ABC> Vol.3 No.1, February 2013

Proteomic studies of arbuscular mycorrhizal associations

DownloadDownload as PDF (Size:163KB) Full-Text HTML PP. 48-58   DOI: 10.4236/abc.2013.31007


Arbuscular mycorrhizal (AM) fungi are soil-borne microorganisms forming mutualistic associations with the vast majority of land plants, including most agricultural relevant crops. In this association the plant provides the fungus with plant photosynthates allowing it to complete its life cycle, while the fungus provides the plant with mineral nutrients, mainly phosphorus and can also help the plant to tolerate biotic and abiotic stresses. In regard to these benefits there is growing interest on the use of AM fungi to improve productivity and sustainability in agricultural systems. AM fungi and their interactions with plants have been extensively studied using proteomic techniques, but some difficulties have been faced. 1) Little is known about the AM fungal typical protein repertoire because it is currently impossible to grow AM fungi in pure axenic cultures; 2) Plant tissues often contain high amounts of interfering substances that make protein extraction for the study of AM interactions a difficult procedure; 3) Most nutrient exchanges between AM fungi and their host plants involve participation of membrane proteins, still poorly resolved in most separation techniques. Finally, 4) the formation of the arbuscule is an asynchronous process, making it difficult to distinguish which proteins are essential in the early or late stages of AM associations. In this review we present a historical summary of how these difficulties have been overcome by technological advances in proteomics and we discuss current and future trends in the study of the proteins involved in AM interactions.


Cite this paper

Couto, M. , Lovato, P. , Wipf, D. and Dumas-Gaudot, E. (2013) Proteomic studies of arbuscular mycorrhizal associations. Advances in Biological Chemistry, 3, 48-58. doi: 10.4236/abc.2013.31007.


[1] Smith, S.E. and Smith, F.A. (1990) Structure and function of the interfaces in biotrophic symbioses as they relate to nutrient transport. New Phytologist, 114, 1-38. doi:10.1111/j.1469-8137.1990.tb00370.x
[2] Harrier, L.A. and Watson, C.A. (2004) The potential role of arbuscular mycorrhizal (AM) fungi in the bioprotection of plants against soil-borne pathogens in organic and/ or other sustainable farming systems. Pest Management Science, 60, 149-157. doi:10.1002/ps.820
[3] Azcón-Aguilar, C. and Barea, J.M. (1997) Applying mycorrhiza biotechnology to horticulture: Significance and potentials. Scientia Horticulturae, 68, 1-24. doi:10.1016/S0304-4238(96)00954-5
[4] Berta, G., Fusconi, A. and Trotta, A. (1993) VA mycorrhizal infection and the morphology and function of root systems. Environmental and Experimental Botany, 33, 159-173. doi:10.1016/0098-8472(93)90063-L
[5] Smith, S.E. and Gianinazzipearson, V. (1988) Physiological Interactions between Symbionts in Vesicular Arbuscular Mycorrhizal Plants. Annual Review of Plant Physiology and Plant Molecular Biology, 39, 221-244. doi:10.1146/annurev.pp.39.060188.001253
[6] Smith, F.W., Rae, A.L. and Hawkesford, M.J. (2000) Molecular mechanisms of phosphate and sulphate transport in plants. Biochimica et Biophysica Acta-Biomem branes, 1465, 236-245.
