The proteome response of potato leaves to priming agents and S-nitrosoglutathione

Plant Science

Volumn 198, Issue , 2013, Pages 83-90

  Arasimowicz Jelonek, Magdalena ^a   Kosmala, Arkadiusz ^b   Janus, Łukasz ^c   Abramowski, Dariusz ^c   Floryszak Wieczorek, Jolanta ^c  

^a ADAM MICKIEWICZ UNIVERSITY   (Poland)

^b INSTITUTE OF PLANT GENETICS   (Poland)

^c POZNA UNIVERSITY OF LIFE SCIENCES   (Poland)

Author keywords

Inducers of plant resistance; Nitric oxide; Potato; Priming; Proteome

Indexed keywords

2,6 DICHLOROISONICOTINIC ACID; 2,6-DICHLOROISONICOTINIC ACID; 3 AMINOBUTYRIC ACID; 3-AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID; AMINOBUTYRIC ACID DERIVATIVE; ISONICOTINIC ACID; LAMINARAN; NITRIC OXIDE; PHYTOHORMONE; POLYSACCHARIDE; PROTEOME; S NITROSOGLUTATHIONE; VEGETABLE PROTEIN;

ADAPTATION; ARTICLE; DISEASE RESISTANCE; METABOLISM; MICROBIOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PHYTOPHTHORA INFESTANS; PLANT LEAF; POTATO;

ADAPTATION, PHYSIOLOGICAL; AMINOBUTYRATES; DISEASE RESISTANCE; GAMMA-AMINOBUTYRIC ACID; ISONICOTINIC ACIDS; NITRIC OXIDE; PHYTOPHTHORA INFESTANS; PLANT GROWTH REGULATORS; PLANT LEAVES; PLANT PROTEINS; POLYSACCHARIDES; PROTEOME; S-NITROSOGLUTATHIONE; SOLANUM TUBEROSUM; STRESS, PHYSIOLOGICAL;

SOLANUM TUBEROSUM;

EID: 84869232452     PISSN: 01689452     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plantsci.2012.10.004     Document Type: Article

References (70)

