vavilovВавиловский журнал генетики и селекцииVavilov Journal of Genetics and Breeding2500-3259Institute of Cytology and Genetics of Siberian Branch of the RAS10.18699/VJGB-22-96vavilov-3581Research ArticleЭВОЛЮЦИОННАЯ КОМПЬЮТЕРНАЯ БИОЛОГИЯEVOLUTIONARY COMPUTATIONAL BIOLOGYПромоторы генов, кодирующих β-амилазу, альбумин и глобулин пищевых растений в сравнении с непищевыми, характеризуются более низкой аффинностью к ТАТА-связывающему белку: in silico анализRussian Science Foundation grant No. 20-14-00140 supported this study. The authors are thankful to the multi-access Center “Bioinformatics” for the use of computational resources as supported by Russian government project FWNR-2022-0020 and the Russian Federal Science and Technology Program for the Development of Genetic Technologies.https://orcid.org/0000-0002-0347-2252ВишневскийО. В.VishnevskyO. V.

Новосибирск

Novosibirsk

https://orcid.org/0000-0002-2724-5441ЧадаеваИ. В.ChadaevaI. V.

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Novosibirsk

https://orcid.org/0000-0002-1467-9312ШарыповаЕ. Б.SharypovaE. B.

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Novosibirsk

ХандаевБ. М.KhandaevB. M.

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Novosibirsk

ЗолотареваК. А.ZolotarevaK. A.

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Novosibirsk

КазачекА. В.KazachekA. V.

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Novosibirsk

https://orcid.org/0000-0003-2715-9612ПономаренкоП. М.PonomarenkoP. M.

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Novosibirsk

https://orcid.org/0000-0001-9132-7997ПодколодныйН. Л.PodkolodnyN. L.

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Novosibirsk

https://orcid.org/0000-0003-4795-0954РассказовД. А.RasskazovD. A.

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Novosibirsk

https://orcid.org/0000-0002-4304-1190БогомоловА. Г.ZemlyanskayaE. V.

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Novosibirsk

https://orcid.org/0000-0003-4359-6089ПодколоднаяО. А.BogomolovA. G.

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Novosibirsk

https://orcid.org/0000-0003-3247-0114СавинковаЛ. К.PodkolodnayaO. A.

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Novosibirsk

https://orcid.org/0000-0003-4543-4104ЗемлянскаяЕ. В.SavinkovaL. K.

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Novosibirsk

https://orcid.org/0000-0003-1663-318XПономаренкоМ. П.PonomarenkoM. P.

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Novosibirsk

pon@bionet.nsc.ruФедеральный исследовательский центр Институт цитологии и генетики Сибирского отделения Российской академии наукРоссияInstitute of Cytology and Genetics of the Siberian Branch of the Russian Academy of SciencesRussian FederationФедеральный исследовательский центр Институт цитологии и генетики Сибирского отделения Российской академии наук; Институт вычислительной математики и математической геофизики Сибирского отделения Российской академии наукРоссияInstitute of Cytology and Genetics of the Siberian Branch of the Russian Academy of Sciences; Institute of Computational Mathematics and Mathematical Geophysics of the Siberian Branch of the Russian Academy of SciencesRussian Federation202204012023268798­-805Copyright © Вишневский О.В., Чадаева И.В., Шарыпова Е.Б., Хандаев Б.М., Золотарева К.А., Казачек А.В., Пономаренко П.М., Подколодный Н.Л., Рассказов Д.А., Богомолов А.Г., Подколодная О.А., Савинкова Л.К., Землянская Е.В., Пономаренко М.П., 20232023Вишневский О.В., Чадаева И.В., Шарыпова Е.Б., Хандаев Б.М., Золотарева К.А., Казачек А.В., Пономаренко П.М., Подколодный Н.Л., Рассказов Д.А., Богомолов А.Г., Подколодная О.А., Савинкова Л.К., Землянская Е.В., Пономаренко М.П.Vishnevsky O.V., Chadaeva I.V., Sharypova E.B., Khandaev B.M., Zolotareva K.A., Kazachek A.V., Ponomarenko P.M., Podkolodny N.L., Rasskazov D.A., Zemlyanskaya E.V., Bogomolov A.G., Podkolodnaya O.A., Savinkova L.K., Ponomarenko M.P.This work is licensed under a Creative Commons Attribution 4.0 License.https://vavilov.elpub.ru/jour/article/view/3581

