Abstract
Olive pollen is one of the main causes of allergic disease in the Mediterranean area. Ten different proteins with allergenic activity have been described in olive pollen, with major allergen Ole e 1. Olea europaea L. may cause allergenic effects of different severity depending on the Ole e 1 content of cultivars. In this paper, we aimed to assess the heterogeneity of two olive cultivars concerning concentrations of the major allergen Ole e 1 during a period of 2 years. Pollens from two most common olive cultivars, known as “Gemlik” and “Celebi,” were analyzed on regular basis. Ole e 1 amounts were measured by double-sandwich enzyme-linked immunosorbent assay (ELISA). The results were expressed as μg of Ole e 1 per μg of total freeze-dried extract. Comparisons of Ole e 1 levels were made both between individual trees and between cultivars. It was analyzed the influence of some meteorological parameters on pollen counts/allergenic content on a local scale, for 2 years. Pollen sampling was carried out continuously for 2 years, using a Hirst-type volumetric trap. “Gemlik” had the higher value (mean ± standard deviation) of Ole e 1 content (2.44 ±0.70 and 1.87 ±1.03 μg/μg, respectively) when compared to “Celebi” (2.16 ±0.86 and 0.20 ±0.30 μg/μg, respectively) in the years 2013 and 2015. In our research, daily variations were observed in pollen samples of two olive cultivars and even different trees of the same cultivar. Furthermore, during certain sampling days, discrepancies between airborne pollen counts and Ole e 1 concentrations were detected for both cultivars. It was found that meteorological changes, especially temperature and precipitation fluctuations, could affect airborne pollen and Ole e 1 allergen levels in the atmosphere. Therefore, pollen samples of different O. europaea cultivars demonstrated great differences in Ole e 1 content. We believe that these findings were a result of alternate bearing behavior modulated by meteorological factors.




Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Akkaya M, Celenk S, Canıtez Y, Çekiç Ş, Malyer H, Sapan N (2018) Bursa atmosferindeki bazı allerjik polenler ile allerjik duyarlanma ilişkisinin araştırılması. XXV. Ulusal Allerji & Klinik İmmunoloji Kongresi, Oral presentation, 17-21 November, Antalya-Turkey
Alché JD, Castro AJ, Olmedilla A, Fernández MC, Rodríguez R, Villalba M, Rodríguez-García MI (1999) The major olive pollen allergen (Ole e I) shows both gametophytic and sporophytic expression during anther development, and its synthesis and storage takes place in the RER. J Cell Sci 112(Pt 15):2501–2509
Alché JD, M'rani-Alaoui M, Castro AJ, Rodríguez-García MI (2004) Ole e 1, the major allergen from olive (Olea europaea L.) pollen, increases its expression and is released to the culture medium during in vitro germination. Plant Cell Physiol 45(9):1149–1157
Alché JD, Castro AJ, Jiménez-López JC, Morales S, Zafra A, Hamman-Khalifa AM, Rodríguez-García MI (2007) Differential characteristics of olive pollen from different cultivars: biological and clinical implications. J Investig Allergol Clin Immunol 17(Suppl 1):17–23
Arilla MC, Eraso E, Ibarrola I, Algorta J, Martínez A, Asturias JA (2002) Monoclonal antibody-based method for measuring olive pollen major allergen Ole e1. Ann Allergy Asthma Immunol 89(1):83–89
Arilla MC, Ibarrola I, Mir A, Monteseirín J, Conde J, Martínez A, Asturias JA (2005) Development of a sandwich-type ELISA for measuring Pla a 1, the major allergen of Platanus acerifolia pollen. Int Arch of Allergy Inmunol 138(2):127–133
Arilla MC, González-Rioja R, Ibarrola I, Mir A, Monteseirín J, Conde J, Martínez A, Asturias JA (2006) A sensitive monoclonal antibody- based ELISA to quantifity Parietaria judaica major allergens, Par j1 and Par j2. Clin Exp Alllergy 36(1):87–93
