vavilovВавиловский журнал генетики и селекцииVavilov Journal of Genetics and Breeding2500-3259Institute of Cytology and Genetics of Siberian Branch of the RAS10.18699/VJ21.009vavilov-2918Research ArticleБИОИНФОРМАТИКА И СИСТЕМНАЯ КОМПЬЮТЕРНАЯ БИОЛОГИЯBIOINFORMATICS AND COMPUTATIONAL SYSTEMS BIOLOGYАвтоматическое фенотипирование морфологии колоса тетра- и гексаплоидных видов пшеницы методами компьютерного зренияAutomatic morphology phenotyping of tetra- and hexaploid wheat spike using computer vision methodshttps://orcid.org/0000-0002-3011-6288ПронозинА. Ю.PronozinA. Yu.

Новосибирск

Novosibirsk

ПаулишА. А.PaulishA. A.

Новосибирск

Novosibirsk

ЗаварзинЕ. А.ZavarzinE. A.

Новосибирск

Novosibirsk

ПриходькоА. Ю.PrikhodkoA. Yu.

Новосибирск

Novosibirsk

ПрохошинН. М.ProkhoshinN. M.

Новосибирск

Novosibirsk

https://orcid.org/0000-0002-1084-9521КручининаЮ. В.KruchininaYu. V.

Новосибирск

Novosibirsk

ГончаровН. П.GoncharovN. P.

Новосибирск

Novosibirsk

КомышевЕ. Г.KomyshevE. G.

Новосибирск

Novosibirsk

ГенаевМ. А.GenaevM. A.

Новосибирск

Novosibirsk

mag@bionet.nsc.ruФедеральный исследовательский центр Институт цитологии и генетики Сибирского отделения Российской академии наукРоссияInstitute of Cytology and Genetics of Siberian Branch of the Russian Academy of SciencesRussian FederationНовосибирский национальный исследовательский государственный университетРоссияNovosibirsk State UniversityRussian FederationФедеральный исследовательский центр Институт цитологии и генетики Сибирского отделения Российской академии наук; Курчатовский геномный центр Института цитологии и генетики Сибирского отделения Российской академии наукРоссияInstitute of Cytology and Genetics of Siberian Branch of the Russian Academy of Sciences; Kurchatov Genomics Center of the Institute of Cytology and Genetics of Siberian Branch of the Russian Academy of SciencesRussian FederationФедеральный исследовательский центр Институт цитологии и генетики Сибирского отделения Российской академии наук; Новосибирский государственный аграрный университетРоссияInstitute of Cytology and Genetics of Siberian Branch of the Russian Academy of Sciences; Novosibirsk State Agrarian UniversityRussian FederationФедеральный исследовательский центр Институт цитологии и генетики Сибирского отделения Российской академии наук; Новосибирский национальный исследовательский государственный университет; Курчатовский геномный центр Института цитологии и генетики Сибирского отделения Российской академии наукРоссияInstitute of Cytology and Genetics of Siberian Branch of the Russian Academy of Sciences; Novosibirsk State University; Kurchatov Genomics Center of the Institute of Cytology and Genetics of Siberian Branch of the Russian Academy of SciencesRussian Federation2021150320212517181Copyright © Пронозин А.Ю., Паулиш А.А., Заварзин Е.А., Приходько А.Ю., Прохошин Н.М., Кручинина Ю.В., Гончаров Н.П., Комышев Е.Г., Генаев М.А., 20212021Пронозин А.Ю., Паулиш А.А., Заварзин Е.А., Приходько А.Ю., Прохошин Н.М., Кручинина Ю.В., Гончаров Н.П., Комышев Е.Г., Генаев М.А.Pronozin A.Y., Paulish A.A., Zavarzin E.A., Prikhodko A.Y., Prokhoshin N.M., Kruchinina Y.V., Goncharov N.P., Komyshev E.G., Genaev M.A.This work is licensed under a Creative Commons Attribution 4.0 License.https://vavilov.elpub.ru/jour/article/view/2918

