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Comparative proteomic analysis of leaf tissue from tomato plants colonized with Rhizophagus irregularis

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Abstract

A comparative proteomic approach was performed to analyze the differential accumulation of leaf proteins in response to the symbiosis between Solanum lycopersicum and the arbuscular mycorrhizal fungus (AMF) Rhizophagus irregularis. Protein profiling was examined in leaves from tomato plants colonized with AMF (M), as well as non-colonized plants fertilized with low phosphate (20 μM P; NM-LP) and non-colonized plants fertilized with regular phosphate Hoagland’s solution (200 μM P; NM-RP). Comparisons were made between these groups, and 2D-SDS-PAGE revealed that 27 spots were differentially accumulated in M vs. NM-LP. Twenty-three out of the 27 spots were successfully identified by mass spectrometry. Two of these proteins, 2-methylene-furan-3-one reductase and auxin-binding protein ABP19a, were up-accumulated in M plants. The down-accumulated proteins in M plants were associated mainly with photosynthesis, redox, and other molecular functions. Superoxide dismutase, harpin binding protein, and thioredoxin peroxidase were down-accumulated in leaves of M tomato plants when compared to NM-LP and NM-RP, indicating that these proteins are responsive to AMF colonization independently of the phosphate regime under which they were grown. 14-3-3 protein was up-accumulated in NM-RP vs. NM-LP plants, whereas it was down-accumulated in M vs. NM-LP and M vs. NM-RP, regardless of their phosphate nutrition. This suggests a possible regulation by P nutrition and AMF colonization. Our results demonstrate AMF-induced systemic changes in the expression of tomato leaf proteins, including the down-accumulation of proteins related to photosynthesis and redox function.

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References

  • Aloui A, Recorbet G, Robert F, Schoefs B, Bertrand M, Henry C, Gianinazzi-Pearson V, Dumas-Gaudot E, Aschi-Smiti S (2011) Arbuscular mycorrhizal symbiosis elicits shoot proteome changes that are modified during cadmium stress alleviation in Medicago truncatula. BMC Plant Biol. doi:10.1186/1471-2229-11-75

    PubMed  PubMed Central  Google Scholar 

  • Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53(372):1331–1341. doi:10.1093/jexbot/53.372.1331

    Article  CAS  PubMed  Google Scholar 

  • Amiour N, Recorbet G, Robert F, Gianinazzi S, Dumas-Gaudot E (2006) Mutations in DMI3 and SUNN modify the appressorium-responsive root proteome in arbuscular mycorrhiza. Mol Plant-Microbe In. doi:10.1094/MPMI-19-0988

    Google Scholar 

  • Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639

    Article  CAS  PubMed  Google Scholar 

  • Benabdellah K, Azcón-Aguilar C, Ferrol N (2000) Alterations in the plasma membrane polypeptide pattern of tomato roots (Lycopersicum esculentum) during the development of arbuscular mycorrhiza. J Exp Bot. doi:10.1093/jexbot/51.345.747

    PubMed  Google Scholar 

  • Bestel-Corre G, Dumas-Gaudot E, Poinsot V, Dieu M, Dierick JF, Van Tuinen D, Remacle J, Gianinazzi-Pearson V, Gianinazzi S (2002) Proteome analysis and identification of symbiosis-related proteins from Medicago truncatula Gaertn. by two-dimensional electrophoresis and mass spectrometry. Electrophoresis. doi:10.1002/1522-2683(200201)

    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. doi:10.1007/s00572-003-0280-3

    PubMed  Google Scholar 

  • Black KG, Mitchell DT, Osborne BA (2000) Effect of mycorrhizal-enhanced leaf phosphate status on carbon partitioning, translocation and photosynthesis in cucumber. Plant Cell Environ. doi:10.1046/j.1365-3040.2000.00598.x

