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Organelles Proteomics


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Proteomic Analysis of Soybean Leaves in a Compatible and an Incompatible Interaction with Phakopsora Pachyrhizi

Mateus Rodrigues Pereira
  • Departamento de Biologia Geral, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil
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/ Bianca Castro Gouvêa
  • Departamento de Biologia Geral, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil
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/ Francismar Corrêa Marcelino-Guimarães / Humberto Josué de Oliveira Ramos
  • Instituto de Biotecnologia Aplicada à Agropecuária (BIOAGRO), Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil
  • Departamento de Bioquímica e Biologia Molecular, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil
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/ Maurilio Alves Moreira
  • Instituto de Biotecnologia Aplicada à Agropecuária (BIOAGRO), Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil
  • Departamento de Bioquímica e Biologia Molecular, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil
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/ Everaldo Gonçalves de Barros
  • Corresponding author
  • Departamento de Biologia Geral, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil
  • Instituto de Biotecnologia Aplicada à Agropecuária (BIOAGRO), Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil
  • Programa de Pós-Graduação em Ciências Genômicas e Biotecnologia, Universidade Católica de Brasília, Brasília, DF, Brazil
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  • Other articles by this author:
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Published Online: 2013-11-07 | DOI: https://doi.org/10.2478/orpr-2013-0004

Abstract

Asian soybean rust (ASR), which is incited by the fungus Phakopsora pachyrhizi, is considered one of the most aggressive diseases to the soybean culture. There are no commercial cultivars immune to the pathogen and the control measure currently used is the application of fungicides that harms the environment and increases production costs. For a better understanding of the host’s response to the pathogen at the molecular level, two soybean genotypes were analyzed (PI561356, resistant to ASR and Embrapa 48, susceptible) at 72 hours and 192 hours after inoculation with spores of P. pachyrhizi. Leaf protein profiles of the plants were compared by two-dimensional electrophoresis associated with mass spectrometry (MS). Twenty-two protein spots presented different levels when the two treatments were compared (inoculated vs. non-inoculated). From those, twelve proteins were identified by MS analysis. Some of them are involved in metabolic pathways related to plant defense against pathogens, as in the case of carbonic anhydrase, 1-deoxy-D-xylulose- 5-phosphate reductoisomerase, fructose-bisphosphate aldolase and glutamine synthetase. The possible biochemical-physiological meanings of our findings are discussed.

Keywords: Glycine max; Phakopsora pachyrhizi; 2-D electrophoresis; MALDI; mass spectrometry

References

  • [1] Juliatti F.C., Polizel A.C., Balardin R.S., Vale F.X.R., Soybean rust: epidemiology and management for a re-emerging disease, Revis. Anu. Patol. Plantas, 2005, 13, 351-395. [In Port.]Google Scholar

  • [2] Sinclair J.B., Backman P.A., Compendium of Soybean Diseases, 3rd ed, American Phytopathological Society Press, St Paul, MN, 1989Google Scholar

  • [3] Silva V.A.S., Juliatti F.C., Silva L.A.S., Interaction between partial genetic resistance and fungicides in the control of asian soybean rust, Pesqui. Agropecu. Bras., 2007, 42 (9), 1261-1268. [in Port.]CrossrefGoogle Scholar

  • [4] Miles M.R., Bonde M.R., Nester S.E., Berner D.K., Frederick R.D., Hartman G.L., Characterizing resistance to Phakopsora pachyrhizi in soybean, Plant Dis., 2011, 95 (5), 577-581CrossrefGoogle Scholar

  • [5] Yorinori J.T., Paiva W.M., Frederick R.D., Costamilan L.M., Bertagnolli P.F., Hartman G.E., et al., Epidemics of soybean rust (Phakopsora pachyrhizi) in Brazil and Paraguay from 2001 to 2003, Plant Dis., 2005, 89, 675-677Google Scholar

  • [6] Hartman G.L., Hill C.B., Twizeyimana M., Miles M.R., Bandyopadhyay R., Interaction of soybean and Phakopsora pachyrhizi, the cause of soybean rust, CAB Rev. Perspect. Agric. Vet. Sci. Nutr. Nat. Resour., 2011, 6, doi:10.1079/ PAVSNNR20116025CrossrefGoogle Scholar

  • [7] Miles M.R., Frederick R.D., Hartman G.L., Evaluation of soybean germplasm for resistance to Phakopsora pachyrhizi, Online, Plant Health Progress, 2006 doi:10.1094/PHP-2006-0104-01-RS.CrossrefGoogle Scholar