Внутривидовая классификация культурных растений необходима для эффективного сохранения биологического разнообразия видов, изучения их происхождения, определения филогении и проведения межвидовой гибридизации при селекции. Современные возделываемые виды пшениц произошли от трех диких диплоидных предков в результате гибридизации и нескольких раундов удвоения геномов и представлены ди-, тетра- и гексаплоидными видами. Поэтому идентификация плоидности пшениц и определение их геномного состава являются одними из основных этапов их классификации на основе визуального анализа фенотипических признаков колоса. Цель работы – исследование морфологических характеристик колосьев полиплоидных видов пшеницы методами высокопроизводительного фенотипирования. Выполнено фенотипирование количественных характеристик колоса 17 видов пшеницы (595 растений, 3348 изображений), включая восемь тетраплоидных: Triticum aethiopicum, T. dicoccoides, T. dicoccum, T. durum, T. militinae, T. polonicum, T. timopheevii, T. turgidum и девять гексаплоидных: T. compactum, T. aestivum (в том числе изогенная линия сорта Новосибирская 67 АНК-23), T. antiquorum, T. spelta (включая стародавний сорт T. spelta Rother Sommer Kolben), T. petropavlovskyi, T. yunnanense, T. macha, T. sphaerococcum, T. vavilovii. Морфология колоса описана на основе девяти количественных признаков, включающих форму, размер и остистость. Признаки были получены в результате анализа цифровых изображений с помощью программы WERecognizer. Кластерный анализ растений по характеристикам формы колоса и сравнение их распределений у тетра- и гексаплоидных видов показали более высокую вариабельность признаков у гексаплоидных видов по сравнению с тетраплоидными. При этом сами виды в пространстве характеристик колоса формируют два кластера. К первому относятся преимущественно гексаплоидные виды, за исключением одного тетраплоидного, дикорастущего T. dicoccoides, ко второму – тетраплоидные, за исключением трех гексаплоидных, T. compactum, T. antiquorum, T. sphaerococcum, и i:АНК-23. Показано, что морфологические характеристики колосьев для гекса- и тетраплоидных видов, полученные на основе компьютерного анализа изображений, демонстрируют различия, которые в дальнейшем могут быть использованы для разработки методики эффективной классификации растений по плоидности и их видовой принадлежности в автоматическом режиме.

Intraspecific classification of cultivated plants is necessary for the conservation of biological diversity, study of their origin and their phylogeny. The modern cultivated wheat species originated from three wild diploid ancestors as a result of several rounds of genome doubling and are represented by di-, tetra- and hexaploid species. The identification of wheat ploidy level is one of the main stages of their taxonomy. Such classification is possible based on visual analysis of the wheat spike traits. The aim of this study is to investigate the morphological characteristics of spikes for hexa- and tetraploid wheat species based on the method of high-performance phenotyping. Phenotyping of the quantitative characteristics of the spike of 17 wheat species (595 plants, 3348 images), including eight tetraploids (Triticum aethiopicum, T. dicoccoides, T. dicoccum, T. durum, T. militinae, T. polonicum, T. timopheevii, and T. turgidum) and nine hexaploids (T. compactum, T. aestivum, i:ANK-23 (near-isogenic line of T. aestivum cv. Novosibirskaya 67), T. antiquorum, T. spelta (including cv. Rother Sommer Kolben), T. petropavlovskyi, T. yunnanense, T. macha, T. sphaerococcum, and T. vavilovii), was performed. Wheat spike morphology was described on the basis of nine quantitative traits including shape, size and awns area of the spike. The traits were obtained as a result of image analysis using the WERecognizer program. A cluster analysis of plants according to the characteristics of the spike shape and comparison of their distributions in tetraploid and hexaploid species showed a higher variability of traits in hexaploid species compared to tetraploid ones. At the same time, the species themselves form two clusters in the visual characteristics of the spike. One type is predominantly hexaploid species (with the exception of one tetraploid, T. dicoccoides). The other group includes tetraploid ones (with the exception of three hexaploid ones, T. compactum, T. antiquorum, T. sphaerococcum, and i:ANK-23). Thus, it has been shown that the morphological characteristics of spikes for hexaploid and tetraploid wheat species, obtained on the basis of computer analysis of images, include differences, which are further used to develop methods for plant classifications by ploidy level and their species in an automatic mode.

