References

vavilov

Вавиловский журнал генетики и селекции

Vavilov Journal of Genetics and Breeding

2500-3259

Institute of Cytology and Genetics of Siberian Branch of the RAS

10.18699/VJGB-22-51

vavilov-3432

Research Article

СЕЛЕКЦИЯ РАСТЕНИЙ НА ПРОДУКТИВНОСТЬ

Использование пырея среднего (Thinopyrum intermedium) в селекции

The use of wheatgrass (Thinopyrum intermedium) in breeding

https://orcid.org/0000-0003-3574-2875

Потоцкая

И. В.

Pototskaya

I. V.

Омск

Omsk

iv.pototskaya@omgau.org

https://orcid.org/0000-0003-4767-9957

Шаманин

В. П.

Shamanin

V. P.

Омск

Omsk

https://orcid.org/0000-0003-1031-3417

Айдаров

А. Н.

Aydarov

A. N.

Омск

Omsk

https://orcid.org/0000-0001-7082-5655

Моргунов

А. И.

Morgounov

A. I.

Рияд

Riyadh

Омский государственный аграрный университет им. П.А. СтолыпинаРоссияOmsk State Agrarian University named after P.A. StolypinRussian Federation

Продовольственная и сельскохозяйственная организацияСаудовская АравияFood and Agriculture OrganizationSaudi Arabia

2022

01092022

265413421

2022

Потоцкая И.В., Шаманин В.П., Айдаров А.Н., Моргунов А.И.

Pototskaya I.V., Shamanin V.P., Aydarov A.N., Morgounov A.I.

This work is licensed under a Creative Commons Attribution 4.0 License.

https://vavilov.elpub.ru/jour/article/view/3432

Пырей средний (Th. intermedium) традиционно применялся в селекции пшеницы для получения пшенично-пырейных гибридов и сортов с интрогрессиями новых генов хозяйственно ценных признаков. Однако в 1980-х гг. в США из множества многолетних видов растений пырей был выбран для доместикации с целью создания сортов двойного направления использования – на зерно (альтернатива многолетней пшенице) и сено. В результате были выведены сорта пырея Kеrnza (The Land Institute, Канзас) и MN-Clearwater (Миннесотский университет, Миннесота). В Омском ГАУ из популяции Th. intermedium, полученной из The Land Institute, массовым отбором наиболее зимостойких биотипов с последующим их объединением создан сорт Сова. Средняя урожайность зерна сорта Сова составляет 9.2 ц/га, зеленой массы – 210.0 ц/га, сена – 71.0 ц/га. Пырей средний – культура с большим производственным потенциалом, полезными экологическими свойствами и ценным зерном для функционального питания. Во многих публикациях показаны преимущества возделывания сорта Kеrnza по сравнению с однолетними культурами: сокращение стока нитратов в грунтовые воды, увеличение секвестрации почвенного углерода, снижение энергетических и экономических затрат. Однако в России селекционные программы, направленные на доместикацию многолетних культур, весьма ограниченны. В настоящем обзоре рассматриваются основные задачи, стоящие перед селекцией и направленные на повышение урожайности зерна и эффективности возделывания пырея среднего в качестве многолетней зерновой и кормовой культуры. Для их решения используются как традиционные, так и современные биотехнологические и молекулярно-цитогенетические подходы. Важнейшей задачей считается передача целевых генов Th. intermedium в современные сорта пшеницы и сокращение дозы хроматина, несущего гены нежелательных признаков дикорастущего сородича. Получена первая консенсусная генетическая карта пырея среднего, содержащая 10 029 маркеров и представляющая интерес для поиска ценных генов и их интродукции в геном пшеницы. Представлены результаты исследований по оценке питательных и технологических свойств зерна пырея и полученных из него продуктов питания в сравнении с пшеницей.