  • [8] Soares R.M., Rubin S.A.L., Wielewicki A.P., Ozelame J.G., Fungicidas no controle da ferrugem asiática (Phakopsora pachyrhizi) e produtividade da soja, Cienc. Rural, 2004, 34(4), 1245-1247 [In Port.]CrossrefGoogle Scholar

  • [9] Yorinori J.T., Paiva W.M., Ferrugem da soja: Phakopsora pachyrhizi Sydow, Londrina: Embrapa Soja, 1 Folder, 2002 [In Port.]Google Scholar

  • [10] Zambolim L., Manejo Integrado da Ferrugem Asiática da Soja, In: Zambolim L. (Editor), Ferrugem Asiática da Soja, Ed. UFV, Viçosa, Cap.5, p. 73-98, 2006Google Scholar

  • [11] Yorinori J.T., Nunes Júnior J., Lazzarotto J.J., Ferrugem asiática da Soja no Brasil: Evolução, importância econômica e controle, Londrina: Embrapa Soja, 36p, 2004 (Documentos, 247).Google Scholar

  • [12] Cheng Y.W., Chan K.L., The breeding of rust resistant soybean Tainung 3, J. Taiwan Agr. Res., 1968, 17, 30-35Google Scholar

  • [13] Hidayat O.O., Somaatmadja S., Screening of soybean breeding lines for resistance to soybean rust (Phakopsora pachyrhizi Sydow), Soybean Rust Newsl., 1977, 1, 9-22Google Scholar

  • [14] Bromfield K.R., Hartwig E.E., Resistance to soybean rust and mode of inheritance, Crop Sci., 1980, 20, 254-255Google Scholar

  • [15] Hartwig E.E., Identification of a fourth major gene conferring resistance to soybean rust, Crop Sci., 1986, 26, 1135-1136CrossrefGoogle Scholar

  • [16] Garcia A., Calvo E.S., Kiihl R.A.S., Harada A., Hiromoto D.M., Vieira L.G., Molecular mapping of soybean rust (Phakopsora pachyrhizi) resistance genes: discovery of a novel locus and alleles, Theor. Appl. Genet., 2008, 117, 545-553CrossrefGoogle Scholar

  • [17] Li S., Smith J.R., Ray J.D., Frederick R.D., Identification of a new soybean rust resistance gene in PI 567102B, Theor. Appl. Genet., 2012, 125(1), 133-42CrossrefGoogle Scholar

  • [18] Bonde M.R., Nester S.E., Austin C.N., Stone C.L., Frederick R.D., Hartman G.L., et al., Evaluation of virulence of Phakopsora pachyrhizi and P. meibomiae isolates, Plant Dis., 2006, 90 (6), 708-716CrossrefGoogle Scholar

  • [19] Kim K., Unfried J.R., Hyten D.L., Frederick R.D., Hartman G.L., Nelson R.L., et al., Molecular mapping of soybean rust resistance in soybean accession PI 561356 and SNP haplotype analysis of the Rpp1 region in diverse germplasm, Theor. Appl. Genet., 2012, 125, 1339-1352 Google Scholar

  • [20] Goellner K., Loehrer M., Langenbach C., Conrath U.W.E., Koch E., Schaffrath U., Phakopsora pachyrhizi, the causal agent of Asian soybean rust, Mol. Plant Pathol., 2010, 11(2), 169-177CrossrefGoogle Scholar

  • [21] Wang Y., Yuan X., Hu H., Liu Y., Sun W., Shan Z., et al., Proteomic Analysis of Differentially Expressed Proteins in Resistant Soybean Leaves after Phakopsora pachyrhizi Infection, J. Phytopathol., 2012, 160, 554-560Google Scholar

  • [22] Panthee D.R., Yuan J.S., Wright D.L., Marois J.J., Mailhot D., Stewart Jr. C.N., Gene expression analysis in soybean in response to the causal agent of Asian soybean rust (Phakopsora pachyrhizi Sydow) in an early growth stage, Funct. Integr. Genomics, 2007, 7, 291-301CrossrefGoogle Scholar

  • [23] Panthee D.R., Marois J.J., Wright D.L., Narváez D., Yuan J.S., Stewart Jr. C.N., Differential expression of genes in soybean in response to the causal agent of Asian soybean rust (Phakopsora pachyrhizi Sydow) is soybean growth stage-specific, Theor. Appl. Genet., 2009, 118, 359-370CrossrefGoogle Scholar

  • [24] Mortel M.V. de, Recknor J.C., Graham M.A., Nettleton D., Dittman J.D., Nelson R.T., et al., Distinct biphasic mRNA changes in response to Asian soybean rust infection, Mol. Plant-Microbe Interact. (MPMI), 2007, 20, 887-899CrossrefGoogle Scholar

