Common ragweed (Ambrosia artemisiifolia L.): Allergenicity and molecular characterization of pollen after plant exposure to elevated NO2

Plant Cell and Environment

Volumn 39, Issue 1, 2016, Pages 147-164

  Zhao, Feng ^a   Elkelish, Amr ^a,b   Durner, Jörg ^a,c   Lindermayr, Christian ^a   Winkler, J Barbro ^a   Ruioff, Franziska ^d   Behrendt, Heidrun ^c,e   Traidl Hoffmann, Claudia ^c,e   Holzinger, Andreas ^f   Kofler, Werner ^f   Braun, Paula ^g   Von Toerne, Christine ^a   Hauck, Stefanie M ^a   Ernst, Dieter ^a,e   Frank, Ulrike ^a,e  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b Suez Canal University   (Egypt)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d UNIVERSITY OF MUNICH   (Germany)

^e CK CARE   (Switzerland)

^f UNIVERSITY OF INNSBRUCK   (Austria)

^g MUNICH UNIVERSITY OF APPLIED SCIENCES   (Germany)

Author keywords

Allergen; Immune serum; Immunoblot; NO2; Pollen; Proteome; Ragweed; S nitrosylation

Indexed keywords

ALLERGY; CELLS AND CELL COMPONENTS; CLIMATE CHANGE; DICOTYLEDON; HEALTH RISK; IMMUNE RESPONSE; MOLECULAR ANALYSIS; NITROUS OXIDE; POLLEN; POLYMER; PROTEIN; PUBLIC HEALTH; WEED;

NORTH AMERICA;

AMBROSIA; AMBROSIA ARTEMISIIFOLIA; HEVEA BRASILIENSIS;

ALLERGEN; NITROGEN DIOXIDE; PLANT ANTIGEN; PLANT EXTRACT; PLANT PROTEIN; RAGWEED POLLEN;

AIR POLLUTION; CLIMATE CHANGE; CLUSTER ANALYSIS; DRUG EFFECTS; EUROPE; GENETICS; HUMAN; IMMUNOLOGY; RAGWEED; SEASON; TWO DIMENSIONAL GEL ELECTROPHORESIS;

AIR POLLUTION; ALLERGENS; AMBROSIA; ANTIGENS, PLANT; CLIMATE CHANGE; CLUSTER ANALYSIS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; EUROPE; HUMANS; NITROGEN DIOXIDE; PLANT EXTRACTS; PLANT PROTEINS; SEASONS;

EID: 84955185039     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12601     Document Type: Article

References (114)