пшеницаморфология колосафеномикаобработка изображенийкомпьютерное зрениемашинное обучениебиотехнологииwheat spike morphologywheatphenomicsimage processingcomputer visionmachine learningbiotechnologyPreparation of spike samples, phenotyping, development of algorithms for shape analysis and classification were funded by the Kurchatov Genome Center of the Institute of Cytology and Genetics of Siberian Branch of the Russian Academy of Sciences, agreement with the Ministry of Education and Science of the Russian Federation No. 075-15-2019-1662. Cultivation of experimental plants and de visu determination of their species belonging by the traits determining the architectonics of the spike were supported by grant of Russian Science Foundation 16-16-10021. The data were processed using the resources of the Bioinformatics Center supported by the budget project No. 0259-2021-0009. The authors A.A.P., E.A.Z., A.Yu.P., and N.M.P. were supported by the Mathematical Center in Akademgorodok, agreement with the Ministry of Science and Higher Education of the Russian Federation No. 075-15-2019-1675. The authors are grateful to D.A. Afonnikov for comments and recommendations during the work and I.G. Chukhina (VIR, St. Petersburg) for providing photos of herbarium specimens of T. petropavlovskyi.ReferencesAfonnikov D.A., Genaev M.A., Doroshkov A.V., Komyshev E.G., Pshenichnikova T.A. Methods of high-throughput plant phenotyping for large-scale breeding and genetic experiments. Russ. J. Genet. 2016;52(7):688-701. DOI 10.1134/S1022795416070024.Afonnikov D.A., Genaev M.A., Doroshkov A.V., Komyshev E.G., Pshenichnikova T.A. Methods of high-throughput plant phenotyping for large-scale breeding and genetic experiments. Russ. J. Genet. 2016;52(7):688-701. DOI 10.1134/S1022795416070024.Boguslavsky R.L. A new botanical form of hexaploid wheat. NauchnoTekhnicheskiy Byulleten VIR = Scientific and Technological Bulletin of the Vavilov Institute of Plant Industry. 1982;119:73-74. (in Russian)Boguslavsky R.L. A new botanical form of hexaploid wheat. NauchnoTekhnicheskiy Byulleten VIR = Scientific and Technological Bulletin of the Vavilov Institute of Plant Industry. 1982;119:73-74. (in Russian)Chen Z.J. Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu. Rev. Plant Biol. 2007;58:377-406. DOI 10.1146/annurev.arplant.58.032806.103835.Chen Z.J. Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu. Rev. Plant Biol. 2007;58:377-406. DOI 10.1146/annurev.arplant.58.032806.103835.Comai L. The advantages and disadvantages of being polyploid. Nat. Rev. Genet. 2005;6(11):836-846. DOI 10.1038/nrg1711.Comai L. The advantages and disadvantages of being polyploid. Nat. Rev. Genet. 2005;6(11):836-846. DOI 10.1038/nrg1711.Demidchik V.V., Shashko A.Y., Bandarenka V.Y., Smolikova G.N., Przhevalskaya D.A., Charnysh M.A., Pozhvanov G.A., Barkovskyi A.V., Smolich I.I., Sokolik A.I., Yu M., Medvedev S.S., Plant phenomics: fundamental bases, software and hardware platforms, and machine learning. Russ. J. Plant Physiol. 