Abstract
The ectomycorrhizal basidiomycete Suillus luteus (L.:Fr.), a typical pioneer species which associates with young pine trees colonizing disturbed sites, is a common root symbiont found at heavy metal contaminated sites. Three Cd-sensitive and three Cd-tolerant isolates of S. luteus, isolated respectively from non-polluted and a heavy metal-polluted site in Limburg (Belgium), were used for a transcriptomic analysis. We identified differentially expressed genes by cDNA-AFLP analysis. The possible roles of some of the encoded proteins in heavy metal (Cd) accumulation and tolerance are discussed. Despite the high conservation of coding sequences in S. luteus, a large intraspecific variation in the transcript profiles was observed. This variation was as large in Cd-tolerant as in sensitive isolates and may help this pioneer species to adapt to novel environments.
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References
Adriaensen K, Vrålstad T, Noben JP, Vangronsveld J, Colpaert JV (2005) Copper adapted Suillus luteus, a symbiotic solution for pines colonising Cu mine spoil. Appl Environ Microb 11:7279–7284
Agerer R (2001) Exploration types of ectomycorrhizae—a proposal to classify ectomycorrhizal mycelial systems according to their patterns of differentiation and putative ecological importance. Mycorrhiza 11:107–114
Ahonen-Jonnarth U, Finlay RD (2001) Effects of elevated nickel and cadmium concentrations on growth and nutrient uptake of mycorrhizal and non-mycorrhizal Pinus sylvestris seedlings. Plant Soil 236:129–138
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Angelini R, Tisi A, Rea G, Chen MM, Botta M, Federico R, Cona A (2008) Involvement of polyamine oxidase in wound healing. Plant Physiol 146:162–177
Ashkannejhad S, Horton TR (2006) Ectomycorrhizal ecology under primary succession on coastal sand dunes: interactions involving Pinus contorta, suilloid fungi and deer. New Phytol 169:345–354
Bachem CW, van der Hoeven RS, de Bruijn SM, Vreugdenhil D, Zabeau M et al (1996) Visualization of differential gene expression using a novel method of RNA fingerprinting based on AFLP: analysis of gene expression during potato tuber development. Plant J 9:745–753
Bachem CW, Oomen RJF, Visser RG (1998) Transcript imaging with cDNA-AFLP: a step-by-step protocol. Plant Mol Biol Rep 16:157–173
Bellion M, Courbot M, Jacob C, Blaudez D, Chalot M (2006) Extracellular and cellular mechanisms sustaining metal tolerance in ectomycorrhizal fungi. FEMS Microbiol Lett 254:173–181
Bellion M, Courbot M, Jacob C, Guinet F, Blaudez D, Chalot M (2007) Metal induction of a Paxillus involutus metallothionein and its heterologous expression in Hebeloma cylindrosporum. New Phytol 174:151–158
Blaudez D, Botton B, Chalot M (2000) Cadmium uptake and subcellular compartmentation in the ectomycorrhizal fungus Paxillus involutus. Microbiology 146:1109–1117
Breyne P, Dreesen R, Cannoot B, Rombaut D, Vandepoele K et al (2003) Quantitative cDNA-AFLP analysis for genome-wide expression studies. Mol Genet Genomics 269:173–179
Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719
Colpaert JV, Vanden Koornhuyse P, Adriaensen K, Vangronsveld J (2000) Genetic variation and heavy metal tolerance in the ectomycorrhizal basidiomycete Suillus luteus. New Phytol 147:367–379
Colpaert JV, Muller LAH, Lambaerts M, Adriansen K, Vangronsveld J (2004) Evolutionary adaptation to Zn toxicity in populations of Suilloid fungi. New Phytol 162:549–560
Colpaert JV, Adriaensen K, Muller LAH, Lambaerts M, Faes C, Carleer R, Vangronsveld J (2005) Element profiles and growth in Zn-sensitive and Zn-resistant Suilloid fungi. Mycorrhiza 15:628–634
Courbot M, Diez L, Ruotolo R, Chalot M, Leroy P (2004) Cadmium-responsive thiols in the ectomycorrhizal fungus Paxillus involutus. Appl Environ Microb 70:7413–7417
Craciun AR, Courbot M, Bourgis F, Salis P, Saumitou-Laprade P, Verbruggen N (2006) Comparative cDNA-AFLP analysis of Cd-tolerant and -sensitive genotypes derived from crosses between the Cd hyperaccumulator Arabidopsis halleri and Arabidopsis lyrata ssp petraea. J Exp Bot 57:2967–2983
Ditt RF, Nester RW, Comai L (2001) Plant gene expression response to Agrobacterium tumefaciens. P Natl Acad Sci USA 98:10954–10959
Frost MR, Guggenheim JA (1999) Prevention of depurination during elution facilitates the re-amplification of DNA from differential display gels. Nucleic Acids Res 27:e6
Fusco N, Micheletto L, Dal Corso G, Borgato L, Furini A (2005) Identification of cadmium-regulated genes by cDNA-AFLP in the heavy metal accumulator Brassica juncea L. J Exp Bot 57:3017–3027