Wheatgrass (Th. intermedium) has been traditionally used in wheat breeding for obtaining wheat-wheatgrass hybrids and varieties with introgressions of new genes for economically valuable traits. However, in the 1980s in the United States wheatgrass was selected from among perennial plant species as having promise for domestication and the development of dual-purpose varieties for grain (as an alternative to perennial wheat) and hay. The result of this work was the creation of the wheatgrass varieties Kernza (The Land Institute, Kansas) and MN-Clearwater (University of Minnesota, Minnesota). In Omsk State Agrarian University, the variety Sova was developed by mass selection of the most winter-hardy biotypes with their subsequent combination from the population of wheatgrass obtained from The Land Institute. The average grain yield of the variety Sova is 9.2 dt/ha, green mass is 210.0 dt/ ha, and hay is 71.0 dt/ha. Wheatgrass is a crop with a large production potential, beneficial environmental properties, and valuable grain for functional food. Many publications show the advantages of growing the Kernza variety compared to annual crops in reducing groundwater nitrate contamination, increasing soil carbon sequestration, and reducing energy and economic costs. However, breeding programs for domestication of perennial crops are very limited in Russia. This paper presents an overview of main tasks faced by breeders, aimed at enhancing the yield and cultivating wheatgrass efficiency as a perennial grain and fodder crop. To address them, both traditional and modern biotechnological and molecular cytogenetic approaches are used. The most important task is to transfer target genes of Th. intermedium to modern wheat varieties and decrease the level of chromatin carrying undesirable genes of the wild relative. The first consensus map of wheatgrass containing 10,029 markers was obtained, which is important for searching for genes and their introgressions to the wheat genome. The results of research on the nutritional and technological properties of wheatgrass grain for the development of food products as well as the differences in the quality of wheatgrass grain and wheat grain are presented.

многолетняя культурапшеницадоместикацияотборгеныэкология

perennial cropwheatdomesticationselectiongenesecology

References1

Abraha M., Chen J., Chu H., Zenone T., John R., Su Y.J., Hamilton S.K., Robertson G.P. Evapotranspiration of annual and perennial biofuel crops in a variable climate. Glob. Change Biol. Bioenergy. 2015;7(6):1344-1356. DOI 10.1111/GCBB.12239.

Abraha M., Gelfand I., Hamilton S.K., Shao C., Su Y.J., Robertson G.P., Chen J. Ecosystem water-use efficiency of annual corn and perennial grasslands: contributions from land-use history and species composition. Ecosystems. 2016;19(6):1001-1012. DOI 10.1007/s10021-016-9981-2.

Amaducci S., Facciotto G., Bergante S., Perego A., Serra P., Ferrarini A., Chimento C. Biomass production and energy balance of herbaceous and woody crops on marginal soils in the Po valley. Glob. Change Biol. Bioenergy. 2016;9(1):31-45. DOI 10.1111/gcbb.12341.

Bajgain P., Zhang X., Anderson J.A. Genome-wide association study of yield component traits in Intermediate Wheatgrass and implications in genomic selection and breeding. G3: Genes Genomes Genetics (Bethesda). 2019;9(8):2429-2439. DOI 10.1534/g3.119.400073.

Bajgain P., Zhang X., Jungers J.M., DeHaan L.R., Heim B., Sheaffer C.C., Wyse D.L., Anderson J.A. MN-Clearwater, the first food-grade intermediate wheatgrass (Kernza perennial grain) cultivar. J. Plant Regist. 2020;14(3):288-297. DOI 10.1002/plr2.20042.

Becker R., Meyer D., Wagoner P., Saunders R.M. Alternative crops for sustainable agricultural systems. Agric. Ecosyst. Environ. 1992;40(1-4):265-274. DOI 10.1016/0167-8809(92)90097-U.

Becker R., Wagoner P., Hanners G.D., Saunders R.M. Compositional, nutritional and functional-evaluation of intermediate wheatgrass (Thinopyrum intermedium). J. Food Process. Preserv. 1991;15(1):63-77. DOI 10.1111/j.1745-4549.1991.tb00154.x.