2020;67:397-412. DOI 10.1134/S1021443720030061.Demidchik V.V., Shashko A.Y., Bandarenka V.Y., Smolikova G.N., Przhevalskaya D.A., Charnysh M.A., Pozhvanov G.A., Barkovskyi A.V., Smolich I.I., Sokolik A.I., Yu M., Medvedev S.S., Plant phenomics: fundamental bases, software and hardware platforms, and machine learning. Russ. J. Plant Physiol. 2020;67:397-412. DOI 10.1134/S1021443720030061.Dorofeev V.F. Intraspecific taxonomy of wheat. Doklady VASKhNIL = Reports of the Academy of Agricultural Sciences. 1985;9:1-4. (in Russian)Dorofeev V.F. Intraspecific taxonomy of wheat. Doklady VASKhNIL = Reports of the Academy of Agricultural Sciences. 1985;9:1-4. (in Russian)Dorofeev V.F., Filatenko A.A., Migushova E.F., Udachin R.A., Yakubtsiner M.M. Flora of Cultivated Plants of USSR. Vol. 1. Wheat. Leningrad: Kolos Publ., 1979. (in Russian)Dorofeev V.F., Filatenko A.A., Migushova E.F., Udachin R.A., Yakubtsiner M.M. Flora of Cultivated Plants of USSR. Vol. 1. Wheat. Leningrad: Kolos Publ., 1979. (in Russian)Dorofeev V.F., Rudenko M.I., Filatenko A.A., Baras J., Segnalova J., Lemann H. (Compilators). Тhе Intеrnаtiоnаl Соmесоn List оf Dеsсriрtоrs for the Gеnus Тritiсum L. Leningrad: VIR Publ., 1984. (in Russian)Dorofeev V.F., Rudenko M.I., Filatenko A.A., Baras J., Segnalova J., Lemann H. (Compilators). Тhе Intеrnаtiоnаl Соmесоn List оf Dеsсriрtоrs for the Gеnus Тritiсum L. Leningrad: VIR Publ., 1984. (in Russian)Finigan P., Tanurdzic M., Martienssen R.A. Origins of novel phenotypic variation in polyploids. In: Polyploidy and Genome Evolution. Berlin; Heidelberg: Springer Press, 2012;57-76. DOI 10.1007/978-3-642-31442-1_4.Finigan P., Tanurdzic M., Martienssen R.A. Origins of novel phenotypic variation in polyploids. In: Polyploidy and Genome Evolution. Berlin; Heidelberg: Springer Press, 2012;57-76. DOI 10.1007/978-3-642-31442-1_4.Genaev M.A., Komyshev E.G., Fu Hao, Koval V.S., Goncharov N.P., Afonnikov D.A. SpikeDroidDB: an information system for annotation of morphometric characteristics of wheat spike. Vavilovskii Zhurnal Genetiki i Selektsii = Vavilov Journal of Genetics and Breeding. 2018;22(1):132-140. DOI 10.18699/VJ18.340. (in Russian)Genaev M.A., Komyshev E.G., Fu Hao, Koval V.S., Goncharov N.P., Afonnikov D.A. SpikeDroidDB: an information system for annotation of morphometric characteristics of wheat spike. Vavilovskii Zhurnal Genetiki i Selektsii = Vavilov Journal of Genetics and Breeding. 2018;22(1):132-140. DOI 10.18699/VJ18.340. (in Russian)Genaev M.A., Komyshev E.G., Smirnov N.V., Kruchinina Y.V., Goncharov N.P., Afonnikov D.A. Morphometry of the wheat spike by analyzing 2D images. Agronomy. 2019;9(7):390. DOI 10.3390/agronomy9070390.Genaev M.A., Komyshev E.G., Smirnov N.V., Kruchinina Y.V., Goncharov N.P., Afonnikov D.A. Morphometry of the wheat spike by analyzing 2D images. Agronomy. 2019;9(7):390. DOI 10.3390/agronomy9070390.Golovnina K.A., Kondratenko E.Ya., Blinov A.G., Goncharov N.P. Phylogeny of the A genome of wild and cultivated wheat species. Russ. J. Genet. 