    Google Scholar 

  • Boldt K, Pörs Y, Haupt B, Bitterlich M, Kühn C, Grimm B, Franken P (2011) Photochemical processes, carbon assimilation and RNA accumulation of sucrose transporter genes in tomato arbuscular mycorrhiza. J Plant Physiol. doi:10.1016/j.jplph.2011.01.026

    PubMed  Google Scholar 

  • Bona E, Cattaneo C, Cesaro P, Marsano F, Lingua G, Cavaletto M, Berta G (2010) Proteomic analysis of Pteris vittata fronds: two arbuscular mycorrhizal fungi differentially modulate protein expression under arsenic contamination. Proteomics. doi:10.1002/pmic.200900436

    PubMed  Google Scholar 

  • Brown MS, Bethlenfalvay GJ (1988) The Glycine-Glomus-Rhizobium symbiosis. VII. photosynthetic nutrient use efficiency in nodulated, mycorrhizal soybeans. Plant Physiol 86(4):1292–1297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bunney TD, Van den Wijngaard PW, De Boer AH (2002) 14-3-3 protein regulation of proton pumps and ion channels. Plant Mol Biol. doi:10.1023/A:1021231805697

    PubMed  Google Scholar 

  • Buttery RG, Takeoka GR, Ling LC (1995) Furaneol: odor threshold and importance to tomato aroma. J Agric Food Chem. doi:10.1021/jf00054a042

    Google Scholar 

  • Campos-Soriano L, García-Martínez J, San SB (2011) The arbuscular mycorrhizal symbiosis promotes the systemic induction of regulatory defence-related genes in rice leaves and confers resistance to pathogen infection. Mol Plant Pathol. doi:10.1111/J.1364-3703.2011.00773.X

    PubMed  Google Scholar 

  • Caravaca F, Alguacil MM, Hernández JA, Roldán A (2005) Involvement of antioxidant enzyme and nitrate reductase activities during water stress and recovery of mycorrhizal Myrtus communis and Phillyrea angustifolia plants. Plant Sci. doi:10.1016/j.plantsci.2005.03.013

    Google Scholar 

  • Cartieaux F, Thibaud MC, Zimmerli L, Lessard P, Sarrobert C, David P, Gerbaud A, Robaglia C, Somerville S, Nussaume L (2003) Transcriptome analysis of Arabidopsis colonized by a plant-growth promoting rhizobacterium reveals a general effect on disease resistance. Plant J. doi:10.1046/j.1365-313X.2003.01867.x

    PubMed  Google Scholar 

  • Cervantes-Gámez RG, Bueno-Ibarra MA, Cruz-Mendívil A, Calderón-Vázquez CL, Ramírez-Douriet CM, Maldonado-Mendoza IE, Villalobos-López MA, Valdez-Ortíz A, López-Meyer M (2015) Arbuscular mycorrhizal symbiosis-induced expression changes in Solanum lycopersicum leaves revealed by RNA-seq analysis. Plant Mol Biol Rep. doi:10.1007/s11105-015-0903-9

    Google Scholar 

  • Chabot S, Becard G, Piche Y (1992) Life cycle of Glomus intraradix in root organ culture. Mycologia 84(3):315–321

    Article  Google Scholar 

  • Chen PS Jr, Toribara TY, Warner H (1956) Microdetermination of phosphorous. Anal Chem. doi:10.1021/ac60119a033

    Google Scholar 

  • Chiou CY, Wu K, Yeh KW (2008) Characterization and promoter activity of chromoplast specific carotenoid associated gene (CHRC) from Oncidium Gower Ramsey. Biotechnol Lett. doi:10.1007/s10529-008-9767-5

    PubMed  Google Scholar 

  • 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. doi:10.1016/j.envexpbot.2011.08.012

    Google Scholar 

  • Colditz F, Braun HP, Jacquet C, Niehaus K, Krajinski F (2005) Proteomic profiling unravels insights into the molecular background underlying increased Aphanomyces euteiches-tolerance of Medicago truncatula. Plant Mol Biol. doi:10.1007/s11103-005-0184-z

