DOI QR코드

DOI QR Code

Analysis of gene expression in red maple (Acer rubrum) and trembling aspen (Populus tremuloides) populations from a mining region

  • Kalubi, K.N. (Biomolecular Sciences Program, Laurentian University) ;
  • Michael, P. (Biomolecular Sciences Program, Laurentian University) ;
  • Omri, A. (Biomolecular Sciences Program, Laurentian University)
  • Received : 2017.08.21
  • Accepted : 2018.02.07
  • Published : 2018.11.30

Abstract

The Greater Sudbury Region has been known as one of the most ecologically disturbed areas in Canada for the past century. Plant adaptation to environmental stressors often results in modifications in gene expression at the transcriptional level. The main objective of the present study was to compare the expression of genes associated with nickel resistance in Acer rubrum and Populus tremuloides growing in areas contaminated and uncontaminated with metals. Primers targeting Nramps4, Nas 3, At2G, MRP4 and alpha-tubulin genes were used to amplify cDNA of both species. The expression of the At2G gene, was $2{\times}$ and $9{\times}$ higher in P. tremuloides than in A. rubrum for St. Charles (uncontaminated site) and Kelly Lake (metal contaminated site), respectively. There was a much smaller difference between the two species for the Nramps 4 gene as its expression was $2.5{\times}$ and $3{\times}$ higher in P. tremuloides compared to A. rubrum from St. Charles and Kelly Lake, respectively. The same trend was observed for the MRP4 gene whose expression was $2{\times}$ and $14{\times}$ higher in P. tremuloides than in A. rubrum from St. Charles and Kelly Lake, respectively. For the Nas 3 gene, the expression was similar in both sites. This gene was upregulated $11{\times}$ and $10{\times}$ in P. tremuloides compared to A. rubrum in samples from St. Charles and Kelly Lake, respectively. In general, no significant difference was observed between the metal contaminated and uncontaminated sites for gene expression. In depth analysis revealed that AT2G and MRP4 genes were significantly down regulated in A. rubrum from the metal contaminated sites compared to those from uncontaminated areas, but environmental factors driving this differential gene expression couldn't be established.

Keywords

Acknowledgement

Supported by : Natural Sciences and Engineering Council of Canada (NSERC)

