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Ionome and expression level of Si transporter genes (Lsi1, Lsi2, and Lsi6) affected by Zn and Si interaction in maize

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Abstract

Zinc (Zn) is an essential microelement involved in various plant physiological processes. However, in excess, Zn becomes toxic and represents serious problem for plants resulting in Zn toxicity symptoms and decreasing biomass production. The effect of high Zn and its combination with silicon (Si) on ionome and expression level of ZmLsi genes was investigated in maize (Zea mays, L; hybrid Novania). Plants were cultivated hydroponically in different treatments: control (C), Zn (800 μM ZnSO4 · 7H2O), Si5 (5 mM of sodium silicate solution), and Si5 + Zn (combination of Zn and Si treatments). Growth of plants cultivated for 10 days was significantly inhibited in the presence of high Zn concentration and also by Zn and Si interaction in plants. Based on principal component analysis (PCA) and mineral element concentration in tissues, root ionome was significantly altered in both Zn and Si5 + Zn treatments in comparison to control. Mineral elements Mn, Fe, Ca, P, Mg, Ni, Co, and K significantly decreased, and Se increased in Zn and Si5 + Zn treatments. Shoot ionome was less affected than root ionome. Concentration of shoot Cu, Mn, and P decreased, and Mo increased in Zn and Si5 + Zn treatments. The PCA also revealed that the responsibility for ionome changes is mainly due to Zn exposure and also, but less, by Si application to Zn stressed plants. Expression level of Lsi1 and Lsi2 genes for the Si influx and efflux transporters was downregulated in roots after Si supply and even more downregulated by Zinc alone and also by Zn and Si interaction. Expression level of shoot Lsi6 gene was differently regulated in the first and second leaf. These results indicate negative effect of high Zn alone and also in interaction with Si on Lsi gene expression level and together with ionomic data, it was shown that homeostatic network of mineral elements was disrupted and caused negative alterations in mineral nutrition of young maize plants.

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Abbreviations

PCA:

Principal component analysis

RT:

Number of root tips

RV:

Root volume

TRL:

Total root length

TRS:

Total root surface area

ZmLsi :

Zea mays Si transporter gene

References

  • Bokor B, Vaculík M, Slováková Ľ, Masarovič D, Lux A (2014) Silicon does not always mitigate zinc toxicity in maize. Acta Physiol Plant 36:733–743

    Article  CAS  Google Scholar 

  • Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytol 173:677–702

    Article  CAS  Google Scholar 

  • Cabannes E, Buchner P, Broadley MR, Hawkesford MJ (2011) A comparison of sulfate and selenium accumulation in relation to the expression of sulfate transporter genes in Astragalus species. Plant Physiol 157:2227–2239

    Article  CAS  Google Scholar 

  • Chiba Y, Mitani N, Yamaji N, Ma JF (2009) HvLsi1 is a silicon influx transporter in barley. Plant J 57:810–818

    Article  CAS  Google Scholar 

  • Chen Z, Shinano T, Ezawa T, Wasaki J, Kimura K, Osaki M, Zhu Y (2009) Elemental interconnections in Lotus japonicus: a systematic study of the effects of elements additions on different natural variants. Soil Sci Plant Nutr 55:91–101

    Article  CAS  Google Scholar 

  • Currie HA, Perry CC (2007) Silica in plants: biological, biochemical and chemical studies. Ann Bot 100:1383–1389

    Article  CAS  Google Scholar 

  • Dibb DW, Thompson WR (1985) Interaction of potassium with other nutrients. In: Munson RD (ed) Potassium in agriculture. Madison, Wisconsin, USA, pp 515–533

    Google Scholar 

  • Deshmukh RK, Vivancos J, Guérin V, Sonah H, Labbé C, Belzile F, Bélanger RR (2013) 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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Epstein E (1999) Silicon. Annu Rev Plant Physiol Plant Mol Biol 50:641–664

    Article  CAS  Google Scholar 

  • Gutierrez-Carbonell E, Lattanzio G, Sagardoy R, Rodríguez-Celma J, Ruiz JJR, Matros A, Abadía A, Abadía J, López-Millán A-F (2013) Changes induced by zinc toxicity in the 2-DE protein profile of sugar beet roots. J Proteomics 94:149–161

    Article  CAS  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Soil Circ Univ Calif Agric Exp Station, Berkley, p 347

    Google Scholar 

  • Horiguchi T, Morita S (1987) Mechanism of manganese toxicity and tolerance of plants. VI Effect of silicon on alleviation of manganese toxicity of barley J Plant Nutr 10:2299–2310

    CAS  Google Scholar 

  • Hove RM, Bhave M (2011) Plant aquaporins with non-aqua functions: deciphering the signature sequences. Plant Mol Biol 75:413–430

