Advertisement

Environmental Science and Pollution Research

, Volume 21, Issue 3, pp 1723–1737 | Cite as

Epigenetic control of heavy metal stress response in mycorrhizal versus non-mycorrhizal poplar plants

  • Angela Cicatelli
  • Valeria Todeschini
  • Guido Lingua
  • Stefania Biondi
  • Patrizia Torrigiani
  • Stefano Castiglione
Research Article

Abstract

It was previously shown that arbuscular mycorrhizal fungi (AMF) exert a significant improvement of growth in a tolerant white poplar (Populus alba L.) clone (AL35) grown on Cu- and Zn-polluted soil via foliar alterations in the levels of defence/stress-related transcripts and molecules. However, nothing is known about the epigenetic changes which occur during tolerance acquisition in response to heavy metals (HMs) in the same mycorrhizal vs. non-mycorrhizal poplar plants. In order to analyse the epigenome in leaves of AL35 plants inoculated or not with AMF and grown in a greenhouse on multimetal polluted or unpolluted soil, the Methylation Sensitive Amplification Polymorphism (MSAP) approach was adopted to detect cytosine DNA methylation. Modest changes in cytosine methylation patterns were detected at first sampling (4 months from planting), whereas extensive alterations (hypomethylation) occurred at second sampling (after 6 months) in mycorrhizal plants grown in the presence of HMs. The sequencing of MSAP fragments led to the identification of genes belonging to several Gene Ontology categories. Seven MSAP fragments, selected on the basis of DNA methylation status in treated vs control AL35 leaves at the end of the experiment, were analysed for their transcript levels by means of qRT-PCR. Gene expression varied in treated samples relative to controls in response to HMs and/or AMF inoculation; in particular, transcripts of genes involved in RNA processing, cell wall and amino acid metabolism were upregulated in the presence of AMF with or without HMs.

Keywords

Arbuscular mycorrhizal fungi DNA methylation Epigenome Heavy metals MSAP technique Poplar 

Notes

Acknowledgments

This research was supported by funds from the Italian Ministry for Education, University and Scientific Research (PRIN 2003077418) and from the Italian Ministry of Environment, Land and Sea Protection (‘Research and development in biotechnology applied to the protection of the environment’ in collaboration with The People’s Republic of China) to S.C., and it is also part of the doctorate carried out by A.C. at the Federico II University of Naples (IT).

Supplementary material

11356_2013_2072_MOESM1_ESM.docx (12 kb)
ESM 1 (DOCX 12 kb).