1. Conrath U. Molecular aspects of defence priming. Trends Plant Sci. 2011, 16:524-531.
2. Conrath U. Priming of induced plant defense responses. Advances in Botanical Research 2009, Academic Press, London, pp. 361-395.
3. Bruce T.J.A., Matthes M.C., Napier J.A., Pickett J.A. Stressful " memories" of plants: evidence and possible mechanisms. Plant Sci. 2007, 173:603-608.
4. Jaskiewicz M., Conrath U., Peterhänsel C. Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep. 2011, 12:50-55.
5. Beckers G.J.M., Jaskiewicz M., Liu Y., Underwood W.R., He S.Y., Zhang S., Conrath U. Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell 2009, 21:944-953.
6. Tjaden J., Mohlmann T., Kampfenkel K., Henrichs G., Neuhaus H.E. Altered plastidic ATP/ADP-transporter activity influences potato (Solanum tuberosum L.) tuber morphology yield and composition of tuber starch. Plant J. 1998, 16:531-540.
7. Geigenberger P., Stamme C., Tjaden J., Schultz A., Quick P.W., Betsche T., Kersting H.J., Neuhaus H.E. Tuber physiology and properties of starch from tubers of transgenic potato plants with altered plastidic adenylate transporter activity. Plant Physiol. 2001, 125:1667-1678.
8. Linke C., Conrath U., Jeblick W., Betsche T., Mahn A., During K., Neuhaus H.E. Inhibition of the plastidic ATP/ADP transporter protein primes potato tubers for augmented elicitation of defense responses and enhances their resistance against Erwinia carotovora. Plant Physiol. 2002, 129:1607-1615.
9. Conrath U., Linke C., Jeblick W., Geigenberger P., Quick W.P., Neuhaus H.E. Enhanced resistance to Phytophthora infestans and Alternaria solani in leaves and tubers, respectively, of potato plants with decreased activity of the plastidic ATP/ADP transporter. Planta 2003, 19:75-83.
10. Schmitz G., Reinhold T., Göbel C., Feussner I., Neuhaus H.E., Conrath U. Limitation of nocturnal ATP import into chloroplasts seems to affect hormonal crosstalk, prime defense, and enhance disease resistance in Arabidopsis thaliana. Mol. Plant Microbe Interact. 2010, 23:1584-1591.
11. Van Hulten M., Pelser M., van Loon L.C., Pieterse C.M.J., Ton J. Costs and benefits of priming for defense in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:5602-5607.
12. Walters D.R., Paterson L., Walsh D.J., Havis N.D. Priming for plant defense in barley provides benefits only under high disease pressure. Physiol. Mol. Plant Pathol. 2009, 73:95-100.
13. Worrall D., Holroyd G.H., Moore J.P., Glowacz M., Croft P., Taylor J.E., et al. Treating seeds with activators of plant defence generates longlasting priming of resistance to pests and pathogens. New Phytol. 2012, 193:770-778.
14. Conrath U., Pieterse C.M.J., Mauch-Mani B. Priming in plant-pathogen interactions. Trends Plant Sci. 2002, 7:210-216.
15. Conrath U., Beckers G.J.M., Flors V., García-Agustín P., Jakab G., Mauch F., Newman M.A., Pieterse C.M.J., Poinssot B., Pozo M.J., Pugin A., Schaffrath U., Ton J., Wendehenne D., Zimmerli L., Mauch-Mani B. Priming: getting ready for battle. Mol. Plant Microbe Interact. 2006, 19:1062-1671.
16. Delledonne M., Xia Y., Dixon R.A., Lamb C. Nitric oxide functions as a signal in plant disease resistance. Nature 1998, 394:585-588.
17. Moreau M., Lindermayr C., Durner J., Klessig D.F. NO synthesis and signaling in plants-where do we stand?. Physiol. Plant. 2010, 138:372-383.
18. Lindermayr C., Durner J. S-Nitrosylation in plants: pattern and function. J. Proteomics 2009, 73:1-9.
19. Chaki M., Valderrama R., Fernandez-Ocana A.M., Carreras A., Lopez-Jaramillo J., Luque F., et al. Protein targets of tyrosine nitration in sunflower (Helianthus annuus L.) hypocotyls. J. Exp. Bot. 2009, 60:4221-4234.
20. Gaupels F., Kuruthukulangarakoola G.T., Durner J. Upstream and downstream signals of nitric oxide in pathogen defence. Curr. Opin. Plant Biol. 2011, 14:707-714.
21. Kosmala A., Bocian A., Rapacz M., Jurczyk B., Zwierzykowski Z. Identification of leaf proteins differentially accumulated during cold acclimation between Festuca pratensis plants with distinct levels of frost tolerance. J. Exp. Bot. 2009, 60:3595-3609.
22. Bocian A., Kosmala A., Rapacz M., Jurczyk B., Marczak Ł., Zwierzykowski Z. Differences in leaf proteome response to cold acclimation between Lolium perenne plants with distinct levels of frost tolerance. J. Plant Physiol. 2011, 168:1271-1279.
23. Hurkman W.J., Tanaka C.K. Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis. Plant Physiol. 1986, 81:802-806.
24. Neuhoff V., Arold N., Taube D., Ehrhardt W. Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 1988, 9:255-262.