Barber D, Carpizo J, Garcia-Rumbao MC, Polo F, Juan F (1990) Allergenic variability in olea pollen. Ann Allergy 64(1):43–46
Barral P, Batanero E, Palomares O, Quiralte J, Villalba M, Rodríguez R (2004) A major allergen from pollen defines a novel family of plant proteins and shows intra- and interspecies cross-reactivity. J Immunol 172(6):3644–3651
Barut E, Ipek A, Gulen H (2009) Distribution Of Olive (Olea europaea L.) Genotypes in the southern Marmara region of Turkey. Pak J Bot 41(3):1077–1080
Batanero E, Villalba M, Rodríguez R (1994) Glycosylation site of the major allergen from olive tree. Allergenic implications of the carbohydrate moiety. Mol Immunol 31(1):31–37
Bateman A, Coin L, Durbin R, Finn RD, Hollich V, Griffiths-Jones S, Khanna A, Marshall M, Moxon S, Sonnhammer ELL, Studholme DJ, Yeats C, Eddy SR (2004) The Pfam protein families database. Nucleic Acids Res 32:D138–D141 Database issue
Brito FF, Gimeno PM, Carnés J, Martín R, Fernández-Caldas E, Lara P, López-Fidalgo J, Guerra F (2011) Olea europaea pollen counts and aeroallergen levels predict clinical symptoms in patients allergic to olive pollen. Ann Allergy Asthma Immunol 106(2):146–152
Buters JTM, Thibaudon M, Smith M, Kennedy R, Rantio-Lehtimaki A, Albertini R, Reese G, Weber B, Galan C, Brandao R, Antunes CM, Jager S, Berger U, Celenk S, Grewling L, Jackowiak B, Sauliene I, Weichenmeier I, Pusch G, Sarioglu H, Ueffing M, Behrendt H, Prank M, Sofiev M, Cecchi L (2012) Release of bet v 1 from birch pollen from 5 European countries. Results from the HIALINE study. Atmos Environ 55:496–505
Buters J, Prank M, Sofiev M, Pusch G, Albertini R, Annesi-Maesano I, Antunes C, Behrendt H, Berger U, Brandao R, Celenk S, Galan C, Grewling Ł, Jackowiak B, Kennedy R, Rantio-Lehtimäki A, Reese G, Sauliene I, Smith M, Thibaudon M, Weber B, Cecchi L (2015) HIALINE working group. Variation of the group 5 grass pollen allergen content of airborne pollen in relation to geographic location and time in season. J Allergy Clin Immunol 136(1):87–95
Carnés Sánchez J, Iraola VM, Sastre J, Florido F, Boluda L, Fernández-Caldas E (2002) Allergenicity and immunochemical characterization of six varieties of Olea europaea. Allergy 57(4):313–318
Castro AJ (2001) Aproximación a la función biológica del alérgeno mayoritario del polen del olivo (Ole e 1). Implicaciones clínicas y ambientales. Doctoral thesis. Granada (Spain): University of Granada
Castro AJ, Alché JD, Cuevas J, Romero PJ, Alché V, Rodríguez-García MI (2003) Pollen from different olive tree cultivars contains varying amounts of the major allergen Ole e 1. Int Arch Allergy Immunol 131(3):164–173
Conde-Hernández J, Conde-Hernández P, González-Quevedo MT, Conde-Alcañiz MA, Conde-Alcañiz EM, Crespo-Moreira P, Cabanillas-Platero M (2002) Antigenic and allergenic differences between 16 different cultivars of Olea europaea. Allergy 57(Suppl 71):60–65
D'Amato G (1998) Pollen allergy in the Mediterranean area. Rev Fr Allergol 38(1):160–162
D'Amato G, Liccardi G (1994) Pollen-related allergy in the European Mediterranean area. Clin Exp Allergy 24(3):210–219
D'Amato G, Cecchi L, Bonini S, Nunes C, Annesi-Maesano I, Behrendt H, Liccardi G, Popov T, van Cauwenberge P (2007a) Allergenic pollen and pollen allergy in Europe. Allergy. 62(9):976–990
D'Amato G, Liccardi G, Frenguelli G (2007b) Thundestorm-asthma and pollen allergy. Allergy 62(1):11–16
Devalia JL, Rusznak C, Davies RJ (1998) Allergen/irritant interaction–its role in sensitization and allergic disease. Allergy 53:335–345
Dıraman H (2010) Characterization by chemometry of the most important domestic and foreign olive cultivars from the National Olive Collection Orchard of Turkey. Grasas Aceites 61(4):341–351