2009;45(11):1360-1367. DOI 10.1134/S1022795409110106.Golovnina K.A., Kondratenko E.Ya., Blinov A.G., Goncharov N.P. Phylogeny of the A genome of wild and cultivated wheat species. Russ. J. Genet. 2009;45(11):1360-1367. DOI 10.1134/S1022795409110106.Goncharov N.P. Comparative-genetic analysis – a base for wheat taxonomy revision. Czech J. Genet. Plant Breed. 2005;41:52-55.Goncharov N.P. Comparative-genetic analysis – a base for wheat taxonomy revision. Czech J. Genet. Plant Breed. 2005;41:52-55.Goncharov N.P. Manual Book of Common and Hard Wheat Varieties. Novosibirsk: SO RAN Publ., 2009. (in Russian)Goncharov N.P. Manual Book of Common and Hard Wheat Varieties. Novosibirsk: SO RAN Publ., 2009. (in Russian)Goncharov N.P. Genus Triticum L. taxonomy: the present and the future. Plant Syst. Evol. 2011;295(1-4):1-11. DOI 10.1007/s00606-011-0480-9.Goncharov N.P. Genus Triticum L. taxonomy: the present and the future. Plant Syst. Evol. 2011;295(1-4):1-11. DOI 10.1007/s00606-011-0480-9.Goncharov N.P., Kondratenko E.Ya. Wheat origin, domestication and evolution. Informatsionnyy Vestnik VOGiS = The Herald of Vavilov Society for Geneticists and Breeders. 2008;12(1/2):159-179. (in Russian)Goncharov N.P., Kondratenko E.Ya. Wheat origin, domestication and evolution. Informatsionnyy Vestnik VOGiS = The Herald of Vavilov Society for Geneticists and Breeders. 2008;12(1/2):159-179. (in Russian)Goncharov N.P., Shumny V.K. From preservation of genetic collections to organization of National project of plant gene pools conservation in permafrost. Informatsionnyy Vestnik VOGiS = The Herald of Vavilov Society for Geneticists and Breeders. 2008;12(4):509-523. (in Russian)Goncharov N.P., Shumny V.K. From preservation of genetic collections to organization of National project of plant gene pools conservation in permafrost. Informatsionnyy Vestnik VOGiS = The Herald of Vavilov Society for Geneticists and Breeders. 2008;12(4):509-523. (in Russian)Hammer K., Filatenko A.A., Pistrick K. Taxonomic remarks on Triticum L. and ×Triticosecale Wittm. Genet. Resour. Crop Evol. 2011; 58(1):3-10. DOI 10.1007/s10722-010-9590-4.Hammer K., Filatenko A.A., Pistrick K. Taxonomic remarks on Triticum L. and ×Triticosecale Wittm. Genet. Resour. Crop Evol. 2011; 58(1):3-10. DOI 10.1007/s10722-010-9590-4.Johnson S.C. Hierarchical clustering schemes. Psychometrika. 1967; 32(3):241-254.Johnson S.C. Hierarchical clustering schemes. Psychometrika. 1967; 32(3):241-254.Koval S.F. The catalog of near-isogenic lines of Novosibirskaya-67 common wheat and principles of their use in experiments. Russ. J. Genet. 1997;33(8):995-1000.Koval S.F. The catalog of near-isogenic lines of Novosibirskaya-67 common wheat and principles of their use in experiments. Russ. J. Genet. 1997;33(8):995-1000.Liu W., Zheng Y., Song S., Huo B., Li D., Wang J. In vitro induction of allohexaploid and resulting phenotypic variation in Populus. Plant Cell Tiss. Organ Cult. 2018;134(2):183-192. DOI 10.1007/s11240018-1411-z.Liu W., Zheng Y., Song S., Huo B., Li D., Wang J. In vitro induction of allohexaploid and resulting phenotypic variation in Populus. Plant Cell Tiss. Organ Cult. 2018;134(2):183-192. DOI 10.1007/s11240018-1411-z.Müllner D. Modern hierarchical, agglomerative clustering algorithms. arXiv. 