Abstract
The proteomic profiles of primary needles from Cr2-resistant and cr2-susceptible Pinus monticola seedlings were analysed post Cronartium ribicola inoculation by 2-DE. One hundred-and-five protein spots exhibiting significant differential expression were identified using LC–MS/MS. Functional classification showed that the most numerous proteins are involved in defence signalling, oxidative burst, metabolic pathways, and other physiological processes. Our results revealed that differential expression of proteins in response to C. ribicola inoculation was genotype- and infection-stage dependent. Responsive proteins in resistant seedlings with incompatible white pine blister rust (WPBR) interaction included such well-characterized proteins as heat shock proteins (HSPs), reactive oxygen species (ROS) scavenging enzymes, and intermediate factors functioning in the signal transduction pathways triggered by well-known plant R genes, as well as new candidates in plant defence like sugar epimerase, GTP-binding proteins, and chloroplastic ribonucleoproteins. Fewer proteins were regulated in susceptible seedlings; most of them were in common with resistant seedlings and related to photosynthesis among others. Quantitative RT-PCR analysis confirmed HSP- and ROS-related genes played an important role in host defence in response to C. ribicola infection. To the best of our knowledge, this is the first comparative proteomics study on WPBR interactions at the early stages of host defence, which provides a reference proteomic profile for other five-needle pines as well as resistance candidates for further understanding of host resistance in the WPBR pathosystem.
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Abbreviations
- CAN:
-
Acetonitrile
- 2-DE:
-
Two-dimensional electrophoresis
- H2O2 :
-
Hydrogen peroxide
- Hpi:
-
Hours post inoculation
- HSP:
-
Heat shock protein
- HR:
-
Hypersensitive response
- LC-MS/MS:
-
Liquid chromatography-tandem mass spectrometry
- LRR:
-
Leucine-rich repeat
- PRX:
-
Peroxiredoxin
- RT-qPCR:
-
Quantitative reverse transcription-polymerase chain reaction
- RLK:
-
Receptor-like kinase
- ROS:
-
Reactive oxygen species
- RuBisCO:
-
Ribulose-1,5-bisphosphate carboxylase oxygenase
- SOD:
-
Superoxide dismutase
- WWP:
-
Western white pine
- WPBR:
-
White pine blister rust
References
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
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399
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
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
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
Chelikani P, Fita I, Loewen PC (2004) Diversity of structures and properties among catalases. Cell Mol Life Sci 61:192–208
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
Cho HY, Park JA, Pai HS (2008) Physiological function of NbRanBP1 in Nicotiana benthaminana. Mol Cells 26:270–277
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
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
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
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
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
Gelhaye E, Rouhier N, Navrot N, Jacquot JP (2005) The plant thioredoxin system. Cell Mol Life Sci 62:24–35
Grant JJ, Loake GJ (2000) Role of reactive oxygen intermediates and cognate redox signalling in disease resistance. Plant Physiol 124:21–29
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
Huckelhoven R (2007) Cell wall-associated mechanisms of disease resistance and susceptibility. Annu Rev Phytopathol 45:101–127
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
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
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
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
Kinloch BB Jr (2003) White pine blister rust in North America: past and prognosis. Phytopathology 93:1044–1047
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
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
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
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
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
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
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
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
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
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
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
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
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
Ma Q-H (2007) Small GTP-binding proteins and their functions in plants. J Plant Growth Regul 26:369–388
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
Margaria P, Palmano S (2011) Response of the Vitis vinifera L. cv. ‘Nebbiolo’ proteome to Flavescence dorée phytoplasma infection. Proteomics 11:212–224
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
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
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
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
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
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
O’Farrell PH (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250:4007–4021
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
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
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
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
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
Shiu SH, Bleecker AB (2001) Plant receptor-like kinase gene family: diversity, function, and signaling. Sci STKE RE22
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
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
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
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
Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403:41–45
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
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
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
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
Timperio AM, Egidi MG, Zolla L (2008) Proteomics applied on plant abiotic stresses: role of heat shock proteins (HSP). J Proteomics 71:391–411
Torres MA, Jones JDG, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol 141:373–378
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
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
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
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)
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
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
Acknowledgments
This research was supported in part by the Canadian Forest Service and the CFS-Genomics R&D Initiative fund awarded to JJL. We thank T. Holmes for the microscopy work, and Dr. E. Becker and H. Williams for their critical review of the manuscript.
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Zamany, A., Liu, JJ. & Ekramoddoullah, A.K.M. Comparative proteomic profiles of Pinus monticola needles during early compatible and incompatible interactions with Cronartium ribicola . Planta 236, 1725–1746 (2012). https://doi.org/10.1007/s00425-012-1715-x
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DOI: https://doi.org/10.1007/s00425-012-1715-x