Berry P.M., Kindred D.R., Olesen J.E., Jorgensen L.N., Paveley N.D. Quantifying the effect of interactions between disease control, nitrogen supply and land use change on the greenhouse gas emissions associated with wheat production. Plant Pathol. 2010;59(4):753-763. DOI 10.1111/j.1365-3059.2010.02276.x.

Cattani D.J, Asselin S.R. Extending the growing season: forage seed production and perennial grains. Can. J. Plant Sci. 2017;98(2):235-246. DOI 10.1139/cjps-2017-0212.

Chen Q. Detection of alien chromatin introgression from Thinopyrum into wheat using S genomic DNA as a probe – a landmark approach for Thinopyrum genome research. Cytogenet. Genome Res. 2005;109(1-3):350-359. DOI 10.1159/000082419.

Chen Q., Conner R.L., Laroche A., Thomas J.B. Genome analysis of Thinopyrum intermedium and Th. ponticum using genomic in situ hybridization. Genome. 1998;41(4):580-586. DOI 10.1139/G98-055.

Chimento C., Amaducci S. Characterization of fine root system and potential contribution to soil organic carbon of six perennial bioenergy crops. Biomass Bioenergy. 2015;83(12):116-122. DOI 10.1016/j.biombioe.2015.09.008.

Cox T.S., Van Tassel D.L., Cox C.M., Dehaan L.R. Progress in breeding perennial grains. Crop Pasture Sci. 2010;61(7):513-521. DOI 10.1071/CP09201.

Crain J., Bajgain P., Anderson J., Zhang X., DeHaan L., Poland J. Enhancing crop domestication through genomic selection, a case study of intermediate wheatgrass. Front. Plant Sci. 2020;11(3):319. DOI 10.3389/fpls.2020.00319.

Crain J., Haghighattalab A., DeHaan L., Poland J. Development of whole-genome prediction models to increase the rate of genetic gain in intermediate wheatgrass (Thinopyrum intermedium) breeding. Plant Genome. 2021;14(4):e20089. DOI 10.1002/tpg2.20089.

Crews T.E., Carton W., Olsson L. Is the future of agriculture perennial? Imperatives and opportunities to reinvent agriculture by shifting from annual monocultures to perennial polycultures. Glob. Sustain. 2018;1(e11):1-18. DOI 10.1017/sus.2018.11.

Cui L., Ren Y., Murray T.D., Yan W., Guo Q., Niu Y., Sun Y., Li H. Development of perennial wheat through hybridization between wheat and wheatgrasses: a review. Engineering. 2018;4(4):507-513. DOI 10.1016/j.eng.2018.07.003.

Culman S.W., Snapp S.S., Ollenburger M., Basso B., DeHaan L.R. Soil and water quality rapidly responds to the perennial grain Kernza wheatgrass. Agron. J. 2013;105(3):735-744. DOI 10.2134/agronj2012.0273.

DeHaan L.R., Christians M., Crain J., Poland J. Development and evolution of an Intermediate wheatgrass domestication program. Sustainability. 2018;10(5):1499. DOI 10.3390/SU10051499.

DeHaan L.R., Van Tassel D.L. Useful insights from evolutionary biology for developing perennial grain crops. Am. J. Bot. 2014;101(10):1801-1819. DOI 10.3732/ajb.1400084.

DeHaan L.R., Van Tassel D.L., Cox T.S. Perennial grain crops: a synthesis of ecology and plant breeding. Renew. Agric. Food Syst. 2005;20(1):5-14. DOI 10.1079/RAF200496.

de Oliveira G., Brunsell N.A., Crewsb T.E., DeHaanb L.R., Vicoc G. Carbon and water relations in perennial Kernza (Thinopyrum intermedium): an overview. Plant Sci. 2019;295(6):110279. DOI 10.1016/j.plantsci.2019.110279.

de Oliveira G., Brunsell N.A., Sutherlin C.E., Crews T.E., De- Haan L.R. Energy, water and carbon exchange over a perennial Kernza wheatgrass crop. Agric. For. Meteorol. 2018;249(2):120-137. DOI 10.1016/J.AGRFORMET.2017.11.022.