    PubMed  Google Scholar 

  • Couto MSR, Lovato PE, Wipf D, Dumas-Gaudot E (2013) Proteomic studies of arbuscular mycorrhizal associations. Adv Biol Chem. doi:10.4236/abc.2013.31007

    Google Scholar 

  • de Carvalho-Niebel F, Lescure N, Cullimore JV, Gamas P (1998) The Medicago truncatula MtAnn1 gene encoding an annexin is induced by Nod factors and during the symbiotic interaction with Rhizobium meliloti. Mol Plant Microbe Interact. doi:10.1094/MPMI.1998.11.6.504

    Google Scholar 

  • de Carvalho-Niebel F, Timmers AC, Chabaud M, Defaux-Petras A, Barker DG (2002) The Nod factor-elicited annexin MtAnn1 is preferentially localised at the nuclear periphery in symbiotically activated root tissues of Medicago truncatula. Plant J. doi:10.1046/j.1365-313X.2002.01429.x

    PubMed  Google Scholar 

  • Doner LW, Bécard G (1991) Solubilization of gellan gels by chelation of cations. Biotechnol Tech. doi:10.1007/BF00152749

    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. doi:10.1111/j.1469-8137.2009.03031.x

    PubMed  Google Scholar 

  • Fitze D, Wiepning A, Kaldorf M, Ludwig-Muller J (2005) Auxins in the development of an arbuscular mycorrhizal symbiosis in maize. J Plant Physiol. doi:10.1016/j.jplph.2005.01.014

    PubMed  Google Scholar 

  • Fridovich I (1995) Superoxide radical and superoxide dismutases. Annu Rev Biochem 64:97–112. doi:10.1146/annurev.bi.64.070195.000525

    Article  CAS  PubMed  Google Scholar 

  • Fulgosi H, Soll J, Maraschin SF, Korthout HA, Wang M, Testerink C (2002) 14-3-3 proteins and plant development. Plant Mol Biol. doi:10.1023/A:1021295604109

    PubMed  Google Scholar 

  • Garg N, Chandel S (2015) Role of arbuscular mycorrhiza in arresting reactive oxygen species (ROS) and strengthening antioxidant defense in Cajanus cajan (L.) Millsp. nodules under salinity (NaCl) and cadmium (Cd) stress. Plant Growth Regul 75(2):521–534. doi:10.1007/s10725-014-0016-8

    Article  CAS  Google Scholar 

  • Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytol. doi:10.1111/j.1469-8137.1980.tb04556.x

    Google Scholar 

  • Gomez SK, Javot H, Deewatthanawong P, Torres-Jerez I, Tang Y, Blancaflor EB, Udvardi MK, Harrison MJ (2009) Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis. BMC Plant Biol. doi:10.1186/1471-2229-9-10

    PubMed  PubMed Central  Google Scholar 

  • Guether M, Balestrini R, Hannah M, He J, Udvardi MK, Bonfante P (2009) Genome-wide reprogramming of regulatory networks, transport, cell wall and membrane biogenesis during arbuscular mycorrhizal symbiosis in Lotus japonicus. New Phytol. doi:10.1111/j.1469-8137.2008.02725.x

    Google Scholar 

  • Guimil S, Chang HS, Zhu T, Sesma A, Osbourn A, Roux C, Loannidis V, Oakeley EJ, Docquier M, Descombes P, Briggs SP, Paszkowski U (2005) Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proc Natl Acad Sci U S A. doi:10.1073/pnas.0502999102

    PubMed  PubMed Central  Google Scholar 

  • Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol. doi:10.1146/annurev.micro.58.030603.123749

    PubMed  Google Scholar 

  • Hause B, Mrosk C, Isayenkov S, Strack D (2007) Jasmonates in arbuscular mycorrhizal interactions. Phytochemistry. doi:10.1016/j.phytochem.2006.09.025

