Comparative proteomic profiles of Pinus monticola needles during early compatible and incompatible interactions with Cronartium ribicola

Planta

Volumn 236, Issue 6, 2012, Pages 1725-1746

  Zamany, Arezoo ^a   Liu, Jun Jun ^a   Ekramoddoullah, Abul K M ^a  

^a LAURENTIAN FORESTRY CENTRE   (Canada)

Author keywords

Cronartium ribicola; Defence response; Pinus monticola; Quantitative RT PCR; White pine blister rust

Indexed keywords

MESSENGER RNA; PLANT RNA; PROTEOME; VEGETABLE PROTEIN;

ARTICLE; BASIDIOMYCETES; COMPARATIVE STUDY; GENE EXPRESSION REGULATION; GENETICS; GENOTYPE; HOST PATHOGEN INTERACTION; IMMUNOLOGY; LIQUID CHROMATOGRAPHY; METABOLISM; MICROBIOLOGY; MUTATION; PHYSIOLOGY; PINE; PLANT DISEASE; PLANT IMMUNITY; PLANT LEAF; PROTEOMICS; SEEDLING; TANDEM MASS SPECTROMETRY; TIME; TWO DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS;

BASIDIOMYCOTA; CHROMATOGRAPHY, LIQUID; GENE EXPRESSION REGULATION, PLANT; GENOTYPE; HOST-PATHOGEN INTERACTIONS; MUTATION; PINUS; PLANT DISEASES; PLANT IMMUNITY; PLANT LEAVES; PLANT PROTEINS; PROTEOME; PROTEOMICS; RNA, MESSENGER; RNA, PLANT; SEEDLING; TANDEM MASS SPECTROMETRY; TIME FACTORS; TWO-DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS;

CRONARTIUM RIBICOLA; PINUS MONTICOLA;

EID: 84869497302     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-012-1715-x     Document Type: Article

References (68)