[7] Bago, B., Donaire, J.P. and Azcón-Aguilar, C. (1997) ATPase activities of root microsomes from mycorrhizal sunflower (Helianthus annuus) and onion (Allium cepa) plants. New Phytologist, 136, 305-311. doi:10.1046/j.1469-8137.1997.00741.x
[8] Bago, B., Pfeffer, P.E. and Shachar-Hill, Y. (2000) Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiology, 124, 949-957. doi:10.1104/pp.124.3.949
[9] Bago, B., et al. (2002) Tracking metabolism and imaging transport in arbuscular mycorrhizal fungi. Metabolism and transport in AM fungi. Plant and Soil, 244, 189-197. doi:10.1023/A:1020212328955
[10] Pfeffer, P.E., et al. (1999) Carbon uptake and the meta bolism and transport of lipids in an arbuscular mycorrhiza. Plant Physiology, 120, 587-598. doi:10.1104/pp.120.2.587
[11] Azcón-Aguilar, C. and Barea, J.M. (1996) Arbuscular mycorrhizas and biological control of soil-borne plant pathogens—An overview of the mechanisms involved. Mycorrhiza, 6, 457-464. doi:10.1007/s005720050147
[12] Abbaspour, H., et al. (2012) Tolerance of Mycorrhiza infected Pistachio (Pistacia vera L.) seedling to drought stress under glasshouse conditions. Journal of Plant Physiology, 169, 704-709. doi:10.1016/j.jplph.2012.01.014
[13] Boomsma, C.R. and Vyn, T.J. (2008) Maize drought tolerance: Potential improvements through arbuscular mycorrhizal symbiosis? Field Crops Research, 108, 14 31. doi:10.1016/j.fcr.2008.03.002
[14] Giri, B., Kapoor, R. and Mukerji, K.G. (2007) Improved tolerance of Acacia nilotica to salt stress by arbuscular mycorrhiza, Glomus fasciculatum may be partly related to elevated K/Na ratios in root and shoot tissues. Microbial Ecology, 54, 753-760. doi:10.1007/s00248-007-9239-9
[15] Langenfeld-Heyser, R., et al. (2007) Paxillus involutus mycorrhiza attenuate NaCl-stress responses in the salt sensitive hybrid poplar Populus (X) canescens. Mycorrhiza, 17, 121-131. doi:10.1007/s00572-006-0084-3
[16] Al-Karaki, G., McMichael, B. and Zak, J. (2004) Field response of wheat to arbuscular mycorrhizal fungi and drought stress. Mycorrhiza, 14, 263-269. doi:10.1007/s00572-003-0265-2
[17] Ruiz-Lozano, J.M., et al. (2009) Exogenous ABA accentuates the differences in root hydraulic properties between mycorrhizal and non mycorrhizal maize plants through regulation of PIP aquaporins. Plant Molecular Biology, 70, 565-579. doi:10.1007/s11103-009-9492-z
[18] Hildebrandt, U., Regvar, M. and Bothe, H. (2007) Arbus cular mycorrhiza and heavy metal tolerance. Phytochemistry, 68, 139-146. doi:10.1016/j.phytochem.2006.09.023
[19] Davies, F.T., et al. (2001) Mycorrhizal fungi enhance accumulation and tolerance of chromium in sunflower (Helianthus annuus). Journal of Plant Physiology, 158, 777-786. doi:10.1078/0176-1617-00311
[20] Christie, P., Li, X.L. and Chen, B.D. (2004) Arbuscular mycorrhiza can depress translocation of zinc to shoots of host plants in soils moderately polluted with zinc. Plant and Soil, 261, 209-217. doi:10.1023/B:PLSO.0000035542.79345.1b
[21] Lecomte, J., St-Arnaud, M. and Hijri, M. (2011) Isolation and identification of soil bacteria growing at the expense of arbuscular mycorrhizal fungi. FEMS Microbiology Letters, 317, 43-51. doi:10.1111/j.1574-6968.2011.02209.x
[22] Wang, Y.Y., et al. (2008) Diversity and infectivity of arbuscular mycorrhizal fungi in agricultural soils of the Sichuan Province of mainland China. Mycorrhiza, 18, 59-68. doi:10.1007/s00572-008-0161-x
[23] Gange, A.C., Lindsay, D.E. and Ellis, L.S. (1999) Can arbuscular mycorrhizal fungi be used to control the undesirable grass Poa annua on golf courses? Journal of Applied Ecology, 36, 909-919. doi:10.1046/j.1365-2664.1999.00456.x
[24] Schü?ler, A., Schwarzott, D. and Walker, C. (2001) A new fungal phylum, the Glomeromycota: Phylogeny and evolution. Mycological Research, 105, 1413-1421. doi:10.1017/S0953756201005196
[25] Dassi, B., et al. (1999) Different polypeptide profiles from tomato roots following interactions with arbuscular mycorrhizal (Glomus mosseae) or pathogenic (Phytoph thora parasitica) fungi. Symbiosis, 26, 65-77.
[26] Dumas-Gaudot, E., et al. (2004) Proteomics as a way to identify extra-radicular fungal proteins from Glomus intraradices—RiT-DNA carrot root mycorrhizas. Fems Microbiology Ecology, 48, 401-411. doi:10.1016/j.femsec.2004.02.015
[27] Ferrol, N., et al. (2004) Genomics of arbuscular mycorrhizal fungi. In: Dilip, K.A. and George, G.K., Eds., Applied Mycology and Biotechnology, Elsevier, New York, 379-403.