    PubMed  Google Scholar 

  • Hohnjec N, Vieweg MF, Puhler A, Becker A, Kuster H (2005) Overlaps in the transcriptional profiles of Medicago truncatula roots inoculated with two different Glomus fungi provide insights into the genetic program activated during arbuscular mycorrhiza. Plant Physiol. doi:10.1104/pp.104.056572

    PubMed  PubMed Central  Google Scholar 

  • Jami SK, Clark GB, Turlapati SA, Handley C, Roux SJ, Kirti PB (2008) Ectopic expression of an annexin from Brassica juncea confers tolerance to abiotic and biotic stress treatments in transgenic tobacco. Plant Physiol Biochem. doi:10.1016/j.plaphy.2008.07.006

    PubMed  Google Scholar 

  • Johnson CR (1984) Phosphorus nutrition on mycorrhizal colonization, photosynthesis, growth and nutrient composition of Citrus aurantium. Plant Soil. doi:10.1007/BF02232937

    Google Scholar 

  • Kaldorf M, Ludwig-Muller J (2000) AM fungi might affect the root morphology of maize by increasing indole-3-butyric acid biosynthesis. Physiol Plant. doi:10.1034/j.1399-3054.2000.100109.x

    Google Scholar 

  • Kapoor R, Sharma D, Bhatnagar AK (2008) Arbuscular mycorrhizae in micropropagation systems and their potential applications. Sci Hortic. doi:10.1016/j.scienta.2008.02.002

    Google Scholar 

  • Kim YS, Min JK, Kim D, Jung J (2001) A soluble auxin-binding protein, ABP57. purification with anti-bovine serum albumin antibody and characterization of its mechanistic role in the auxin effect on plant plasma membrane H+-ATPase. J Biol Chem. doi:10.1074/jbc.M009416200

    Google Scholar 

  • Klein D, Fink B, Arold B, Eisenreich W, Schwab W (2007) Functional characterization of enone oxidoreductases from strawberry and tomato fruit. J Agric Food Chem. doi:10.1021/jf071055o

    PubMed  Google Scholar 

  • Langenkamper G, Monach N, Broin M, Cuiné S, Becuwe N, Kuntz M, Rey P (2001) Accumulation of plastid lipid-associated proteins (fibrillin/CDSP34) upon oxidative stress, ageing and biotic stress in Solanaceae and in response to drought in other species. J Exp Bot. doi:10.1093/jexbot/52.360.1545

    PubMed  Google Scholar 

  • Leitner-Dagan Y, Ovadis M, Shklarman E, Elad Y, David DR, Vainstein A (2006) Expression and functional analyses of the plastid lipid-associated protein CHRC suggest its role in chromoplastogenesis and stress. Plant Physiol. doi:10.1104/pp.106.082404

    PubMed  PubMed Central  Google Scholar 

  • 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(6):e38662. doi:10.1371/journal.pone.0038662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liochev S, Fridovich I (1994) The role of superoxide anion radicals in the production of hydroxyl radicals: in vitro and in vivo. Free Radic Biol Med 16(1):29–33

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Blaylock LA, Endre G, Cho J, Town CD, VandenBosch KA, Harrison MJ (2003) Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of an arbuscular mycorrhizal symbiosis. Plant Cell. doi:10.1105/tpc.014183

    Google Scholar 

  • Liu J, Maldonado-Mendoza I, López-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. doi:10.1111/j.1365-313X.2007.03069.x

    PubMed Central  Google Scholar 

  • Ludwig-Muller J, Guther M (2007) Auxins as signals in arbuscular mycorrhiza formation. Plant Signal Behav 2(3):194–196