Divashuk M.G., Kroupin P.Yu., Fesenko I.A., Belov V.I., Razumova O.V., Korotaeva A.A., Karlov G.I. About possible use of Agropyron Vp-1 ( Viviparous-1) genes-homolog for improvement of soft wheat. Sel’skokhozyaistvennaya Biologiya = Agricultural Biology. 2011;46(5):40-44. (in Russian)

Gill B.S., Friebe B., Raupp W.J., Wilson D.L., Cox T.S., Sears R.G., Brown-Guedira G.L., Fritz A.K. Wheat Genetics Resource Center: the first 25 years. Adv. Agron. 2006;85(12):73-136. DOI 10.1016/S0065-2113(05)89002-9.

Glover J.D., Reganold J.P., Bell L.W., Borevitz J., Brummer E.C., Buckler E.S., Cox C.M., Cox T.S., Crews T.E., Culman S.W., De- Haan L.R., Eriksson D., Gill B.S., Holland J., Hu F., Hulke B.S., Ibrahim A.M.H., Jackson W., Jones S.S., Murray S.C., Paterson A.H., Ploschuk E., Sacks E.J., Snapp S., Tao D., Van Tassel D.L., Wade L.J., Wyse D.L., Xuet Y. Agriculture. Increased food and ecosystem security via perennial grains. Science. 2010;328(5986):1638-1639. DOI 10.1126/science.1188761.

Hayes R.C., Wang S., Newell M.T., Turner K., Larsen J. The performance of early-generation perennial winter cereals at 21 sites across four continents. Sustainability. 2018;10(4):1124. DOI 10.3390/su10041124.

Hu L., Li G., Zhan H., Liu C., Yang Z. New St-chromosome-specific molecular markers for identifying wheat – Thinopyrum intermedium derivative lines. J. Genet. 2012;91(2):e69-e74.

IPCC, 2019: Climate Change and Land: an IPCC special report on climate change, desertification, land degradation, sustainable land management, food security, and greenhouse gas fluxes in terrestrial ecosystems [P.R. Shukla, J. Skea, E. Calvo Buendia, V. Masson-Delmotte, H.-O. Pörtner, D.C. Roberts, P. Zhai, R. Slade, S. Connors, R. van Diemen, M. Ferrat, E. Haughey, S. Luz, S. Neogi, M. Pathak, J. Petzold, J. Portugal Pereira, P. Vyas, E. Huntley, K. Kissick, M. Belkacemi, J. Malley (Eds.)]. Jungers J.M., DeHaan L.R., Betts K.J., Sheaffer C.C., Wyse D.L. Intermediate wheatgrass grain and forage yield responses to nitrogen fertilization. Agron. J. 2017;109(2):462-472. DOI 10.2134/agronj2016.07.0438.

Jungers J.M., DeHaan L.R., Mulla D.J., Sheaffer C.C., Wyse D.L. Reduced nitrate leaching in a perennial grain crop compared to maize in the Upper Midwest, USA. Agric. Ecosyst. Environ. 2019;272(2):63-73. DOI 10.1016/j.agee.2018.11.007.

Kantarski T., Larson S., Zhang X., DeHaan L., Borevitz J., Anderson J., Poland J. Development of the first consensus genetic map of intermediate wheatgrass (Thinopyrum intermedium) using genotyping- by-sequencing. Theor. Appl. Genet. 2017;130(1):137-150. DOI 10.1007/s00122-016-2799-7.