    Article  CAS  Google Scholar 

  • Jiang HM, Yang JC, Zhang JF (2007) Effects of external phosphorus on the cell ultrastructure and the chlorophyll content of maize under cadmium and zinc stress. Environ Pollut 147:750–756

    Article  CAS  Google Scholar 

  • Kaya C, Tuna AL, Sonmez O, Ince F, Higgs D (2009) Mitigation effects of silicon on maize plants grown at high zinc. J Plant Nutr 32:1788–1798

    Article  CAS  Google Scholar 

  • Kim Y-H, Khan AL, Kim D-H, Lee S-Y, Kim K-M, Waqas M, Jung H-Y, Shin J-H, Kim J-G, Lee I-J (2014) Silicon mitigates heavy metal stress by regulating P-type heavy metal ATPases, Oryza sativa low silicon genes, and endogenous phytohormones. BMC Plant Bio 14:1–13

    Google Scholar 

  • Lahner B, Gong J, Mahmoudian M, Smith EL, Abid KB, Rogers EE, Guerinot ML, Harper JF, Ward JM, Mcintyre L, Schroeder JI, Salt DE (2003) Genomic scale profiling of nutrient and trace elements in Arabidopsis thaliana. Nat Biotechno 21:1215–1221

    Article  CAS  Google Scholar 

  • Lukačová Z, Švubová R, Kohanová J, Lux A (2013) Silicon mitigates the Cd toxicity in maize in relation to cadmium translocation, cell distribution, antioxidant enzymes stimulation and enhanced endodermal apoplasmic barrier development. Plant Growth Regul 70:89–103

    Article  Google Scholar 

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

    Article  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 440:688–691

    Article  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 448:209–211

    Article  CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press Ltd., London, San Diego

    Google Scholar 

  • Martinka M, Vaculík M, Lux A (2014) Plant cell responses to cadmium and zinc. In: Nick P, Opatrný Z (eds) Applied plant cell biology. Cellular Tools and Approaches for Plant Biotechnology. Heidelberg, New York, Dordrecht, London, Springer, pp 209–246

    Chapter  Google Scholar 

  • Masarovič D, Slováková Ľ, Bokor B, Bujdoš M, Lux A (2012) Effect of silicon application on Sorghum bicolor exposed to toxic concentration of zinc. Biologia 67:706–712

    Google Scholar 

  • Milner MJ, Seamon J, Craft E, Kochian LV (2013) Transport properties of members of the ZIP family in plants and their role in Zn and Mn homeostasis. J Exp Bot 64:369–381

    Article  CAS  Google Scholar 

  • Mitani N, Yamaji N, Ma JF (2008) Characterization of substrate specificity of a rice silicon transporter, Lsi1. Pflugers Arch 456:679–686

    Article  CAS  Google Scholar 

  • 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 66:231–240

    Article  CAS  Google Scholar 

  • Mitani N, Yamaji N, Ma JF (2009a) Identification of maize silicon influx transporters. Plant Cell Physiol 50:5–12

    Article  CAS  Google Scholar 

  • Mitani N, Chiba Y, Yamaji N, Ma JF (2009b) Identification and characterization of maize and barley Lsi2-like silicon efflux transporters reveals a distinct silicon uptake system from that in rice. Plant Cell 21:2133–2142

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Päivöke AEA (2003) Mineral elements and phytase activity in Pisum sativum grown at different Zn supply levels in the greenhouse. Environ Exp Bot 49:285–294

    Article  Google Scholar 

  • Pignattelli S, Colzi I, Buccianti A, Cattani I, Beone GM, Schat H, Gonnelli G (2013) A multielement analysis of Cu induced changes in the mineral profiles of Cu sensitive and tolerant populations of Silene paradoxa L. Environ Exp Bot 96:20–27

    Article  CAS  Google Scholar 

  • Puig S, Peñarrubia L (2009) Placing metal micronutrients in context: transport and distribution in plants. Curr Opin Plant Biol 12:299–306

    Article  CAS  Google Scholar 

  • Remans T, Opdenakker K, Guisez Y, Carleer R, Schat H, Vangronsveld J, Cuypers A (2012) Exposure of Arabidopsis thaliana to excess Zn reveals a Zn-specific oxidative stress signature. Environ Exp Bot 84:61–71

    Article  CAS  Google Scholar 

  • Sagardoy R, Morales F, López-Millán AF, Abadía A, Abadía J (2009) Effects of zinc toxicity on sugar beet (Beta vulgaris L.) plants grown in hydroponics. Plant Biol 11:339–350