Принято считать, что при доместикации пищевых растений отбор шел на урожайность, технологичность переработки в продукты питания, устойчивость к патогенам и стрессовым воздействиям окружающей среды. При этом также могли оцениваться вкусовые качества продуктов питания растительного происхождения и их ценность для здоровья. Однако неясно, проводил ли человек в прошлом наряду с положительным отбором на полезные свойства растений одновременно отбор против таких вредоносных свойств, как способность вызывать аллергические реакции. Этот вопрос становится все более актуальным по мере роста аллергизации населения как вызова современной медицине. В связи с этим селекционерами уже ведутся интенсивные исследования по созданию гипоаллергенных форм пищевых растений. В этой работе рассмотрены альбумин, глобулин и β­амилаза мягкой пшеницы Triticum aestivum L. (1753), идентифицированные ранее как мишени для атак иммуноглобулинов класса Е человека. Нашей целью было найти на геномном уровне следы отрицательного отбора в прошлом против гипераллергенности трех белков (альбумин, глобулин и β­амилаза) при одомашнивании предковых форм современных пищевых растений. Для этого мы сфокусировали поиск на сайте связывания ТАТА­связывающего белка (ТВР) как локализованном в узком районе [–70; –20] относительно старта транскрипции, консервативном, необходимом для первичной инициации транскрипции и наиболее изученном регуляторном сигнале в геномах эукариот. Ранее нами был создан свободно доступный веб­сервис Plant_SNP_TATA_Z­tester для оценки величин равновесной константы диссоциации (KD) комплексов ТВР с проксимальными промоторами генов растений по их последовательностям ДНК длиной 90 п. о. В настоящей работе с его по мощью проанализированы 363 последовательности ДНК промоторов генов 43 видов растений. Обнаружено, что пищевые растения, в сравнении с непищевыми, характеризуются достоверно более низкой аффинностью ТBP к проксимальным промоторам их генов, гомологичных генам глобулина, альбумина и β­амилазы мягкой пшеницы как пищевых аллергенов ( p< 0.01, Z­критерий Фишера). Это свидетельствует об отборе при доместикации пищевых растений в прошлом на снижение уровня данных аллергенных белков.

It is generally accepted that during the domestication of food plants, selection was focused on their productivity, the ease of their technological processing into food, and resistance to pathogens and environmental stressors. Besides, the palatability of plant foods and their health benefits could also be subjected to selection by humans in the past. Nonetheless, it is unclear whether in antiquity, aside from positive selection for beneficial properties of plants, humans simultaneously selected against such detrimental properties as allergenicity. This topic is becoming increasingly relevant as the allergization of the population grows, being a major challenge for modern medicine. That is why intensive research by breeders is already underway for creating hypoallergenic forms of food plants. Accordingly, in this paper, albumin, globulin, and β­amylase of common wheat Triticum aestivum L. (1753) are analyzed, which have been identified earlier as targets for attacks by human class E immunoglobulins. At the genomic level, we wanted to find signs of past negative selection against the allergenicity of these three proteins (albumin, globulin, and β­amylase) during the domestication of ancestral forms of modern food plants. We focused the search on the TATA­binding protein (TBP)­binding site because it is located within a narrow region (between positions –70 and –20 relative to the corresponding transcription start sites), is the most conserved, necessary for primary transcription initiation, and is the best­studied regulatory genomic signal in eukaryotes. Our previous studies presented our publicly available Web service Plant_SNP_TATA_Z­tester, which makes it possible to estimate the equilibrium dissociation constant (KD) of TBP complexes with plant proximal promoters (as output data) using 90 bp of their DNA sequences (as input data). In this work, by means of this bioinformatics tool, 363 gene promoter DNA sequences representing 43 plant species were analyzed. It was found that compared with non­food plants, food plants are characterized by significantly weaker affinity of TBP for proximal promoters of their genes homologous to the genes of commonwheat globulin, albumin, and β­amylase (food allergens) (p< 0.01, Fisher’s Z­test). This evidence suggests that in the past humans carried out selective breeding to reduce the expression of food plant genes encoding these allergenic proteins.