  • [25] Pham T.A., Miles M.R., Frederick R.D., Hill C.B., Hartman G.L., Differential responses of resistant soybean entries to isolates of Phakopsora pachyrhizi, Plant Dis., 2009, 93, 224-228Google Scholar

  • [26] Tremblay A., Hosseini P., Alkharouf N.W., Li S., Matthews B.F., Transcriptome analysis of a compatible response by Glycine max to Phakopsora pachyrhizi infection, Plant Sci., 2010, 179, 183-193Google Scholar

  • [27] Wilkins M.R., Sanchez J.C., Gooley A.A., Appel R.D., Humphery-Smith I., Hochstrasser D.F., et al., Progress with proteome projects: why all proteins expressed by genome should be identified and how to do it, Biotechnol. Genet. Eng. Rev., 1996, 13, 19-50CrossrefGoogle Scholar

  • [28] Wang W., Scali M., Vignani R., Spadafora A., Sensi E., Mazzuca S., et al., Protein extraction for two-dimensional electrophoresis from olive leaf, a plant tissue containing high levels of interfering compounds, Electrophoresis, 2003, 24 (14), 2369-2375CrossrefGoogle Scholar

  • [29] Bradford M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem., 1976, 72, 248-254CrossrefGoogle Scholar

  • [30] Anonymous: 2-D Electrophoresis: Principles and Methods - Handbook 80-6429-60AC, GE Healthcare, Piscataway 2004.Google Scholar

  • [31] Laemmli U.K., Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature, 1970, 227, 680-685Google Scholar

  • [32] Shevchenko A., Tomas H., Havlis J., Olsen J.V., Mann M., In-gel digestion for mass spectrometric characterization of proteins and proteomes, Nature, 2006, 1(6), 2856-2860Google Scholar

  • [33] Hill M.K., Lyon K.J., Lyon B.R., Identification of disease response genes expressed in Gossypium hirsutum upon infection with the wilt pathogen Verticillium dahliae, Plant Mol. Biol., 1999, 40, 289-296CrossrefGoogle Scholar

  • [34] Zhao C.J., Wang A.R., Shi Y.J., Wang L.Q., Liu W.D., Wang Z.H., et al., Identification of defense-related genes in rice responding to challenge by Rhizoctonia solani, Theor. Appl. Genet., 2008, 116, 501-516Google Scholar

  • [35] Liao M., Li Y., Wang Z., Identification of elicitor-responsive proteins in rice leaves by a proteomic approach, Proteomics, 2009, 9, 2809-2819CrossrefGoogle Scholar

  • [36] Brommer U.A., Thiele B.J., The translationally controlled tumour protein (TCTP), Int. J. Biochem. Cell Biol., 2004, 36, 379-385CrossrefGoogle Scholar

  • [37] Sage-Ono K., Ono M., Harada H., Kamada H., Dark-induced accumulation of mRNA for a homolog of translationally controlled tumor protein (TCTP) in Pharbitis, Plant Cell Physiol., 1998, 39, 357-360CrossrefGoogle Scholar

  • [38] Ermolayev V., Weschke W., Manteuffel R., Comparison of Alinduced gene expression in sensitive and tolerant soybean cultivars, J. Exp. Bot., 2003, 54, 2745-2756CrossrefGoogle Scholar

  • [39] Lee J.Y., Lee D.H., Use of serial analysis of gene expression technology to reveal changes in gene expression in Arabidopsis pollen undergoing cold stress, Plant Physiol., 2003, 132, 517-529Google Scholar

  • [40] Veena, Jiang H., Doerge R.W., Gelvin S.B., Transfer of T-DNA and Vir proteins to plant cells by Agrobacterium tumefaciens induces expression of host genes involved in mediating transformation and suppresses host defense gene expression, Plant J., 2003, 35, 219-236Google Scholar

  • [41] Sprunck S., Baumann U., Edwards K., Langridge P., Dresselhaus T., The transcript composition of egg cells changes significantly following fertilization in wheat (Triticum aestivum L.), Plant J., 2005, 41, 660-672PubMedCrossrefGoogle Scholar

  • [42] Vincent D., Ergu¨l A., Bohlman M.C., Tattersall E.A.R., Tillett R.L., Wheatley M.D., et al., Proteomic analysis reveals differences between Vitis vinifera L. cv. Chardonnay and cv. Cabernet Sauvignon and their responses to water deficit and salinity, J. Exp. Bot., 2007, 58, 1873-1892CrossrefGoogle Scholar

  • [43] MacDonald S.M., Rafnar T., Langdon J., Lichtenstein L.M., Molecular identification of an IgE-dependent histaminereleasing factor, Science, 1995, 269, 688-690Google Scholar

