Skip to main content
SpringerLink
Log in

Oak protein profile alterations upon root colonization by an ectomycorrhizal fungus

  • Original Article
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

An increased knowledge on the real impacts of ectomycorrhizal symbiosis in forest species is needed to optimize forest sustainable productivity and thus to improve forest services and their capacity to act as carbon sinks. In this study, we investigated the response of an oak species to ectomycorrhizae formation using a proteomics approach complemented by biochemical analysis of carbohydrate levels. Comparative proteome analysis between mycorrhizal and nonmycorrhizal cork oak plants revealed no differences at the foliar level. However, the protein profile of 34 unique oak proteins was altered in the roots. Consistent with the results of the biochemical analysis, the proteome analysis of the mycorrhizal roots suggests a decreasing utilization of sucrose for the metabolic activity of mycorrhizal roots which is consistent with an increased allocation of carbohydrates from the plant to the fungus in order to sustain the symbiosis. In addition, a promotion of protein unfolding mechanisms, attenuation of defense reactions, increased nutrient mobilization from the plant-fungus interface (N and P), as well as cytoskeleton rearrangements and induction of plant cell wall loosening for fungal root accommodation in colonized roots are also suggested by the results. The suggested improvement in root capacity to take up nutrients accompanied by an increase of root biomass without apparent changes in aboveground biomass strongly re-enforces the potential of mycorrhizal inoculation to improve cork oak forest resistance capacity to cope with coming climate change.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abdallah C, Valot B, Guillier C, Mounier A, Balliau T, Zivy M, van Tuinen D, Renaut J, Wipf D, Dumas-Gaudot E, Recorbet G (2014) The membrane proteome of Medicago truncatula roots displays qualitative and quantitative changes in response to arbuscular mycorrhizal symbiosis. J Proteomics 108:354–368. doi:10.1016/j.jprot.2014.05.028

    Article  CAS  PubMed  Google Scholar 

  • Alvarez M, Huygens D, Díaz LM, Villanueva CA, Heyser W, Boeckx P (2012) The spatial distribution of acid phosphatase activity in ectomycorrhizal tissues depends on soil fertility and morphotype, and relates to host plant phosphorus uptake. Plant Cell Environ 35:126–135. doi:10.1111/j.1365-3040.2011.02422.x

    Article  CAS  PubMed  Google Scholar 

  • Alvarez M, Huygens D, Fernandez C, Gacitua Y, Olivares E, Saavedra I, Alberdi M, Valenzuela E (2009) Effect of ectomycorrhizal colonization and drought on reactive oxygen species metabolism of Nothofagus dombeyi roots. Tree Physiol 29:1047–1057. doi:10.1093/treephys/tpp038

    Article  CAS  PubMed  Google Scholar 

  • Baptista P, Martins A, Pais MS, Tavares RM, Lino-Neto T (2007) Involvement of reactive oxygen species during early stages of ectomycorrhiza establishment between Castanea sativa and Pisolithus tinctorius. Mycorrhiza 17:185–193. doi:10.1007/s00572-006-0091-4

    Article  CAS  PubMed  Google Scholar 

  • Bestel-Corre G, Dumas-Gaudot E, Gianinazzi S (2004) Proteomics as a tool to monitor plant-microbe endosymbioses in the rhizosphere. Mycorrhiza 14:1–10. doi:10.1007/s00572-003-0280-3

    Article  CAS  PubMed  Google Scholar 

  • Boca S, Koestler F, Ksas B, Chevalier A, Leymarie J, Fekete A, Mueller MJ, Havaux M (2014) Arabidopsis lipocalins AtCHL and AtTIL have distinct but overlapping functions essential for lipid protection and seed longevity. Plant Cell Environ 37:368–381. doi:10.1111/pce.12159

    Article  CAS  PubMed  Google Scholar 

  • Book AJ, Gladman NP, Lee S, Scalf M, Smith LM, Vierstra RD (2010) Affinity purification of the Arabidopsis 26 S proteasome reveals a diverse array of plant proteolytic complexes. J Biol Chem 285:25554–25569. doi:10.1074/jbc.M110.136622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burgess T, Dell B (1996) Changes in protein biosynthesis during the differentiation of Pisolithus–Eucaliptus grandis ectomycorrhiza. Can J Bot 74:553–560