Jacob C, Courbot ML, Martin F, Brun A, Chalot M (2004) Transcriptomic responses to cadmium in the ectomycorrhizal fungus Paxillus involutus. FEBS Lett 576:423–427
Kieffer P, Schröder P, Dommes J, Hoffmann L, Renauta J, Hausman J-F (2009) Proteomic and enzymatic response of poplar to cadmium stress. J Proteomics 72:379–396
Kozdroj J, Piotrowska-Seget Z, Krupa P (2007) Mycorrhizal fungi and ectomycorrhiza associated bacteria isolated from an industrial desert soil protect pine seedlings against Cd(II) impact. Ecotoxicology 16:449–456
Krznaric E (2009) Heavy metal tolerant Suillus luteus: new insights into the Cd tolerance mechanism, the protection of the host plant and Zn-Cd interactions. Ph.D. thesis
Krznaric E, Verbruggen N, Vangronsveld J, Colpaert JV (2009) Cd-tolerant Suillus luteus: a fungal insurance for pines exposed to Cd. Environ Pollut 157:1581–1585
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948
Martin F, Aerts A, Ahrén D, Brun A, Danchin EG et al (2008) The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452:88–92
Molesini B, Rotino GL, Spena A, Pandolfini T (2009) Expression profile analysis of early fruit development in iaaM-parthenocarpic tomato plants. BMC Res Notes 2:143
Muller LAH, Lambaerts M, Vangronsveld J, Colpaert JV (2004) AFLP-based assessment of the effects of environmental heavy metal pollution on the genetic structure of pioneer populations of Suillus luteus. New Phytol 164:297–303
Muller LAH, Craciun AR, Ruytinx J, Lambaerts M, Verbruggen N, Vangronsveld J, Colpaert JV (2007a) Gene expression profiling of a Zn-tolerant and a Zn-sensitive Suillus luteus isolate exposed to increased external zinc concentrations. Mycorrhiza 17:571–580
Muller LAH, Vangronsveld J, Colpaert JV (2007b) Genetic structure of Suillus luteus populations in heavy metal polluted and nonpolluted habitats. Mol Ecol 16:4728–4737
Neill S, Desikan R, Hancock J (2002) Hydrogen peroxide signalling. Curr Opin Plant Biol 5:388–395
Oleksiak MF, Churchill GA, Crawford DL (2002) Variation in gene expression within and among natural populations. Nat Genet 32:261–266
Roelofs D, Janssens TKS, Timmermans MJTN, Nota B, Mariën J et al (2009) Adaptive differences in gene expression associated with heavy metal tolerance in the soil arthropod Orchesella cincta. Mol Ecol 18:3227–3239
Rohde A, Ruttink T, Hostyn V, Sterck L, Van Driessche K, Boerjan W (2007) Gene expression during the induction, maintenance, and release of dormancy in apical buds of poplar. J Exp Bot 58:4047–4060
Semane B, Dupae J, Cuypers A, Noben J-P, Tuomainen M et al (2010) Leaf proteome responses of Arabidopsis thaliana exposed to mild cadmium stress. J Plant Physiol 167:247–254
Smeets K, Opdenakker K, Remans T, Van Sanden S, Van Belleghem F et al (2009) Oxidative stress-related responses at the transcriptional and enzymatic levels after exposure to Cd or Cu in a multipollution context. J Plant Physiol 166:1982–1992
Storey JD, Madeoy J, Strout JL, Wurfel M, Ronald J, Akey JM (2007) Gene-expression variation within and among human populations. Am J Hum Genet 80:502–509
Taylor JH, Peterson CA (2005) Ectomycorrhizal impacts on nutrient uptake pathways in woody roots. New Forest 30:203–214
Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:research0034.0031-research0034.0011
Verbruggen N, Hermans C, Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 184:759–776
Vesk PA, Ashford AE, Markovina AL, Allaway WG (2000) Apoplasmic barriers and their significance in the exodermis and sheath of Eucalyptus pilularis-Pisolithus tinctorius ectomycorrhizas. New Phytol 145:333–346
Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252
Zhang J, Hu M, Li JT, Guan JP, Yang B, Shu WS, Liao B (2009) A transcriptional profile of metallophyte Viola baoshanensis involved in general and species-specific cadmium-defense mechanisms. J Plant Physiol 166:862–870
Acknowledgements
This work was supported by a grant from the Fonds National de la Recherche Scientifique (2.4.602.05.F F.R.F.C.), the Fund for Scientific Research–Flanders (FWO-project G.0325.05) and from the Belgian Science Policy Office (BELSPO, project IAPV/33).
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Ruytinx and Craciun contributed equally to this work.
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Ruytinx, J., Craciun, A.R., Verstraelen, K. et al. Transcriptome analysis by cDNA-AFLP of Suillus luteus Cd-tolerant and Cd-sensitive isolates. Mycorrhiza 21, 145–154 (2011). https://doi.org/10.1007/s00572-010-0318-2
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DOI: https://doi.org/10.1007/s00572-010-0318-2