  • [44] Cans C., Passer B.J., Shalak V., Nancy-Portebois V., Crible V., Amzallag N., et al., Translationally controlled tumor protein acts as a guanine nucleotide dissociation inhibitor on the translation elongation factor eEF1A, Proc. Natl. Acad. Sci. USA, 2003, 100, 13892-13897Google Scholar

  • [45] Arcuri F., Papa S., Meini A., Carducci A., Romagnoli R., Bianchi L., et al., The translationally controlled tumor protein is a novel calcium binding protein of the human placenta and regulates calcium handling in trophoblast cells, Biol. Reprod., 2005, 73, 745-751CrossrefGoogle Scholar

  • [46] Thiele H., Berger M., Skalweit A., Thiele B.J., Expression of the gene and processed pseudogenes encoding the human and rabbit translationally controlled tumour protein (TCTP), Eur. J. Biochem., 2000, 267, 5473-5481 Google Scholar

  • [47] Li F., Zhang D., Fujise K., Characterization of fortilin, a novel antiapoptotic protein, J. Biol. Chem., 2001, 276, 47542-47549Google Scholar

  • [48] Lam E., Kato N., Lawton M., Programmed cell death, mitochondria and the plant hypersensitive response, Nature, 2001, 411, 848-853Google Scholar

  • [49] Heath M.C., Hypersensitive response-relatived death, Plant Mol. Biol., 2000, 44, 321-334CrossrefGoogle Scholar

  • [50] Tsunezuka H., Fujiwara M., Kawasaki T., Shimamoto K., Proteome analysis of programmed cell death and defense signaling using the rice lesion mimic mutant cdr2, Mol. Plant- Microbe Interact., 2005, 18, 52-59CrossrefGoogle Scholar

  • [51] Tani T., Yamamoto H., Nucleic acid and protein synthesis in association with the resistance of oat leaves to crown rust, Physiol. Plant Pathol., 1978, 12, 113-121CrossrefGoogle Scholar

  • [52] Manners J.M., Scott K.J., Translational activity of polysomes of barley leaves during infection by Ersiphe graminis f.sp. hordei, Phytopathology, 1983, 73, 1386-1392CrossrefGoogle Scholar

  • [53] Manners J.M., Scott K.J., Reduced translatable messenger RNA activities in leaves of barley infected with Ersiphe graminis f.sp. hordei, Physiol. Plant Pathol., 1985, 26, 297-308CrossrefGoogle Scholar

  • [54] Heath M.C., Signaling between pathogenic rust fungi and resistant or susceptible host plants, Ann. Bot., 1997, 80, 713-720Google Scholar

  • [55] Mould M.J.R., Heath M.C., Ultrastructural evidence of differential changes in transcription, translation, and cortical microtubules during in planta penetration of cells resistant or susceptible to rust infection, Physiol. Mol. Plant Pathol., 1999, 55, 225-236CrossrefGoogle Scholar

  • [56] Yamamoto H., Tani T., Hokin H., Protein synthesis linked with resistance of oat leaves to crown rust fungus, Jpn J. Phytopathol., 1976, 42, 583-590CrossrefGoogle Scholar

  • [57] Ellis R.J., Van Der Vies S.M., The Rubisco subunit binding protein, Photosynth. Res., 1988, 16 (1-2), 101-115CrossrefGoogle Scholar

  • [58] Pageau K., Reisdorf-Cren M., Morot-Gaudry J.F., Masclaux- Daubresse C., The two senescence-related markers, GS1 (cytosolic glutamine synthetase) and GDH (glutamate dehydrogenase), involved in nitrogen mobilization, are differentially regulated during pathogen attack and by stress hormones and reactive oxygen species in Nicotiana tabacum L. leaves, J. Exp. Bot., 2006, 57(3), 547-557Google Scholar

  • [59] Solomon P.S., Tan K.C., Oliver R.P., The nutrient supply of pathogenic fungi; a fertile field for study, Mol. Plant Pathol., 2003, 4, 203-210CrossrefGoogle Scholar

  • [60] Talbot N.J., McCafferty H.R.K., Ma M., Moore K., Hamer J.E., Nitrogen starvation of the rice blast fungus Magnaporthe grisea may act as an environmental cue for disease symptom expression, Physiol. Mol. Plant Pathol., 1997, 50, 179-195CrossrefGoogle Scholar

  • [61] Krishnan H.B., Natarajan S.S., Bennett J.O., Sicher R.C., Protein and metabolite composition of xylem sap from fieldgrown soybeans (Glycine max), Planta, 2011, 233, 921-931Google Scholar