    Article  CAS  Google Scholar 

  • Cairney JWG (2011) Ectomycorrhizal fungi: the symbiotic route to the root for phosphorus in forest soils. Plant Soil 344:51–71. doi:10.1007/s11104-011-0731-0

    Article  CAS  Google Scholar 

  • Cairney JWG, Chambers SM (1997) Interactions between Pisolithus tinctorius and its hosts: a review of current knowledge. Mycorrhiza 7:117–131. doi:10.1007/s005720050172

    Article  Google Scholar 

  • Cangahuala-Inocente GC, Da Silva MF, Johnson JM, Manga A, van Tuinen D, Henry C, Lovato PE, Dumas-Gaudot E (2011) Arbuscular mycorrhizal symbiosis elicits proteome responses opposite of P-starvation in SO4 grapevine rootstock upon root colonisation with two Glomus species. Mycorrhiza 21:473–493. doi:10.1007/s00572-010-0352-0

    Article  CAS  PubMed  Google Scholar 

  • Caplan JL, Zhu X, Mamillapalli P, Marathe R, Anandalakshmi R, Dinesh-Kumar SP (2009) Induced ER-chaperones regulate a novel receptor-like kinase to mediate a viral innate immune response. Cell Host Microbe 19:457–469. doi:10.1016/j.chom.2009.10.005

    Article  Google Scholar 

  • Charron JB, Ouellet F, Houde M, Sarhan F (2008) The plant apolipoprotein D ortholog protects Arabidopsis against oxidative stress. BMC Plant Biol 8:86. doi:10.1186/1471-2229-8-86

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen R, Zhao X, Shao Z, Zhu L, He G (2007) Multiple isoforms of UDP-glucose pyrophosphorylase in rice. Physiol Plant 12:725–736. doi:10.1111/j.1399-3054.2007.00865.x

    Article  Google Scholar 

  • Dickie IA, Montgomery RA, Reich PB, Schnitzer SA (2007) Physiological and phenological responses of oak seedlings to oak forest soil in the absence of trees. Tree Physiol 27:133–140. doi:10.1093/treephys/27.1.133

    Article  CAS  PubMed  Google Scholar 

  • Dixon RA, Harrison MJ, Paiva NL (1995) The isoflavonoid phytoalexin pathway: from enzymes to genes to transcription factors. Physiol Plant 93:385–392. doi:10.1111/j.1399-3054.1995.tb02243.x

    Article  CAS  Google Scholar 

  • Duddridge JA (1986) The development and ultrastructure of ectomycorrhizas. III. Compatible and incompatible interactions between Suillus grevillei (Klotzsch) Sing. and 11 species of ectomycorrhizal hosts in vitro in the absence of exogenous carbohydrate. New Phytol 103:457–464

    Article  CAS  Google Scholar 

  • Espinosa F, Garrido I, Ortega A, Casimiro I, Alvarez-Tinaut MC (2014) Redox activities and ROS, NO and phenylpropanoids production by axenically cultured intact olive seedling roots after interaction with a mycorrhizal or a pathogenic fungus. PLoS One 9(6):e100132. doi:10.1371/journal.pone.0100132

    Article  PubMed  PubMed Central  Google Scholar 

  • Felten J, Kohler A, Morin E, Bhalerao RP, Palme K, Martin F, Ditengou FA, Legue V (2009) The ectomycorrhizal fungus Laccaria bicolor stimulates lateral root formation in poplar and Arabidopsis through auxin transport and signalling. Plant Physiol 151:1991–2005. doi:10.1104/pp.109.147231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fini A, Frangi P, Amoroso G, Piatti R, Faoro M, Bellasio C, Ferrini F (2011) Effect of controlled inoculation with specific mycorrhizal fungi from the urban environment on growth and physiology of containerized shade tree species growing under different water regimes. Mycorrhiza 21:703–719. doi:10.1007/s00572-011-0370-6