2011;1109.2378.Müllner D. Modern hierarchical, agglomerative clustering algorithms. arXiv. 2011;1109.2378.Palmova E.F. Introduction to Wheat Ecology. Moscow; Leningrad: Selkhozgiz Publ., 1935. (in Russian)Palmova E.F. Introduction to Wheat Ecology. Moscow; Leningrad: Selkhozgiz Publ., 1935. (in Russian)Pedregosa F., Varoquaux G., Gramfort A., Michel V., Thirion B., Grisel O., Blondel M., Müller A., Nothman J., Louppe G., Prettenhofer P., Weiss R., Dubourg V., Vanderplas J., Passos A., Cournapeau D., Brucher M., Perrot M., Duchesnay E. Scikit-learn: Machine learning in Python. J. Mach. Learn. Res. 2011;12:2825-2830.Pedregosa F., Varoquaux G., Gramfort A., Michel V., Thirion B., Grisel O., Blondel M., Müller A., Nothman J., Louppe G., Prettenhofer P., Weiss R., Dubourg V., Vanderplas J., Passos A., Cournapeau D., Brucher M., Perrot M., Duchesnay E. Scikit-learn: Machine learning in Python. J. Mach. Learn. Res. 2011;12:2825-2830.Robinson D.O., Coate J.E., Singh A., Hong L., Bush M., Doyle J.J., Roeder A.H. Ploidy and size at multiple scales in the Arabidopsis sepal. Plant Cell. 2018;30(10):2308-2329. DOI 10.1105/tpc.18.00344.Robinson D.O., Coate J.E., Singh A., Hong L., Bush M., Doyle J.J., Roeder A.H. Ploidy and size at multiple scales in the Arabidopsis sepal. Plant Cell. 2018;30(10):2308-2329. DOI 10.1105/tpc.18.00344.Rodionov A.V., Amosova A.V., Belyakov E.A., Zhurbenko P.M., Mikhailova Y.V., Punina E.O., Shneyer V.S., Loskutov I.G., Muravenko O.V. Genetic consequences of interspecific hybridization, its role in speciation and phenotypic diversity of plants. Russ. J. Genet. 2019;55(3):278-294. DOI 10.1134/S1022795419030141.Rodionov A.V., Amosova A.V., Belyakov E.A., Zhurbenko P.M., Mikhailova Y.V., Punina E.O., Shneyer V.S., Loskutov I.G., Muravenko O.V. Genetic consequences of interspecific hybridization, its role in speciation and phenotypic diversity of plants. Russ. J. Genet. 2019;55(3):278-294. DOI 10.1134/S1022795419030141.Rodionov A.V., Shneyer V.S., Gnutikov A.A., Nosov N.N., Punina E.O., Zhurbenko P.M., Loskutov I.G., Muravenko O.V. Species dialectics: from initial uniformity, through the greatest possible diversity to ultimate uniformity. Botanicheskiy Zhurnal = Botanical Journal. 2020; 105(9):835-853. DOI 10.31857/S0006813620070091. (in Russian)Rodionov A.V., Shneyer V.S., Gnutikov A.A., Nosov N.N., Punina E.O., Zhurbenko P.M., Loskutov I.G., Muravenko O.V. Species dialectics: from initial uniformity, through the greatest possible diversity to ultimate uniformity. Botanicheskiy Zhurnal = Botanical Journal. 