пищевые аллергеныальбуминглобулинβ­амилазагенпромотормягкая пшеница Triticum aestivum L. (1753)растенияTATA­связывающий белокTATA­боксдоместикацияотбороценки in silicofood allergenalbuminglobulinβ­amylasegenepromotercommon wheat Triticum aestivum L. (1753)plantsTATA­binding proteinTATA boxdomesticationselectionin silico estimateRussian Science Foundation grant No. 20-14-00140 supported this study. The authors are thankful to the multi-access Center “Bioinformatics” for the use of computational resources as supported by Russian government project FWNR-2022-0020 and the Russian Federal Science and Technology Program for the Development of Genetic Technologies.ReferencesArkova O., Kuznetsov N., Fedorova O., Savinkova L. A real­time study of the interaction of TBP with a TATA box­containing duplex identical to an ancestral or minor allele of human gene LEP or TPI. J. Biomol. Struct. Dyn. 2017;35(14):3070-3081. DOI 10.1080/07391102.2016.1241190.Arkova O., Kuznetsov N., Fedorova O., Savinkova L. A real­time study of the interaction of TBP with a TATA box­containing duplex identical to an ancestral or minor allele of human gene LEP or TPI. J. Biomol. Struct. Dyn. 2017;35(14):3070-3081. DOI 10.1080/07391102.2016.1241190.Auble D.T. The dynamic personality of TATA­binding protein. Trends Biochem. Sci. 2009;34(2):49-52. DOI 10.1016/j.tibs.2008.10.008.Auble D.T. The dynamic personality of TATA­binding protein. Trends Biochem. Sci. 2009;34(2):49-52. DOI 10.1016/j.tibs.2008.10.008.Benson D.A., Clark K., Karsch­Mizrachi I., Lipman D.J., Ostell J., Sayers E.W. GenBank. Nucleic Acids Res. 2015;43(Database issue):D30-D35. DOI 10.1093/nar/gku1216.Benson D.A., Clark K., Karsch­Mizrachi I., Lipman D.J., Ostell J., Sayers E.W. GenBank. Nucleic Acids Res. 2015;43(Database issue):D30-D35. DOI 10.1093/nar/gku1216.Berg O.G., von Hippel P.H. Selection of DNA binding sites by regulatory proteins. Statistical­mechanical theory and application to operators and promoters. J. Mol. Biol. 1987;193(4):723­750. DOI 10.1016/0022-2836(87)90354-8.Berg O.G., von Hippel P.H. Selection of DNA binding sites by regulatory proteins. Statistical­mechanical theory and application to operators and promoters. J. Mol. Biol. 1987;193(4):723­750. DOI 10.1016/0022-2836(87)90354-8.Bucher P. Weight matrix descriptions of four eukaryotic RNA polymerase II promoter elements derived from 502 unrelated promoter sequences. J. Mol. Biol. 1990;212(4):563-578. DOI 10.1016/00222836(90)90223­9.Bucher P. Weight matrix descriptions of four eukaryotic RNA polymerase II promoter elements derived from 502 unrelated promoter sequences. J. Mol. Biol. 1990;212(4):563-578. DOI 10.1016/00222836(90)90223­9.Cavazza A., Mattarozzi M., Franzoni A., Careri M. A spotlight on analytical prospects in food allergens: From emerging allergens and novel foods to bioplastics and plant­based sustainable food contact materials. Food Chem. 2022;388:132951. DOI 10.1016/j.foodchem. 2022.132951.Cavazza A., Mattarozzi M., Franzoni A., Careri M. A spotlight on analytical prospects in food allergens: From emerging allergens and novel foods to bioplastics and plant­based sustainable food contact materials. Food Chem. 2022;388:132951. DOI 10.1016/j.foodchem. 