    Article  PubMed  Google Scholar 

  • Fiorilli V, Catoni M, Miozzi L, Novero M, Accotto GP, Lanfranco L (2009) Global and cell-type gene expression profiles in tomato plants colonized by an arbuscular mycorrhizal fungus. New Phytol 184:975–987. doi:10.1111/j.1469-8137.2009.03031.x

    Article  CAS  PubMed  Google Scholar 

  • Flores-Monterroso A, Canales J, de la Torre F, Ávila C, Cánovas FM (2013) Identification of genes differentially expressed in ectomycorrhizal roots during the Pinus pinaster–Laccaria bicolor interaction. Planta 237:1637–1650. doi:10.1007/s00425-013-1874-4

    Article  CAS  PubMed  Google Scholar 

  • Frettinger P, Derory J, Herrmann S, Plomion C, Lapeyrie F, Oelmüller R, Martin F, Buscot F (2007) Transcriptional changes in two types of pre-mycorrhizal roots and in ectomycorrhizas of oak microcuttings inoculated with Piloderma croceum. Planta 225:331–340. doi:10.1007/s00425-006-0355-4

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Garrido JM, Ocampo J (2002) Regulation of the plant defence response in arbuscular mycorrhizal symbiosis. J Exp Bot 53:1377–1386. doi:10.1093/jexbot/53.373.1377

    Article  CAS  PubMed  Google Scholar 

  • Gobom J, Nordhoff E, Mirgorodskaya E, Ekman R, Roepstorff P (1999) Sample purification and preparation technique based on nano-scale reversed-phase columns for the sensitive analysis of complex peptide mixtures by matrix-assisted laser desorption/ionization mass spectrometry. J Mass Spectrom 34:105–116. doi:10.1002/(SICI)1096-9888(199902)34:2<105::AID-JMS768>3.0.CO;2-4

    Article  CAS  PubMed  Google Scholar 

  • Grant WD, West AW (1986) Measurement of ergosterol, diaminopimelic acid and glucosamine in soil: evaluation as indicators of microbial biomass. J Microbiol Methods 6:47–54. doi:10.1016/0167-7012(86)90031-X

    Article  CAS  Google Scholar 

  • Guy CL, Huber JLA, Huber SC (1992) Sucrose phosphate synthase and sucrose accumulation at low temperature. Plant Physiol 100:502–508, 10.1104/pp.100.1.502

  • Harrison MD, Jones CE, Dameron CT (1999) Copper chaperones: function, structure and copper-binding properties. J Biol Inorg Chem 4:145–153

    Article  CAS  PubMed  Google Scholar 

  • Hartung W, Ratcliffe RG (2002) Utilization of glycine and serine as nitrogen sources in the roots of Zea mays and Chamaegigas intrepidus. J Exp Bot 53:2305–2314. doi:10.1093/jxb/erf092

    Article  CAS  PubMed  Google Scholar 

  • Heller G, Adomas A, Li G, Osborne J, van Zyl L, Sederoff R, Finlay RD, Stenlid J, Asiegbu FO (2008) Transcriptional analysis of Pinus sylvestris roots challenged with the ectomycorrhizal fungus Laccaria bicolor. BMC Plant Biol 8:19. doi:10.1186/1471-2229-8-19

    Article  PubMed  PubMed Central  Google Scholar 

  • Hilbert JL, Costa G, Martin F (1991) Ectomycorrhizin synthesis and polypeptide changes during the early stage of eucalypt mycorrhiza development. Plant Physiol 97:977–984, 10.1104/pp.97.3.977

  • Hemmingsen SM, Woolford C, van der Vies SM, Tilly K, Dennis DT, Georgopoulos CP, Hendrix RW, Ellis RJ (1988) Homologous plant and bacterial proteins chaperone oligomeric protein assembly. Nature 333:330–334. doi:10.1038/333330a0

    Article  CAS  PubMed  Google Scholar 

  • Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195. doi:10.1023/A:1013351617532