2020; 105(9):835-853. DOI 10.31857/S0006813620070091. (in Russian)Romanov B.V., Pimonov K.I. Phenomogenomics of Production Traits of Wheat Species. Persianovsky: Donskoy GAU Publ., 2018. (in Russian)Romanov B.V., Pimonov K.I. Phenomogenomics of Production Traits of Wheat Species. Persianovsky: Donskoy GAU Publ., 2018. (in Russian)Sinskaya E.N. Historical Geography of Cultural Flora (At the Dawn of Agriculture). Leningrad: Kolos Publ., 1969. (in Russian)Sinskaya E.N. Historical Geography of Cultural Flora (At the Dawn of Agriculture). Leningrad: Kolos Publ., 1969. (in Russian)Snedecor G.W., Cochran W.G. Statistical Methods. Ames, Iowa: Iowa State University Press, 1989.Snedecor G.W., Cochran W.G. Statistical Methods. Ames, Iowa: Iowa State University Press, 1989.Tan F., Tu H., Liang W., Long J.M., Wu X.M., Zhang H.Y., Guo W.W. Comparative metabolic and transcriptional analysis of a doubled diploid and its diploid citrus rootstock (C. junos cv. Ziyang xiangcheng) suggests its potential value for stress resistance improvement. BMC Plant Biol. 2015;15:89. DOI 10.1186/s12870-015-0450-4.Tan F., Tu H., Liang W., Long J.M., Wu X.M., Zhang H.Y., Guo W.W. Comparative metabolic and transcriptional analysis of a doubled diploid and its diploid citrus rootstock (C. junos cv. Ziyang xiangcheng) suggests its potential value for stress resistance improvement. BMC Plant Biol. 2015;15:89. DOI 10.1186/s12870-015-0450-4.Udachin R.A., Migushova E.F. New in the knowledge of the genus Triticum. Vestnik Selskokhozyaystvennoy Nauki = Herald of Agricultural Sciences. 1970;9:20-24. (in Russian)Udachin R.A., Migushova E.F. New in the knowledge of the genus Triticum. Vestnik Selskokhozyaystvennoy Nauki = Herald of Agricultural Sciences. 1970;9:20-24. (in Russian)van der Maaten L., Hinton G. Visualizing data using t-SNE. J. Mach. Learn. Res. 2008;9:2579-2605.van der Maaten L., Hinton G. Visualizing data using t-SNE. J. Mach. Learn. Res. 2008;9:2579-2605.van Slageren M., Payne T. Concepts and nomenclature of the Farro wheats, with special reference to Emmer, Triticum turgidum subsp. dicoccum (Poaceae). Kew Bull. 2013;68:477-494. DOI 10.1007/S12225-013-9459-8.van Slageren M., Payne T. Concepts and nomenclature of the Farro wheats, with special reference to Emmer, Triticum turgidum subsp. dicoccum (Poaceae). Kew Bull. 2013;68:477-494. DOI 10.1007/S12225-013-9459-8.Virtanen P., Gommers R., Oliphant T.E., Haberland M., Reddy T., Cournapeau D., Burovski E., Peterson P., Weckesser W., Bright J., van der Walt S.J., Brett M., Jones E., Kern R., Larson E., Carey C.J., Polat I., Feng Yu, Moore E.W., VanderPlas J., Laxalde D., Perktold J., Cimrman R., Henriksen I., Quintero E.A., Harris C.R., Archibald A.M., Riberio A.H., Pedregosa F., van Mulbregt P. SciPy 1.0 Contributors. SciPy 1.0 – fundamental algorithms for scientific computing in Python. Nat. Meth. 2020;17(3):261-272. DOI 10.1038/s41592-019-0686-2.Virtanen P., Gommers R., Oliphant T.E., Haberland M., Reddy T., Cournapeau D., Burovski E., Peterson P., Weckesser W., Bright J., van der Walt S.J., Brett M., Jones E., Kern R., Larson E., Carey C.J., Polat I., Feng Yu, Moore E.W., VanderPlas J., Laxalde D., Perktold J., Cimrman R., Henriksen I., Quintero E.A., Harris C.R., Archibald A.M., Riberio A.H., Pedregosa F., van Mulbregt P. SciPy 1.0 Contributors. SciPy 1.0 – fundamental algorithms for scientific computing in Python. Nat. Meth. 2020;17(3):261-272. DOI 10.1038/s41592-019-0686-2.Watanabe N., Bannikova S.V., Goncharov N.P. Inheritance and chromosomal location of the genes for long glume phenotype found in Portuguese landraces of hexaploid wheat, ‘Arrancada’. J. Genet. Breed. 