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Identification of quantitative trait loci affecting ectomycorrhizal symbiosis in an interspecific F1 poplar cross and differential expression of genes in ectomycorrhizas of the two parents: Populus deltoides and Populus trichocarpa

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Abstract

A Populus deltoides × Populus trichocarpa F1 pedigree was analyzed for quantitative trait loci (QTLs) affecting ectomycorrhizal development and for microarray characterization of gene networks involved in this symbiosis. A 300 genotype progeny set was evaluated for its ability to form ectomycorrhiza with the basidiomycete Laccaria bicolor. The percentage of mycorrhizal root tips was determined on the root systems of all 300 progeny and their two parents. QTL analysis identified four significant QTLs, one on the P. deltoides and three on the P. trichocarpa genetic maps. These QTLs were aligned to the P. trichocarpa genome and each contained several megabases and encompass numerous genes. NimbleGen whole-genome microarray, using cDNA from RNA extracts of ectomycorrhizal root tips from the parental genotypes P. trichocarpa and P. deltoides, was used to narrow the candidate gene list. Among the 1,543 differentially expressed genes (p value ≤ 0.05; ≥5.0-fold change in transcript level) having different transcript levels in mycorrhiza of the two parents, 41 transcripts were located in the QTL intervals: 20 in Myc_d1, 14 in Myc_t1, and seven in Myc_t2, while no significant differences among transcripts were found in Myc_t3. Among these 41 transcripts, 25 were overrepresented in P. deltoides relative to P. trichocarpa; 16 were overrepresented in P. trichocarpa. The transcript showing the highest overrepresentation in P. trichocarpa mycorrhiza libraries compared to P. deltoides mycorrhiza codes for an ethylene-sensitive EREBP-4 protein which may repress defense mechanisms in P. trichocarpa while the highest overrepresented transcripts in P. deltoides code for proteins/genes typically associated with pathogen resistance.

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References

  • Barker SJ, Tagu D, Delp G (1998) Regulation of root and fungal morphogenesis in mycorrhizal symbiosis. Plant Physiol 116:1201–1207

    Article  CAS  Google Scholar 

  • Blée E, Schuber F (1992) Occurrence of fatty acid epoxide hydrolases in soybean (Glycine max). Purification and characterization of the soluble form. Biochem J 282:711–714

    Google Scholar 

  • Bradshaw HD, Stettler RF (1993) Molecular genetics of growth and development in Populus. I. Triploidy in hybrid poplars. Theor Appl Genet 86:301–307

    Article  Google Scholar 

  • Cornelius J (1994) Heritabilities and additive genetic coefficient of variation in forest trees. Can J For Res 24:372–379

    Article  Google Scholar 

  • Di Battista C, Selosse MA, Bouchard D, Stenström E, Le Tacon F (1996) Variations in symbiotic efficiency, phenotypic characters and ploidy level among different isolates of the ectomycorrhizal basidiomycete Laccaria bicolor strain S238. Mycol Res 100:1315–1324

    Article  Google Scholar 

  • Duponnois R, Garbaye J (1991) Mycorrhization helper bacteria associated with Douglas fir-Laccaria laccata symbiosis: effects in aseptic and glasshouse conditions. Ann Sci For 48:239–251

    Article  Google Scholar 

  • Eulgem T, Rushton PJ, Schmelzer E, Hahlbrock K, Somssich IE (1999) Early nuclear events in plant defense signaling: rapid gene activation by WRKY transcription factors. EMBO J 18:4689–4699

    Article  PubMed  CAS  Google Scholar 

  • Faivre-Rampant P, Bastien C, Augustin S, Breton V, Delplanque A, Mourier MC, Kertadikara A, Laurans F, Lefèvre F, Lesage MC, Menard M, Pinon J, Saintagne C, Valadon A, Villar M, Prat D (1999) Locating genomic regions involved in pest resistance in poplars. Proceedings of the International Poplar Symposium II, IUFRO, Orléans, France pp31