1. Abat J.K. & Deswal R. (2009) 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 9, 4368-4380.
2. Ackaert C., Kofler S., Horejs-Hoeck J., Zulehner N., Asam C., von Grafenstein S., ... Duschl A. (2014) The impact of nitration on the structure and immunogenicity of the major birch pollen allergen Bet v 1.0101. PLoS ONE 9, e104520.
3. 2. World Allergy Organization Journal S198-S199. DOI: 10.1097/01.WOX.0000301890.70413.51.
4. Astier J., Rasul S., Koen E., Manzoor H., Besson-Bard A., Lamotte O., ... Wendehenne D. (2011) S-nitrosylation: an emerging post-translational protein modification in plants. Plant Science 181, 527-533.
5. Bachi A., Dalle-Donne I. & Scaloni A. (2013) Redox proteomics: chemical principles, methodological approaches and biological/biomedical promises. Chemical Reviews 113, 596-698.
6. Baker H.G. & Baker I. (1979) Starch angiosperm pollen grains and its evolutionary significance. American Journal of Botany 66, 591-600.
7. Bashir M.E.H., Lui J.H., Palnivelu R., Naclerio R.M. & Preuss D. (2013a) Pollen lipidomics: lipid profiling exposes a notable diversity in 22 allergenic pollen and potential biomarkers of the allergic immune response. PLoS ONE 8, e57566.
8. Bashir M.E.H., Ward J.M., Cummings M., Karrar E.E., Root M., Mohamed A.A., ... Preuss D. (2013b) Dual function of novel pollen coat (surface) proteins: IgE-binding capacity and proteolytic activity disrupting the airway epithelial barrier. PLoS ONE 8, e53337.
9. Beck I., Jochner S., Gilles S., McIntyre M., Buters J.T.M., Schmidt-Weber C., ... Traidl-Hoffmann C. (2013) High environmental ozone levels lead to enhanced allergenicity of birch pollen. PLoS ONE 8, e80147.
10. Behrendt H., Becker W.M., Fritzsche C., Sliwa-Tomczok W., Tomczok J., Friedrichs K.H. & Ring J. (1997) Air pollution and allergy: experimental studies on modulation of allergen release from pollen by air pollutants. International Archives of Allergy and Immunology 113, 69-74.
11. Birky C.W. (1995) Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proceedings of the National Academy of Sciences 92, 11331-11338.
12. Bryce M., Drews O., Schenk M.F., Menzel A., Estrella N., Weichenmeier I., ... Traidl-Hoffmann C. (2010) Impact of urbanization on the proteome of birch pollen and its chemotactic activity on human granulocytes. International Archives of Allergy and Immunology 151, 46-55.
13. Buters J.T.M., Kasche A., Weichenmeier I., Schober W., Klaus S., Traidl-Hoffmann C., ... Behrendt H. (2008) Year-to-year variation in release of Bet v 1 allergen from birch pollen: evidence for geographical differences between West and South Germany. International Archives of Allergy and Immunology 145, 122-130.
14. Castro A.J., Alché J.D., Cuevas J., Romero P.J., Alché V. & Rodríguez-García M.I. (2003) Pollen from different olive tree cultivars contains varying amounts of the major allergen Ole e 1. International Archives of Allergy and Immunology 131, 164-173.
15. Chehregani A., Majde A., Moin M., Gholami M., Shariatzadeh M.A. & Nassiri H. (2004) Increasing allergy potency of Zinnia pollen grains in polluted areas. Ecotoxicology and Environmental Safety 58, 267-272.
16. Chen W.J., Lo W.J., Cheng B.M. & Lee Y.P. (1992) Photolysis of nitric acid in solid nitrogen. The Journal of Chemical Physics 97, 7167-7173.
17. 3 gases. Plant Biology 9, 730-735.
18. Cieslik S. (2009) Ozone fluxes over various plant ecosystems in Italy: a review. Environmental Pollution 157, 1487-1496.
19. Corriveau J.L. & Coleman A.W. (1988) Rapid screening method to detect potential biparental inheritance of plastid DNA and results for over 200 angiosperm species. American Journal of Botany 75, 14443-11458.