[28] Young, J.P.W. (2012) A molecular guide to the taxonomy of arbuscular mycorrhizal fungi. New Phytologist, 193, 823-826. doi:10.1111/j.1469-8137.2011.04029.x
[29] Dumas, E., Gianinazzi-Pearson, V. and Gianinazzi, S. (1989) Production of new soluble proteins during VA endomycorrhiza formation. Agriculture, Ecosystems and Environment, 29, 111-114. doi:10.1016/0167-8809(90)90264-E
[30] Dumas-Gaudot, E., et al. (1992) Chitinase, chitosanase and β-1,3-glucanase activities in Allium and Pisum roots colonized by Glomus species. Plant Science, 84, 17-24. doi:10.1016/0168-9452(92)90203-X
[31] G?rg, A., Weiss, W. and Dunn, M.J. (2004) Current two dimensional electrophoresis technology for proteomics. Proteomics, 4, 3665-3685. doi:10.1002/pmic.200401031
[32] Hochstrasser, D.F., et al. (1988) Methods for increasing the resolution of two-dimensional protein electrophoresis. Analytical Biochemistry, 173, 424-435. doi:10.1016/0003-2697(88)90209-6
[33] Dumas-Gaudot, E., et al. (1994) Chitinase isoforms in roots of various pea genotypes infected with arbuscular mycorrhizal fungi. Plant Science, 99, 27-37. doi:10.1016/0168-9452(94)90117-1
[34] Wu, B., et al. (2011) Study of metal-containing proteins in the roots of Elsholtzia splendens using LA-ICP-MS and LC-tandem mass spectrometry. International Journal of Mass Spectrometry, 307, 85-91. doi:10.1016/j.ijms.2011.01.018
[35] Pozo, M.A.J., et al. (1999) β-1,3-Glucanase activities in tomato roots inoculated with arbuscular mycorrhizal fungi and/or Phytophthora parasitica and their possible involvement in bioprotection. Plant Science, 141, 149 157. doi:10.1016/S0168-9452(98)00243-X
[36] Arines, J., Palma, J.M. and Vilari?o, A. (1993) Comparison of protein patterns in non-mycorrhizal and vesi cular-arbuscular mycorrhizal roots of red clover. New Phytologist, 123, 763-768. doi:10.1111/j.1469-8137.1993.tb03787.x
[37] Arines, J., et al. (1994) Protein patterns and superoxide dismutase activity in non-mycorrhizal and arbuscular mycorrhizal Pisum sativum L. plants. Plant and Soil, 166, 37-45. doi:10.1007/BF02185479
[38] Slezack, S., et al. (2001) Purification and partial amino acid sequencing of a mycorrhiza-related chitinase isoform from Glomus mosseae-inoculated roots of Pisum sativum L. Planta, 213, 781-787. doi:10.1007/s004250100551
[39] Maldonado, A.M., et al. (2008) Evaluation of three different protocols of protein extraction for Arabidopsis thaliana leaf proteome analysis by two-dimensional electrophoresis. Journal of Proteomics, 71, 461-472. doi:10.1016/j.jprot.2008.06.012
[40] Faurobert, M., Pelpoir, E. and Cha?b, J. (2006) Phenol extraction of proteins for proteomic studies of recalcitrant plant tissues. In: Zivy, M., Ed., Plant Proteomics. Methods and Protocols, Humana Press, Totowa, 9-14. doi:10.1385/1-59745-227-0:9
[41] Carpentier, S.C., et al. (2005) Preparation of protein extracts from recalcitrant plant tissues: An evaluation of different methods for two-dimensional gel electrophoresis analysis. Proteomics, 5, 2497-2507. doi:10.1002/pmic.200401222
[42] Bona, E., et al. (2010) Proteomic analysis of Pteris vittata fronds: Two arbuscular mycorrhizal fungi differentially modulate protein expression under arsenic contamination. Proteomics, 10, 3811-3834. doi:10.1002/pmic.200900436
[43] Schuster, A.M. and Davies, E. (1983) Ribonucleic acid and protein metabolism in pea epicotyls I. The aging process. Plant Physiology, 73, 809-816. doi:10.1104/pp.73.3.809
[44] Hurkman, W.J. and Tanaka, C.K. (1986) Solubilization of plant membrane-proteins for analysis by two-dimensional gel-electrophoresis. Plant Physiology, 81, 802-806. doi:10.1104/pp.81.3.802
[45] Saravanan, R.S. and Rose, J.K.C. (2004) A critical evaluation of sample extraction techniques for enhanced proteomic analysis of recalcitrant plant tissues. Proteomics, 4, 2522-2532. doi:10.1002/pmic.200300789
[46] Jellouli, N., et al. (2010) Evaluation of protein extraction methods for vitis vinifera leaf and root proteome analysis by two-dimensional electrophoresis. Journal of Integra tive Plant Biology, 52, 933-940. doi:10.1111/j.1744-7909.2010.00973.x
[47] Simoneau, P., et al. (1994) Accumulation of new polypeptides in Ri T-DNA-transformed roots of tomato (Lycopersicon esculentum) during the development of vesicular-arbuscular mycorrhizae. Applied and Environ mental Microbiology, 60, 1810-1813.