    Article  CAS  Google Scholar 

  • Hughes AL, Powell DW, Bard M, Eckstein J, Barbuch R, Link AJ, Espenshade PJ (2007) Dap1/PGRMC1 binds and regulates cytochrome P450 enzymes. Cell Metab 5:143–149. doi:10.1016/j.cmet.2006.12.009

    Article  CAS  PubMed  Google Scholar 

  • Inohara N, Nuñez G (2002) ML—a conserved domain involved in innate immunity and lipid metabolism. Trends Biochem Sci 27:219–221, 10.1016/S0968-0004(02)02084-4

  • Jelenska J, Kang Y, Greenberg JT (2014) Plant pathogenic bacteria target the actin microfilament network involved in the trafficking of disease defense components. BioArchitecture 4:149–153. doi:10.4161/19490992.2014.980662

    Article  PubMed  PubMed Central  Google Scholar 

  • Johansson T, Le Quere A, Ahren D, Soderstrom B, Erlandsson R, Lundeberg J, Uhlen M, Tunlid A (2004) Transcriptional responses of Paxillus involutus and Betula pendula during formation of ectomycorrhizal root tissue. Mol Plant Microbe Interact 17:202–215. doi:10.1094/MPMI.2004.17.2.202

    Article  PubMed  Google Scholar 

  • Kang Y, Jelenska J, Cecchini NM, Li Y, Lee MW, Kovar DR, Greenberg JT (2014) HopW1 from Pseudomonas syringae disrupts the actin cytoskeleton to promote virulence in Arabidopsis. PLoS Pathog 10:e1004232, 10.1371/journal.ppat.1004232

  • Kleczkowski LA, Geisler M, Ciereszko I, Johansson H (2004) UDP-glucose pyrophosphorylase. An old protein with new tricks. Plant Physiol 134:912–918. doi:10.1104/pp.103.036053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuhn H, Küster H, Requena N (2010) Membrane steroid-binding protein 1 induced by a diffusible fungal signal is critical for mycorrhization in Medicago truncatula. New Phytol 185:716–733. doi:10.1111/j.1469-8137.2009.03116.x

    Article  CAS  PubMed  Google Scholar 

  • Lambertson D, Chen L, Madura K (2003) Investigating the importance of proteasome-interaction for Rad23 function. Curr Genet 42:199–208. doi:10.1007/s00294-002-0350-7

    CAS  PubMed  Google Scholar 

  • Laurent P, Voiblet C, Tagu D, de Carvalho D, Nehls U, De Bellis R, Balestrini R, Bauw G, Bonfante P, Martin F (1999) A novel class of ectomycorrhiza-regulated cell wall polypeptides in Pisolithus tinctorius. Mol Plant-Microbe Interact 12:862–871. doi:10.1094/MPMI.1999.12.10.862

    Article  CAS  PubMed  Google Scholar 

  • Le Quéré A, Wright D, Soderstrom B, Tunlid A, Johansson T (2005) Global patterns of gene regulation associated with the development of ectomycorrhiza between birch (Betula pendula Roth.) and Paxillus involutus (Batsch) Fr. Mol Plant Microbe Interact 18:659–673. doi:10.1094/MPMI-18-0659

    Article  PubMed  Google Scholar 

  • Li L, Cheng XF, Leshkevich J, Umezawa T, Harding SA, Chiang VL (2001) The last step of syringyl monolignol biosynthesis in angiosperms is regulated by a novel gene encoding sinapyl alcohol dehydrogenase. Plant Cell 13:1567–1586, 10.1105/TPC.010111

  • Liu JJ, Ekramoddoullah AKM (2006) The family 10 of plant pathogenesis-related proteins: their structure, regulation, and function in response to biotic and abiotic stresses. Physiol Mol Plant Pathol 68:3–13, 10.1016/j.pmpp.2006.06.004