Klimushina M.V., Kroupin P.Yu., Bazhenov M.S., Karlov G.I., Divashuk M.G. Waxy gene-orthologs in wheat Thinopyrum amphidiploids. Agronomy. 2020;10(7):963. DOI 10.3390/agronomy10070963.

Kocheshkova A.A., Kroupin P.Y., Bazhenov M.S., Karlov G.I., Pochtovyy A.A., Upelniek V.P., Belov V.I., Divashuk M.G. Preharvest sprouting resistance and haplotype variation of ThVp-1 gene in the collection of wheat-wheatgrass hybrid. PLoS One. 2017;12(11):e0188049. DOI 10.1371/journal.pone.0188049.

Kroupin P.Yu., Divashuk M.G., Fesenko I.A., Karlov G.I. Adaptation of microsatellite SSR-markers of wheat for the genome analysis of wheatgrass, intermediate wheatgrass, and wheat–wheatgrass hybrids. Izvestija Timirjazevskoj Sel’skohozjajstvennoj Akademii = Proceedings of the Timiryazev Agricultural Academy. 2011;3:49-57. (in Russian)

Kroupin P.Yu., Divashuk M.G., Karlov G.I. Gene resources of perennial wild cereals involved in breeding to improve wheat crop. Sel’skokhozyaistvennaya Biologiya = Agricultural Biology. 2019; 54(3):409-425. DOI 10.15389/agrobiology.2019.3.409eng.

Lanker M., Bell M., Picasso V.D. Farmer perspectives and experiences introducing the novel perennial grain Kernza intermediate wheatgrass in the US Midwest. Renew. Agric. Food Syst. 2020;35(6):653-662. DOI 10.1017/ S1742170519000310.

Larson S., DeHaan L., Poland J., Zhang X., Dorn K., Kantarski T., Anderson J., Schmutz J., Grimwood J., Jenkins J., Shu S., Crain J., Robbins M., Jensen K. Genome mapping of quantitative trait loci (QTL) controlling domestication traits of inter-mediate wheatgrass (Thinopyrum intermedium). Theor. Appl. Genet. 2019;132(6):2325-2351. DOI 10.1007/s00122-019-03357-6.

Li G.R., Liu C., Li C.H., Zhao J.M., Zhou L., Dai G., Yang E.N., Yang Z.J. Introgression of a novel Thinopyrum intermedium St- chromosome-specific HMW-GS gene into wheat. Mol. Breed. 2013; 31(2):843-853. DOI 10.1007/s11032-013-9838-8.

Li G., Wang H., Lang T., Li J., La S., Yang E., Yang Z. New molecular markers and cytogenetic probes enable chromosome identification of wheat-Thinopyrum intermedium introgression lines for improving protein and gluten contents. Planta. 2016;244(6):865-876. DOI 10.1007/s00425-016-2554-y.

Mahelka V., Kopecky D., Pastova L. On the genome constitution and evolution of intermediate wheatgrass (Thinopyrum intermedium: Poaceae, Triticeae). BMC Evol. Biol. 2011;11(1):127. DOI 10.1186/1471-2148-11-127.

Marti A., Bock J.E., Pagani M.A., Ismail B., Seetharaman K. Structural characterization of proteins in wheat flour doughs enriched with intermediate wheatgrass (Thinopyrum intermedium) flour. Food Chem. 2016;194(3):994-1002. DOI 10.1016/j.foodchem.2015.08.082.

Marti A., Qiu X., Schoenfuss T.C., Seetharaman K. Characteristics of perennial wheatgrass (Thinopyrum intermedium) and refined wheat flour blends: impact on rheological properties. Cereal. Chem. 2015; 92(5):434-440. DOI 10.1094/CCHEM-01-15-0017-R.

Martynov S.P., Dobrotvorskaya T.V., Krupnov V.A. Genealogical analysis of the use of two wheatgrass (Agropyron) species in common wheat (Triticum aestivum L.) breeding for disease resistance. Russ. J. Genet. 2016;52(2):154-163. DOI 10.1134/S1022795416020071.