  • Felten J, Legué V, Ditengou FA (2010) Lateral root stimulation in the early interaction between Arabidopsis thaliana and the ectomycorrhizal fungus Laccaria bicolor. Plant Signal Behav 5:1–4

    Article  Google Scholar 

  • Frey-Klett P, Pierrat JC, Garbaye J (1997) Location and survival of mycorrhiza helper Pseudomonas fluorescens during establishment of ectomycorrhizal symbiosis between Laccaria bicolor and Douglas-fir. Appl Environ Microbiol 63:139–144

    PubMed  CAS  Google Scholar 

  • Gay G, Normand L, Marmeisse R, Sotta B, Debaud JC (1994) Auxin overproducer mutants of Hebeloma cylindrosporum Romagnesi have increased mycorrhizal activity. New Phytol 128:645–657

    Article  CAS  Google Scholar 

  • Gomi K, Yamamato H, Akimitsu K (2003) Epoxide hydrolase: a mRNA induced by the fungal pathogen Alternaria alternata on rough lemon (Citrus jambhiri Lush). Plant Mol Biol 53:189–199

    Article  PubMed  CAS  Google Scholar 

  • Grattapaglia D, Sederoff R (1994) Genetic linkage maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudo-testcross mapping strategy and RAPD markers. Genetics 137:1121–1137

    PubMed  CAS  Google Scholar 

  • Hamberg M, Fahlstadius P (1992) On the specificity of a fatty acid epoxygenase in broad bean (Vicia faba L.). Plant Physiol 99:987–995

    Google Scholar 

  • Hao D, Ohme-Takagi M, Sarai A (1998) Unique mode of GCC box recognition by the DNA-binding domain of ethylene-responsive element-binding factor (ERF Domain) in plants. J Biol Chem 273:26857–26861

    Article  PubMed  CAS  Google Scholar 

  • Hirota A, Kato T, Fukaki H, Aida M, Tasaka M (2002) The auxin-regulated AP2/EREBP gene PUCHI is required for morphogenesis in the early lateral root primordium of Arabidopsis. Plant Cell 19:2156–2168

    Article  Google Scholar 

  • Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP (2003) Speed, exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249–264

    Article  PubMed  Google Scholar 

  • Jorge V, Dowkiw A, Faivre-Rampant P, Bastien C (2005) Genetic architecture of qualitative and quantitative Melampsora larici-populina leaf rust resistance in hybrid poplar: genetic mapping and QTL detection. New Phytol 167:113–127

    Article  PubMed  CAS  Google Scholar 

  • Karabaghli-Degron C, Sotta B, Bonnet M, Gay G, Le Tacon F (1998) The auxin transport inhibitor 2, 3, 5-triiodobenzoic acid (TIBA) inhibits the stimulation of in vitro lateral root formation and the colonization of the tap-root cortex of Norway spruce (Picea abies) seedlings by the ectomycorrhizal fungus Laccaria bicolor. New Phytol 140(4):723–733

    Article  CAS  Google Scholar 

  • Kariola T, Brader G, Li J, Palva ET (2005) Chlorophyllase 1 a damage control enzyme affects the balance between defensepathways in plants. Plant Cell 17:282–294

    Google Scholar 

  • Kato T, Yamaguchi Y, Uehara T, Yokoyama T, Namai T, Yamanaka S (1983) Defense mechanism of the rice plant against rice blast disease. Naturwissenschaften 70:200–201

    Google Scholar 

  • Kato T, Yamaguchi Y, Abe N, Uehara T, Namai T, Kodama M, Shiobara Y (1985) Structure and synthesis of unsaturated trihydroxy C18 fatty acids in rice plants suffering from rice blast disease. Tetrahedron Lett 26:2357–2360

    Google Scholar 

  • Kiyosue T, Beetham JK, Pinot F, Hammock BD, Yamaguchi-Shinozaki K, Shinozaki K (1994) Characterization of an Arabidopsis cDNA for a soluble epoxide hydrolase gene that is inducible by auxin and water stress. Plant J 6:259–269