  • Luo ZB, Janz D, Jiang X, Gobel C, Wildhagen H, Tan Y, Rennenberg H, Feussner I, Polle A (2009) Upgrading root physiology for stress tolerance by ectomycorrhizas: insights from metabolite and transcriptional profiling into reprogramming for stress anticipation. Plant Physiol 151:1902–1917. doi:10.1104/pp.109.143735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo Z-B, Lic K, Gaic Y, Göbeld C, Wildhagene H, Jiangc X, Feußnerd I, Rennenberge H, Polle A (2011) The ectomycorrhizal fungus Paxillus involutus modulates leaf physiology of poplar towards improved salt tolerance. Environ Exp Bot 72:304–311, doi:10.1016/j.envexpbot.2011.04.008

  • Martin F, Aerts A, Ahren D et al (2008) Symbiosis insights from the genome of the mycorrhizal basidiomycete Laccaria bicolor. Nature 452:88–92. doi:10.1038/nature06556

    Article  CAS  PubMed  Google Scholar 

  • Martin F, Deraruelle C, Hilbert JL (1990) An improved ergosterol assay to estimate fungal biomass in ectomycorrhizas. Mycol Res 94:1059–1064. doi:10.1016/S0953-7562(09)81333-6

    Article  Google Scholar 

  • Martin F, Kohler A, Murat C et al (2010) Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464:1033–1038. doi:10.1038/nature08867

    Article  CAS  PubMed  Google Scholar 

  • Martin F, Nehls U (2009) Harnessing ectomycorrhizal genomics for ecological insights. Curr Opin Plant Biol 12:508–515, doi:10.1016/j.pbi.2009.05.007

  • Martins A, Casimiro A, Pais MS (1997) Influence of mycorrhization on physiological parameters of micropropagated Castanea sativa Mill. plants. Mycorrhiza 7:161–165. doi:10.1007/s005720050176

    Article  CAS  Google Scholar 

  • Meyer Y, Verdoucq L, Vignols F (1999) Plant thioredoxins and glutaredoxins: identity and putative roles. Trends Plant Sci 4:10, 10.1016/S1360-1385(99)01475-2

  • Miedes E, Vanholme R, Boerjan W, Molina A (2014) The role of the secondary cell wall in plant resistance to pathogens. Front Plant Sci 5:358. doi:10.3389/fpls.2014.00358

    Article  PubMed  PubMed Central  Google Scholar 

  • Miura K, Jin JB, Hasegawa PM (2007) Sumoylation, a posttranslational regulatory process in plants. Curr Opin Plant Biol 10:495–502, 10.1016/j.pbi.2007.07.002

  • Monteiro F, Sebastiana M, Pais MS, Figueiredo A (2013) Reference gene selection and validation for the early responses to downy mildew infection in susceptible and resistant Vitis vinifera cultivars. PLoS One 8:e72998, 10.1371/journal.pone.0072998

  • Müller T, Avolio M, Olivi M, Benjdia M, Rikirsch E, Kasaras A, Fitz M, Chalot M, Wipf D (2007) Nitrogen transport in the ectomycorrhiza association: the Hebeloma cylindrosporum-Pinus pinaster model. Phytochemistry 68:41–51. doi:10.1016/j.phytochem.2006.09.021

    Article  PubMed  Google Scholar 

  • Nehls U, Gohringer F, Wittulsky S, Dietz S (2010) Fungal carbohydrate support in the ectomycorrhizal symbiosis: a review. Plant Biol 12:292–301. doi:10.1111/j.1438-8677.2009.00312.x

    Article  CAS  PubMed  Google Scholar 

  • Novatchkova M, Budhiraja R, Coupland G, Eisenhaber F, Bachmair A (2004) SUMO conjugation in plants. Planta 220:1–8. doi:10.1007/s00425-004-1370-y

    Article  CAS  PubMed  Google Scholar 

  • Penheiter AR, Klucas RV, Sarath G (1998) Purification and characterization of a soybean root nodule phosphatase expressed in Pichia pastoris. Protein Expr Purif 14:125–130. doi:10.1006/prep.1998.0935

    Article  CAS  PubMed  Google Scholar 

  • Prasad TK, Stewart CR (1992) cDNA clones encoding Arabidopsis thaliana and Zea mays mitochondrial chaperonin HSP60 and gene expression during seed germination and heat shock. Plant Mol Biol 18:873–885. doi:10.1007/BF00019202