25. Floryszak-Wieczorek J., Arasimowicz-Jelonek M., Milczarek G., Janus Ł., Pawlak-Sprada S., Abramowski D., Deckert J., Billert H. Nitric oxide-mediated stress imprint in potato as an effect of exposure to a priming agent. Mol. Plant Microbe Interact. 2012, 25:1469-1477.
26. Andreu A.B., Guevara M.G., Wolski E.A., Daleo G.R., Caldiz D.O. Enhancement of natural disease resistance in potatoes by chemicals. Pest. Manag. Sci. 2006, 62:162-170.
27. Cohen Y.R. β-Aminobutyric acid-induced resistance against plant pathogens. Plant Dis. 2002, 86:448-457.
28. Li Y., Tian Z., Liu J., Xie C. Comparative cDNA-AFLP analysis reveals that dl-β-amino-butyric acid induces resistance through early activation of the host-defense genes in potato. Physiol. Plant. 2009, 136:19-29.
29. Si-Ammour A., Mauch-Mani B., Mauch F. Quantification of induced resistance against Phytophthora species expressing GFP as a vital marker: β-aminobutyric acid but not BTH protects potato and Arabidopsis from infection. Mol. Plant Pathol. 2003, 4:237-248.
30. Tanou G., Fotopoulos V., Molassiotis A. Priming against environmental challenges and proteomics in plants: update and agricultural perspectives. Front. Plant Sci. 2012, 3:216.
31. Zimmerli L., Jakab G., Metraux J.P., Mauch-Mani B. Potentiation of pathogen-specific defense mechanisms in Arabidopsis by β-aminobutyric acid. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:12920-12925.
32. Zimmerli L., Metraux J.P., Mauch-Mani B. Betaaminobutyric acid-induced protection of Arabidopsis against the necrotrophic fungus Botrytis cinerea. Plant Physiol. 2001, 126:517-523.
33. Ton J., Mauch-Mani B. β-amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose. Plant J. 2004, 38:119-130.
34. Jakab G., Ton J., Flors V., Zimmerli L., Métraux J.P., Mauch-Mani B. Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses. Plant Physiol. 2005, 139:267-274.
35. Macarisin D., Wisniewski M.E., Bassett C., Thannhauser T. Proteomic analysis of b-aminobutyric acid priming and abscisic acid - induction of drought resistance in crabapple (Malus pumila): effect on general metabolism, the phenylpropanoid pathway and cell wall enzymes. Plant Cell Environ. 2009, 32:1612-1631.
36. Hamiduzzaman M.M., Jakab G., Barnavon L., Neuhaus J.M., Mauch-Mani B. β-Aminobutyric acid-induced resistance against downy mildew in grapevine acts through the potentiation of callose formation and jasmonic acid signaling. Mol. Plant Microbe Interact. 2005, 18:819-829.
37. Klarzynski O., Plesse B., Joubert J.M., Yvin J.C., Kopp M., Kloareg B., Fritig B. Linear beta-1,3-glucans are elicitors of defense responses in tobacco. Plant Physiol. 2000, 124:1027-1038.
38. Aziz A., Poinssot B., Daire X., Adrian M., Bézier A., Lambert B., Joubert J.M., Pugin A. Laminarin elicits defense responses in grapevine and induces protection against Botrytis cinerea and Plasmopara viticola. Mol. Plant Microbe Interact. 2003, 116:1118-1128.
39. Van Loon L.C. Induced resistance in plants and the role of pathogenesis-related proteins. Eur. J. Plant Pathol. 1997, 103:753-765.
40. Mou Z., Fan W., Dong X. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 2003, 113:935-944.
41. Kato H., Takemoto D., Kawakita K. Proteomic analysis of S-nitrosylated proteins in potato plant. Physiol. Plant. 2012, 10.1111/j.1399-3054.2012.01684.x.
42. Abat J.K., Mattoo A.K., Deswal R. S-nitrosylated proteins of a medicinal CAM plant Kalanchoe pinnata - ribulose-1,5-bisphosphate carboxylase/oxygenase activity targeted for inhibition. FEBS J. 2008, 275:2862-2872.
43. Floryszak-Wieczorek J., Arasimowicz-Jelonek M. Interplay between nitric oxide and other signals involved in plant resistance to pathogens. Nitric Oxide in Plant Physiology 2010, 139-159. Wiley-Blackwell, Weinheim. S. Hayat, M. Mori, J. Pichtel, A. Ahmad (Eds.).
44. Feechan A., Kwon E., Yun B.W., Wang Y., Pallas J.A., Loake G.J. A central role for S-nitrosothiols in plant disease resistance. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:8054-8059.
45. Lindermayr C., Saalbach G., Durner J. Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol. 2005, 137:921-930.
46. Holtgrefe S., Gohlke J., Starmann J., Druce S., Klocke S., Altmann B., Wojtera J., Lindermayr C., Scheibe R. Regulation of plant cytosolic glyceraldehyde 3-phosphate dehydrogenase isoforms by thiol modifications. Physiol. Plant. 2008, 133:211-228.
47. Lozano-Juste J., Colom-Moreno R., Leon J. In vivo protein tyrosine nitration in Arabidopsis thaliana. J. Exp. Bot. 2011, 62:3501-3517.
48. Abat J.K., Deswal R. Differential modulation of S-nitrosoproteome of Brassica juncea by low temperature: change in S-nitrosylation of Rubisco is responsible for the inactivation of its carboxylase activity. Proteomics 2009, 9:4368-4380.