Nikitina E., Kuznetsova V., Kroupin P., Karlov G.I., Divashuk M.G. Development of specific Thinopyrum cytogenetic markers for wheat-wheatgrass hybrids using sequencing and qPCR data. Int. J. Mol. Sci. 2020;21(12):4495. DOI 10.3390/ijms21124495.

Plotnikova L.Ya., Seryukov G.M., Shvarts Yu.K. Сytophysiological resistantance mechanisms to leaf rust in wheat–Agropyron hybrids created on the base of Agropyron elongatum. Mikologiya i Fitopatologiya = Mycology and Phytopathology. 2011;45(5):443-454. (in Russian)

Pochtovyi A.A., Karlov G.I., Divashuk M.G. Creation of molecular markers of DREB genes of wheatgrass origin, improving drought tolerance in cereal genomes. Vestnik Bashkirskogo Universiteta = Bulletin of the Bashkir University. 2013;18(3):745-747. (in Russian)

Pugliese J.Y., Culman S.W., Sprunger C.D. Harvesting forage of the perennial grain crop Kernza (Thinopyrum intermedium) increases root biomass and soil nitrogen cycling. Plant Soil. 2019;437(2):241-254. DOI 10.1007/s11104-019-03974-6.

Qiao L., Liu S., Li J., Li S., Yu Z., Liu C., Li X., Liu J., Ren Y., Zhang P., Zhang X., Yang Z., Chang Z. Development of sequence- tagged site marker set for identification of J, JS, and St sub-genomes of Thinopyrum intermedium in wheat background. Front. Plant Sci. 2021;12(6):685216. DOI 10.3389/fpls.2021.685216.

Rahardjo C.P., Gajadeera C.S., Simsek S., Annor G., Schoenfuss T.C., Marti A., Ismail B.P. Chemical characterization, functionality, and baking quality of intermediate wheatgrass (Thinopyrum intermedium). J. Cereal Sci. 2018;83(9):266-274. DOI 10.1016/j.jcs.2018.09.002.

Razmakhnin E.P. The gene pool of Agropyron glaucum as a source for increasing common wheat biodiversity. Informatsionnyy Vestnik VOGiS = The Herald of Vavilov Society for Geneticists and Breeders. 2008;12(4):701-709. (in Russian)

Razmakhnin E.P., Razmakhnina T.M., Kozlov V.E., Gordeeva E.I., Goncharov N.P., Galitsyn Y.G., Veprev S.G., Chekurov V.M. Raise of high frost-resistant Agropyron–Triticum hybrids. Vavilovskii Zhurnal Genetiki i Selektsii = Vavilov Journal of Genetics and Breeding. 2012;16(1):240-249. (in Russian)

Ryan M.R., Сrews T., Culman S., DeHaan L.R., Jungers J.M., Bakker M. Managing for multifunctionality in perennial grain crops. Bioscience. 2018;68(4):294-304. DOI 10.1093/BIOSCI/BIY014.

Salina E.A., Adonina I.G., Badaeva E.D., Kroupin P.Yu., Stasyuk A., Leonova I.N., Shishkina A.A., Divashuk M.G., Starikova E.V., Khuat T.M.L., Syukov V.V., Karlov G.I. A Thinopyrum intermedium chromosome in bread wheat cultivars as a source of genes conferring resistance to fungal diseases. Euphytica. 2015;201(3):91-101. DOI 10.1007/s10681_014_1344_5.

Sandukhadze B.I., Mamedov R.Z., Krakhmalyova M.S., Bugrova V.V. Scientific breeding of winter bread wheat in the Non- Сhernozem zone of Russia: the history, methods and results. Vavilovskii Zhurnal Genetiki i Selektsii = Vavilov Journal of Genetics and Breeding. 2021;25(4):367-373. DOI 10.18699/VJ21.53-o.