    Article  PubMed  PubMed Central  Google Scholar 

  • Manthey K, Krajinski F, Hohnjec N, Firnhaber C, Puhler A, Perlick AM, Kuster H (2004) Transcriptome profiling in root nodules and arbuscular mycorrhiza identifies a collection of novel genes induced during Medicago truncatula root endosymbioses. Mol Plant-Microbe Interact. doi:10.1094/MPMI.2004.17.10.1063

    PubMed  Google Scholar 

  • Millner PD, Kitt DG (1992) The Beltsville method for soilless production of vesicular-arbuscular mycorrhizal fungi. Mycorrhiza 2:9–15

    Article  Google Scholar 

  • Mora-Romero GA, González-Ortiz MA, Quiroz-Figueroa F, Calderon-Vazquez CL, Medina-Godoy S, Maldonado-Mendoza I, Arroyo-Becerra A, Perez-Torres A, Alatorre-Cobos F, Sánchez F, Lopez-Meyer M (2015a) PvLOX2 silencing in common bean roots impairs arbuscular mycorrhiza-induced resistance without affecting symbiosis establishment. Funct Plant Biol. doi:10.1071/FP14101

    Google Scholar 

  • Mora-Romero GA, Cervantes-Gámez RG, Galindo-Flores H, González-Ortiz MA, Félix-Gastélum R, Maldonado-Mendoza IE, Salinas-Pérez R, León-Félix J, Martínez-Valenzuela MC, López-Meyer M (2015b) Mycorrhiza-induced protection against pathogens is both genotype-specific and graft-transmissible. Symbiosis. doi:10.1007/s13199-015-0334-2

    Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    Article  CAS  PubMed  Google Scholar 

  • Ohmiya A, Tanaka Y, Kadowaki KI, Hayashi T (1998) Cloning of genes encoding auxin-binding proteins (ABP19/20) from peach: significant peptide sequence similarity with germin-like proteins. Plant Cell Physiol 39(5):492–499

    Article  CAS  PubMed  Google Scholar 

  • Oldroyd GED, Downie JA (2004) Calcium, kinases and nodulation signalling in legumes. Nat Rev Mol Cell Biol. doi:10.1038/nrm1424

    PubMed  Google Scholar 

  • Parádi I, Bratek Z, Lang F (2003) Influence of arbuscular mycorrhiza and phosphorus supply on polyamine content, growth and photosynthesis of Plantago lanceolata. Biol Plant. doi:10.1023/A:1024819729317

    Google Scholar 

  • Parniske M (2004) Molecular genetics of the arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 7(4):414–421. doi:10.1016/j.pbi.2004.05.011

    Article  CAS  PubMed  Google Scholar 

  • Peng JL, Dong HS, Dong HP, Delaney TP, Bonasera JM, Beer SV (2003) Harpin-elicited hypersensitive cell death and pathogen resistance require the NDR1 and EDS1 genes. Physiol Mol Plant Pathol. doi:10.1016/S0885-5765(03)00078-X

    Google Scholar 

  • Perkins DN, Pappin DJ, Creasy DM, Cottrell JS (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis. doi:10.1002/(SICI)1522-2683(19991201

    PubMed  Google Scholar 

  • Peterson RL, Massicotte HB, Melville LH. (2004) Mycorrhizas: Anatomy and Cell Biology. NRC Research Press. pp. 173

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Brit Mycol Soc 55(1):158–161

    Article  Google Scholar 

  • Porcel R, Ruiz-Lozano JM (2004) Arbuscular mycorrhizal influence on leaf water potential, solute accumulation, and oxidative stress in soybean plants subjected to drought stress. J Exp Bot. doi:10.1093/jxb/erh188

    PubMed  Google Scholar 

  • Porcel R, Aroca R, Cano C, Bago A, Ruiz-Lozano JM (2006) Identification of a gene from the arbuscular mycorrhizal fungus Glomus intraradices encoding for a 14-3-3 protein that is up-regulated by drought stress during the AM symbiosis. Microb Ecol. doi:10.1007/s00248-006-9015-2