Efe R, Soykan A, Curebal I, Sonmez S (2013) Olive and olive oil in Edremit Region. Edremit Municipality Cultural Publication No: 9, ISBN:978-605-62253-3-8
Erel R, Yermiyahu U, Van Opstal J, Ben Gal A, Schwartz A (2013) The importance of olive (Olea europaea L.) tree nutritional status on its productivity. Sci Hortic 159:8–18
Fernández-Caldas E, Carnés J, Iraola V, Casanovas M (2007) Comparison of the allergenicity and Ole e 1 content of 6 varieties of Olea europaea pollen collected during 5 consecutive years. Ann Allergy Asthma Immunol 98(5):464–470
Fernández-González D, González Parrado Z, Vega Maray AM, Valencia Barrera RM, Camazón Izquierdo B, De Nuntiis P, Mandrioli P (2010) Platanus pollen allergen, Pla a1: quantification in the atmosphere and influence on a sensitizing population. Clin Exp Allergy 40(11):1701–1708
Fernández-González D, Rodríguez-Rajo FJ, González-Parrado Z, Valencia-Barrera R, Jato V, Grau SM (2011) Differences in atmospheric emissions of Poaceae pollen and Lol p 1 allergen. Aerobiologia 27:301–309
Fernández-González M, González-Fernández E, Fernández-González D, Javier Rodríguez-Rajo F (2020) Secondary outcomes of the Ole e 1 proteins involved in pollen tube development: impact on allergies. Front Plant Sci 11:974
Fleming DM, Crombie DL (1987) Prevalence of asthma and hay fever in England and Wales. Br Med J (Clin Res Ed) 294(6567):279–283
Galán C, Antunes C, Brandao R, Torres C, Garcia-Mozo H, Caeiro E, Ferro R, Prank M, Sofiev M, Albertini R, Berger U, Cecchi L, Celenk S, Grewling L, Jackowiak B, Jäger S, Kennedy R, Rantio-Lehtimäki A, Reese G, Sauliene I, Smith M, Thibaudon M, Weber B, Weichenmeier I, Pusch G, Buters JTM (2013) Airborne olive pollen counts are not representative of exposure to the major olive allergen Ole e 1. Allergy 68(6):809–812
Galán C, Smith M, Thibaudon M, Frenguelli G, Oteros JA, Gehrig R, Berger U, Clot B, Brandao R (2014) EAS QC working group. Pollen monitoring: minimum requirements and reproducibility of analysis. Aerobiologia 30:385–395
Geller-Bernstein C, Arad G, Keynan N, Lahoz C, Cardaba B, Waisel Y (1996) Hypersensitivity to pollen of Olea europaea in Israel. Allergy 51(5):356–359
Grote M, Valenta R, Reichelt R (2003) Abortive pollen germination: a mechanism of allergen release in birch, alder and hazel revealed by immunogold electronmicroscopy. J Allergy Clin Immunol 111:1017–1023
Hamman-Khalifa AM. (2005) Utilización de marcadores relacionados con la alergenicidady la biosíntesis de lípidos para la discriminación entre cultivares de olivo. Doctoral thesis. Granada (Spain): University of Granada
Hamman-Khalifa AM, Alché JD, Rodríguez-García MI (2003) Discriminación molecular en el polen de variedades españolas y marroquíes de olivo (Olea europaea L.). Polen 13:219–225
Hirst JM (1952) An automatic volumetric spore-trap. Ann Appl Biol 39:257–265
Jaradat ZW, Al Bzour A, Ababneh Q, Shdiefat S, Jaradat S, Al Domi H (2012) Identification of allergenic pollen grains in 36 olive (Olea europaea) cultivars grown in Jordan. Food Agric Immunol 23(3):255–264
Kirmaz C, Yuksel H, Bayrak P, Yilmaz O (2005) Symptoms of the olive pollen allergy: do they really occur only in the pollination season? J Investig Allergol Clin Immunol 15(2):140–145
Knox RB (1993) Grass pollen, thunderstorms and asthma. Clin Exp Allergy 23:354–359
Lauzurica P, Gurbindo C, Maruri N, Galocha B, Diaz R, Gonzalez J, García R, Lahoz C (1988a) Olive (Olea europaea) pollen allergens-I. Immunochemical characterization by immunoblotting, CRIE and immunodetection by a monoclonal antibody. Mol Immunol 25(4):329–335
Lauzurica P, Maruri N, Galocha B, Gonzalez J, Diaz R, Palomino P, Hernandez D, García R, Lahoz C (1988b) Olive (Olea europaea) pollen allergens. II. Isolation and characterization of two major antigens. Mol Immunol 25(4):337–344