[48] Samra, A., Dumas-Gaudot, E. and Gianinazzi, S. (1997) Detection of symbiosis-related polypeptides during the early stages of the establishment of arbuscular mycor rhiza between Glomus mosseae and Pisum sativum roots. New Phytologist, 135, 711-722. doi:10.1046/j.1469-8137.1997.00695.x
[49] Aloui, A., et al. (2011) Arbuscular mycorrhizal symbiosis elicits shoot proteome changes that are modified during cadmium stress alleviation in Medicago truncatula. BMC Plant Biology, 11, 75. doi:10.1186/1471-2229-11-75
[50] Bona, E., et al. (2011) Proteomic analysis as a tool for investigating arsenic stress in Pteris vittata roots colonized or not by arbuscular mycorrhizal symbiosis. Jour nal of Proteomics, 74, 1338-1350. doi:10.1016/j.jprot.2011.03.027
[51] Cangahuala-Inocente, G.C., et al. (2011) Arbuscular mycorrhizal symbiosis elicits proteome responses oppo site 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
[52] Dumas-Gaudot, E., et al. (2004) A technical trick for studying proteomics in parallel to transcriptomics in symbiotic root-fungus interactions. Proteomics, 4, 451 453. doi:10.1002/pmic.200300627
[53] Dumas-Gaudot, E., et al. (2009) Functional genomic of arbuscular mycorrhizal symbiosis: Why and how using proteomics symbiotic fungi. In: Varma, A. and Kharkwal, A.C. Ed., Springer, Berlin, 243-274.
[54] Aloui, A., et al. (2009) On the mechanisms of cadmium stress alleviation in Medicago truncatula by arbuscular mycorrhizal symbiosis: A root proteomic study. Proteo mics, 9, 420-433. doi:10.1002/pmic.200800336
[55] Recorbet, G., et al. (2010) Identification of in planta expressed arbuscular mycorrhizal fungal proteins upon comparison of the root proteomes of Medicago truncatula colonised with two Glomus species. Fungal Genetics and Biology, 47, 608-618. doi:10.1016/j.fgb.2010.03.003
[56] Xiong, J., et al. (2011) Simultaneous isolation of DNA, RNA, and protein from Medicago truncatula L. Elec trophoresis, 32, 321-330. doi:10.1002/elps.201000425
[57] Wang, W., et al. (2003) Protein extraction for two dimensional electrophoresis from olive leaf, a plant tissue containing high levels of interfering compounds. Electro phoresis, 24, 2369-2375. doi:10.1002/elps.200305500
[58] Wang, W., et al. (2006) A universal and rapid protocol for protein extraction from recalcitrant plant tissues for proteomic analysis. Electrophoresis, 27, 2782-2786. doi:10.1002/elps.200500722
[59] Cox, J. and Mann, M. (2011) Quantitative, high-resolution proteomics for data-driven systems biology. Annual Review of Biochemistry, 80, 273-299.
[60] Yates, J.R., Ruse, C.I. and Nakorchevsky, A. (2009) Proteomics by mass spectrometry: Approaches, advances and applications. Annual Review of Biomedical Enginee ring, 11, 49-79. doi:10.1146/annurev-bioeng-061008-124934
[61] Harrison, M.J. (9-14 August 1998) Biotrophic interfaces and nutrient transport in plant fungal symbioses. 11th International Workshop on Plant Membrane Biology, Cambridge.
[62] Gianinazzi-Pearson, V. (1996) Plant cell responses to arbuscular mycorrhizal fungi: Getting to the roots of the symbiosis. Plant Cell, 8, 1871-1883.