References

  1. Aina R, Sgorbati S, Santagostino A, Labra M, Ghiani A, Citterio S (2004) Specific hypomethylation of DNA is induced by heavy metals in white clover and industrial hemp. Physiol Plant 121:472–480CrossRefGoogle Scholar
  2. Anand SS (2005) Protective effect of vitamin B6 in chromium-induced oxidative stress in liver. J Appl Toxicol 25:440–443CrossRefGoogle Scholar
  3. Arsova B, Hoja U, Wimmelbacher M, Greiner E, Uestuen S, Melzer M, Petersen K, Lein W, Boernke F (2010) Plastidial thioredoxin z interacts with two fructokinase-like proteins in a thiol-dependent manner: evidence for an essential role in chloroplast development in Arabidopsis and Nicotiana benthamiana. Plant Cell 22:1498–1515CrossRefGoogle Scholar
  4. Baldantoni D, Bellino A, Cicatelli A, Castiglione S (2011) Artificial mycorrhization does not influence the effects of iron availability on Fe, Zn, Cu, Pb and Cd accumulation in leaves of a heavy metal tolerant white poplar clone. Plant Biosystems 145:236–240CrossRefGoogle Scholar
  5. Berta G, Sgorbati S, Soler V, Fusconi A, Trotta A, Citterio A, Bottone MG, Sparvoli E, Scannerini S (1990) Variations in chromatin structure in host nuclei of a vesicular Arbuscular Mycorrhiza. New Phytol 114:199–205CrossRefGoogle Scholar
  6. Boyko A, Kovalchuk I (2008) Epigenetic control of plant stress response. Environ Mol Mutagen 49:61–72CrossRefGoogle Scholar
  7. Boyko A, Kovalchuk I (2011a) Genetic and epigenetic effects of plant–pathogen interactions: an evolutionary perspective. Mol Plant 4:1014–1023CrossRefGoogle Scholar
  8. Boyko A, Kovalchuk I (2011b) Genome instability and epigenetic modification—heritable responses to environmental stress? Curr Opin Plant Biol 14:260–266CrossRefGoogle Scholar
  9. Braunschweig M, Jagannathan V, Gutzwiller A, Bee G (2012) Investigations on transgenerational epigenetic response down the male line in F2 pigs. PloS one 7:e30583CrossRefGoogle Scholar
  10. Cao D, Gao X, Liu J, Wang X, Geng S, Yang C, Liu B, Shi D (2012) Root-specific DNA methylation in Chloris virgata, a natural alkaline-resistant halophyte, in response to salt and alkaline stresses. Plant Mol Biol Rep 30:1102–1109CrossRefGoogle Scholar
  11. Castiglione S, Todeschini V, Franchin C et al (2009) Clonal differences in survival capacity, copper and zinc accumulation, and correlation with leaf polyamine levels in poplar: a large-scale field trial on heavily polluted soil. Environ Pollut 157:2108–2117CrossRefGoogle Scholar
  12. Chetyrkin SV, Mathis ME, Ham AJ, Hachey DL, Hudson BG, Voziyan PA (2008) Propagation of protein glycation damage involves modification of tryptophan residues via reactive oxygen species: inhibition by pyridoxamine. Free Rad Biol Med 44:1276–1285CrossRefGoogle Scholar
  13. Chinnusamy V, Zhu JK (2009) Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol 12:133–139CrossRefGoogle Scholar
  14. Choi CS, Sano H (2007) Abiotic-stress induces demethylation and transcriptional activation of a gene encoding a glycerophosphodiesterase-like protein in tobacco plants. Mol Genetics Genomics 277:589–600CrossRefGoogle Scholar
  15. Christophersen H.M., Smith F.A. & Smith S.E. (2012) Unraveling the influence of Arbuscular Mycorrhizal colonization on arsenic olerance in medicago: Glomus mosseae is more effective than G. intraradices, associated with lower expression of root epidermal Pi transporter genes. Frontiers in physiology 3, 91Google Scholar
  16. Cicatelli A, Lingua G, Todeschini V, Biondi S, Torrigiani P, Castiglione S (2010) Arbuscular mycorrhizal fungi restore normal growth in a white poplar clone grown on heavy metal-contaminated soil, and this is associated with upregulation of foliar metallothionein and polyamine biosynthetic gene expression. Ann Bot 106:791–802CrossRefGoogle Scholar
  17. Cicatelli A, Lingua G, Todeschini V, Biondi S, Torrigiani P, Castiglione S (2012) Arbuscular mycorrhizal fungi modulate the leaf transcriptome of a Populus alba L. clone grown on a zinc and copper-contaminated soil. Environ Exp Bot 75:25–35CrossRefGoogle Scholar
  18. Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212:475–486CrossRefGoogle Scholar
  19. Da K, Nowak J, Flinn B (2012) Potato cytosine methylation and gene expression changes induced by a beneficial bacterial endophyte, Burkholderia phytofirmans strain PsJN. Plant Physiol Biochem 50:24–34CrossRefGoogle Scholar