Lombardero M, Quirce S, Duffort O, Barber D, Carpizo J, Chamorro MJ, Lezaun A, Carreira J (1992) Monoclonal antibodies against Olea europaea major allergen: allergenic activity of affinity purified allergen and depleted extract and development of a radioimmunoassay for the quantitation of the allergen. J Allergy Clin Immunol 89(4):884–894
Machia L, Caiaffa MF, D'Amato G, Tursi A (1991) Allergenic significance of Oleaceae pollen. In: D'Amato G, Spieksma FTM, Bonini S (eds) Allergenic pollen and pollinosis in Europe. Blackwell Scientific Publications, London, pp 87–93
Moreno-Grau S, Elvira-Rendueles B, Moreno J, García Sánchez A, Vergara N, Asturias JA, Arilla MC, Ibarrola I, Seoane-Camba JA, Suárez-Cervera M (2006) Correlation between Olea europaea and Parietaria judaica pollen counts and quantification of their major allergens ole e 1 and Par j 1–Par j 2. Ann Allergy Asthma Immunol 96(6):858–864
Moreno-Grau S, Aira MJ, Elvira-Rendueles B, Fernández-González M, Fernández-González D, García-Sánchez A, Martínez-García MJ, Moreno JM, Negral L, Vara A, Rodríguez-Rajo FJ (2016) Assessment of the Olea pollen and its major allergen Ole e 1 concentrations in the bioearosol of two biogeographical areas. Atmos Environ 145:264–271
Napoli A, Aiello D, Di Donna L, Sajjad A, Perri E, Sindona G (2006) Profiling of hydrophilic proteins from Olea europaea olive pollen by MALDI TOF mass spectrometry. Anal Chem 78(10):3434–3443
Obispo TM, Melero JA, Carpizo JA, Carreira J, Lombardero M (1993) The main allergen of Oleaeuropaea (Ole e I) is also present in other species of the Oleaceae family. Clin Exp Allergy 23(4):311–316
Peternel R, Srnec L, Culig J, Zaninović K, Mitić B, Vukusić I (2004) Atmospheric pollen season in Zagreb (Croatia) and its relationship with temperature and precipitation. Int J Biometeorol 48(4):186–191
Plaza MP, Alcázar P, Galán C (2016) Correlation between airborne Olea europaea pollen concentrations and levels of the major allergen Ole e 1 in Córdoba, Spain, 2012–2014. Int J Biometeorol 60:1841–1847
Ribeiro H, Morales S, Salmerón C, Cruz A, Calado L, Rodríguez-García MI, Alché JD, Abreu I (2013) Analysis of the pollen allergen content of twelve olive cultivars grown in Portugal. Aerobiologia 29(4):513–521
Rodríguez Rajo F, Jato V, González Parrado Z, Elvira-Rendueles B, Moreno-Grau S, Vega-Maray A, Fernández González D, Asturias JA, Suárez CM (2011) The combination of airborne pollen and allergen quantification to reliably assess the real pollinosis risk in different bioclimatic areas. Aerobiología 27(1):1–12
Rodríguez R, Villalba M, Batanero E, Gonzalez EM, Monsalve RI, Huecas S, Tejera ML, Ledesma A (2002) Allergenic diversity of the olive pollen. Allergy 57(Suppl 71):6–16
Rodríguez R, Villalba M, Batanero E, Palomares O, Quiralte J, Salamanca G, Sirvent S, Castro L, Prado N (2007) Olive pollen recombinant allergens: Value in diagnosis and immunotherapy. J Investig Allergol Clin Immunol 17(Suppl 1):4–10
Singer BD, Ziska LH, Frenz DA, Gebhard DE (2005) Increasing Amb a 1 content in common ragweed (Ambrosia artemisiifolia L.) as a function of rising atmospheric CO2. Funct. Plant Biol 32:667–670
Soleimani A, Morales S, Jimenez-Lopez JC, Castro AJ, Rodríguez-García MI, Alché JD (2013) Differential expression and sequence polymorphism of the olive pollen allergen Ole e 1 in two Iranian cultivars. Iran J Allergy Asthma Immunol 12(1):18–28
Solomon WR, Burge HA, Muilenberg ML (1983) Allergen carriage by atmospheric aerosol. I: ragweed pollen determinants in smaller micronic fractions. J Allergy Clin Immunol 72:443–447
