Allergenicity of Bet v 1 in wheat pollen after exposure to drought stress as a model for climate change

Document Type : Research Paper

Authors

1 Ardabil Agricultural and Natural Resources Research and Education Center, Agriculture Research, Education and Extension Organization (AREEO), Ardabil, Iran

2 Department of Plant Production and Genetics, Faculty of Agriculture, University of Zanjan, Zanjan, Iran

3 Department of Agronomy and Plant Breeding, Faculty of Agriculture, University of Zanjan, Zanjan, Iran

Abstract

In the 21st century, climate changes and global warming have become critical concerns, in that they can affect many of the natural phenomena. It is reported that aeroallergen sensitization is influenced by changes in climate. Bet v 1 is an important birch pollen respiratory allergen and a prototype for the PR-10 protein family, which has been reported in wheat pollen. Two wheat genotypes were exposed to water deficit at the meiosis stage of anthers to investigate the effect of drought stress changes on wheat pollen Bet v 1 expression. Then, mature anthers of wheat underwent molecular experiments in the anthesis stage. Expression analysis was carried out, using Real-time PCR, on the Bet v 1 gene that encodes allergens. The results indicated the induction of Bet v 1 in both genotypes in the water deficit condition. The genotype which had been improved by breeders for tolerating drought more than the other genotype revealed more increase in Bet v 1 expression. Given the great spread of wheat, especially improved genotypes worldwide as a pivotal and crop plant and regarding wheat pollen effect on provoking allergy in humans, Bet v 1 can cause new distress in human society. Therefore, this finding is considered as a new verification of concerns of climate change on human health, which emphasizes the importance of efforts to alleviate climate changes to avoid the risk of public health.

Keywords


Article Title [Persian]

آلرژی زایی Bet v 1 در دانه گرده گندم در مواجهه با تنش خشکی، مدلی برای تغییرات اقلیمی

Authors [Persian]

  • نسترن مهری 1
  • رضا فتوت 2
  • احسان محسنی فرد 3
1 مرکز تحقیقات و آموزش کشاورزی و منابع طبیعی استان اردبیل، سازمان تحقیقات، آموزش و ترویج کشاورزی، اردبیل
2 گروه تولید و ژنتیک گیاهی، دانشکده کشاورزی،دانشگاه زنجان، ایران
3 گروه تولید و ژنتیک گیاهی، دانشکده کشاورزی، دانشگاه زنجان، زنجان
Abstract [Persian]

تغییرات اقلیمی و گرمایش جهانی از مشکلات اساسی قرن 21 ام محسوب می‌شود، به نحوی که می‌تواند بسیاری از پدیده‌های طبیعی را تحت تأثیر قرار دهد. گزارش‌هایی وجود دارند مبنی بر این که حساسیت‌زایی آلرژن‌ها تحت تأثیر تغییرات اقلیمی قرار دارند. آلرژن Bet v 1 آلرژن تنفسی مهم دانه گرده درخت غان و پروتوتایپی از خانواده پروتئینی RP-10 است که در دانه گرده گندم گزارش شده است. جهت بررسی اثر تغییرات تنش خشکی روی بیان ژن Bet v 1 در دانه گرده گندم، دو ژنوتیپ گندم در مرحله میوز بساک تحت تأیر تنش خشکی قرار گرفتند. سپس بساک‌های بالغ گندم در مرحله گرده‌افشانی مورد آزمایش‌های مولکولی قرار گرفتند. تجزیه بیان ژن Bet v 1 که کدکننده آلرژن است، با استفاده از دستگاه Real-time PCR انجام گرفت. نتایج نشان‌دهنده القای Real-time PCR در هر دو ژنوتیپ بود. ژنوتیپی که توسط اصلاح‌کنندگان برای تحمل گرما اصلاح شده بود، دارای افزایش بیان بیشتر ژن Bet v 1 بود. به دلیل گسترش گندم، به ویژه گندم‌های اصلاح شده، به عنوان گیاه اساسی و با در نظر گرفتن اثر دانه گرده گندم روی افزایش آلرژی در انسان، ژن Bet v 1 می‌تواند مشکل جدیدی در جامعه بشریت باشد. بنابراین، این یافته تأیید جدیدی است از نگرانی در مورد اثر تغییرات اقلیمی روی سلامت انسان که بر اهمیت تلاش برای کاهش تغییرات اقلیمی جهت پرهیز از به مخاطره انداختن سلامت عمومی تأکید دارد.