[63] Bonfante, P. and Perotto, S. (1995) Tansley-review No-82—Strategies of arbuscular mycorrhizal fungi when infecting host plants. New Phytologist, 130, 3-21. doi:10.1111/j.1469-8137.1995.tb01810.x
[64] Javot, H., et al. (2007) A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sci ences of the United States of America, 104, 1720-1725. doi:10.1073/pnas.0608136104
[65] Gianinazzi-Pearson, V., et al. (1991) Enzymatic studies on the metabolism of vesicular arbuscular mycorrhizas. 5. Is H+-atpase a component of atp-hydrolyzing enzyme activities in plant fungus interfaces. New Phytologist, 117, 61-74. doi:10.1111/j.1469-8137.1991.tb00945.x
[66] Smith, S.E. and Read, D.J. (1997) Uptake, translocation and transfer of nutrients in mycorrhizal symbioses. Myco rrhizal Symbiosis, 2nd Edition, Academic Press, London, 379. doi:10.1016/B978-012652840-4/50015-2
[67] Ramos, A.C., et al. (2009) Arbuscular mycorrhizal fungi induce differential activation of the plasma membrane and vacuolar H+ pumps in maize roots. Mycorrhiza, 19, 69-80. doi:10.1007/s00572-008-0204-3
[68] Harrison, M.J., Dewbre, G.R. and Liu, J. (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell, 14, 2413-2429. doi:10.1105/tpc.004861
[69] Pumplin, N., et al. (2012) Polar localization of a symbiosis-specific phosphate transporter is mediated by a transient reorientation of secretion. Proceedings of the National Academy of Sciences of the United States of America, 109, E665-E672.
[70] Guether, M., et al. (2009) A mycorrhizal-specific am monium transporter from Lotus japonicus acquires nitro gen released by arbuscular mycorrhizal fungi. Plant Physiology, 150, 73-83. doi:10.1104/pp.109.136390
[71] Kobae, Y., et al. (2010) Localized expression of arbu scular mycorrhiza-inducible ammonium transporters in soybean. Plant and Cell Physiology, 51, 1411-1415. doi:10.1093/pcp/pcq099
[72] Doidy, J., et al. (2012) Sugar transporters in plants and in their interactions with fungi. Trends in Plant Science, 17, 413-422. doi:10.1016/j.tplants.2012.03.009
[73] Harrison, M.J. (1997) The arbuscular mycorrhizal symbiosis: An underground association. Trends in Plant Science, 2, 54-60. doi:10.1016/S1360-1385(97)82563-0
[74] Boldt, K., et al. (2011) Photochemical processes, carbon assimilation and RNA accumulation of sucrose trans porter genes in tomato arbuscular mycorrhiza. Journal of Plant Physiology, 168, 1256-1263. doi:10.1016/j.jplph.2011.01.026
[75] Helber, N., et al. (2011) A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus Glomus sp is crucial for the symbiotic relationship with plants. Plant Cell, 23, 3812-3823. doi:10.1105/tpc.111.089813
[76] Cameron, D.D., et al. (2008) Giving and receiving: Measuring the carbon cost of mycorrhizas in the green orchid, Goodyera repens. New Phytologist, 180, 176-184. doi:10.1111/j.1469-8137.2008.02533.x
[77] Guether, M., et al. (2011) LjLHT1.2-a mycorrhiza inducible plant amino acid transporter from Lotus japonicus. Biology and Fertility of Soils, 47, 925-936. doi:10.1007/s00374-011-0596-7
[78] Talbot, J.M. and Treseder, K.K. (2010) Controls over mycorrhizal uptake of organic nitrogen. Pedobiologia, 53, 169-179. doi:10.1016/j.pedobi.2009.12.001
[79] Benabdellah, K., Azcón-Aguilar, C. and Ferrol, N. (1998) Soluble and membrane symbiosis-related polypeptides associated with the development of arbuscular mycorr hizas in tomato (Lycopersicon esculentum). New Phytologist, 140, 135-143. doi:10.1046/j.1469-8137.1998.00255.x
[80] Benabdellah, K., Azcon-Aguilar, C. and Ferrol, N. (2000) Alterations in the plasma membrane polypeptide pattern of tomato roots (Lycopersicon esculentum) during the development of arbuscular mycorrhiza. Journal of Expe rimental Botany, 51, 747-754. doi:10.1093/jexbot/51.345.747