  20. Damari-Weissler H, Kandel-Kfir M, Gidoni D, Mett A, Belausov E, Granot D (2006) Evidence for intracellular spatial separation of hexokinases and fructokinases in tomato plants. Planta 224:1495–1502CrossRefGoogle Scholar
  21. Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833CrossRefGoogle Scholar
  22. Demeulemeester MAC, Van Stallen N, De Proft MP (1999) Degree of DNA methylation in chicory (Cichorium intybus L.): influence of plant age and vernalization. Plant Sci 142:101–108CrossRefGoogle Scholar
  23. Dixon RA (2001) Natural products and plant disease resistance. Nature 411:843–847CrossRefGoogle Scholar
  24. Dowen RH, Pelizzola M, Schmitz RJ, Lister R, Dowen JM, Nery JR, Dixon JE, Ecker JR (2012) Widespread dynamic DNA methylation in response to biotic stress. Proc Natl Acad Sci U S A 109:E2183–E2191CrossRefGoogle Scholar
  25. Gao L, Geng Y, Li B, Chen J, Yang J (2010) Genome-wide DNA methylation alterations of Alternanthera philoxeroides in natural and manipulated habitats: implications for epigenetic regulation of rapid responses to environmental fluctuation and phenotypic variation. Plant Cell Environ 33:1820–1827CrossRefGoogle Scholar
  26. German MA, Asher I, Petreikov M, Dai N, Schaffer AA, Granot D (2004) Cloning, expression and characterization of LeFRK3, the fourth tomato (Lycopersicon esculentum Mill.) gene encoding fructokinase. Plant Sci 166:285–291CrossRefGoogle Scholar
  27. Giachetti G, Sebastiani L (2006) Metal accumulation in poplar plant grown with industrial wastes. Chemosphere 64:446–454CrossRefGoogle Scholar
  28. Grafi G, Zemach A, Pitto L (2007) Methyl-CpG-binding domain (MBD) proteins in plants. Biochimica et Biophysica Acta-Gene Structure and Expression 1769:287–294CrossRefGoogle Scholar
  29. Greco M, Chiappetta A, Bruno L, Bitonti MB (2012) In Posidonia oceanica cadmium induces changes in DNA methylation and chromatin patterning. J Exp Bot 63:695–709CrossRefGoogle Scholar
  30. Henderson IR, Jacobsen SE (2007) Epigenetic inheritance in plants. Nature 447:418–424CrossRefGoogle Scholar
  31. Hildebrandt U, Regvar M, Bothe H (2007) Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry 68:139–146CrossRefGoogle Scholar
  32. Huang S, Zeng H, Zhang J, Wei S, Huang L (2011) Interconversions of different forms of vitamin B-6 in tobacco plants. Phytochemistry 72:2124–2129CrossRefGoogle Scholar
  33. Ishitani R, Yokoyama S, Nureki O (2008) Structure, dynamics, and function of RNA modification enzymes. Curr Opin Struct Biol 18:330–339CrossRefGoogle Scholar
  34. Jaccard P (1908) Nouvelles recherches sur la distribution florale. Bulletin des Société Vaudoise des Sciences Naturelles 44:223–270Google Scholar
  35. Kabouw P, van Dam NM, van der Putten WH, Biere A (2012) How genetic modification of roots affects rhizosphere processes and plant performance. J Exp Bot 63:3475–3483CrossRefGoogle Scholar
  36. Karan R, DeLeon T, Biradar H, Subudhi PK (2012) Salt stress induced variation in DNA methylation pattern and its influence on gene expression in contrasting rice genotypes. PloS one 7:e40203CrossRefGoogle Scholar
  37. Kohler A, Rinaldi C, Duplessis S, Baucher M, Geelen D, Duchaussoy F, Meyers BC, Boerjan W, Martin F (2008) Genome-wide identification of NBS resistance genes in Populus trichocarpa. Plant Mol Biol 66:619–636CrossRefGoogle Scholar
  38. Kumar M, Bijo A, Baghel RS, Reddy C, Jha B (2012) Selenium and spermine alleviate cadmium induced toxicity in the red seaweed Gracilaria dura by regulating antioxidants and DNA methylation. Plant Physiol Biochem 51:129–138CrossRefGoogle Scholar
  39. Labra M, Ghiani A, Citterio S, Sgorbati S, Sala F, Vannini C, Ruffini-Castiglione M, Bracale M (2002) Analysis of cytosine methylation pattern in response to water deficit in pea root tips. Plant Biol 4:694–699CrossRefGoogle Scholar
  40. Labra M, Grassi F, Imazio S, Di Fabio T, Citterio S, Sgorbati S, Agradi E (2004) Genetic and DNA-methylation changes induced by potassium dichromate in Brassica napus L. Chemosphere 54:1049–1058CrossRefGoogle Scholar
  41. Lewis MW, Leslie ME, Liljegren SJ (2006) Plant separation: 50 ways to leave your mother. Curr Opin Plant Biol 9:59–65CrossRefGoogle Scholar