Keywords [Persian]

  • آلرژن تنفسی
  • آلرژی دانه گرده درخت غان
  • بیان ژن
  • گرمایش جهانی
Albertine JM, Manning WJ, DaCosta M, Stinson KA, Muilenberg ML, and Rogers CA, 2014. Projected carbon dioxide to increase grass pollen and allergen exposure despite higher ozone levels. PloS One 9: e111712.
Anderson JT, Inouye DW, McKinney AM, Colautti RI, and Mitchell-Olds T, 2012. Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change. Proceedings of the Royal Society of London B: Biological Sciences  279(1743): 3843-3852.
Anenberg SC, Weinberger KR, Roman H, Neumann JE, Crimmins A, Fann N, Martinich J, and Kinney PL, 2017. Impacts of oak pollen on allergic asthma in the United States and potential influence of future climate change. GeoHealth 1: 80-92.
Assarehzadegan MA, Shakurnia, A, and Amini A, 2013. The most common aeroallergens in a tropical region in Southwestern Iran. World Allergy Organization Journal 6: 7.
Behrendt H and Ring J, 2012. Climate change, environment and allergy. In: Ring J, Darsow U, and Behrendt H (eds.). New Trends in Allergy and Atopic Eczema. Pp 7-14. Karger Publishers, Switzerland.
Blankestijn MA, Knulst AC, Knol EF, Le TM, Rockmann H, Otten HG, and Klemans RJ, 2017. Sensitization to PR-10 proteins is indicative of distinctive sensitization patterns in adults with a suspected food allergy. Clinical and Translational Allergy 7: 42.
Botton A, Lezzer P, Dorigoni A, Barcaccia G, Ruperti B, and Ramina A, 2008. Genetic and environmental factors affecting allergen-related gene expression in apple fruit (Malus domestica L. Borkh). Journal of Agricultural and Food Chemistry 56: 6707-6716.
Bouzid M, Colón-González FJ, Lung T, Lake IR, and Hunter PR, 2014. Climate change and the emergence of vector-borne diseases in Europe: case study of dengue fever. BMC Public Health 14: 781.
Boyer J and Westgate M, 2004. Grain yields with limited water. Journal of Experimental Botany 55: 2385-2394.
Butterworth MK, Morin CW, and Comrie AC, 2017. An analysis of the potential impact of climate change on dengue transmission in the southeastern United States. Environmental Health Perspectives 125: 579.
Calinger KM, Queenborough S, and Curtis PS, 2013. Herbarium specimens reveal the footprint of climate change on flowering trends across north‐central North America. Ecology Letters 16: 1037-1044.
Caminade C, Kovats S, Rocklov J, Tompkins AM, Morse AP, Colón-González FJ, Stenlund H, Martens P, and Lloyd SJ, 2014. Impact of climate change on global malaria distribution. Proceedings of the National Academy of Sciences 111: 3286-3291.
Cecchi L, d’Amato G, Ayres J, Galan C, Forastiere F, Forsberg B, Gerritsen J, Nunes C, Behrendt H, and Akdis C, 2010. Projections of the effects of climate change on allergic asthma: the contribution of aerobiology. Allergy 65: 1073-1081.
Ciprandi G, Comite P, Mussap M, De Amici M, Quaglini S, Barocci F, Marseglia G, and Scala E, 2016. Profiles of birch sensitization (Bet v 1, Bet v 2, and Bet v 4) and oral allergy syndrome across Italy. Journal of Investigational Allergology and Clinical Immunology 26: 244-248.
Dai A, 2011. Drought under global warming: a review. Wiley Interdisciplinary Reviews: Climate Change 2: 45-65.
Ebi KL, 2011. Climate Change and Health. In: Nriagu, J (ed). Encyclopedia of Environmental Health. Pp. 680-689. Elsevier, Netherlands.
Ebi KL and Bowen K, 2016. Extreme events as sources of health vulnerability: Drought as an example. Weather and Climate Extremes 11: 95-102.