[81] Colditz, F., et al. (2004) Proteomic approach: Identi fication of Medicago truncatula proteins induced in roots after infection with the pathogenic oomycete Aphano myceseuteiches. Plant Molecular Biology, 55, 109-120. doi:10.1007/s11103-004-0499-1
[82] Valot, B., Gianinazzi, S. and Eliane, D.G. (2004) Sub cellular proteomic analysis of a Medicago truncatula root microsomal fraction. Phytochemistry, 65, 1721-1732. doi:10.1016/j.phytochem.2004.04.010
[83] Valot, B., et al. (2005) Identification of membrane associated proteins regulated by the arbuscular mycorrhi zal symbiosis. Plant Molecular Biology, 59, 565-580. doi:10.1007/s11103-005-8269-2
[84] Valot, B., et al. (2006) A mass spectrometric approach to identify arbuscular mycorrhiza-related proteins in root plasma membrane fractions. Proteomics, 6, S145-S155. doi:10.1002/pmic.200500403
[85] Abdallah, C., et al. (2012) Optimization of iTRAQ label ling coupled to OFFGEL fractionation as a proteomic workflow to the analysis of microsomal proteins of Medi cago truncatula roots. Proteome Science, 10, 37. doi:10.1186/1477-5956-10-37
[86] Bécard, G. and Fortin, J.A. (1988) Early events of vesicular-arbuscular mycorrhiza formation on Ri T-DNA transformed roots. New Phytologist, 108, 211-218. doi:10.1111/j.1469-8137.1988.tb03698.x
[87] Recorbet, G., et al. (2009) Fungal proteins in the extra radical phase of arbuscular mycorrhiza: A shotgun prote omic picture. New Phytologist, 181, 248-260. doi:10.1111/j.1469-8137.2008.02659.x
[88] Daher, Z., et al. (2010) Proteomic analysis of Medicago truncatula root plastids. Proteomics, 10, 2123-2137. doi:10.1002/pmic.200900345
[89] Dumas-Gaudot, E., et al. (1994) Changes in polypeptide patterns in tobacco roots colonized by two Glomus species. Mycorrhiza, 4, 215-221. doi:10.1007/BF00206783
[90] Bestel-Corre, G., et al. (2002) Proteome analysis and identification of symbiosis-related proteins from Medi cago truncatula Gaertn. by two-dimensional electropho resis and mass spectrometry. Electrophoresis, 23, 122 137. doi:10.1002/1522-2683(200201)23:1<122::AID-ELPS122>3.0.CO;2-4
[91] Amiour, N., et al. (2006) Mutations in DMI3 and SUNN modify the appressorium-responsive root proteome in arbuscular mycorrhiza. Molecular Plant-Microbe Interac tions, 19, 988-997. doi:10.1094/MPMI-19-0988
[92] Schenkluhn, L., et al. (2010) Differential gel electro phoresis (DIGE) to quantitatively monitor early symbiosis and pathogenesis-induced changes of the Medicago truncatula root proteome. Journal of Proteomics, 73, 753-768. doi:10.1016/j.jprot.2009.10.009
[93] Genre, A., et al. (2005) Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago trun catula root epidermal cells before infection. Plant Cell, 17, 3489-3499. doi:10.1105/tpc.105.035410
[94] Genre, A., et al. (2008) Prepenetration apparatus assem bly precedes and predicts the colonization patterns of arbuscular mycorrhizal fungi within the root cortex of both Medicago truncatula and Daucus carota. Plant Cell, 20, 1407-1420. doi:10.1105/tpc.108.059014
[95] Gaude, N., et al. (2012) Cell type-specific protein and transcription profiles implicate periarbuscular membrane synthesis as an important carbon sink in the mycorrhizal symbiosis. Plant Signaling and Behavior, 7, 461-464. doi:10.4161/psb.19650
[96] ünlü, M., Morgan, M.E. and Minden, J.S. (1997) Difference gel electrophoresis: A single gel method for detecting changes in protein extracts. Electrophoresis, 18, 2071-2077. doi:10.1002/elps.1150181133
[97] Tisserant, E., et al. (2012) The transcriptome of the arbu scular mycorrhizal fungus Glomus intraradices (DAOM 197198) reveals functional tradeoffs in an obligate symbiont. New Phytologist, 193, 755-769. doi:10.1111/j.1469-8137.2011.03948.x

comments powered by Disqus

Copyright © 2014 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.