20. Cortegano I., Civantos E., Aceituno E., del Moral A., López E., Lombardero M., ... Lahoz C. (2004) Cloning and expression of a major allergen from Cupressus arizonica pollen, Cup a 3, a PR-5 protein expressed under polluted environment. Allergy 59, 485-490.
21. 2 on Betula pendula, Ostrya carpinifolia and Carpinus betulus pollen fertility and human allergenicity. Environmental Pollution 186, 50-55.
22. D'Amato G., Cecchi L., Bonini S., Nunes C., Annesi-Maesano I., Behrendt H., ... van Cauwenberge P. (2007) Allergenic pollen and pollen allergy in Europe. Allergy 62, 976-990.
23. Dai S., Li L., Chen T., Chong K., Xue Y. & Wang T. (2006) Proteomic analyses of Oryza sativa mature pollen reveal novel proteins associated with pollen germination and tube growth. Proteomics 6, 2504-2529.
24. Dai S.J., Wang T., Yan X.F. & Chen S.X. (2007) Proteomics of pollen development and germination. Journal of Proteome Research 6, 4556-4563.
25. Diethart B., Sam S. & Weber M. (2007) Walls of allergenic pollen: special reference to the endexine. Grana 46, 164-175.
26. Edlund A.F., Swanson R. & Preuss D. (2004) Pollen and stigma structure and function: the role of diversity in pollination. Plant Cell 16, S84-S97.
27. Egli B., Kölling K., Köhler C., Zeeman S.C. & Streb S. (2010) Loss of cytosolic phosphoglucomutase compromises gametophyte development in Arabidopsis. Plant Physiology 154, 1659-1671.
28. 2 and drought stress on the growth and pollen production of common ragweed (Ambrosia artemisiifolia). Julius-Kühn-Archiv, 139-147.
29. 2: the relative roles of diffusion and biochemical processes. Plant, Cell and Environment 29, 1742-1750.
30. Elmayan T. & Simon-Plas F. (2007) Regulation of plant NADPH oxidase. Plant Signaling & Behavior 2, 505-507.
31. Fares A., Rossignol M. & Peltier J.B. (2011) Proteomics investigation of endogenous S-nitrosylation in Arabidopsis. Biochemical and Biophysical Research Communications 416, 331-336.
32. Frank l.E. & Friedman J.H. (1993) A statistical view of some chemometrics regression tools. Technometrics 35, 109-135.
33. 2 and drought stress. Ambroisie 29, 32-43.
34. Franze T., Weller M.G., Niessner R. & Pöschl U. (2003) Enzyme immunoassays for the investigation of protein nitration by air pollutants. Analyst 128, 824-831.
35. Franze T., Weller M.G., Niessner R. & Pöschl U. (2005) Protein nitration by polluted air. Environmental Science & Technology 39, 1673-1678.
36. Fratelli M., Demol H., Puype M., Casagrande S., Eberini I., Salmona M., ... Ghezzi P. (2002) Identification by redox proteomics of glutathionylated proteins in oxidatively stressed human T lymphocytes. Proceedings of the National Academy of Sciences 99, 3505-3510.
37. Gadermaier G., Hauser M. & Ferreira F. (2014) Allergens of weed pollen: an overview on recombinant and natural molecules. Methods 66, 55-66.
38. Gallois J.-L., Guyon-Debast A., Lécureuil A., Vezon D., Carpentier V., Bonhomme S. & Guerche P. (2009) The Arabidopsis proteasome RPT5 subunits are essential for gametophyte development and show accession-dependent redundancy. Plant Cell 21, 442-459.
39. Gerber E., Schaffner U., Gassmann A., Hinz H.L., Seier M. & Müller-Schärer H. (2011) Prospects for biological control of Ambrosia artemisiifolia in Europe: learning from the past. Weed Research 51, 559-573.
40. Ghiani A., Aina R., Asero R., Bellotto E. & Citterio S. (2012) Ragweed pollen collected along high-traffic roads shows a higher allergenicity than pollen sampled in vegetated areas. Allergy 67, 887-894.
41. Gilles S., Behrendt H., Ring J. & Traidl-Hoffmann C. (2012) The pollen enigma: modulation of the allergic immune response by non-allergenic, pollen-derived compounds. Current Pharmaceutical Design 18, 2314-2319.