El Kelish A, Zhao F, Heller W, Durner J, Winkler JB, Behrendt H, Traidl-Hoffmann C, Horres R, Pfeifer M, and Frank U, 2014. Ragweed (Ambrosia artemisiifolia) pollen allergenicity: SuperSAGE transcriptomic analysis upon elevated CO2 and drought stress. BMC Plant Biology 14: 176.
FAO, 2019. FAOSTAT. Agriculture Organization of the United Nations Statistics Division. Economic and Social Development Department, Rome, Italy. http://faostat3. fao. org/home/E.
Fereidouni M, Hossini RF, Azad FJ, Assarezadegan MA, and Varasteh A, 2009. Skin prick test reactivity to common aeroallergens among allergic rhinitis patients in Iran. Allergologia et Immunopathologia 37: 73-79.
Fotovat R, Alikhani M, Valizadeh M, Mirzaei M, and H Salekdeh G, 2017. A proteomics approach to discover drought tolerance proteins in wheat pollen grain at meiosis stage. Protein and Peptide Letters 24: 26-36.
Ghaffari J and Aarabi M, 2013. The prevalence of pediatric asthma in the Islamic Republic of Iran: a systematic review and meta-analysis. Journal of Pediatrics Review 1: 2-11.
Hales S, Edwards SJ, and Kovats RS, 2003. Impacts on health of climate extremes. Climate change and health: risks and responses. World Health Organization, Geneva, Switzerland.
Hamaoui-Laguel L, Vautard R, Liu L, Solmon F, Viovy N, Khvorostyanov D, Essl F, Chuine I, Colette A, and Semenov MA, 2015. Effects of climate change and seed dispersal on airborne ragweed pollen loads in Europe. Nature Climate Change 5: 766-771.
Höflich C, Balakirski G, Hajdu Z, Baron JM, Kaiser L, Czaja K, Merk HF, Gerdsen S, Strassen U, and Bas M, 2016. Potential health risk of allergenic pollen with climate change associated spreading capacity: ragweed and olive sensitization in two German federal states. International Journal of Hygiene and Environmental Health 219: 252-260.
Iran Communication and Information Technology Organization, 2016. Deputy of Planning and Economic Affairs, Tehran, Iran. http://maj.ir/Dorsapax/userfiles/Sub65/Amarnamehj194-95-site.pdf. Accessed 11 March 2018.
Kim SH, Park HS, and Jang JY, 2011. Impact of meteorological variation on hospital visits of patients with tree pollen allergy. BMC Public Health 11: 890.
Kleine-Tebbe J, Ballmer-Weber B, Breiteneder H, and Vieths S, 2017a. Bet v 1 and its homologs: triggers of tree-pollen allergy and birch pollen-associated cross-reactions. In: Kleine-Tebbe J and Jakob T (eds.). Molecular Allergy Diagnostics. Pp. 21-42. Springer, Germany.
Kleine-Tebbe J, Ollert M, Radauer C, and Jakob T, 2017b. Introduction to molecular allergology: protein families, databases, and potential benefits. In: Kleine-Tebbe J and Jakob T (eds.). Molecular Allergy Diagnostics. Pp. 3-19. Springer, Germany.
LaDeau SL and Clark J, 2006. Pollen production by Pinus taeda growing in elevated atmospheric CO2. Functional Ecology 20: 541-547.
Lake IR, Jones NR, Agnew M, Goodess CM, Giorgi F, Hamaoui-Laguel L, Semenov MA, Solomon F, Storkey J, and Vautard R, 2017. Climate change and future pollen allergy in Europe. Environmental Health Perspectives 125: 385.
Livak KJ and Schmittgen TD, 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25: 402-408.
Mehri N, Fotovat R, Mirzaei M, Mohseni Fard E, Parsamatin P, Hasan MT, Wu Y, Ghaffari MR, and Hosseini Salekdeh G, 2020. Proteomic analysis of wheat contrasting genotypes reveals the interplay between primary metabolic and regulatory pathways in anthers under drougt stress. Journal of Proteomics. 226: 103895.