2004;58:273-278.Watanabe N., Bannikova S.V., Goncharov N.P. Inheritance and chromosomal location of the genes for long glume phenotype found in Portuguese landraces of hexaploid wheat, ‘Arrancada’. J. Genet. Breed. 2004;58:273-278.Williams J.H., Oliveira P.E. For things to stay the same, things must change: polyploidy and pollen tube growth rates. Ann. Bot. 2020; 125(6):925-935. DOI 10.1093/aob/mcaa007.Williams J.H., Oliveira P.E. For things to stay the same, things must change: polyploidy and pollen tube growth rates. Ann. Bot. 2020; 125(6):925-935. DOI 10.1093/aob/mcaa007.Yakubtsiner M.M. More on Chinese wheats. Botanicheskiy Zhurnal = Botanical Journal. 1959;44(10):1425-1436. (in Russian)Yakubtsiner M.M. More on Chinese wheats. Botanicheskiy Zhurnal = Botanical Journal. 1959;44(10):1425-1436. (in Russian)Yang W., Feng H., Zhang X., Zhang J., Doonan J.H., Batchelor W.D., Xiong L., Yan J. Crop phenomics and high-throughput phenotyping: past decades, current challenges, and future perspectives. Mol. Plant. 2020;13(2):187-214. DOI 10.1016/j.molp.2020.01.008.Yang W., Feng H., Zhang X., Zhang J., Doonan J.H., Batchelor W.D., Xiong L., Yan J. Crop phenomics and high-throughput phenotyping: past decades, current challenges, and future perspectives. Mol. Plant. 2020;13(2):187-214. DOI 10.1016/j.molp.2020.01.008.Zatybekov A., Anuarbek S., Abugalieva S., Turuspekov Y. Phenotypic and genetic variability of a tetraploid wheat collection grown in Kazakhstan. Vavilovskii Zhurnal Genetiki i Selektsii = Vavilov Journal of Genetics and Breeding. 2020;24(6):605-612. DOI 10.18699/VJ20.654.Zatybekov A., Anuarbek S., Abugalieva S., Turuspekov Y. Phenotypic and genetic variability of a tetraploid wheat collection grown in Kazakhstan. Vavilovskii Zhurnal Genetiki i Selektsii = Vavilov Journal of Genetics and Breeding. 2020;24(6):605-612. DOI 10.18699/VJ20.654.Zhang Y., Zhao C., Du J., Guo X., Wen W., Gu S., Wang J., Fan J. Crop phenomics: current status and perspectives. Front. Plant Sci. 2019; 10:714. DOI 10.3389/fpls.2019.00714.Zhang Y., Zhao C., Du J., Guo X., Wen W., Gu S., Wang J., Fan J. Crop phenomics: current status and perspectives. Front. Plant Sci. 2019; 10:714. DOI 10.3389/fpls.2019.00714.Zuev E.V., Amri A., Brykova A.N., Pyukkenen V.P., Mitrofanova O.P. Atlas of the Diversity of Soft Wheat (Triticum aestivum L.) by Ear and Grain Characteristics. St. Petersburg: Kopi-R Publ., 2019. (in Russian)Zuev E.V., Amri A., Brykova A.N., Pyukkenen V.P., Mitrofanova O.P. Atlas of the Diversity of Soft Wheat (Triticum aestivum L.) by Ear and Grain Characteristics. St. Petersburg: Kopi-R Publ., 2019. (in Russian)

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