Genetic diversity, distribution and domestication history of the neglected GGAtAt genepool of wheat

Theoretical and Applied Genetics https://doi.org/10.1007/s00122-021-03912-0 ORIGINAL ARTICLE Genetic diversity, distribution and domestication history of the neglected GGAtAt genepool of wheat Ekaterina D. Badaeva1,2 · Fedor A. Konovalov3,4 · Helmut Knüpffer4 · Agostino Fricano5 · Alevtina S. Ruban4,6 · Zakaria Kehel7 · Svyatoslav A. Zoshchuk2 · Sergei A. Surzhikov2 · Kerstin Neumann4 · Andreas Graner4 · Karl Hammer4 · Anna Filatenko4,8 · Amy Bogaard9 · Glynis Jones10 · Hakan Özkan11 · Benjamin Kilian4,12 Received: 13 May 2021 / Accepted: 7 July 2021 © The Author(s) 2021, corrected publication 2021 Abstract Key message We present a comprehensive survey of cytogenetic and genomic diversity of the GGAtAt genepool of wheat, thereby unlocking these plant genetic resources for wheat improvement. Abstract Wheat yields are stagnating around the world and new sources of genes for resistance or tolerances to abiotic traits are required. In this context, the tetraploid wheat wild relatives are among the key candidates for wheat improvement. Despite its potential huge value for wheat breeding, the tetraploid GGAtAt genepool is largely neglected. Understanding the population structure, native distribution range, intraspecific variation of the entire tetraploid GGAtAt genepool and its domestication history would further its use for wheat improvement. The paper provides the first comprehensive survey of genomic and cytogenetic diversity sampling the full breadth and depth of the tetraploid GGAtAt genepool. According to the results obtained, the extant GGAtAt genepool consists of three distinct lineages. We provide detailed insights into the cytogenetic composition of GGAtAt wheats, revealed group- and population-specific markers and show that chromosomal rearrangements play an important role in intraspecific diversity of T. araraticum. The origin and domestication history of the GGAtAt lineages is discussed in the context of state-of-the-art archaeobotanical finds. We shed new light on the complex evolutionary history of the GGAtAt wheat genepool and provide the basis for an increased use of the GGAtAt wheat genepool for wheat improvement. The findings have implications for our understanding of the origins of agriculture in southwest Asia. Introduction We dedicate this article to our visionary colleagues Moshe Feldman and Francesco Salamini. Communicated by Jochen Reif. * Ekaterina D. Badaeva 1 2 N.I. Vavilov Institute of General Genetics, Russian Academy of Sciences, Moscow, Russia Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, Moscow, Russia The domestication of plants since the Neolithic Age resulted in the crops that feed the world today. However, successive rounds of selection during the history of domestication led to a reduction in genetic diversity, which now limits the ability 6 KWS SAAT SE & Co. KGaA, Einbeck, Germany 7 International Center for the Agricultural Research in the Dry Areas (ICARDA), Rabat, Morocco 8 Independent Researcher, St. Petersburg, Russia 9 School of Archaeology, Oxford, UK 10 Department of Archaeology, University of Sheffield, Sheffield, UK 3 Independent Clinical Bioinformatics Laboratory, Moscow, Russia 11 4 Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Gatersleben, Germany Department of Field Crops, Faculty of Agriculture, University of Çukurova, Adana, Turkey 12 5 Council for Agricultural Research and Economics – Research Centre for Genomics & Bioinformatics, Fiorenzuola d’Arda (PC), Italy Global Crop Diversity Trust, Bonn, Germany 13 Vol.:(0123456789) Theoretical and Applied Genetics of the crops to further evolve (Tanksley and McCouch 1997; van Heerwaarden et al. 2010). This is exacerbated by the demand for high crop productivity under climate change. Crop wild relatives (CWR) represent a large pool of beneficial allelic variation and are urgently required to improve the elite genepools (Dempewolf et al. 2017; Kilian et al. 2021). Bread wheat (T. aestivum L., 2n = 6x = 42, BBAADD) and durum wheat (T. durum Desf., 2n = 4x = 42, BBAA) are the staple crops for about 40% of the world’s population. But as wheat yields are stagnating around the world (Iizumi et al. 2017; Ray et al. 2013, 2012), new sources of genes for resistance or tolerances to abiotic traits such as drought and heat are required. In this context, the wheat wild relatives are among the key sources for bread wheat and durum wheat improvement (Dante et al. 2013; Placido et al. 2013; Zhang et al. 2017). However, in nature, no wild hexaploid wheat has ever been found. Only two wild tetraploid wheat species (2n = 4x = 28) were discovered, namely (1) wild emmer wheat T. dicoccoides (Körn. ex Asch. et Graebn.) Körn. ex Schweinf. (Schweinfurth 1908) [syn. T. turgidum subsp. dicoccoides (Körn. ex Asch. & Graebn.) Thell.] and (2) Armenian, or Araratian emmer T. araraticum Jakubz. (Jakubziner 1947) [syn. T. timopheevii (Zhuk.) Zhuk. subsp. armeniacum (Jakubz.) van Slageren)]. Morphologically, both species are very similar but differ in their genome constitution (Zohary et al. 2012). Triticum dicoccoides has the genome formula BBAA and T. araraticum has GGAtAt (Jiang and Gill 1994). The wheat section Timopheevii mainly consists of wild tetraploid Triticum araraticum (GGAtAt), domesticated tetraploid T. timopheevii (Zhuk.) Zhuk. (Timopheev’s wheat, GGAtAt) and hexaploid T. zhukovskyi Menabde et Ericzjan (2n = 6x = 42, GGAtAtAmAm) (Dorofeev et al. 1979; Goncharov 2012). Wild T. araraticum was first collected by M.G. Tumanyan and A.G. Araratyan during 1925–28 southeast of Erevan, Armenia (Tumanyan 1930; Nazarova 2007), soon after the discovery of domesticated T. timopheevii by P.M. Zhukovsky (Zhukovsky 1928) (Supplementary Material S1). Subsequently, T. araraticum was found in several other locations in Armenia and Azerbaijan (Dorofeev et al. 1979; Jakubziner 1933, 1959), as well as in Iran, Iraq and Turkey. Single herbarium specimens resembling T. araraticum have been sporadically recorded among T. dicoccoides accessions collected from the Fertile Crescent (Jakubziner 1932; Sachs 1953). However, only botanical expeditions from the University of California at Riverside (USA) to Turkey in 1965, to the Fertile Crescent in 1972–1973 (Johnson and Hall 1967; Johnson and Waines 1977) and the Botanical Expedition of Kyoto University to the Northern Highlands of Mesopotamia in 1970 (Tanaka and Ishii 1973; Tanaka and Kawahara 1976) significantly expanded our understanding 13 of the natural distribution of T. araraticum. More recently, T. araraticum was found in northwestern Syria (Valkoun et al. 1998). Especially in southeastern Anatolia, Turkey, the distribution area of T. araraticum overlaps with the distribution range of T. dicoccoides. From the western to eastern Fertile Crescent, it is assumed that T. araraticum gradually substitutes T. dicoccoides (Johnson 1975), and T. dicoccoides is absent from Transcaucasia (Özkan et (...truncated)