Stratford S, Barne W, Hohorst DL, Sagert JG, Cotter R, Golubiewski A, Showalter AM, McCormick S, Bedinger P (2001) A leucine-rich repeat region is conserved in pollen extensin-like (Pex) proteins in monocots and dicots. Plant Mol Biol 46(1):43–56
Suárez-Cervera M, Seoane-Camba JA (2005) Biología celular del polen: origen y función de los alérgenos polínicos. In: Valero Santiago AL, Cadahía García A (eds) Polinosis II. Polen y Alergia. Empreso en España, Spain, pp 39–50
Suárez-Cervera M, Vega-Maray A, Castells T, Rodríguez-Rajo FJ, Asturias JA, Le Thomas A, Seoane-Cam JA (2008) An approach to the knowledge of pollen and allergen diversity through lipid transfer protein localization in taxonomically distant pollen grains. Grana 47:272–284
Turkeltaub PC, Gergen PJ (1991) Prevalence of upper and lower respiratory conditions in the U.S. population by social and environmental factors: data from the second National Health and Nutrition Examination Survey 1976 to 1980 (NHANES II). Ann Allergy 67(2 Pt 1):147–154
Vara A, Fernández-González M, Aira MJ, Rodríguez-Rajo FJ (2016a) Oleaceae cross-reactions as potential pollinosis cause in urban areas. Sci Total Environ 542:435–440
Vara A, Fernández-González M, Aira MJ, Rodríguez-Rajo FJ (2016b) Fraxinus pollen and allergen concentrations in Ourense (South-Western Europe). Environ Res 147:241–248
Villalba M, López-Otín C, Martín-Orozco E, Monsalve RI, Palomino P, Lahoz C, Rodríguez R (1990) Isolation of three allergenic fractions of the major allergen from Olea europaea pollen and N-terminal amino acid sequence. Biochem Biophys Res Commun 172(2):523–528
Villalba M, Batanero E, López-Otín C, Sánchez LM, Monsalve RI, González de la Peña MA, Lahoz C, Rodríguez R (1993) Amino acid sequence of Ole e I, the major allergen from olive tree pollen (Olea europaea). Eur J Biochem 216(3):863–869
Waisel Y, Geller-Bernstein C (1996) Reliability of olive pollen extracts for skin prick tests. J Allergy Clin Immunol 98(3):715–716
Waisel Y, Geller-Bernstein C, Keynan N, Arad G (1996) Antigenicity of the pollen proteins of various cultivars of Olea europaea. Allergy 51(11):819–825
Wüthrich B (1989) Epidemiology of the allergic diseases: are they really on the increase? Int Arch Allergy Appl Immunol 90(1):3–10
Zohary D, Hopf M (1994) Olive: Olea europaea. Domestication of plants in the Old World. Clarendon Press, Oxford, pp 137–143
Zohary D, Spiegel-Roy P (1975) Beginnings of fruit growing in the old world. Science 187(4174):319–327
Acknowledgements
The authors would like to thank Prof. Dr. Hulusi MALYER who passed away on November 10, 2020 due to a heart attack during the treatment of COVID-19 for the assistance of field studies and all of the persons who provide technical support to this study.
Availability of data and materials
All data generated or analyzed during this study are included in this published article (and its supplementary information files).
Funding
This study was funded by the Scientific Research Unit of Bursa Uludag University (project number UAP(F) 2011/76 and KUAP(F) 2016/22).
Author information
Authors and Affiliations
Contributions
Sevcan Celenk designed the study and collected the pollen samples. Sevcan Celenk and Buse Vatansever performed the laboratory experiments, analyzed the data, and did the statistical analysis. All authors wrote and read the manuscript and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable
Consent for publication
Not applicable
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Lotfi Aleya
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Celenk, S., Vatansever, B. Assessment of heterogeneity of two cultivars of Olea europaea based on the study of their Ole e 1 protein content. Environ Sci Pollut Res 28, 33545–33556 (2021). https://doi.org/10.1007/s11356-021-13122-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-13122-2