    Article  CAS  PubMed  Google Scholar 

  • Qiang X, Zechmann B, Reitz MU, Kogel KH, Schäfer P (2012) The mutualistic fungus Piriformospora indica colonizes Arabidopsis roots by inducing an endoplasmic reticulum stress-triggered caspase-dependent cell death. Plant Cell 24:794–809. doi:10.1105/tpc.111.093260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raasi S, Pickart CM (2003) Rad23 ubiquitin-associated domains (UBA) inhibit 26 S proteasome-catalyzed proteolysis by sequestering lysine 48-linked polyubiquitin chains. J Biol Chem 278:8951–8959. doi:10.1074/jbc.M212841200

    Article  CAS  PubMed  Google Scholar 

  • Radauer C, Lackner P, Breiteneder H (2008) The Bet v 1 fold: an ancient, versatile scaffold for binding of large, hydrophobic ligands. BMC Evol Biol 8:286. doi:10.1186/1471-2148-8-286

    Article  PubMed  PubMed Central  Google Scholar 

  • Ray S, Anderson JM, Urmeev FI, Goodwin SB (2003) Rapid induction of a protein disulphide isomerase and defense-related genes in wheat in response to the hemibiotrophic fungal pathogen Mycosphaerella graminicola. Plant Mol Biol 53:701–714. doi:10.1023/B:PLAN.0000019120.74610.52

    Article  CAS  PubMed  Google Scholar 

  • Rodrigues CI, Maia R, Maguas C (2010) Comparing total nitrogen and crude protein content of green coffee beans (Coffea spp.) from different geographical origins. Coffee Sci 5:197–205

    Google Scholar 

  • Rose CM, Venkateshwaran M, Volkening JD et al (2012) Rapid phosphoproteomic and transcriptomic changes in the rhizobia legume symbiosis. Mol Cell Proteomics 11:724–744. doi:10.1074/mcp.M112.019208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C (T) method. Nat Protoc 3:1101–1108. doi:10.1038/nprot.2008.73

    Article  CAS  PubMed  Google Scholar 

  • Sebastiana M, Figueiredo A, Monteiro F et al (2013a) A possible approach for gel-based proteomic studies in recalcitrant woody plants. SpringerPlus 2:210. doi:10.1186/2193-1801-2-210

    Article  PubMed  PubMed Central  Google Scholar 

  • Sebastiana M, Pereira V, Alcantara A, Pais M, Silva A (2013b) Ectomycorrhizal inoculation with Pisolithus tinctorius increases the performance of Quercus suber L. (cork oak) nursery and field seedlings. New For 44:937–949. doi:10.1007/s11056-013-9386-4

    Article  Google Scholar 

  • Sebastiana M, Vieira B, Lino-Neto T, Monteiro F, Figueiredo A, Sousa L, Pais MS, Tavares R, Paulo OS (2014) Oak root response to ectomycorrhizal symbiosis establishment: RNA-Seq derived transcript identification and expression profiling. PLoS One 9:e98376. doi:10.1371/journal.pone.0098376

    Article  PubMed  PubMed Central  Google Scholar 

  • Selles B, Jacquot J, Rouhier N (2011) Comparative genomic study of protein disulfide isomerases from photosynthetic organisms. Genomics 97:37–50. doi:10.1016/j.ygeno.2010.10.001

    Article  CAS  PubMed  Google Scholar 

  • Serrato AJ, Guilleminot J, Meyer Y, Vignols F (2008) AtCXXS: atypical members of the Arabidopsis thaliana thioredoxin h family with a remarkably high disulfide isomerase activity. Physiol Plant 133:611–622. doi:10.1111/j.1399-3054.2008.01093.x

    Article  CAS  PubMed  Google Scholar 

  • Shin L, Lo J, Yeh K (2012) Copper chaperone antioxidant protein1 is essential for copper homeostasis. Plant Physiol 159:1099–1110. doi:10.1104/pp.112.195974