  • [62] Rep M., Dekker H.L., Vossen J.H., de Boer A.D., Houterman P.M., Speijer D., et al., Mass spectrometric identification of isoforms of PR proteins in xylem sap of fungus-infected tomato, Plant Physiol., 2002, 130, 904-917 Google Scholar

  • [63] Buhtz A., Kolasa A., Arlt K., Walz C., Kehr J., Xylem sap protein composition is conserved among different plant species, Planta, 2004, 219, 610-618Google Scholar

  • [64] Subramanian S., Cho U-H., Keyes C., Yu O., Distinct changes in soybean xylem sap proteome in response to pathogenic and symbiotic microbe interactions, BMC Plant Biol., 2009, 9, 119CrossrefGoogle Scholar

  • [65] Badger M.R., Price G.D., The role of carbonic anhydrase in photosynthesis, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1994, 45, 369-392CrossrefGoogle Scholar

  • [66] Slaymaker D.H., Navarre D.A., Clark D., del Pozo O., Martin G.B., Klessig D.F., The tobacco salicylic acid-binding protein 3 (SABP3) is the chloroplast carbonic anhydrase, which exhibits antioxidant activity and plays a role in the hypersensitive defense response, Proc. Natl. Acad. Sci. USA, 2002, 99 (18), 11640-11645CrossrefGoogle Scholar

  • [67] Loake G., Grant M., Salicylic acid in plant defence - the players and protagonists, Curr. Opin. Plant Biol., 2007, 10, 466-472CrossrefGoogle Scholar

  • [68] Restrepo S., Myers K.L., del Pozo O., Martin G.B., Hart A.L., Buell C.R., et al., Gene profiling of a compatible interaction between Phytophthora infestans and Solanum tuberosum suggests a role for carbonic anhydrase, Mol. Plant-Microbe Interact., 2005, 18(9), 913-922CrossrefGoogle Scholar

  • [69] Estévez J.M., Cantero A., Reindl A., Reichler S., León P., 1-Deoxy-D-xylulose-5-phosphate synthase, a limiting enzyme for plastidic isoprenoid biosynthesis in plants, J. Biol. Chem., 2001, 276 (25), 22901-22909 Google Scholar

  • [70] Hasunuma T., Takeno S., Hayashi S., Sendai M., Bamba T., Yoshimura S., et al., Overexpression of 1-Deoxy-Dxylulose-5-phosphate reductoisomerase gene in chloroplast contributes to increment of isoprenoid production, J. Biosci. Bioeng., 2008, 105(5), 518-526Google Scholar

  • [71] Wanke M., Skorupinska-Tudek K., Swiezewska E., Isoprenoid biosynthesis via 1-deoxy-D-xylulose 5-phosphate/2-Cmethyl- D-erythritol 4-phosphate (DOXP/MEP) pathway, Acta Biochim. Pol., 2001, 48(3), 663-672Google Scholar

  • [72] Flors C., Nonell S., Light and singlet oxygen in plant defense against pathogens: phototoxic phenalenone phytoalexins, Acc. Chem. Res., 2006, 39 (5), 293-300CrossrefGoogle Scholar

  • [73] Kirby J., Keasling J.D., Biosynthesis of Plant Isoprenoids: Perspectives for Microbial Engineering, Annu. Rev. Plant Biol., 2009, 60, 335-355CrossrefGoogle Scholar

  • [74] Laxalt A.M., Cassia R.O., Sanllorenti P.M., Madrid E.A., Andreu A.B., Daleo G.R., et al., Accumulation of cytosolic glyceraldehyde-3-phosphate dehydrogenase RNA under biological stress conditions and elicitor treatments in potato, Plant Mol. Biol., 1996, 30(5), 961-972Google Scholar

  • [75] Chen Z., Silva H., Klessig D.F., Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid, Science, 1993, 262, 1883-1886Google Scholar

  • [76] Zaffagnini M., Michelet L., Marchand C., Sparla F., Decottignies P., Le Maréchal P., et al., The thioredoxinindependent isoform of chloroplastic glyceraldehyde-3-phosphate dehydrogenase is selectively regulated by glutathionylation, FEBS J., 2007, 274, 212-226 Google Scholar

About the article

Received: 2013-09-12

Accepted: 2013-10-10

Published Online: 2013-11-07

Published in Print: 2014-01-01


Citation Information: Organelles Proteomics, Volume 1, Issue 1, ISSN (Online) 2084-722X, DOI: https://doi.org/10.2478/orpr-2013-0004.

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© 2013 Mateus Rodrigues Pereira et al.. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. BY-NC-ND 3.0

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