    Article  CAS  Google Scholar 

  • Salt DE, Baxter I, Lahner B (2008) Ionomics and the study of the plant ionome. Annu Rev Plant Biol 59:709–733

    Article  CAS  Google Scholar 

  • Sárdi K, Balázsy Á, Salamon B (2012) Interrelations in phosphorus and potassium accumulation characteristics of plants grown in different soil types. Commun Soil Sci Plant Anal 43:324–333

    Article  Google Scholar 

  • Sinclair SA, Krämer U (2012) The zinc homeostasis network of land plants. Biochim Biophys Acta 1823:1553–1567

    Article  CAS  Google Scholar 

  • Singh UM, Sareen P, Sengar RS, Kumar A (2013) Plant ionomics: a newer approach to study mineral transport and its regulation. Acta Physiol Plant 35:2641–2653

    Article  CAS  Google Scholar 

  • Sors TG, Ellis DR, Na GN, Lahner B, Lee S, Leustek T, Pickering IJ, Salt DE (2005) Analysis of sulfur and selenium assimilation in Astragalus plants with varying capacities to accumulate selenium. Plant J 42:785–797

    Article  CAS  Google Scholar 

  • Schaller J, Brackhage C, Gessner MO, Bäuker E, Dudel EG (2012) Silicon supply modifies C:N:P stoichiometry and growth of Phragmites australis. Plant Biol 14:392–396

    Article  CAS  Google Scholar 

  • Shanmugam V, Lo J-C, Wu C-L, Wang S-L, Lai C-C, Connolly EL, Huang J-L, Yeh K-C (2011) Differential expression and regulation of iron-regulated metal transporters in Arabidopsis halleri and Arabidopsis thaliana—the role in zinc tolerance. New Phytol 190:125–137

    Article  CAS  Google Scholar 

  • Shanmugam V, Lo J-C, Yeh K-C (2013) Control of Zn uptake in Arabidopsis halleri: a balance between Zn and Fe. Front. Plant Sci 4:1–5

    Google Scholar 

  • Shi Q, Bao Z, Zhu Z, He Y, Qian Q, Yu J (2005) Silicon-mediated alleviation of Mn toxicity in Cucumis sativus in relation to activities of superoxide dismutase and ascorbate peroxidase. Phytochemistry 66:1551–1559

    Article  CAS  Google Scholar 

  • Song A, Li P, Li P, Fan F, Nikolic M, Liang Y (2011) The alleviation of zinc toxicity by silicon is related to zinc transport and antioxidative reaction in rice. Plant Soil 344:319–333

    Article  CAS  Google Scholar 

  • Tian T, Ali B, Qin Y, Malik Z, Gill RA, Ali S, Zhou W (2014) Alleviation of lead toxicity by 5-aminolevulinic acid is related to elevated growth, photosynthesis, and suppressed ultrastructural damages in oilseed rape. Biomed Res Int 2014:1–11

    Google Scholar 

  • Yamaji N, Mitatni N, Ma JF (2008) A transporter regulating silicon distribution in rice shoots. Plant Cell 20:1381–1389

    Article  CAS  Google Scholar 

  • Yue X, Zhao XY, Fei YK, Zhang X (2012) Correlation of aquaporins and transmembrane solute transporters revealed by genome-wide analysis in developing maize leaf. Comp Funct Genomics 2012:1–14

    Article  Google Scholar 

  • Vaculík M, Landberg T, Greger M, Luxová M, Stoláriková M, Lux A (2012) Silicon modifies root anatomy, and uptake and subcellular distribution of cadmium in young maize plants. Ann Bot 110:433–443

    Article  Google Scholar 

  • Wang C, Zhang SH, Wang PF, Hou J, Zhang WJ, Li W, Lin ZP (2009) The effect of excess Zn on mineral nutrition and antioxidative response in rapeseed seedlings. Chemosphere 75:1468–1476

    Article  CAS  Google Scholar 

  • Zangi R, Filella M (2012) Transport routes of metalloids into and out of the cell: a review of the current knowledge. Chem-Biol Interact 197:47–57

    Article  CAS  Google Scholar 

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Acknowledgment

The work was supported by the Slovak Research and Development Agency under the contract Nr. APVV-0140-10 and also by the project implementation: Comenius University in Bratislava Science Park supported by the Research and Development Operational Programme funded by the ERDF Grant number: ITMS 26240220086.

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Correspondence to Boris Bokor.

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Responsible editor: Philippe Garrigues

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Bokor, B., Bokorová, S., Ondoš, S. et al. Ionome and expression level of Si transporter genes (Lsi1, Lsi2, and Lsi6) affected by Zn and Si interaction in maize. Environ Sci Pollut Res 22, 6800–6811 (2015). https://doi.org/10.1007/s11356-014-3876-6

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