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simoneau P, Viemont JD, Moreau JC, Strullu DG (1993) Symbiosis-related polypeptides associated with the early stages of ectomycorrhiza organogenesis in birch (Betula pendula Roth). New Phytol 124:495–504

    Article  CAS  Google Scholar 

  • Slajcherova K, Fiserova J, Fischer L, Schwarzerova K (2012) Multiple actin isotypes in plants: diverse genes for diverse roles? Front Plant Sci 3:226. doi:10.3389/fpls.2012.00226

    Article  PubMed  PubMed Central  Google Scholar 

  • Smith S, Read D (1997) Mycorrhizal symbiosis. Academic, London

    Google Scholar 

  • Tada Y, Spoel SH, Pajerowska-Mukhtar K et al (2008) Plant immunity requires conformational charges of NPR1 via S-nitrosylation and thioredoxins. Science 321:952–956. doi:10.1126/science.1156970

    Article  CAS  PubMed  Google Scholar 

  • Timonen S, Peterson RL (1993) Cytoskeleton in mycorrhizal symbiosis. Plant Soil 244:199–210. doi:10.1023/A:1020209213524

    Article  Google Scholar 

  • Tran HT, Hurley BA, Plaxton WC (2010) Feeding hungry plants: the role of purple acid phosphatases in phosphate nutrition. Plant Sci 179:14–27, 10.1016/j.plantsci.2010.04.005

  • Unlu M, Morgan ME, Minden JS (1997) Difference gel electrophoresis: a single gel method for detecting changes in protein extracts. Electrophoresis 18:2071–2077. doi:10.1002/elps.1150181133

    Article  CAS  PubMed  Google Scholar 

  • Valot B, Dieu M, Recorbet G, Raes M, Gianinazzi S, Dumas-Gaudot E (2005) Identification of membrane-associated proteins regulated by the arbuscular mycorrhizal symbiosis. Plant Mol Biol 59:565–580. doi:10.1007/s11103-005-8269-2

    Article  CAS  PubMed  Google Scholar 

  • Vincent D, Kohler A, Claverol S, Solier E, Joets J, Gibon J, Lebrun M-H, Plomion C, Martin F (2012) Secretome of the free-living mycelium from the ectomycorrhizal basidiomycete Laccaria bicolor. J Proteome Res 11:157–171. doi:10.1021/pr200895f

    Article  CAS  PubMed  Google Scholar 

  • Vizcaino JA, Deutsch EW, Wang R et al (2014) ProteomeXchange provides globally coordinated proteomics data submission and dissemination. Nat Biotechnol 32:223–226. doi:10.1038/nbt.2839

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wan CY, Wilkins TA (1994) A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.). Anal Biochem 223:7–12. doi:10.1006/abio.1994.1538

    Article  CAS  PubMed  Google Scholar 

  • Wang D, Weaver ND, Kesarwani M, Dong X (2005) Induction of protein secretory pathway is required for systemic acquired resistance. Science 308:1036–1040. doi:10.1126/science.1108791

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Li Z, Qian W, Guo W, Gao X, Huang L, Wang H, Zhu H, Wu J, Wang D, Liu D (2011) The Arabidopsis purple acid phosphatase AtPAP10 is predominantly associated with the root surface and plays an important role in plant tolerance to phosphate limitation. Plant Physiol 157:1283–1299, doi:10.1104/pp.111.183723

  • Wilkinson B, Gilbert HF (2004) Protein disulfide isomerase. Biochim Biophys Acta 1699:35–44. doi:10.1016/j.bbapap.2004.02.017

    Article  CAS  PubMed  Google Scholar 

  • Xu X-H, Wang C, Li S-X et al (2015) Friend or foe: differential responses of rice to invasion by mutualistic or pathogenic fungi revealed by RNAseq and metabolite profiling. Sci Rep 5:13624. doi:10.1038/srep13624

    Article  PubMed  PubMed Central  Google Scholar 

  • Zouari I, Salvioli A, Chialva M, Novero M, Miozzi L, Tenore GC, Bagnaresi P, Bonfante P (2014) From root to fruit: RNA-Seq analysis shows that arbuscular mycorrhizal symbiosis may affect tomato fruit metabolism. BMC Genomics 15:221. doi:10.1186/1471-2164-15-221