2022.132951.Choukrallah M.A., Kobi D., Martianov I., Pijnappel W.W., Mischerikow N., Ye T., Heck A.J., Timmers H.T., Davidson I. Interconversion between active and inactive TATA­binding protein transcription complexes in the mouse genome. Nucleic Acids Res. 2012;40(4): 1446-1459. DOI 10.1093/nar/gkr802.Choukrallah M.A., Kobi D., Martianov I., Pijnappel W.W., Mischerikow N., Ye T., Heck A.J., Timmers H.T., Davidson I. Interconversion between active and inactive TATA­binding protein transcription complexes in the mouse genome. Nucleic Acids Res. 2012;40(4): 1446-1459. DOI 10.1093/nar/gkr802.Coleman R.A., Pugh B.F. Evidence for functional binding and stable sliding of the TATA binding protein on nonspecific DNA. J. Biol. Chem. 1995;270(23):13850-13859. DOI 10.1074/jbc.270.23.13850.Coleman R.A., Pugh B.F. Evidence for functional binding and stable sliding of the TATA binding protein on nonspecific DNA. J. Biol. Chem. 1995;270(23):13850-13859. DOI 10.1074/jbc.270.23.13850.Delgadillo R.F., Whittington J.E., Parkhurst L.K., Parkhurst L.J. The TATA­binding protein core domain in solution variably bends TATA sequences via a three­step binding mechanism. Biochemistry. 2009; 48(8):1801-1809. DOI 10.1021/bi8018724.Delgadillo R.F., Whittington J.E., Parkhurst L.K., Parkhurst L.J. The TATA­binding protein core domain in solution variably bends TATA sequences via a three­step binding mechanism. Biochemistry. 2009; 48(8):1801-1809. DOI 10.1021/bi8018724.Drachkova I., Savinkova L., Arshinova T., Ponomarenko M., Peltek S., Kolchanov N. The mechanism by which TATA­box polymorphisms associated with human hereditary diseases influence interactions with the TATA­binding protein. Hum. Mutat. 2014;35(5):601­608. DOI 10.1002/humu.22535.Drachkova I., Savinkova L., Arshinova T., Ponomarenko M., Peltek S., Kolchanov N. The mechanism by which TATA­box polymorphisms associated with human hereditary diseases influence interactions with the TATA­binding protein. Hum. Mutat. 2014;35(5):601­608. DOI 10.1002/humu.22535.Fire A., Samuels M., Sharp P.A. Interactions between RNA polymerase II, factors, and template leading to accurate transcription. J. Biol. Chem. 1984;259(4):2509-2516. DOI 10.1016/S0021-9258(17)43382­5.Fire A., Samuels M., Sharp P.A. Interactions between RNA polymerase II, factors, and template leading to accurate transcription. J. Biol. Chem. 1984;259(4):2509-2516. DOI 10.1016/S0021-9258(17)43382­5.Flatters D., Lavery R. Sequence­dependent dynamics of TATA­Box binding sites. Biophys. J. 1998;75(1):372-381. DOI 10.1016/S00063495(98)77521­6.Flatters D., Lavery R. Sequence­dependent dynamics of TATA­Box binding sites. Biophys. J. 1998;75(1):372-381. DOI 10.1016/S00063495(98)77521­6.Hahn S., Buratowski S., Sharp P.A., Guarente L. Yeast TATA­binding protein TFIID binds to TATA elements with both consensus and nonconsensus DNA sequences. Proc. Natl. Acad. Sci. USA. 1989; 86(15):5718-5722. DOI 10.1073/pnas.86.15.5718.Hahn S., Buratowski S., Sharp P.A., Guarente L. Yeast TATA­binding protein TFIID binds to TATA elements with both consensus and nonconsensus DNA sequences. Proc. Natl. Acad. Sci. USA. 1989; 86(15):5718-5722. DOI 10.1073/pnas.86.15.5718.Hong L., Pan M., Xie X., Liu K., Yang J., Wang S., Wang S. Aptamerbased fluorescent biosensor for the rapid and sensitive detection of allergens in food matrices. Foods. 2021;10(11):2598. DOI 10.3390/foods10112598. IUPAC­IUB Commission on Biochemical Nomenclature (CBN). Abbreviations and symbols for nucleic acids, polynucleotides and their constituents. Recommendations 1970. Biochem. J. 1970;120(3): 449-454. DOI 10.1042/bj1200449.Hong L., Pan M., Xie X., Liu K., Yang J., Wang S., Wang S. Aptamerbased fluorescent biosensor for the rapid and sensitive detection of allergens in food matrices. Foods. 