    Article  PubMed  CAS  Google Scholar 

  • Lander ES, Botstein D (1989) Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–199

    PubMed  CAS  Google Scholar 

  • Lefèvre F, Mc G-M, Faivre-Rampant P, Villar M (1998) A single gene cluster controls incompatibility and partial resistance to various Melampsora larici-populina races in hybrid poplars. Phytopathology 88:156–163

    Article  PubMed  Google Scholar 

  • Leubner-Metzger G, Petruzzelli L, Waldvogel R, Vögeli-Lange R, Meins F (1998) Ethylene-responsive element binding protein (EREBP) expression and the transcriptional regulation of class I-1, 3-glucanase during tobacco seed germination. Plant Mol Biol 38:785–795

    Article  PubMed  CAS  Google Scholar 

  • Li J, Brader G, Palva ET (2004) The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 2004(16):319–331

    Article  Google Scholar 

  • Li J, Bradera G, Tapio Palva E (2008) Kunitz trypsin inhibitor: an antagonist of cell death triggered by phytopathogens and fumonisin B1 in Arabidopsis. Mol Plant 1:482–495

    Article  PubMed  CAS  Google Scholar 

  • Martin F, Nehls U (2009) Harnessing ectomycorrhizal genomics for ecological insights. Cur Opin Plant Biol 12:508–515

    Article  CAS  Google Scholar 

  • Martin F, Duplessis S, Ditengou F, Lagrange H, Voiblet C, Lapeyrie F (2003) Developmental cross talking in the ectomycorrhizal symbiosis: signals and communication genes. New Phytol 151:145–154

    Article  Google Scholar 

  • Martin F, Kohler A, Duplessis S (2007) Living in harmony in the wood underground: ectomycorrhizal genomics. Cur Opin Plant Biol 10:204–210

    Article  CAS  Google Scholar 

  • Martin F, Aerts A, Ahrén D, Brun A, Duchaussoy F, Gibon J, Kohler A, Lindquist E, Pereda V, Salamov A, Shapiro HJ, Wuyts J, Blaudez D, Buée M, Brokstein P, Canbäck B, Cohen D, Courty PE, Coutinho PM, Danchin EGJ, Delaruelle C, Detter JC, Deveau A, DiFazio S, Duplessis S, Fraissinet-Tachet L, Lucic E, Frey-Klett P, Fourrey C, Feussner I, Gay G, Grimwood J, Hoegger PJ, Jain P, Kilaru S, Labbé J, Lin YC, Legué V, Le Tacon F, Marmeisse R, Melayah D, Montanini B, Muratet M, Nehls U, Niculita-Hirzel H, Oudot-Le Secq MP, Peter M, Quesneville H, Rajashekar B, Reich M, Rouhier N, Schmutz J, Yin T, Chalot M, Henrissat B, Kües U, Lucas S, Van de Peer Y, Podila G, Polle A, Pukkila PJ, Richardson PM, Rouzé P, Sanders IR, Stajich JE, Tunlid A, Tuskan G, Grigoriev IV (2008) Symbiosis insights from the genome of the mycorrhizal basidiomycete Laccaria bicolor. Nature 452:88–92

    Article  PubMed  CAS  Google Scholar 

  • Masui H, Kondo T, Kojima M (1989) An antifungal compound 9,12,13-trihydroxy-(E)-10- octadecenoic acid from Colocasia antiquorum inoculated with Ceratocystis fimbriata. Phytochemistry 28:2613–2615

    Google Scholar 

  • Nehls U, Mikolajewski S, Magel E, Hampp R (2001) Carbohydrate metabolism in ectomycorrhizas: gene expression, monosaccharide transport and metabolic control. New Phytol 150:533–541

    Article  CAS  Google Scholar 

  • Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7:173–182

    Article  PubMed  CAS  Google Scholar 

  • Ohme-Takagi M, Shinshi H (2000) Three ethylene-responsive transcription factors in tobacco with distinct transactivation functions. Plant J 22:29–38