References

  1. Ahlgren CE, Hansen HL (1957) Some effects of temporary flooding on coniferous trees. J For 55:647-650
  2. Arthur JJ, Leone IA, Flower FB (1981) Flooding and landfill gas effects on red and sugar maples. J Environ Qual 10:431-433
  3. Bagatto G, Crowder AA, Shorthouse JD (1993) Concentrations of metals in tissues of lowbush blueberry (Vaccinium angustifolium) near a copper-nickel smelter at Sudbury, Ontario, Canada: a factor analytic approach. Bull Environ Contam Toxicol 51:600-604
  4. Belouchi A, Kwan T, Gros P (1997) Cloning and characterization of the OsNramp family from Oryza sativa, a new family of membrane proteins possibly implicated in the transport of metal ions. Plant Mol Biol 33:1085-1092 https://doi.org/10.1023/A:1005723304911
  5. Bovet L, Feller U, Martinoia E (2005) Possible involvement of plant ABC transporters in cadmium detoxification: a cDNA sub-microarray approach. Environ Int 31:263-267 https://doi.org/10.1016/j.envint.2004.10.011
  6. Brune A, Urbach W, Dietz K-J (1995) Differential toxicity of heavy metals is partly related to a loss of preferential extraplasmic compartmentation: a comparison of Cd-, Mo-, Ni- and Znstress. New Phytol 129:403-409 https://doi.org/10.1111/j.1469-8137.1995.tb04310.x
  7. Brunner AM, Yakovlev IA, Strauss SH (2004) Validating internal controls for quantitative plant gene expression studies. BMC Plant Biol 4:14 https://doi.org/10.1186/1471-2229-4-14
  8. Curie C, Panaviene Z, Loulergue C, Dellaporta SL, Briat J, Waker E (2001) Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature 409:346-349 https://doi.org/10.1038/35053080
  9. Dietz AC, Schnoor JL (2001) Advances in phytoremediation. Environ Health Perspect 109(Suppl 1):163-168
  10. Djeukam CL, Theriault G, Michael P, Nkongolo KK (2016) Analysis of gene expression associated with copper toxicity in white birch (Betula papyrifera) populations from a mining region. Br Biotechnol J Niger 15:1-10. https ://doi.org/10.9734/BBJ/2016/28425
  11. Freedman B, Hutchinson T (1980) Pollutant inputs from the atmosphere and accumulations in soils and vegetation near a nickel-copper smelter at Sudbury, Ontario, Canada. Can J Bot 58:108-132 https://doi.org/10.1139/b80-014
  12. Freeman J, Persans M, Nieman K, Albrecht C, Peer W, Pickering IJ, Salt D (2004) Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Cell 16:2176-2191 https://doi.org/10.1105/tpc.104.023036
  13. Ghasemi F, Heidari R, Jameii R, Purakbar L (2012) Effects of Ni2 + toxicity on hill reaction and membrane functionality in maize. J Stress Physiol Biochem 8:55-61
  14. Gratton WS, Nkongolo KK, Spiers GA (2000) Heavy metal accumulation in soil and jack pine (Pinus banksiana) needles in Sudbury, Ontario, Canada. Bull Environ Contam Toxicol 64:550-557 https://doi.org/10.1007/s001280000038
  15. Hall JL, Williams LE (2003) Transition metal transporters in plants. J Exp Bot 54:2601-2613 https://doi.org/10.1093/jxb/erg303
  16. Hirt H, Shinozaki K (2004) Plant responses to abiotic stress. Springer, Berlin
  17. Inoue H, Higuchi K, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2003) Three rice nicotianamine synthase genes, OsNAS1, OsNAS2, and OsNAS3 are expressed in cells involved in longdistance transport of iron and differentially regulated by iron. Plant J 36:366-381 https://doi.org/10.1046/j.1365-313X.2003.01878.x
  18. Iyaka YA (2011) Nickel in soils: a review of its distribution and impacts. Sci Res Essays 6:6774-6777
  19. James GI, Courtin GM (1985) Stand structure and growth form of the birch transition community in an industrially damaged ecosystem, Sudbury, Ontario. Can J For Res 15:809-817 https://doi.org/10.1139/x85-131
  20. Jonak C, Nakagami H, Hirt H (2004) Heavy metal stress: activation of distinct mitogen-activated protein kinase pathways by copper and cadmium. Plant Physiol 136:3276-3283 https://doi.org/10.1104/pp.104.045724
  21. Kalubi KN, Mehes-Smith M, Narendrula R, Michael P, Omri A (2015) Molecular analysis of red maple (Acer rubrum) populations from a reclaimed mining region in northern Ontario (Canada): soil metal accumulation and translocation in plants. Ecotoxicology 24:636-647 https://doi.org/10.1007/s10646-014-1411-7
  22. Kovalchuk I, Titov V, Hohn B, Kovalchuk O (2005) Transcriptome profiling reveals similarities and differences in plant responses to cadmium and lead. Mutat Res Mol Mech Mutagen 570:149-161 https://doi.org/10.1016/j.mrfmmm.2004.10.004
  23. Krause CR, Dochinger LS (1987) Sulfur accumulation in red maple leaves exposed to sulfur dioxide. Phytopathology 77:1438-1441 https://doi.org/10.1094/Phyto-77-1438
  24. Lemaire S, Guillon B, Le Marechal P, Keryer E, Miginiac-Maslow M, Decottignies P (2004) New thioredoxin targets in the unicellular photosynthetic eukaryote Chlamydomonas reinhardtii. Proc Natl Acad Sci 101:7475-7480 https://doi.org/10.1073/pnas.0402221101
  25. Lin Y-C, Kao C-H (2005) Ni toxicity of rice seedlings: cell wall peroxidase, lignin, and NiSO4-inhibited root growth nickel toxicity of rice seedlings: cell wall peroxidase, lignin, and NiSO 4 -inhibited root growth. Crop Environ Bioinformatics 2:131-136
  26. Liu J, Han HJ, Kim SH, Lim CO, Yun DJ, Chung WK (2014) ZAT11, a zinc finger transcription factor, is a negative regulator of nickel ion tolerance in Arabidopsis. Plant Cell Rep 33:2015-2021 https://doi.org/10.1007/s00299-014-1675-7
