig U, Bonfante P (2012) Two putative-aquaporin genes are differentially expressed during arbuscular mycorrhizal symbiosis in Lotus japonicus. BMC Plant Biol 12(1):186

    Article  PubMed  CAS  Google Scholar 

  • Gonen T, Sliz P, Kistler J, Cheng Y, Walz T (2004) Aquaporin-0 membrane junctions reveal the structure of a closed water pore. Nature 429(6988):193–197

    Article  PubMed  CAS  Google Scholar 

  • Grégoire C, Rémus-Borel W, Vivancos J, Labbé C, Belzile F, Bélanger RR (2012) Discovery of a multigene family of aquaporin silicon transporters in the primitive plant Equisetum arvense. Plant J72(2):320–330

    Google Scholar 

  • Guntzer F, Keller C, Meunier JD (2012) Benefits of plant silicon for crops: a review. Agron Sustain Dev 32(1):201–213

    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 Ser 41:95–98

    CAS  Google Scholar 

  • Harries WEC, Akhavan D, Miercke LJW, Khademi S, Stroud RM (2004) The channel architecture of aquaporin 0 at a 2.2-A resolution. Proc Natl Acad Sci USA 101:14045–14050

    Article  PubMed  CAS  Google Scholar 

  • Hodson MJ, White PJ, Mead A, Broadley MR (2005) Phylogenetic variation in the silicon composition of plants. Ann Bot 96(6):1027–1046

    Article  PubMed  CAS  Google Scholar 

  • Kaczanowski S, Zielenkiewicz P (2010) Why similar protein sequences encode similar three-dimensional structures? Theor Chem Acc Theory Comput Model (Theoretica Chimica Acta) 125:643–650

  • Kumar S, Nei M, Dudley J, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9(4):299–306

    Article  PubMed  CAS  Google Scholar 

  • Lee JK, Kozono D, Remis J, Kitagawa Y, Agre P, Stroud RM (2005) Structural basis for conductance by the archaeal aquaporin AqpM at 1.68 A. Proc Natl Acad Sci USA 102(52):18932–18937

    Google Scholar 

  • Ma JF, Yamaji N (2006) Silicon uptake and accumulation in higher plants. Trends Plant Sci 11(8):392–397

    Article  PubMed  CAS  Google Scholar 

  • 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(7084):688–691

    Article  PubMed  CAS  Google Scholar 

  • Ma JF, Yamaji N, Mitani N, Tamai K, Konishi S, Fujiwara T, Katsuhara M, Yano M (2007) An efflux transporter of silicon in rice. Nature 448(7150):209–212

    Article  PubMed  CAS  Google Scholar 

  • Matsumoto T, Lian HL, Su WA, Tanaka D, Liu C, Iwasaki I, Kitagawa Y (2009) Role of the aquaporin PIP1 subfamily in the chilling tolerance of rice. Plant Cell Physiol 50(2):216–229

    Article  PubMed  CAS  Google Scholar 

  • Maurel C, Verdoucq L, Luu DT, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Ann Rev Plant Biol 59:595–624

    Article  CAS  Google Scholar 

  • Mitani N, Yamaji N, Ma JF (2008) Characterization of substrate specificity of a rice silicon transporter, Lsi1. Pflügers Archiv Eur J Physiol 456(4):679–686

    Article  CAS  Google Scholar 

  • 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(12):4391–4398

    Article  PubMed  CAS  Google Scholar 

  • Montpetit J, Vivancos J, Mitani-Ueno N, Yamaji N, Rémus-Borel W, Belzile F, Ma FJ, Bélanger RR (2012) Cloning, functional characterization and heterologous expression of TaLsi1, a wheat silicon transporter gene. Plant Mol Biol 79(1–2):35–46

    Article  PubMed  CAS  Google Scholar 

  • Newby ZE, O’Connell LJ, Robles-Colmenares Y, Khademi S, Miercke LJW, Stroud RM (2008) Crystal structure of the aquaglyceroporin PfAQP from the malarial parasite Plasmodium falciparum. Nat Struct Mol Biol 15(6):619–625