    Article  PubMed  Google Scholar 

  • Ohta H, Shida K, Peng LY, Furusawa I, Shishiyama J, Aibara S, Morita Y (1990) The occurrence of lipid hydroperoxide-decomposing activities in rice and the relationship of such activities to the formation of antifungal substances. Plant CellPhysiol 31(8):1117–1122

    Google Scholar 

  • Ohta M, Ohme-Takagi M, Shinshi H (2000) Three ethylene-responsive transcriptional factors in tobacco with distinct transactivation functions. Plant Cell 12:393–404

    Google Scholar 

  • Pachlewski R, Pchlevska J (1974) Studies on symbiotic properties of mycorrhizal fungi of pine (Pinus sylvestris L.) with the aid of the method of mycorrhizal synthesis in pure cultures on agar. PhD Thesis. Forest Institute, Warsaw

    Google Scholar 

  • Peter M, Courty PE, Kohler A, Delaruelle C, Martin D, Tagu D, Frey-Klett P, Duplessis S, Chalot M, Podila G, Martin F (2003) Analysis of expressed sequence tags from the ectomycorrhizal basidiomycete Laccaria bicolor and Pisolithus microcarpus. New Phytol 159:117–129

    Article  CAS  Google Scholar 

  • Peterson L, Bonfante P (1994) Comparative structure of vesicular-arbuscularmycorrhizas and ectomycorrhizas. In: Robson AD, Abbort LK, Malajczuk N (eds) Management of mycorrhizas in agriculture, horticulture and forestery. Kluwer, Dordrecht, pp 79–88

    Google Scholar 

  • Pinot F, Grant DF, Beetham JK, Parker AG, Borhan B, Landt S, Jones AD, Hammock BD (1995) Molecular and biochemical evidence for the involvement of the Asp333-His523 pair in catalytic mechanism of soluble epoxide hydrolase. J Biol Chem 270: 7968–7974

    Google Scholar 

  • Rosado SCS, Kropp BR, Piché Y (1994) Genetics of ectomycorrhizal symbiosis. I. Host plant variability and heritability of ectomycorrhizal root traits. New Phytol 126:105–110

    Article  Google Scholar 

  • Rupp LA, Mudge W (1985) Ethephon and auxin induce mycorrhiza-like changes in the morphology of root organ cultures of mugo pine. Physiol Plant 64:316–322

    Article  CAS  Google Scholar 

  • Rupp LA, DeVries HE, Mudge KW (1989) Effect of aminocyclopropane carboxylic acid and aminoethoxyvinylglycine on ethylene production by ectomycorrhizal fungi. Can J Bot 67:483–485

    Article  CAS  Google Scholar 

  • Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234

    Article  PubMed  CAS  Google Scholar 

  • Slankis V (1950) Effect of α-naphthalene-acetic acid on dichotomous branching of isolated roots of Pinus sylvestris. Physiol Plant 3:40–44

    Article  Google Scholar 

  • Smith SE, Reads DJ (eds) (1997) Mycorrhizal symbiosis. Academic, San Diego

    Google Scholar 

  • Solano R, Ecker JR (1998) Ethylene gas: perception, signaling and response. Cur Opin Plant Biol 1:393–398

    Article  CAS  Google Scholar 

  • Splivallo R, Fischer U, Gobel C, Feussner I, Karlovsky P (2009) Truffles regulate plant root morphogenesis via the production of auxin and ethylene. Plant Physiol 150:218–229

    Article  Google Scholar 

  • Tagu D, Faivre-Rampant P, Lapeyrie Frey-klett P, Vion P, Villar M (2001) Variation in the ability to form ectomycorrhizas in the F1 progeny of an interspecific poplar (Populus spp.) cross. Mycorrhiza 10:237–240

    Article  CAS  Google Scholar 

  • Tagu D, Palin B, Balestrini R, Gelhaye E, Lapeyrie F, Jacquot JP, Sautière PE, Bonfante P, Martin F (2003) Characterization of a symbiosis- and auxin-regulated glutathione-S-transferase from Eucalyptus globulus roots. Plant Physiol Biochem 41:611–618