  27. Makela M, Michael P, Theriault G, Nkongolo KK (2016) High genetic variation among closely related red oak (Quercus rubra) populations in an ecosystem under metal stress: analysis of gene regulation. Genes Genomics 38:967-976 https://doi.org/10.1007/s13258-016-0441-3
  28. Mari S, Gendre D, Pianelli K, Ouerdane L, Lobinski R, Briat JF, Lebrun M, Czernic P (2006) Root-to-shoot long-distance circulation of nicotianamine and nicotianamine-nickel chelates in the metal hyperaccumulator Thlaspi caerulescens. J Exp Bot 57:4111-4122 https://doi.org/10.1093/jxb/erl184
  29. Matters GL, Scandalios JG (1986) Changes in plant gene expression during stress. Dev Genet 7:167-175 https://doi.org/10.1002/dvg.1020070402
  30. Meagher R (2000) Phytoremediation of toxic elemental and organic pollutants. Curr Opin Plant Biol 3:153-162 https://doi.org/10.1016/S1369-5266(99)00054-0
  31. Mehes-Smith M, Nkongolo KK (2015) Physiological and cytological responses of Deschampsia cespitosa and Populus tremuloides to soil metal contamination. Water Air Soil Pollut 226:125 1-12. https ://doi.org/10.1007/s1127 0-015-2382-x
  32. Mizuno T, Usui K, Horie K, Nosaka S, Mizuno N, Obata H (2005) Cloning of three ZIP/Nramp transporter genes from a Ni hyperaccumulator plant Thlaspi japonicum and their Ni2+-transport abilities. Plant Physiol Biochem 43:793-801 https://doi.org/10.1016/j.plaphy.2005.07.006
  33. Nkongolo KK, Spiers G, Beckett P, Narendrula R, Theriault G, Tran A, Kalubi K (2013) Long-term effects of liming on soil chemistry in stable and eroded upland areas in a mining region. Water Air Soil Pollut 224:1618. https ://doi.org/10.1007/s1127 0-013-1618-x
  34. Rodionov DA, Hebbeln P, Gelfand MS, Eitinger T (2006) Comparative and functional genomic analysis of prokaryotic nickel and cobalt uptake transporters: evidence for a novel group of ATP-binding cassette transporters. J Bacteriol 188:317-327 https://doi.org/10.1128/JB.188.1.317-327.2006
  35. Salt DE, Smith RD, Raskin I (1998) Phytoremediation. Annu Rev Plant Physiol Plant Mol Biol 49:643-668 https://doi.org/10.1146/annurev.arplant.49.1.643
  36. Sanita di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41:105-130 https://doi.org/10.1016/S0098-8472(98)00058-6
  37. Schaaf G, Honsbein A, Meda AR, Kirchner S, Wipf D, von Wiren N (2006) AtIREG2 encodes a tonoplast transport protein involved in iron-dependent nickel detoxification in Arabidopsis thaliana roots. J Biol Chem 281:25532-25540 https://doi.org/10.1074/jbc.M601062200
  38. Sodani K, Patel A, Kathawala RJ, Chen Z-S (2012) Multidrug resistance associated proteins in multidrug resistance. Chin J Cancer 31:58-72 https://doi.org/10.5732/cjc.011.10329
  39. Sreekanth TVM, Nagajyothi PC, Lee KD, Prasad TNVKV. (2013) Occurrence, physiological responses and toxicity of nickel in plants. Int J Environ Sci Technol 10:1129-1140 https://doi.org/10.1007/s13762-013-0245-9
  40. Stearns J, Shah S, Greenbeerg B, Dixon DG, Glick BR (2005) Tolerance of transgenic canola expressing 1-aminocyclopropane-1-carboxylic acid deaminase to growth inhibition by nickel. Plant Physiol Biochem 43:701-708 https://doi.org/10.1016/j.plaphy.2005.05.010
  41. Theriault G, Nkongolo KK, Narendrula R, Beckett P (2013) Molecular and ecological characterisation of plant populations from limed and metal-contaminated sites in Northern Ontario (Canada): ISSR analysis of white birch (Betula papyrifera) populations. Chem Ecol 29:573-585 https://doi.org/10.1080/02757540.2013.820715
  42. Theriault G, Nkongolo KK, Michael P (2014) Genetic and metal analyses of fragmented populations of Betula papyrifera (Marsh) in a mining reclaimed region: identification of population-diagnostic molecular marker. Ecol Evol 4:3435-3443 https://doi.org/10.1002/ece3.1195
  43. Theriault G, Michael P, Nkongolo K (2016) Decrypting the regulation and mechanism of nickel resistance in white birch (Betula papyrifera) using cross-species metal-resistance genes. Genes Genomics 38:341-350 https://doi.org/10.1007/s13258-016-0387-5
  44. Thomine S, Lelievre F, Debarbieux E, Schroeder JI, Barbier-Brygoo H (2003) AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency. Plant J 34:685-695 https://doi.org/10.1046/j.1365-313X.2003.01760.x
  45. Van Assche F, Clijsters H (1990) Effects of metals on enzyme activity in plants. Plant Cell Environ 13:195-206 https://doi.org/10.1111/j.1365-3040.1990.tb01304.x
  46. Visioli G, Vincenzi S, Marmiroli M, Marmiroli N (2012) Correlation between phenotype and proteome in the Ni hyperaccumulator Noccaea caerulescens subsp. caerulescens. Environ Exp Bot 77:156-164 https://doi.org/10.1016/j.envexpbot.2011.11.016
  47. Wei W, Chai T, Zhang Y, Han L, Xu J, Guan Z (2008) The Thlaspi caerulescens NRAMP Homologue TcNRAMP3 is capable of divalent cation transport. Mol Biotechnol 41:15-21
  48. Williams LE, Pittman JK, Hall JL (2000) Emerging mechanisms for heavy metal transport in plants. Biochim Biophys Acta 1465:104-126 https://doi.org/10.1016/S0005-2736(00)00133-4

Cited by

  1. Differential effects of nickel dosages on in vitro and in vivo seed germination and expression of a high affinity nickel-transport family protein (AT2G16800) in trembling aspen (Populus tremuloides) vol.28, pp.1, 2018, https://doi.org/10.1007/s10646-018-2003-8