1. Abril N, Gion JM, Kerner R, Müller-Starck G, Cerrillo RM, Plomion C, Renaut J, Valledor L, Jorrin-Novo JV (2011) Proteomics research on forest trees, the most recalcitrant and orphan plant species. Phytochemistry 72: 1219-1242.
2. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55: 373-399.
3. Bechtold U, Karpinski S, Mullineaux PM (2005) The influence of the light environment and photosynthesis on oxidative signalling responses in plant-biotrophic pathogen interactions. Plant Cell Environ 28: 1046-1055.
4. Bhattarai KK, Li Q, Liu Y, Dinesh-Kumar SP, Kaloshian I (2007) The Mi-1-mediated pest resistance requires Hsp90 and Sgt1. Plant Physiol 144: 312-323.
5. Bos JI, Kanneganti T-D, Young C, Cakir C, Huitema E, Win J, Armstrong MR, Birch PR, Kamoun S (2006) The C terminal half of Phytophthora infestans RXLR effector AVR3a is sufficient to trigger R3a-mediated hypersensitivity and suppress INF1-induced cell death in Nicotiana benthamiana. Plant J 48: 165-176.
6. Chelikani P, Fita I, Loewen PC (2004) Diversity of structures and properties among catalases. Cell Mol Life Sci 61: 192-208.
7. Chen H, Xiong L (2005) Pyridoxine is required for post-embryonic root development and tolerance to osmotic and oxidative stresses. Plant J 44: 396-408.
8. Cho HY, Park JA, Pai HS (2008) Physiological function of NbRanBP1 in Nicotiana benthaminana. Mol Cells 26: 270-277.
9. Davidson J, Ekramoddoullah A (1997) Analysis of bark proteins in blister rust-resistant and susceptible western white pine (Pinus monticola). Tree Physiol 17: 663-669.
10. De Gara L, De Pinto MC, Tommasi F (2003) The antioxidant systems vis-à-vis reactive oxygen species during plant-pathogen interaction. Plant Physiol Biochem 41: 863-870.
11. Devoto A, Nieto-Rostro M, Xie D, Ellis C, Harmston R, Patrick E, Davis J, Sherratt L, Coleman M, Turner JG (2002) COI1 links jasmonate signalling and fertility to the SCF ubiquitin-ligase complex in Arabidopsis. Plant J 32: 457-466.
12. Fu ZQ, Guo M, Jeong BR, Tian F, Elthon TE, Cerny RL, Staiger D, Alfano JR (2007) A type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity. Nature 447: 284-288.
13. Gao F, Zhou Y, Zhu W, Li X, Fan L, Zhang G (2009) Proteomic analysis of cold stress-responsive proteins in Thellugiella rosette leaves. Planta 230: 1033-1046.
14. Gelhaye E, Rouhier N, Navrot N, Jacquot JP (2005) The plant thioredoxin system. Cell Mol Life Sci 62: 24-35.
15. Grant JJ, Loake GJ (2000) Role of reactive oxygen intermediates and cognate redox signalling in disease resistance. Plant Physiol 124: 21-29.
16. Hein I, Barciszewska-Pacak M, Hrubikova K, Williamson S et al (2005) Virus-induced gene silencing-based functional characterization of genes associated with powdery mildew resistance in barley. Plant Physiol 138: 2155-2164.
17. Huckelhoven R (2007) Cell wall-associated mechanisms of disease resistance and susceptibility. Annu Rev Phytopathol 45: 101-127.
18. Islam MA, Sturrock RN, Ekramoddoullah A (2008) A proteomics approach to identify proteins differentially expressed in Douglas-fir seedlings infected by Phellinus sulphurascens. J Proteomics 71: 425-438.
19. Jelenska J, van Hal JA, Greenberg JT (2010) Pseudomonas syringae hijacks plant stress chaperone machinery for virulence. Proc Natl Acad Sci USA 107: 13177-13182.
20. Jones AME, Thomas V, Bennett MH, Mansfield J, Grant M (2006) Modifications to the Arabidopsis defense proteome occur prior to significant transcriptional change in response to inoculation with Pseudomonas syringae. Plant Physiol 142: 1603-1620.
21. Kanzaki H, Saitoh H, Ito A, Fujisawa S, Kamoun S, Katou S, Yoshioka H, Terauchi A (2003) Cytosolic HSP90 and HSP70 are essential components of INF1-mediated hypersensitive response and non-host resistance to Pseudomonas cichorii in Nicotiana benthamiana. Mol Plant Pathol 4: 383-391.
22. Kinloch BB Jr (2003) White pine blister rust in North America: past and prognosis. Phytopathology 93: 1044-1047.
23. Kinloch BB Jr, Sniezko RA, Barnes GD, Greathouse TE (1999) A major gene for resistance to white pine blister rust in western white pine from the Western Cascade Range. Phytopathology 89: 861-867.
24. Kuroda H, Takahashi N, Shimada H, Motoaki S, Shinozaki K, Matsui M (2002) Classification and expression analysis of Arabidopsis F-box-containing protein genes. Plant Cell Physiol 43: 1073-1085.