    Article  CAS  Google Scholar 

  • Tagu D, Bastien C, Faivre-Rampant P, Garbaye J, Vion P, Villar M, Martin F (2005) Genetic analysis of phenotypic variation for ectomycorrhiza formation an interspecific F1 poplar full-sib family. Mycorrhiza 15:87–91

    Article  PubMed  CAS  Google Scholar 

  • Tuskan GA, Gunter LE, Yang ZMK, Yin TM, Sewell MM, DiFazio SP (2004) Characterization of microsatellites revealed by genomic sequencing of Populus trichocarpa. Can J For Res 34:85–93

    Article  CAS  Google Scholar 

  • Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao BD, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Déjardin A, dePamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjärvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leplé JC, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouzé P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai CJ, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, Van de Peer Y, Rokhsar D (2006) The genome of black cottonwood, Populus trichocarpa. Science 313:1596–1604

    Article  PubMed  CAS  Google Scholar 

  • Van der Schoot J, Pospiskova M, Vosman B, Smulders MJM (2000) Development and characterization of microsatellite markers in black poplar (Populus nigra L.). Theor Appl Genet 101:317–322

    Article  Google Scholar 

  • Villar M, Lefèvre F, Bradshaw HD, Teissier du Cros E (1996) Molecular genetics of rust resistance in poplars (Melampsora larici-populina Kleb/Populus sp.) by bulked segregant analysis in a 2 × 2 factorial mating design. Genetics 143:531–536

    PubMed  CAS  Google Scholar 

  • Yin TM, DiFazio SP, Gunter LE, Jawdy SS, Tuskan GA (2004) Mapping the rust resistant loci MXC3 and MER in Populus trichocarpa and assessing the intermarker linkage disequilibrium in the MXC3 region. New Phytol 164:95–106

    Article  CAS  Google Scholar 

  • Zou X, Seemann JR, Neuman D, Shen QJ (2004) A WRKY Gene from creosote bush encodes an activator of the abscisic acid signaling pathway. J Biol Chem 279:55770–55779

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This project was supported by grants from the European Commission project ENERGYPOPLAR and EVOLTREE (to FM). JL was supported by a scholarship from the INRA, Region Lorraine, the ORNL, and the U.S. Department of Energy. Oak Ridge National Laboratory (ORNL) is managed by UT-Battelle, LLC for the US Department of Energy under contract no. DE-AC05-00OR2272. We thank Christine Delaruelle, Béatrice Palin, Judith Richter, Verónica Pereda, Saskia Reinhart, Anne Delaruelle, Simon Duchêne, Aurore Coince, and Jean-Louis Churin for their assistance in the inoculation and in measuring the colonization rates. We also thank Denis Tagu for his help and fruitful discussions.

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Authors and Affiliations

  1. UMR 1136, INRA-Nancy Université, Interactions Arbres/Microorganismes, INRA-Nancy, 54280, Champenoux, France

    Jessy Labbé, Annegret Kohler, Patrice Vion, Benoît Marçais, Francis Martin & François Le Tacon

  2. Unité Amélioration Génétique et Physiologie Forestière, INRA-Orléans, 45166, Olivet Cedex, France

    Véronique Jorge & Catherine Bastien

  3. BioSciences Division, Oak Ridge National Laboratory, P.O. Box 2001, Oak Ridge, TN, 37831-6422, USA

    Jessy Labbé & Gerald A. Tuskan

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  1. Jessy Labbé
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  2. Véronique Jorge
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  8. Francis Martin
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  9. François Le Tacon
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Labbé, J., Jorge, V., Kohler, A. et al. Identification of quantitative trait loci affecting ectomycorrhizal symbiosis in an interspecific F1 poplar cross and differential expression of genes in ectomycorrhizas of the two parents: Populus deltoides and Populus trichocarpa . Tree Genetics & Genomes 7, 617–627 (2011). https://doi.org/10.1007/s11295-010-0361-3

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