Pahr S, Constantin C, Mari A, Scheiblhofer S, Thalhamer J, Ebner C, Vrtala S, Mittermann I, and Valenta R, 2012. Molecular characterization of wheat allergens specifically recognized by patients suffering from wheat‐induced respiratory allergy. Clinical and Experimental Allergy 42: 597-609.
Palosuo K, Alenius H, Varjonen E, Koivuluhta M, Mikkola J, Keskinen H, Kalkkinen N, and Reunala T, 1999. A novel wheat gliadin as a cause of exercise-induced anaphylaxis. Journal of Allergy and Clinical Immunology 103: 912-917.
Pfaffl MW, Horgan GW, and Dempfle L, 2002. Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Research 30(9): e36.
Roth-Walter F, Gomez-Casado C, Pacios LF, Mothes-Luksch N, Roth GA, Singer J, Diaz-Perales A, and Jensen-Jarolim E, 2014. Bet v 1 from birch pollen is a lipocalin-like protein acting as allergen only when devoid of iron by promoting Th2 lymphocytes. Journal of Biological Chemistry 289: 17416-17421.
Ryan SJ, McNally A, Johnson LR, Mordecai EA, Ben-Horin T, Paaijmans K, and Lafferty KD, 2015. Mapping physiological suitability limits for malaria in Africa under climate change. Vector-Borne and Zoonotic Diseases 15: 718-725.
Sampson HA, 2001. Utility of food-specific IgE concentrations in predicting symptomatic food allergy. Journal of Allergy and Clinical Immunology 107: 891-896.
Seed and Plant Improvement Institute, 2015. Introduction of crop cultivars (Food Safety and Health). Agricultural Research, Education and Extension Organization Press, Iran. Volume 1(In Persian).
Stemeseder T, Klinglmayr E, Moser S, Lueftenegger L, Lang R, Himly M, Oostingh GJ, Zumbach J, Bathke AC, and Hawranek T, 2017. Cross‐sectional study on allergic sensitization of Austrian adolescents using molecule‐based IgE profiling. Allergy 72: 754-763.
Storkey J, Stratonovitch P, Chapman DS, Vidotto F, and Semenov MA, 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.
Todea, DA, Suatean I, Coman AC, and Rosca LE, 2013. The effect of climate change and air pollution on allergenic potential of pollens. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 41(2):646-650.
Wayne P, Foster S, Connolly J, Bazzaz F, and Epstein P, 2002. Production of allergenic pollen by ragweed and Immunology 88: 279-282.
Westman M, Lupinek C, Bousquet J, Andersson N, Pahr S, Baar A, Bergström A, Holmström M, Stjärne P, and Carlsen KCL, 2015. Early childhood IgE reactivity to pathogenesis-related class 10 proteins predicts allergic rhinitis in adolescence. Journal of Allergy and Clinical Immunology 135: 1199-1206. e1111.
Zareii Kh, 2010. Selection of internal control genes for quantifing gene expression under drought stress in meiosis stage of wheat. Thesis for Master’s degree in Zanjan University, Zanjan, Iran (In Persian).
Zhang Y, Bielory L, Mi Z, Cai T, Robock A, and Georgopoulos P, 2015. Allergenic pollen season variations in the past two decades under changing climate in the United States. Global Change Biology 21: 1581-1589.
Ziello C, Sparks TH, Estrella N, Belmonte J, Bergmann KC, Bucher E, Brighetti MA, Damialis A, Detandt M, and Galán C, 2012. Changes to airborne pollen counts across Europe. PloS One 7: e34076.
Ziska L, Knowlton K, Rogers C, Dalan D, Tierney N, Elder MA, Filley W, Shropshire J, Ford LB, and Hedberg C, 2011. Recent warming by latitude associated with increased length of ragweed pollen season in central North America. Proceedings of the National Academy of Sciences 108: 4248-4251.