42. 2) may reduce pollen viability in Austrian pine (Pinus nigra Arnold) trees - correlative evidence from a field study. Science of the Total Environment 402, 299-305.
43. Grobei M.A., Qeli E., Brunner E., Rehrauer H., Zhang R.X., Roschitzki B., ... Grossniklaus U. (2009) Deterministic protein inference for shotgun proteomics data provides new insights into Arabidopsis pollen development and function. Genome Research 19, 1786-1800.
44. Gruijthuijsen Y.K., Grieshuber I., Stöcklinger A., Tischler U., Fehrenbach T., Weller M.G., ... Duschl A. (2006) Nitration enhances the allergenic potential of proteins. International Archives of Allergy and Immunology 141, 265-275.
45. Han M.-J., Jung K.-H., Yi G. & An G. (2011) Rice Importin β1 gene affects pollen tube elongation. Molecules and Cells 31, 523-530.
46. Hastie T., Tibshirani R. & Friiedmann J.H. (2001) The Elements of Statistical Learning: Data Mining, Inference, and Prediction. Springer, New York.
47. Hess D.T., Matsumoto A., Kim S.O., Marshall H.E. & Stamler J.S. (2005) Protein S-nitrosylation: purview and parameters. Nature Reviews Molecular Cell Biology 6, 150-166.
48. Hodgins K.A., Lai Z., Nurkowski K., Huang J. & Rieseberg L.H. (2013) The molecular basis of invasiveness: differences in gene expression of native and introduced common ragweed (Ambrosia artemisiifolia) in stressful and benign environments. Molecular Ecology 22, 2496-2510.
49. Hodgins K.A. & Rieseberg L. (2011) Genetic differentiation in life-history traits of introduced and native common ragweed (Ambrosia artemisiifolia) populations. Journal of Evolutionary Biology 24, 2731-2749.
50. Holzmeister C., Fröhlich A., Sarioglu H., Bauer N., Durner J. & Lindermayr C. (2011) Proteomic analysis of defense response of wildtype Arabidopsis thaliana and plants with impaired NO- homeostasis. Proteomics 11, 1664-1683.
51. Honour S.L., Bell J.N.B., Ashenden T.W., Cape J.N. & Power S.A. (2009) Responses of herbaceous plants to urban air pollution: effects on growth, phenology and leaf surface characteristics. Environmental Pollution 157, 1279-1286.
52. Huang Z.Y., Gan Z.S., He Y.S., Li Y.H., Liu X.D. & Mu H. (2011) Functional analysis of a rice late pollen-abundant UDP-glucose pyrophosphorylase (OsUgp2) promoter. Molecular Biology Reports 38, 4291-4302.
53. 2 and new onset of self-reported asthma in adults. Epidemiology 20, 119-126.
54. Jaffrey S.R. & Snyder S.H. (2001) The biotin switch method for the detection of S-nitrosylated proteins. Science Signaling 86, pl1.
55. Kanter U., Heller W., Durner J., Winkler J.B., Engel M., Behrendt H., ... Ernst D. (2013) Molecular and immunological characterization of ragweed (Ambrosia artemisiifolia L.) pollen after exposure of the plants to elevated ozone over a whole growing season. PLoS ONE 8, e61518.
56. Karle A.C., Oostingh G.J., Mutschlechner S., Ferreira F., Lackner P., Bohle B., ... Duschl A. (2012) Nitration of the pollen allergen Bet v 1.0101 enhances the presentation of Bet v 1-derived peptides by HLA-DR on human dendritic cells. PLoS ONE 7, e31483.
57. Kato H., Takemoto D. & Kawakita K. (2013) Proteomic analysis of S-nitrosylated proteins in potato plant. Physiologia Plantarum 148, 371-386.
58. Kovacs I. & Lindermayr C. (2013) Nitric oxide-based protein modification: formation and site-specificity of protein S-nitrosylation. Frontiers in Plant Science 4, 137.
59. Kress L.W. & Skelly J.M. (1982) Response of several eastern forest tree species to chronic doses of ozone and nitrogen dioxide. Plant Disease 66, 1149-1152.
60. Laemmli U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