Schipanski M.E., MacDonald G.K., Rosenzweig S., Chappell M.J., Bennett E.M., Kerr R.B., Blesh J., Crews T., Drinkwater L., Lundgren J.G. Realizing resilient food systems. Bioscience. 2016;66(7):600-610. DOI 10.1093/biosci/biw052.

Shamanin V.P., Mоrgоunоv A.I., Aydarov A.N., Shepelev S.S., Chursin A.S., Pоtоtskaya I.V., Khamova O.F., Dehaan L.R. Largegrained wheatgrass variety Sova (Thinopyrum intermedium) as an alternative to perennial wheat. Sel’skokhozyaistvennaya Biologiya = Agricultural Biology. 2021;56(3):450-464. DOI 10.15389/agrobiology.2021.3.450rus. (in Russian)

Sibikeev S.N., Badaeva E.D., Gultyaeva E.I., Druzhin A.E., Shishkina A.A., Dragovich A.Yu., Kroupin P.Yu., Karlov G.I., Khuat T.M., Divashuk M.G. Comparative analysis of Agropyron intermedium (Host) Beauv 6Agi and 6Agi2 chromosomes in bread wheat cultivars and lines with wheat-wheatgrass substitutions. Russ. J. Genet. 2017;53(3):314-324. DOI 10.1134/S1022795417030115.

Sibikeev S.N., Druzhin A.E., Vlasovets L.T., Kalintseva T.V., Golubeva T.D. The strategy of using introgression genes for resistance to leaf rust in the spring bread wheat breeding. Agrarnyj Vestnik Jugo-Vostoka = Agrarian Reporter of South-East. 2018;2(19):15-16. (in Russian)

Sibikeev S.N., Krupnov V.A., Voronina S.A., Badaeva E.D. Identification of an alien chromosome in the bread wheat line Multi 6R. Russ. J. Genet. 2005;41(8):885-889. DOI 10.1007/s11177-005-0176-8.

Springmann M., Clark M., Mason-D’Croz D., Wiebe K., Bodirsky B.L., Lassaletta L., de Vries W., Vermeulen S.J., Herrero M., Carlson K.M., Jonell M., Troell M., DeClerck F., Gordon L.J., Zurayk R., Scarborough P., Rayner M., Loken B., Fanzo J., Godfray H.C.J., Tilman D., Rockström J., Willett W. Options for keeping the food system within environmental limits. Nature. 2018;562(10):519-525. DOI 10.1038/s41586-018-0591-0.

Stavridou E., Hastings A., Webster R.J., Robson P.R. The impact of soil salinity on the yield, composition and physiology of the bioenergy grass Miscanthus × giganteus. Glob. Chang. Biol. Bioenergy. 2016;9(2):92-104. DOI 10.1111/gcbb.12351.

Suneson C., El Sharkawy A., Hall W.E. Progress in 25 years of perennial wheat breeding. Crop Sci. 1963;3(5):437-439. DOI 10.2135/cropsci1963.0011183X000300050021x.

Sutherlin C.E., Brunsell N.A., de Oliveira G., Crews T.E., De- Haan L.R., Vico G. Contrasting physiological and environmental controls of evapotranspiration over Kernza perennial crop, annual crops, and C4 and mixed C3/C4 grasslands. Sustainability. 2019;11(6):1640. DOI 10.3390/su11061640.

Suyker A.E., Verma S.B. Evapotranspiration of irrigated and rainfed maize-soybean cropping systems. Agric. For. Meteorol. 2009;149(3-4):443-452. DOI 10.1016/j.agrformet.2008.09.010.

Tang C., Han R., Zhao J., Qiao L., Zhang S., Qiao L., Ge C., Zheng J., Zheng X., Liu C. Identification, сharacterization, and evaluation of novel stripe rust-resistant wheat–Thinopyrum intermedium chromosome translocation lines. Plant Dis. 2020;104(1):875-881. DOI 10.1094/PDIS-01-19-0001-RE.