49. Cecconi D., Orzetti S., Vandelle E., Rinalducci S., Zolla L., Delledonne M. Protein nitration during defense response in Arabidopsis thaliana. Electrophoresis 2009, 30:2460-2468.
50. Yang E.J., Oh Y.A., Lee E.S., Park A.R., Cho S.K., Yoo Y.J., Park O.K. Oxygen-evolving enhancer protein 2 is phosphorylated by glycine-rich protein 3/wall-associated kinase 1 in Arabidopsis. Biochem. Biophys. Res. Commun. 2003, 305:862-868.
51. Laxalt A.M., Cassia R.O., Sanllorenti P.M., Madrid E.A., Andreu A.B., Daleo G.R., Conde R.D., Lamattina L. Accumulation of cytosolic glyceraldehyde-3-phosphate dehydrogenase RNA underbiological stress conditions and elicitor treatments in potato. Plant Mol. Biol. 1996, 30:961-972.
52. Lee J., Bricker T.M., Lefevre M., Pinson S.R.M., Oard J.H. Proteomic and genetic approaches to identifying defence-related proteins in rice challenged with the fungal pathogen Rhizoctonia solani. Mol. Plant Pathol. 2006, 7:405-416.
53. Brandes N., Schmitt S., Jakob S. Thiol-based redox switches in eukaryotic proteins. Antioxid. Redox Signal. 2009, 11:997-1014.
54. Morigasaki S., Shimada K., Ikner A., Yanagida M., Shiozaki K. Glycolytic enzyme GAPDH promotes peroxide stress signaling through multistep phosphorelay to a MAPK cascade. Mol. Cell 2008, 30:108-113.
55. Hara M.R., Cascio M.B., Sawa A. GAPDH as a sensor of NO stress. Biochim. Biophys. Acta 2006, 1762:502-509.
56. Kornberg M.D., Sen N., Hara M.R., Julur K.R., Nguyen J.V., Snowman A.M., Law L., Hester L.D., Snyder S.H. GAPDH mediates nitrosylation of nuclear proteins. Nat. Cell Biol. 2010, 12:1094-1100.
57. 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. U.S.A. 2002, 99:11640-11645.
58. Wang Y.Q., Feechan A., Yun B.W., Shafiei R., Hofmann A., Taylor P., Xue P., Yang F.Q., Xie Z.S., Pallas J.A., Chu C.C., Loake G.J. S-nitrosylation of AtSABP3 antagonizes the expression of plant immunity. J. Biol. Chem. 2009, 284:2131-2137.
59. Restrepo S., Myers K.L., del Pozo O., Martin G.B., Hart A.L., Buell C.R., Fry W.E., Smart C.D. Gene profiling of a compatible interaction between Phytophthora infestans and Solanum tuberosum suggests a role for carbonic anhydrase. Mol. Plant Microbe Interact. 2005, 18:913-922.
60. Polesani M., Desario F., Ferrarini A., Zamboni A., Pezzotti M., Kortekamp A., Polverari A. cDNA-AFLP analysis of plant and pathogen genes expressed in grapevine infected with Plasmopara viticola. BMC Genomics 2008, 9:142.
61. Milli A., Cecconi D., Bortesi L., Persi A., Rinalducci S., Zamboni A., Zoccatellia G., Lovatoa A., Zollab L., Polverari A. Proteomic analysis of the compatible interaction between Vitis vinifera and Plasmopara viticola. J. Proteomics 2012, 75:1284-1302.
62. Hoang C.V., Chapman K.D. Biochemical and molecular inhibition of plastidial carbonic anhydrase reduces the incorporation of acetate into lipids in cotton embryos and tobacco cell suspensions and leaves. Plant Physiol. 2002, 128:1417-1427.
63. Castillejo M.A., Fernandez-Aparicio M., Rubiales D. Proteomic analysis by two-dimensional differential in gel electrophoresis (2D DIGE) of the early response of Pisum sativum to Orobanche crenata. J. Exp. Bot. 2012, 63:107-119.
64. Koeck T., Fu X., Hazen S.L., Crabb J.W., Stuehr D.J., Aulak K.S. Rapid and selective oxygen-regulated protein tyrosine denitration and nitration in mitochondria. J. Biol. Chem. 2004, 279:27257-27262.
65. Monteiro H.P., Arai R.J., Travassos L.R. Protein tyrosine phosphorylation and protein tyrosine nitration in redox signaling. Antioxid. Redox Signal. 2008, 10:843-889.
66. Kim Y.O., Pan S.O., Jung C.H., Kang H. A zinc finger-containing glycine-rich RNA-binding protein, atRZ-1a, has a negative impact on seed germination and seedling growth of Arabidopsis thaliana under salt or drought stress conditions. Plant Cell Physiol. 2007, 48:1170-1181.
67. Kwak K.J., Kim Y.O., Kang H. Characterization of transgenic Arabidopsis plants overexpressing GR-RBP4 under high salinity, dehydration, or cold stress. J. Exp. Bot. 2005, 56:3007-3016.
68. Simpson G.G. The autonomous pathway: epigenetic and posttranscriptional gene regulation in the control of Arabidopsis flowering time. Curr. Opin. Plant Biol. 2004, 7:570-574.
69. Terzi L.C., Simpson G.G. Regulation of flowering time by RNA processing. Nuclear Pre-mRNA Processing in Plants 2008, 201-218. Springer-Verlag, Berlin Heidelberg. A.S.N. Reddy, M. Golovkin (Eds.).
70. Lorković Z.J. Role of plant RNA-binding proteins in development, stress response and genome organization. Trends Plant Sci. 2009, 14:229-236.