2021;10(11):2598. DOI 10.3390/foods10112598. IUPAC­IUB Commission on Biochemical Nomenclature (CBN). Abbreviations and symbols for nucleic acids, polynucleotides and their constituents. Recommendations 1970. Biochem. J. 1970;120(3): 449-454. DOI 10.1042/bj1200449.Martianov I., Viville S., Davidson I. RNA polymerase II transcription in murine cells lacking the TATA binding protein. Science. 2002; 298(5595):1036-1039. DOI 10.1126/science.1076327.Martianov I., Viville S., Davidson I. RNA polymerase II transcription in murine cells lacking the TATA binding protein. Science. 2002; 298(5595):1036-1039. DOI 10.1126/science.1076327.Mogno I., Vallania F., Mitra R.D., Cohen B.A. TATA is a modular component of synthetic promoters. Genome Res. 2010;20(10):13911397. DOI 10.1101/gr.106732.110.Mogno I., Vallania F., Mitra R.D., Cohen B.A. TATA is a modular component of synthetic promoters. Genome Res. 2010;20(10):13911397. DOI 10.1101/gr.106732.110.Muller F., Lakatos L., Dantonel J., Strahle U., Tora L. TBP is not universally required for zygotic RNA polymerase II transcription in zebrafish. Curr. Biol. 2001;11(4):282-287. DOI 10.1016/s0960-9822(01)00076­8.Muller F., Lakatos L., Dantonel J., Strahle U., Tora L. TBP is not universally required for zygotic RNA polymerase II transcription in zebrafish. Curr. Biol. 2001;11(4):282-287. DOI 10.1016/s0960-9822(01)00076­8.Ponomarenko P., Chadaeva I., Rasskazov D.A., Sharypova E., Kashina E.V., Drachkova I., Zhechev D., Ponomarenko M.P., Savinkova L.K., Kolchanov N. Candidate SNP markers of familial and sporadic Alzheimer’s diseases are predicted by a significant change in the affinity of TATA-binding protein for human gene promoters. Front. Aging Neurosci. 2017;9:231. DOI 10.3389/fnagi.2017.00231.Ponomarenko P., Chadaeva I., Rasskazov D.A., Sharypova E., Kashina E.V., Drachkova I., Zhechev D., Ponomarenko M.P., Savinkova L.K., Kolchanov N. Candidate SNP markers of familial and sporadic Alzheimer’s diseases are predicted by a significant change in the affinity of TATA-binding protein for human gene promoters. Front. Aging Neurosci. 2017;9:231. DOI 10.3389/fnagi.2017.00231.Ponomarenko P.M., Ponomarenko M.P., Drachkova I.A., Lysova M.V., Arshinova T.V., Savinkova L.K., Kolchanov N.A. Prediction of the affinity of the TATA-binding protein to TATA boxes with single nucleotide polymorphisms. Mol. Biol. (Moscow). 2009; 43(3):472­479. DOI 10.1134/S0026893309030157.Ponomarenko P.M., Ponomarenko M.P., Drachkova I.A., Lysova M.V., Arshinova T.V., Savinkova L.K., Kolchanov N.A. Prediction of the affinity of the TATA-binding protein to TATA boxes with single nucleotide polymorphisms. Mol. Biol. (Moscow). 2009; 43(3):472­479. DOI 10.1134/S0026893309030157.Ponomarenko P., Savinkova L., Drachkova I., Lysova M., Arshinova T., Ponomarenko M., Kolchanov N. A step-by-step model of TBP/TATA box binding allows predicting human hereditary diseases by single nucleotide polymorphism. Dokl. Biochem. Biophys. 2008;419:8892. DOI 10.1134/S1607672908020117.Ponomarenko P., Savinkova L., Drachkova I., Lysova M., Arshinova T., Ponomarenko M., Kolchanov N. A step-by-step model of TBP/TATA box binding allows predicting human hereditary diseases by single nucleotide polymorphism. Dokl. Biochem. Biophys. 