25. Lee J, Bricker TM, Lefever M, Pinson SRM, Oard JH (2006) Proteomic and genetic approaches to identifying defence-related proteins in rice challenged with the fungal pathogen Rhizoctonia solani. Mol Plant Pathol 7: 405-416.
26. 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 142: 233-244.
27. Lightfoot DA, Bernhardt K, Mungur R, Nolte S, Ameziane R, Colter A, Jones K, Iqbal MJ, Varsa E, Young B (2007) Improved drought tolerance of transgenic Zea mays plants that express the glutamate dehydrogenase gene (gdhA) of E. coli. Euphytica 156: 103-116.
28. Lippert D, Chowrira S, Ralph SG, Zhuang J, Aeschliman D, Ritland C, Ritland K, Bohlmann J (2007) Conifer defense against insects: proteome analysis of Sitka spruce (Picea sitchensis) bark induced by mechanical wounding or feeding by white pine weevils (Pissodes strobi). Proteomics 7: 248-270.
29. Liu J-J, Ekramoddoullah A (2007) The CC-NBS-LRR subfamily in Pinus monticola: targeted identification, gene expression, and genetic linkage with resistance to Cronartium ribicola. Phytopathology 97: 728-736.
30. Liu J-J, Ekramoddoullah A (2008) Development of leucine-rich repeat polymorphism, amplified fragment length polymorphism, and sequence characterized amplified region markers to the Cronartium ribicola resistance gene Cr2 in western white pine (Pinus monticola). Tree Geneti Genomes 4: 601-610.
31. Liu J-J, Ekramoddoullah A, Yu X (2003) Differential expression of multiple PR10 proteins in western white pine following wounding, fungal infection and cold-hardening. Physiol Plant 119: 544-553.
32. Liu J-J, Ekramoddoullah A, Zamani A (2005) A class IV chitinase is up-regulated by fungal infection and abiotic stresses and associated with slow-canker-growth resistance to Cronartium ribicola in western white pine (Pinus monticola, Dougl. Ex D. Don). Phytopathology 95: 284-291.
33. Liu J-J, Hunt RS, Ekramoddoullah A (2004) Recent insights into western white pine genetic resistance to white blister rust. Recent Res Devel Biotechnol Bioeng 6: 65-76.
34. Liu J-J, Sniezko R, Ekramoddoullah A (2011) Association of a novel Pinus monticola chitinase gene (PmCh4B) with quantitative resistance to Cronartium ribicola. Phytopathology 101: 904-911.
35. Liu J-J, Zamani A, Ekramoddoullah A (2010) Expression profiling of a complex thaumatin-like protein family in western white pine. Planta 231: 637-651.
36. Ma Q-H (2007) Small GTP-binding proteins and their functions in plants. J Plant Growth Regul 26: 369-388.
37. Major IT, Nicole M-C, Duplessis S, Seguin A (2010) Photosynthetic and respiratory changes in leaves of poplar elicited by rust infection. Photosynth Res 104: 41-48.
38. Margaria P, Palmano S (2011) Response of the Vitis vinifera L. cv. 'Nebbiolo' proteome to Flavescence dorée phytoplasma infection. Proteomics 11: 212-224.
39. Mhamdi A, Queval G, Chaouch S, Vanderauwera S, Breusegem FV, Noctor G (2010) Catalase function in plants: a focus on Arabidopsis mutants as stress-mimic models. J Exp Bot 61: 4197-4220.
40. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7: 405-410.
41. Moreno JI, Martin R, Castresana C (2005) Arabidopsis SHMT1, a serine hydroxymethyltransferase that functions in the photorespiratory pathway influences resistance to biotic and abiotic stress. Plant J 41: 451-463.
42. Mungur R, Glass AD, Goodenow DB, Lightfoot DA (2005) Metabolite fingerprinting in transgenic Nicotiana tabacum altered by the Escherichia coli glutamate dehydrogenase gene. J Biomed Biotechnol 2: 198-214.
43. Nanda A, Andrio E, Marino D, Pauly N, Dunand C (2010) Reactive oxygen species during plant-microorganism early interactions. J Integr Plant Biol 52: 195-204.
44. Noctor G, Veljovik-Jovanovik S, Driscoll S, Novitskaya L, Foyer CH (2002) Drought and oxidative load in the leaves of C3 plants: a predominant role for photorespiration? Ann Bot (Lond) 89: 841-850.
45. O'Farrell PH (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250: 4007-4021.
46. Rinaldi C, Kohler A, Frey P, Duchaussoy F, Ningre N, Couloux A, Wincker P, Le Thiec D, Fluch S, Martin F, Duplessis S (2007) Transcript profiling of poplar leaves upon infection with compatible and incompatible strains of the foliar rust Melampsora larici-populina. Plant Physiol 144: 347-366.
47. Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathways collide: the response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134: 1683-1696.
48. Roberts MR, Salinas J, Collinge DB (2002) 14-3-3 proteins and the response to abiotic and biotic stress. Plant Mol Biol 50: 1031-1039.
49. Rösti J, Barton CJ, Albrecht S, Dupree P, Pauly M, Findlay K, Roberts K, Seiferta GJ (2007) UDP-glucose 4-epimerase isoforms UGE2 and UGE4 cooperate in providing UDP-galactose for cell wall biosynthesis and growth of Arabidopsis thaliana. Plant Cell 19: 1565-1579.
50. Rouhier N, Gelhaye E, Gualberto JM, Jordy M-N, Fay ED, Hirasawa M, Duplessis S, Lemaire SD, Frey P, Martin F, Manieri W, Knaff DB, Jacquot J-P (2004) Poplar peroxiredoxin Q. A thioredoxin-linked chloroplast antioxidant functional in pathogen defense. Plant Physiol 134: 1027-1038.
51. Shiu SH, Bleecker AB (2001) Plant receptor-like kinase gene family: diversity, function, and signaling. Sci STKE RE22.
52. Slaymaker DH, Navarre DA, Clark D, del Pozo O, Martin GB, Klessig DF (2002) 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 99: 11640-11645.
53. Smith JA, Blanchette RA, Burnes TA, Jacobs JJ, Higgins L, Witthuhn BA, David AJ, Gillman JH (2006) Proteomic comparison of needles from blister rust-resistant and susceptible Pinus strobus seedlings reveals up regulation of putative disease resistance proteins. Mol Plant-Microbe Interact 19: 150-160.
54. Sniezko RA (2006) Resistance breeding against nonnative pathogens in forest trees-current successes in North America. Can J Plant Pathol 28(Suppl 1): S270-S279.
55. Staal J, Kaliff M, Bohman S, Dixelius C (2006) Transgressive segregation reveals two Arabidopsis TIR-NB-LRR resistance genes effective against Leptosphaeria maculans, causal agent of blackleg disease. Plant J 46: 218-230.
56. Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403: 41-45.
57. Sunkar R, Bartels D, Kirch HH (2003) Overexpression of a stress-inducible aldehyde dehydrogenase gene from Arabidopsis thaliana in transgenic plants improves stress tolerance. Plant J 35: 452-464.
58. Tahara EB, Barros MH, Oliveira GA, Netto LE, Kowaltowski AJ (2007) Dihydrolipoyl dehydrogenase as a source of reactive oxygen species inhibited by caloric restriction and involved in Saccharomyces cerevisiae aging. FASEB J 21: 274-283.
59. Takahashi A, Casais C, Ichimura K, Shirasu K (2003) HSP90 interacts with RAR1 and SGT1 and is essential for RPS2-mediated disease resistance in Arabidopsis. Proc Natl Acad Sci USA 100: 11777-11782.
60. Thao NP, Chen L, Nakashima A, Hara S, Umemura K, Takahashi A, Shirasu K, Kawasaki T, Shimamoto K (2007) RAR1 and HSP90 form a complex with Rac/Rop GTPase and function in innate-immune responses in rice. Plant Cell 19: 4035-4045.
61. Timperio AM, Egidi MG, Zolla L (2008) Proteomics applied on plant abiotic stresses: role of heat shock proteins (HSP). J Proteomics 71: 391-411.
62. Torres MA, Jones JDG, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol 141: 373-378.
63. van Bentem SF, Vossen JH, de Vries KJ, van Wees S, Wladimir IL, Tameling WIL, Dekker HL, de Koster CG, Haring MA, Takken FLW, Cornelissen BJC (2005) Heat shock protein 90 and its co-chaperone protein phosphatise 5 interact with distinct regions of the tomato I-2 disease resistance protein. Plant J 43: 284-298.
64. Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9: 244-252.
65. Xu L, Liu F, Lechner E, Genschik P, Crosby WL, Ma H, Peng W, Huang D, Xie D (2002) The SCF (COI1) ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis. Plant Cell 14: 1919-1935.
66. Zamany A, Liu J-J, Ekramoddoullah A, Sniezko R (2011) Antifungal activity of a Pinus monticola-antimicrobial peptide 1 (Pm-AMP1) and its accumulation in Cronartium ribicola-infected western white pine. Can J Microbiol (in press).
67. Zang A, Xu X, Neill S, Cai W (2010) Overexpression of OsRAN2 in rice and Arabidopsis renders transgenic plants hypersensitive to salinity and osmotic stress. J Exp Bot 61: 777-789.
68. Zulak KG, Khan MF, Alcantara J, Schreimer D, Facchini PJ (2009) Defense response in opium poppy cell cultures revealed by LC-MS/MS proteomics. Mol Cell Proteomics 8: 86-98.