Tsitsin N.V. Perennial Wheat. Moscow, 1978. (in Russian)

Upelniek V.P., Belov V.I., Ivanova L.P., Dolgova S.P., Demidov A.S. Heritage of Academician N.V. Tsitsin: state-of-the-art and potential of the collection of intermediate wheat × couch grass hybrids. Vavilovskii Zhurnal Genetiki i Selektsii = Vavilov Journal of Genetics and Breeding. 2012;16(3):667-674. (in Russian)

Vico G., Brunsell N.A. Tradeoffs between water requirements and yield stability in annual vs. perennial crops. Adv. Water Resour. 2018;112(2):189-202. DOI 10.1016/j.advwatres.2017.12.014.

Wagoner P. Perennial grain development: past efforts and potential for the future. Crit. Rev. Plant Sci. 1990;9(5):381-408. DOI 10.1080/07352689009382298.

Wang H., Cheng S., Shi Y., Zhang S., Yan W., Song W., Yang X., Song Q., Jang B., Qi X., Li X., Friebe B., Zhang Y. Molecular cytogenetic characterization and fusarium head blight resistance of five wheat-Thinopyrum intermedium partial amphiploids. Mol. Cytogenet. 2021;14(3):15. DOI 10.1186/s13039-021-00536-3.

Xi W., Tang Z., Tang S., Yang Z., Luo J., Fu S. New ND-FISHpositive oligo probes for identifying Thinopyrum chromosomes in wheat backgrounds. Int. J. Mol. Sci. 2019;20(8):2031. DOI 10.3390/ijms20082031.

Yu Z., Wang H., Xu Y., Li Y., Lang T., Yang Z., Li G. Characterization of сhromosomal rearrangement in new wheat–Thinopyrum intermedium addition lines carrying Thinopyrum–specific grain hardness genes. Agronomy. 2019;9(1):18. DOI 10.3390/agronomy9010018.

Zeri M., Hussain M.Z., Anderson-Teixeira K.J., DeLucia E., Bernacchi C.J. Water use efficiency of perennial and annual bioenergy crops in central Illinois. J. Geophys. Res. Biogeosci. 2013;118(3):581-589. DOI 10.1002/jgrg.20052.

Zhang P., Dundas I.S., Xu S.S., Friebe B., McIntosh R.A., Raupp W.J. Chromosome engineering techniques for targeted introgression of rust resistance from wild wheat relatives. Methods Mol. Biol. 2017;1659:163-172. DOI 10.1007/ 978-1-4939-7249-4_14.

Zhang X., Cui С., Bao Y., Wang H., Li X. Molecular cytogenetic characterization of a novel wheat-Thinopyrum intermedium introgression line tolerant to phosphorus deficiency. Crop J. 2021;9(4):816-822. DOI 10.1016/j.cj.2020.08.014.

Zhang X., DeHaan L.R., Higgins L., Markowski T.W., Wyse D.L., Anderson J.A. New insights into high-molecular-weight glutenin subunits and subgenomes of the perennial crop Thinopyrum intermedium (Triticeae). J. Cereal Sci. 2014;59(2):203-210. DOI 10.1016/j.jcs.2014.01.008.

Zhang X., Larson S.R., Gao L., DeHaan L.R., Fraser M., Sallam A., Kantarski T., Frels K., Poland J., Wyse D., Anderson J.A. Uncovering the genetic architecture of seed weight and size in Intermediate wheatgrass through linkage and association mapping. Plant Genome. 2017;10(3):1-15. DOI 10.3835/plantgenome2017.03.0022.

Zhong Y., Mogoginta J., Gayin J., Annor G.А. Structural characterization of intermediate wheatgrass (Thinopyrum intermedium) starch. Cereal Chem. 2019;96(5):927-936. DOI 10.1002/cche.10196.

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