    PubMed  Google Scholar 

  • Pozo MJ, Azcón-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol. doi:10.1016/j.pbi.2007.05.004

    PubMed  Google Scholar 

  • Quintana-Rodríguez E, Morales-Vargas AT, Molina-Torres J, Adame-Álvarez RM, Acosta-Gallegos JA, Heil M (2015) Plant volatiles cause direct, induced and associational resistance in common bean to the fungal pathogen Colletotrichum lindemuthianum. J Ecol. doi:10.1111/1365-2745.12340

    Google Scholar 

  • Raab T, López-Ráez JA, Klein D, Caballero JL, Moyano E, Schwab W, Muñoz-Blanco J (2006) FaQR, required for the biosynthesis of the strawberry flavor compound 4-hydroxy-2,5-dimethyl-3(2H)-furanone, encodes an enone oxidoreductase. Plant Cell. doi:10.1105/tpc.105.039784

    PubMed  PubMed Central  Google Scholar 

  • Robb J, Lee B, Nazar RN (2007) Gene suppression in a tolerant tomato-vascular pathogen interaction. Planta. doi:10.1007/s00425-007-0482-6

    PubMed  Google Scholar 

  • Roberts MR, Bowles DJ (1999) Fusicoccin, 14-3-3 proteins, and defense responses in tomato plants. Plant Physiol 119(4):1243–1250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roberts MR, Salinas J, Collinge DB (2002) 14-3-3 proteins and the response to abiotic and biotic stress. Plant Mol Biol. doi:10.1023/A:1021261614491

    Google Scholar 

  • Samra A, Dumas-Gaudot E, Gianinazzi S (1997) Detection of symbiosis-related polypeptides during the early stages of the establishment of arbuscular mycorrhiza between Glomus mosseae and Pisum sativum roots. New Phytol. doi:10.1046/j.1469-8137.1997.00695.x

    Google Scholar 

  • Sánchez-Rocha S, Vargas-Luna M, Gutiérrez- Juárez G, Huerta Franco R, Madueño L, Olalde-Portugal V (2005) Oxygen evolution from tomato (C3) plants with and without mycorrhiza: open photoacoustic cell measurement and statistical analysis. J Phys IV France. doi:10.1051/jp4:2005125185

    Google Scholar 

  • Schutzendubel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot. doi:10.1093/jexbot/53.372.1351

    PubMed  Google Scholar 

  • Shevchenko A, Wilm M, Vorm O, Mann M (1996) Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal Chem. doi:10.1021/ac950914h

    PubMed  Google Scholar 

  • Shevchenko A, Sunyaev S, Loboda A, Shevchenko A, Bork P, Ens W, Standing KG (2001) Charting the proteomes of organisms with unsequenced genomes by MALDI-quadrupole time-of-flight mass spectrometry and BLAST homology searching. Anal Chem. doi:10.1021/ac0013709

    PubMed  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, London, p 605

    Google Scholar 

  • Strack D, Fester T, Hause B, Schliemann W, Walter MH (2003) Arbuscular mycorrhiza: biological, chemical, and molecular aspects. J Chem Ecol. doi:10.1023/A:1025695032113

    PubMed  Google Scholar 

  • Talukdar T, Gorecka KM, de Carvalho-Niebel F, Downie JA, Cullimore J, Pikula S (2009) Annexins - calcium- and membrane-binding proteins in the plant kingdom. potential role in nodulation and mycorrhization in Medicago truncatula. Acta Biochim Pol 56(2):199–210

    CAS  PubMed  Google Scholar 

  • Taylor J, Harrier LA (2003) Expression studies of plant genes differentially expressed in leaf and root tissues of tomato colonised by the arbuscular mycorrhizal fungus Glomus mosseae. Plant Mol Biol. doi:10.1023/A:1022341422133