2008;419:8892. DOI 10.1134/S1607672908020117.Prescott S.L., Logan A.C., Bristow J., Rozzi R., Moodie R., Redvers N., Haahtela T., Warber S., Poland B., Hancock T., Berman B. Exiting the anthropocene: achieving personal and planetary health in the 21st century. Allergy. 2022;77(12):3498-3512. DOI 10.1111/all.15419.Prescott S.L., Logan A.C., Bristow J., Rozzi R., Moodie R., Redvers N., Haahtela T., Warber S., Poland B., Hancock T., Berman B. Exiting the anthropocene: achieving personal and planetary health in the 21st century. Allergy. 2022;77(12):3498-3512. DOI 10.1111/all.15419.Rasskazov D., Chadaeva I., Sharypova E., Zolotareva K., Khandaev B., Ponomarenko P., Podkolodnyy N., Tverdokhleb N., Vishnevsky O., Bogomolov A., Podkolodnaya O., Savinkova L., Zemlyanskaya E.,Rasskazov D., Chadaeva I., Sharypova E., Zolotareva K., Khandaev B., Ponomarenko P., Podkolodnyy N., Tverdokhleb N., Vishnevsky O., Bogomolov A., Podkolodnaya O., Savinkova L., Zemlyanskaya E.,Golubyatnikov V., Kolchanov N., Ponomarenko M. Plant_SNP_ TATA_Z­tester: a Web service that unequivocally estimates the impact of proximal promoter mutations on plant gene expression. Int. J. Mol. Sci. 2022;23(15):8684. DOI 10.3390/ijms23158684.Golubyatnikov V., Kolchanov N., Ponomarenko M. Plant_SNP_ TATA_Z­tester: a Web service that unequivocally estimates the impact of proximal promoter mutations on plant gene expression. Int. J. Mol. Sci. 2022;23(15):8684. DOI 10.3390/ijms23158684.Rhee H., Pugh B. Genome­wide structure and organization of eukaryotic pre­initiation complexes. Nature. 2012;483(7389):295­301. DOI 10.1038/nature10799.Rhee H., Pugh B. Genome­wide structure and organization of eukaryotic pre­initiation complexes. Nature. 2012;483(7389):295­301. DOI 10.1038/nature10799.Savinkova L., Drachkova I., Arshinova T., Ponomarenko P., Ponomarenko M., Kolchanov N. An experimental verification of the predicted effects of promoter TATA-box polymorphisms associated with human diseases on interactions between the TATA boxes and TATA­binding protein. PLoS One. 2013;8(2):e54626. DOI 10.1371/journal.pone.0054626.Savinkova L., Drachkova I., Arshinova T., Ponomarenko P., Ponomarenko M., Kolchanov N. An experimental verification of the predicted effects of promoter TATA-box polymorphisms associated with human diseases on interactions between the TATA boxes and TATA­binding protein. PLoS One. 2013;8(2):e54626. DOI 10.1371/journal.pone.0054626.Savinkova L.K., Ponomarenko M.P., Ponomarenko P.M., Drachkova I.A., Lysova M.V., Arshinova T.V., Kolchanov N.A. TATA box polymorphisms in human gene promoters and associated hereditary pathologies. Biochemistry (Moscow). 2009;74(2):117­129. DOI 10.1134/s0006297909020011.Savinkova L.K., Ponomarenko M.P., Ponomarenko P.M., Drachkova I.A., Lysova M.V., Arshinova T.V., Kolchanov N.A. TATA box polymorphisms in human gene promoters and associated hereditary pathologies. Biochemistry (Moscow). 2009;74(2):117­129. DOI 10.1134/s0006297909020011.Wang Y., Weng J., Zhu C., Ai R., Zhou J., Wang C., Chen Q., Fu L. Allergenicity assessment and allergen profile analysis of different Chinese wheat cultivars. World Allergy Organ. J. 2021;14(7):100559. DOI 10.1016/j.waojou.2021.100559.Wang Y., Weng J., Zhu C., Ai R., Zhou J., Wang C., Chen Q., Fu L. Allergenicity assessment and allergen profile analysis of different Chinese wheat cultivars. World Allergy Organ. J. 2021;14(7):100559. DOI 10.1016/j.waojou.2021.100559.

The authors declare that there are no conflicts of interest present.