61. Lai H.-Y., Tam M.F., Tang R.-B., Chou H., Chang C.-Y., Tsai J.-J. & Shen H.-D. (2002) cDNA cloning and immunological characterization of a newly identified enolase allergen from Penicillium citrinum and Aspergillus fumigatus. International Archives of Allergy and Immunology 127, 181-190.
62. Leiblein-Wild M.C., Kaviani R. & Tackenberg O. (2014) Germination and seedling frost tolerance differ between the native and invasive range in common ragweed. Oecologia 174, 739-750.
63. Leiblein-Wild M.C. & Tackenberg O. (2014) Phenotypic variation of 38 European Ambrosia artemisiifolia populations measured in a common garden experiment. Biological Invasions 16, 2003-2015.
64. 0-ATP synthase, is essential for pollen formation in Arabidopsis thaliana. Plant and Cell Physiology 51, 923-935.
65. Lin A., Wang Y., Tang J., Xue P., Li C., Liu L., ... Chu C. (2012) Nitric oxide and protein S-nitrosylation are integral to hydrogen peroxide-induced leaf cell death in rice. Plant Physiology 158, 451-464.
66. Lindermayr C., Saalbach G. & Durner J. (2005) Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiology 137, 921-930.
67. Lu S., Ren J., Hao X., Liu D., Zhang R., Wu M., ... Wang Q. (2014) Characterization of protein expression of Platanus pollen following exposure to gaseous pollutants and vehicle exhaust particles. Aerobiologia 30, 281-291.
68. Maldonado-Alconada A., Echevarría-Zomeño S., Lindermayr C., Redondo-López I., Durner J. & Jorrín-Novo J. (2011) Proteomic analysis of Arabidopsis protein S-nitrosylation in response to inoculation with Pseudomonas syringae. Acta Physiologiae Plantarum 33, 1493-1514.
69. Mamun A.N.K. (2007) Reversible male sterility in transgenic tobacco carrying a dominant-negative mutated glutamine synthetase gene under the control of microspore-specific promoter. Indian Journal of Experimental Biology 45, 1022-1030.
70. Mascarenhas J.P. (1993) Molecular mechanisms of pollen tube growth and differentiation. The Plant Cell 5, 1303-1314.
71. Merl J., Ueffing M., Hauck S.M. & von Toerne C. (2012) Direct comparison of MS-based label-free and SILAC quantitative proteome profiling strategies in primary retinal Müller cells. Proteomics 12, 1902-1911.
72. Muñoz-Bertomeu J., Cascales-Miñana B., Irles-Segura A., Mateu I., Nunes-Nesi A., Fernie A.R., ... Ros R. (2010) The plastidial glyceraldehyde-3-phosphate dehydrogenase is critical for viable pollen development in Arabidopsis. Plant Physiology 152, 1830-1841.
73. Palevitz B.A., Liu B. & Joshi H.C. (1994) γ-Tubulin in tobacco pollen tubes: association with generative cell and vegetative microtubules. Sexual Plant Reproduction 7, 209-214.
74. Pasqualini S., Tedeschini E., Frenguelli G., Wopfner N., Ferreira F., D'Amato G. & Ederli L. (2011) Ozone affects pollen viability and NAD(P)H oxidase release from Ambrosia artemisiifolia pollen. Environmental Pollution 159, 2823-2830.
75. Pazmandi K., Kumar B.V., Szabo K., Boldogh I., Szoor A., Vereb G., ... Bacsi A. (2012) Ragweed subpollen particles of respirable size activate human dendritic cells. PLoS ONE 7, e52085.
76. Pertl H., Rittmann S., Schulze W.X. & Obermeyer G. (2011) Identification of lily pollen 14-3-3 isoforms and their subcellular and time-dependent expression profile. Biological Chemistry 392, 249-262.
77. Pertl H., Schulze W.X. & Obermeyer G. (2009) The pollen organelle membrane proteome reveals highly spatial-temporal dynamics during germination and tube growth of lily pollen. Journal of Proteome Research 8, 5142-5152.
78. Petersen, A., Schramm G., Schlaak M. & Becker W.M. (1998) Post-translational modifications influence IgE reactivity to the major allergen Phl p 1 of timothy grass pollen. Clinical & Experimental Allergy 28, 315-321.