    Article  PubMed  CAS  Google Scholar 

  • Quigley F, Rosenberg JM, Shachar-Hill Y, Bohnert HJ (2002) From genome to function: the Arabidopsis aquaporins. Genome Biol 3(1):1–17

    Google Scholar 

  • Reidinger S, Ramsey M, Hartley SE (2012) Rapid and accurate analyses of silicon and phosphorus in plants using a portable X-ray fluorescence spectrometer. New Phytol 195(3):699–706

    Article  PubMed  CAS  Google Scholar 

  • Richmond KE, Sussman M (2003) Got silicon? The non-essential beneficial plant nutrient. Curr Opin Plant Biol 6(3):268–272

    Article  PubMed  CAS  Google Scholar 

  • Roulin A, Auer PL, Libault M, Schlueter J, Farmer A, May G, Stacey G, Doerge RW, Jackson SA (2013) The fate of duplicated genes in a polyploid plant genome. Plant J73(1):143–153

    Google Scholar 

  • Sakurai J, Ishikawa F, Yamaguchi T, Uemura M, Maeshima M (2005) Identification of 33 rice aquaporin genes and analysis of their expression and function. Plant Cell Physiol 46(9):1568–1577

    Article  PubMed  CAS  Google Scholar 

  • Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463(7278):178–183

    Article  PubMed  CAS  Google Scholar 

  • Severin AJ, Woody JL, Bolon YT, Joseph B, Diers BW, Farmer AD, Muehlbauer GJ, Nelson RT, Grant D, Specht JE et al (2010) RNA-Seq Atlas of Glycine max: a guide to the soybean transcriptome. BMC Plant Biol 10(10):160

    Article  PubMed  Google Scholar 

  • Shen X, Li X, Li Z, Li J, Duan L, Eneji AE (2010) Growth, physiological attributes and antioxidant enzyme activities in soybean seedlings treated with or without silicon under UV-B radiation stress. J Agron Crop Sci 196(6):431–439

    Article  CAS  Google Scholar 

  • Sonah H, Deshmukh RK, Singh VP, Gupta DK, Singh NK, Sharma TR (2011) Genomic resources in horticultural crops: status, utility and challenges. Biotech Adv 29(2):199–209

    Article  Google Scholar 

  • Wallace IS, Roberts DM (2005) Distinct transport selectivity of two structural subclasses of the nodulin-like intrinsic protein family of plant aquaglyceroporin channels. Biochemistry 44(51):16826–16834

    Article  PubMed  CAS  Google Scholar 

  • Wiederstein M, Sippl MJ (2007) ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Res 35(Suppl 2):W407–W410

    Article  PubMed  Google Scholar 

  • Zhang DY, Ali Z, Wang CB, Xu L, Yi JX, Xu ZL, Liu XQ, He XL, Huang YH, Khan IA et al (2013) Genome-wide sequence characterization and expression analysis of major intrinsic proteins in soybean (Glycine max L.). PLoS ONE 8(2):e56312

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The project was funded by a grant from the Natural Sciences and Engineering Research Council of Canada (NSERC) in collaboration with Syngenta Biotechnology and the Canada Research Chairs Program to RRB. The authors would like to thank the group of Dr. P. Isenring from the Nephrology Research Group of the CHUQ-L’Hôtel-Dieu de Québec Institution for help with the oocyte assays.

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The authors declare that they have no conflict of interest.

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Correspondence to Richard R. Bélanger.

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Deshmukh, R.K., Vivancos, J., Guérin, V. et al. Identification and functional characterization of silicon transporters in soybean using comparative genomics of major intrinsic proteins in Arabidopsis and rice. Plant Mol Biol 83, 303–315 (2013). https://doi.org/10.1007/s11103-013-0087-3

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