    Google Scholar 

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

    PubMed  Google Scholar 

  • Valot B, Negroni L, Zivy M, Gianinazzi S, Dumas-Gaudot E (2006) A mass spectrometric approach to identify arbuscular mycorrhiza-related proteins in root plasma membrane fractions. Proteomics. doi:10.1002/pmic.200500403

    PubMed  Google Scholar 

  • Wang Y, Ohara Y, Nakayashiki H, Tosa Y, Mayama S (2005) Microarray analysis of the gene expression profile induced by the endophytic plant growth-promoting rhizobacteria, Pseudomonas fluorescens FPT9601-T5 in Arabidopsis. Mol Plant Microbe Interact. doi:10.1094/MPMI-18-0385

    Google Scholar 

  • Wang X, Li M, Zhang J, Zhang Y, Zhang G, Wang J (2007) Identification of a key functional region in harpins from Xanthomonas that suppresses protein aggregation and mediates harpin expression in E. coli. Mol Biol Rep. doi:10.1007/s11033-006-9034-6

    Google Scholar 

  • Wang XY, Song CF, Miao WG, Ji ZL, Wang X, Zhang Y, Zhang JH, Hu JS, Borth W, Wang JS (2008) Mutations in the N-terminal coding region of the harpin protein Hpa1 from Xanthomonas oryzae cause loss of hypersensitive reaction induction in tobacco. Appl Microbiol Biotechnol. doi:10.1007/s00253-008-1651-7

    Google Scholar 

  • Whipps JM (2004) Prospects and limitations for mycorrhizas in biocontrol of root pathogens. Can J Bot. doi:10.1139/b04-082

    Google Scholar 

  • Wipf D, Mongelard G, Tuinen D, Gutierrez L, Casieri L (2014) Transcriptional responses of Medicago truncatula upon sulfur deficiency stress and arbuscular mycorrhizal symbiosis. Front Plant Sci 5:680. doi:10.3389/fpls.2014.00680

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu QS, Xia RX (2006) Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of citrus under well-watered and water stress conditions. J Plant Physiol. doi:10.1016/j.jplph.2005.04.024

    Google Scholar 

  • Yang B, Shiping T, Jie Z, Yonghong G (2005) Harpin induces local and systemic resistance against Trichothecium roseum in harvested Hami melons. Postharvest Biol Tec. doi:10.1016/j.postharvbio.2005.05.012

    Google Scholar 

  • Zou YN, Huang YM, Wu QS, He XH (2015) Mycorrhiza-induced lower oxidative burst is related with higher antioxidant enzyme activities, net H2O2effluxes, and Ca2+ influxes in trifoliate orange roots under drought stress. Mycorrhiza 25:143. doi:10.1007/s00572-014-0598-z

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors would like to thank Alicia Chagolla of the Proteomics service lab at CINVESTAV-Irapuato, Gto., Mexico. P-GLI would like to thank CONACYT-Mexico for the scholarship support. This project was funded by SIP-IPN (20131537), CECYT-SINALOA (2007, 2008 and 2009), and CONACYT CB-2008-01-102237. The authors thank Dr. Brandon Loveall of Improvence for English proofreading of the manuscript.

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LIPG participated in the experimental design, conducted most of the experimental work (including 2D-electrophoresis and peptide sequence analyses) and drafted the manuscript. JALV participated in image analysis of the two-dimensional gel using the PD-Quest software, and in critical revision of the manuscript. IEMM, HGF and SCL participated in the experimental work and in critical revision of the manuscript. MLM and SMG conceived the study and participated in its design and coordination, as well as drafting of the manuscript. All authors have read and approved the final manuscript.

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Correspondence to S. Medina-Godoy.

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Peinado-Guevara, L.I., López-Meyer, M., López-Valenzuela, J.A. et al. Comparative proteomic analysis of leaf tissue from tomato plants colonized with Rhizophagus irregularis . Symbiosis 73, 93–106 (2017). https://doi.org/10.1007/s13199-016-0470-3

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