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The authors would like to acknowledge Dr. Andrea Lorentzen from the Department of Biochemistry and Molecular Biology of the University of Southern Denmark for the help provided with protein identification. This study was supported by Fundação para a Ciência e Tecnologia (FCT/MCTES/PIDDAC, Portugal) with the project PTDC/AGR-AAM/105531/2008. JS and JP were funded by the European Research Council Synergy grant ERC-2013-SyG 610028-IMBALANCE-P.

Author information

Authors and Affiliations

  1. Plant Functional Genomics Unit, Biosystems & Integrative Sciences Institute (BioISI), Faculty of Sciences, Lisbon University, Campo Grande, Edificio C2, piso 4, 1749-016, Lisbon, Portugal

    Mónica Sebastiana, Andreia Figueiredo, Filipa Monteiro, Anabela Silva & Maria Salomé Pais

  2. Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, Avenida da Republica, 2780-s157, Oeiras, Portugal

    Joana Martins & Ana Varela Coelho

  3. CSIC, Global Ecology Unit, CREAF-CSIC-UAB, Cerdanyola del Vallès, 08193, Catalonia, Spain

    Jordi Sardans & Josep Peñuelas

  4. CREAF, Cerdanyola del Vallès, 08193, Catalonia, Spain

    Jordi Sardans & Josep Peñuelas

  5. Department of Biochemistry and Molecular Biology, University of Southern Denmark, Campusvej 55, 5230, Odense M, Denmark

    Peter Roepstorff

Authors
  1. Mónica Sebastiana
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joana Martins
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andreia Figueiredo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Filipa Monteiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jordi Sardans
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Josep Peñuelas
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Anabela Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Peter Roepstorff
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Maria Salomé Pais
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Ana Varela Coelho
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mónica Sebastiana.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online resource 1 (Supplementary Table 1)

Quantitative analysis of the protein spots. Column A: spot number; Column B: normalised spot volume in mycorrhizal roots according to Progenesis SameSpot; Column C: spot volume upon correction for the 0.93:0.07 plant-fungal proportion in mycorrhizal roots; Column D: normalised spot volume in non-mycorrhizal roots according to Progenesis SameSpot; Column E: Fold Change (FC) between mycorrhizal and non-mycorrhizal roots calculated as C/D; Column F: for representation proposes, a −1/FC transformation was applied to FC values between 0 and 1 (down-accumulated spots). (XLSX 12 kb)

Online resource 2 (Supplementary Table 2)

Target genes for real-time PCR analysis: accession in cork oak transcriptome database (www.corkoakdb.org), primers sequences, annealing (Ta) and melting (Tm) temperature. (DOCX 12 kb)

Online resource 3 (Supplementary Fig. 1)

The interaction between P. tinctorius and the roots of cork oak. (a) Example of a colonized (right) and a non-colonized (left) plant. (b) Non-inoculated roots. (c) Colonized root, 2 months after inoculation with P. tinctorius. (d) Transverse section of a colonized root (2 months after inoculation) showing the fungal mantle (m) surrounding the root and the Hartig net (hn) on root epidermal cells; scale 50 μm (Sebastiana et al. 2014). (GIF 232 kb)

High resulotion image (TIF 16736 kb)

Online resource 4 (Supplementary Fig. 2)

Representative images of Cy labelled 2-DE gels for mycorrhizal leaves (A) and non-mycorrhizal leaves (B) (GIF 140 kb)

High resulotion image (TIF 14614 kb)

Online resource 5 (Supplementary Table 3)

The identity of differentially expressed protein spots as determined by tandem mass spectrometry. (XLSX 31 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sebastiana, M., Martins, J., Figueiredo, A. et al. Oak protein profile alterations upon root colonization by an ectomycorrhizal fungus. Mycorrhiza 27, 109–128 (2017). https://doi.org/10.1007/s00572-016-0734-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-016-0734-z

Keywords

Search

Navigation