79. Reinmuth-Selzle K., Ackaert C., Kampf C.J., Samonig M., Shiraiwa M., Kofler S., ... Poschl U. (2014) Nitration of the birch pollen allergen Bet v 1.0101: efficiency and site-selectivity of liquid and gaseous nitrating agents. Journal of Proteome Research 13, 1570-1577.
80. Ribarits A., Mamun A.N.K., Li S., Resch T., Fiers M., Heberle-Bors E., ... Touraev A. (2007) Combination of reversible male sterility and doubled haploid production by targeted inactivation of cytoplasmic glutamine synthetase in developing anthers and pollen. Plant Biotechnology Journal 5, 483-494.
81. Ridley B.L., O'Neill M.A. & Mohnen D. (2001) Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry 57, 929-967.
82. Ring J., Krämer U., Schäfer T. & Behrendt H. (2001) Why are allergies increasing? Current Opinion in Immunology 13, 701-708.
83. Roberts M.R., Salinas J. & Collinge D.B. (2002) 14-3-3 proteins and the response to abiotic and biotic stress. Plant Molecular Biology 50, 1031-1039.
84. Rodriguez-Serrano M., Pazmino D.M., Sparkes I., Rochetti A., Hawes C., Romero-Puertas M.C. & Sandalio L.M. (2014) 2, 4-Dichlorophenoxyacetic acid promotes S-nitrosylation and oxidation of actin affecting cytoskeleton and peroxisomal dynamics. Journal of Experimental Botany 65, 4783-4793.
85. 2). International Archives of Allergy and Immunology 143, 127-134.
86. Romero-Puertas M.C., Campostrini N., Mattè A., Righetti P.G., Perazzolli M., Zolla L., ... Delledonne M. (2008) Proteomic analysis of S-nitrosylated proteins in Arabidopsis thaliana undergoing hypersensitive response. Proteomics 8, 1459-1469.
87. Sangwan R.S. & Sangwan-Norrell B.S. (1987) Ultrastructural cytology of plastids in pollen of certain androgenic and nonandrogenic plants. Protoplasma 138, 11-22.
88. Schenk M.F., Cordewener J.H.G., America A.H.P., Peters J., Smulders M.J.M. & Gilissen L. (2011) Proteomic analysis of the major birch allergen Bet v 1 predicts allergenicity for 15 birch species. Journal of Proteomics 74, 1290-1300.
89. Schenk M.F., Cordewener J.H.G., America A.H.P., van't Westende W.P.C., Smulders M.J.M. & Gilissen L. (2009) Characterization of PR-10 genes from eight Betula species and detection of Bet v 1 isoforms in birch pollen. BMC Plant Biology 9, 24.
90. Schmidt H., Gelhaus C., Nebendahl M., Janssen O. & Petersen A. (2010) Characterization of Phleum pratense pollen extracts by 2-D DIGE and allergen immunoreactivity. Proteomics 10, 4352-4362.
91. Simon-Nobbe B., Probst G., Kajava A.V., Oberkofler H., Susani M., Crameri R., ... Breitenbach M. (2000) IgE-binding epitopes of enolases, a class of highly conserved fungal allergens. Journal of Allergy and Clinical Immunology 106, 887-895.
92. 2: effects on allergenicity and germination. Environmental Science & Technology 46, 2406-2412.
93. Storkey J., Stratonovitch P., Chapman D.S., Vidotto F. & Semenov M.A. (2014) A process-based approach to predicting the effect of climate change on the distribution of an invasive allergenic plant in Europe. PLoS ONE 9, e88156.
94. Suárez-Cervera M., Castells T., Vega-Maray A., Civantos E., del Pozo V., Fernández-González D., ... Seoane-Camba J.A. (2008) Effects of air pollution on Cup a 3 allergen in Cupressus arizonica pollen grains. Annals of Allergy, Asthma & Immunology 101, 57-66.
95. Takahashi M., Furuhashi T., Ishikawa N., Horiguchi G., Sakamoto A., Tsukaya H. & Morikawa H. (2014) Nitrogen dioxide regulates organ growth by controlling cell proliferation and enlargement in Arabidopsis. New Phytologist 201, 1304-1315.
96. 2 exposure on asthma in childhood: meta-analysis. Pediatrics International 54, 762-769.