  42. Lingua G, Trotta A, Prigione V, Ugoccioni R, Berta G (2005) Nucleus size in the host cells of an Arbuscular Mycorrhizal system: a mathematical approach to estimate the role of ploidy and chromatin condensation. Caryologia 58:112–121CrossRefGoogle Scholar
  43. Lingua G, Bona E, Todeschini V, Cattaneo C, Marsano F, Berta G, Cavaletto M (2012) Effects of heavy metals and Arbuscular Mycorrhiza on the leaf proteome of a selected poplar clone: a time course analysis. PloS one 7:e38662CrossRefGoogle Scholar
  44. Lingua G, Franchin C, Todeschini V, Castiglione S, Biondi S, Burlando B, Parravicini V, Torrigiani P, Berta G (2008) Arbuscular mycorrhizal fungi differentially affect the response to high zinc concentrations of two registered poplar clones. Environ Pollut 153:137–147CrossRefGoogle Scholar
  45. Lira-Medeiros CF, Parisod C, Fernandes RA, Mata CS, Cardoso MA, Gomes Ferreira PC (2010) Epigenetic variation in mangrove plants occurring in contrasting natural environment. Plos One 5Google Scholar
  46. Liu J, Maldonado-Mendoza I, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ (2007) Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J 50:529–544CrossRefGoogle Scholar
  47. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(−Delta Delta C) method. Methods 25:402–408CrossRefGoogle Scholar
  48. Lu YL, Rong TZ, Cao MJ (2008) Analysis of DNA methylation in different maize tissues. J Genetics Genomics 35:41–48CrossRefGoogle Scholar
  49. Maksymiec W (2007) Signaling responses in plants to heavy metal stress. Acta Physiologiae Plantarum 29:177–187CrossRefGoogle Scholar
  50. Marmiroli M, Visioli G, Maestri E, Marmiroli N (2011a) Correlating SNP genotype with the phenotypic response to exposure to cadmium in Populus spp. Environ Sci Technol 45:4497–4505CrossRefGoogle Scholar
  51. Marmiroli M, Pietrini F, Maestri E, Zacchini M, Marmiroli N, Massacci A (2011b) Growth, physiological and molecular traits in Salicaceae trees investigated for phytoremediation of heavy metals and organics. Tree Physiol 31:1319–1334CrossRefGoogle Scholar
  52. Misteli T (2011) The inner life of the genome. Sci Am 502:66–73CrossRefGoogle Scholar
  53. Mittenhuber G (2001) Phylogenetic analyses and comparative genomics of vitamin B-6 (pyridoxine) and pyridoxal phosphate biosynthesis pathways. J Mol Microbiol Biotechnol 3:1–20Google Scholar
  54. Mrnka L, Kuchar M, Cieslarova Z, Matejka P, Szakova J, Tlustos P, Vosatka M (2012) Effects of endo- and ectomycorrhizal fungi on physiological parameters and heavy metals accumulation of two species from the family Salicaceae. Water Air Soil Pollut 223:399–410CrossRefGoogle Scholar
  55. Nakamura T, Yagi Y, Kobayashi K (2012) Mechanistic insight into pentatricopeptide repeat proteins as sequence-specific RNA-binding proteins for organellar RNAs in plants. Plant Cell Physiol 53:1171–1179CrossRefGoogle Scholar
  56. Ouziad F, Hildebrandt U, Schmelzer E, Bothe H (2005) Differential gene expressions in arbuscular mycorrhizal-colonized tomato grown under heavy metal stress. J Plant Physiol 162:634–649CrossRefGoogle Scholar
  57. Pallara G, Giovannelli A, Traversi ML, Camussi A, Racchi ML (2012) Effect of water deficit on expression of stress-related genes in the cambial region of two contrasting poplar clones. J Plant Growth Reg 31:102–112CrossRefGoogle Scholar
  58. Peng H, Zhang J (2009) Plant genomic DNA methylation in response to stresses: potential applications and challenges in plant breeding. Proc Natl Acad Sci U S A 19:1037–1045Google Scholar
  59. Peretto R, Bettini V, Favaron F, Alghisi P, Bonfante P (1995) Polygalacturonase activity and location in Arbuscular Mycorrhizal roots of Allium porrum L. Mycorrhiza 5:157–163CrossRefGoogle Scholar
  60. Pilon-Smits E (2005) Phytoremediation. Annu Rev Plant Physiol Plant Mol Biol 56:15–39CrossRefGoogle Scholar
  61. Qi D, DeYoung BJ, Innes RW (2012) Structure-function analysis of the coiled-coil and leucine-rich repeat domains of the RPS5 disease resistance protein. Plant Physiol 158:1819–1832CrossRefGoogle Scholar
  62. Rajkumar M, Sandhya S, Prasad MNV, Freitas H (2012) Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol adv 30:1562–1574CrossRefGoogle Scholar
  63. Romera IG, Garrido JMG, Ocampo JA (1991) Pectolytic enzymes in the Vesicular-Arbuscular Mycorrhizal fungus Glomus mosseae. Fems Microbiol Lett 78:343–346CrossRefGoogle Scholar
  64. Sang Y, Locy RD, Goertzen LR, Rashotte AM, Si Y, Kang K, Singh NK (2011) Expression, in vivo localization and phylogenetic analysis of a pyridoxine 5′-phosphate oxidase in Arabidopsis thaliana. Plant Physiol Biochem 49:88–95CrossRefGoogle Scholar
  65. Schaff JE, Nielsen DM, Smith CP, Scholl EH, Bird DM (2007) Comprehensive transcriptome profiling in tomato reveals a role for glycosyltransferase in Mi-mediated nematode resistance. Plant Physiol 144:1079–1092CrossRefGoogle Scholar
  66. Schüßler A. & Walker C. (2012) The Glomeromycota: a species list with new families and genera. The Royal Botanic Garden Edinburgh, The Royal Botanic Garden Kew, Botanische Staatssammlung Munich, Oregon State University, Edinburgh, UK; London, UK; Munich, D; Corvallis, Oregon-US.Google Scholar
  67. Song Y, Ji D, Li S, Wang P, Li Q, Xiang F (2012) The dynamic changes of DNA methylation and histone modifications of salt responsive transcription factor genes in soybean. PloS one 7:e41274CrossRefGoogle Scholar
  68. Steward N, Kusano T, Sano H (2000) Expression of ZmMET1, a gene encoding a DNA methyltransferase from maize, is associated not only with DNA replication in actively proliferating cells, but also with altered DNA methylation status in cold-stressed quiescent cells. Nucleic Acids Res 28:3250–3259CrossRefGoogle Scholar
  69. Todeschini V, Franchin C, Castiglione S, Burlando B, Biondi S, Torrigiani P, Berta G, Lingua G (2007) Responses to copper of two registered poplar clones inoculated or not with arbuscular mycorrhizal fungi. Caryologia 60:146–155CrossRefGoogle Scholar
  70. Torki M, Mandaron P, Mache R, Falconet D (2000) Characterization of a ubiquitous expressed gene family encoding polygalacturonase in Arabidopsis thaliana. Gene 242:427–436CrossRefGoogle Scholar
  71. Tsuge H, Kuroda Y, Iwamoto A, Ohashi K (1982) Partial purification and property of pyridoxine (pyridoxamine)-5′-phosphate oxidase isozymes from wheat seedlings. Arch biochem biophys 217:479–484CrossRefGoogle Scholar
  72. Vaillant I, Schubert I, Tourmente S, Mathieu O (2006) MOM1 mediates DNA-methylation-independent silencing of repetitive sequences in Arabidopsis. Embo Reports 7:1273–1278CrossRefGoogle Scholar
  73. Vogt T, Jones P (2000) Glycosyltransferases in plant natural product synthesis: characterization of a supergene family. Trends Plant Sci 5:380–386CrossRefGoogle Scholar
  74. Wang WS, Pan YJ, Zhao XQ, Dwivedi D, Zhu LH, Ali J, Fu BY, Li ZK (2011) Drought-induced site-specific DNA methylation and its association with drought tolerance in rice (Oryza sativa L.). J Exp Bot 62:1951–1960CrossRefGoogle Scholar
  75. Yuan H, Liu D (2012) Functional disruption of the pentatricopeptide protein SLG1 affects mitochondrial RNA editing, plant development, and responses to abiotic stresses in Arabidopsis. Plant J 70:432–444CrossRefGoogle Scholar
  76. Zhang X, Yazaki J, Sundaresan A et al (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126:1189–1201CrossRefGoogle Scholar
  77. Zhao GS, Winkler ME (1995) Kinetic limitation and cellular amount of pyridoxine (pyridoxamine) 5′-phosphate oxidase of Escherichia coli K-12. J Bacteriol 177:883–891Google Scholar
  78. Zheng H, Zhang Q, Li H, Lin S, An X, Zhang Z (2011) Over-expression of the triploid white poplar PtDrl01 gene in tobacco enhances resistance to tobacco mosaic virus. Plant Biol 13:145–153CrossRefGoogle Scholar
  79. Zsigmond L, Szepesi A, Tari I, Rigo G, Kiraly A, Szabados L (2012) Overexpression of the mitochondrial PPR40 gene improves salt tolerance in Arabidopsis. Plant Sci 182:87–93CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Angela Cicatelli
    • 1
  • Valeria Todeschini
    • 2
  • Guido Lingua
    • 2
  • Stefania Biondi
    • 3
  • Patrizia Torrigiani
    • 4
  • Stefano Castiglione
    • 1
  1. 1.Dipartimento di Chimica e BiologiaUniversità di SalernoFiscianoItaly
  2. 2.Dipartimento di Scienze e Innovazione TecnologicaUniversità del Piemonte OrientaleAlessandriaItaly
  3. 3.Dipartimento BiGeAUniversità di BolognaBolognaItaly
  4. 4.Dipartimento di Scienze AgrarieUniversità di BolognaBolognaItaly

Personalised recommendations