97. Tang L.Y., Matsushima R. & Sakamoto W. (2012) Mutations defective in ribonucleotide reductase activity interfere with pollen DNA degradation mediated by DPD1 exonuclease. The Plant Journal 70, 637-649.
98. Temple S.J., Vance C.P. & Gantt J.S. (1998) Glutamate synthase and nitrogen assimilation. Trends in Plant Science 3, 51-56.
99. Thyssen G., Svab Z. & Maliga P. (2012) Exceptional inheritance of plastids via pollen in Nicotiana sylvestris with no detectable paternal mitochondrial DNA in the progeny. Plant Journal 72, 84-88.
100. Traidl-Hoffmann C., Kasche A., Menzel A., Jakob T., Thiel M., Ring J. & Behrendt H. (2003) Impact of pollen on human health: more than allergen carriers? International Archives of Allergy and Immunology 131, 1-13.
101. Untersmayr E., Diesner S.C., Oostingh G.J., Selzle K., Pfaller T., Schultz C., ... Duschl A. (2010) Nitration of the egg-allergen ovalbumin enhances protein allergenicity but reduces the risk for oral sensitization in a murine model of food allergy. PLoS ONE 5, e14210.
102. Vanzo E., Ghirardo A., Merl-Pham J., Lindermayr C., Heller W., Hauck S.M., ... Schnitzler J.-P. (2014) S-nitroso-proteome in poplar leaves in response to acute ozone stress. PLoS ONE 9, e106886.
103. Vidali L. & Hepler P.K. (2001) Actin and pollen tube growth. Protoplasma 215, 64-76.
104. Vigh-Conrad K.A., Conrad D.F. & Preuss D. (2010) A protein allergen microarray detects specific IgE to pollen surface, cytoplasmic, and commercial allergen extracts. PLoS ONE 5, e10174.
105. Wagner S., Breiteneder H., Simon-Nobbe B., Susani M., Krebitz M., Niggemann B., ... Hoffmann-Sommergruber K. (2000) Hev b 9, an enolase and a new cross-reactive allergen from Hevea latex and molds. European Journal of Biochemistry 267, 7006-7014.
106. Wang X.-L., Takai T., Kamijo S., Gunawan H., Ogawa H. & Okumura K. (2009) NADPH oxidase activity in allergenic pollen grains of different plant species. Biochemical and Biophysical Research Communications 387, 430-434.
107. Wopfner N., Gadermaier G., Egger M., Asero R., Ebner C., Jahn-Schmid B. & Ferreira F. (2005) The spectrum of allergens in ragweed and mugwort pollen. International Archives of Allergy and Immunology 138, 337-346.
108. Xue Y., Liu Z., Gao X., Jin C., Wen L., Yao X. & Ren J. (2010) GPS-SNO: computational prediction of protein S-nitrosylation sites with a modified GPS algorithm. PLoS ONE 5, e11290.
109. Yemets A.I., Krasylenko Y.A., Lytvyn D.I., Sheremet Y.A. & Blume Y.B. (2011) Nitric oxide signalling via cytoskeleton in plants. Plant Science 181, 545-554.
110. 2+-permeable membrane channels and is coupled to negative regulation on glutamate decarboxylase. Journal of Experimental Botany 65, 3235-3248.
111. Zhang Q., Liu Y. & Sodmergen (2003) Examination of the cytoplasmic DNA in male reproductive cells to determine the potential for cytoplasmic inheritance in 295 angiosperm species. Plant and Cell Physiology 44, 941-951.
112. Zhao Z. & Assmann S.M. (2011) The glycolytic enzyme, phosphoglycerate mutase, has critical roles in stomatal movement, vegetative growth, and pollen production in Arabidopsis thaliana. Journal of Experimental Botany 62, 5179-5189.
113. Zimmermann B. & Kohler A. (2014) Infrared spectroscopy of pollen identifies plant species and genus as well as environmental conditions. PLoS ONE 9, e95417.
114. Ziska L., Knowlton K., Rogers C., Dalan D., Tierney N., Elder M.A., ... Frenz D. (2011) Recent warming by latitude associated with increased length of ragweed pollen season in central North America. Proceedings of the National Academy of Sciences of the United States of America 108, 4248-4251.