Aegilops tauschii Coss. molecular phylogeny in comparison with proteins electrophoretic polymorphism

Abstract

In the case of Aegilops tauschii the comparison of intraspecies molecular phylogeny based on DNA sequences of nuclear gene Got2 with electrophoretic polymorphism of allozymes and hystone H1 proteins is actually a comparison of the one detailed phylogenetic tree with a set of low resolution trees. It could help to understand peculiarities of the species evolutionary history and role of cross-pollination in it. Proteins polymorphism patterns rather satisfactory corresponded to Got2 DNA tree. Electrophoretic polymorphism of essentially polymorphic in Ae. tauschii subsp. strangulata protein encoding loci considered (Ak, Est2, Got1, Got3, Hst2, Hst3) and essentially polymorphic in Ae. tauschii subsp. tauschii locus Fdp displayed correspondence with the molecular phylogenetic tree: each allele was common or predominant on some branches of the tree and rare or absent on the other. In contrast, alleles of Cat2 locus, Cat2³⁵ and Cat2¹⁴⁰, were “scattered” sporadically through Ae. tauschii subsp. tauschii branches on phylogenetic tree. Also in Ae. tauschii subsp. tauschii a set of different extremely rare allozyme alleles, Acph4¹¹³, Aco2¹¹⁰, Mdh1¹¹³, Nadhd1⁸⁸, was found among three out of four accessions belonging to one of the relict clades of this subspecies on the molecular phylogenetic tree. The data obtained displayed that subsp. tauschii, now being relatively less polymorphic than subsp. strangulata, in ancient times had good opportunities for genetic exchange between its different phylogenetic lineages, all but one of which are relicts in present time. And the patterns of Hst3⁹⁷⁷ allele occurrences indicated cross-pollination between subsp. tauschii and subsp. strangulata.

Acta Biologica Sibirica 9: 1167–1180 (2023) doi: 10.5281/zenodo.10400957

Corresponding author: Alexander J. Dudnikov (dudnikov@bionet.nsc.ru)

Academic editor: R. Yakovlev | Received 1 December 2022 | Accepted 30 November 2023 | Published 20 December 2023

http://zoobank.org/A9E11092-8926-4FD7-BA8E-B757763F5EE9

Citation: Dudnikov AJ (2023) Aegilops tauschii Coss. molecular phylogeny in comparison with proteins electrophoretic polymorphism. Acta Biologica Sibirica 9: 1167–1180. https://doi.org/10.5281/zenodo.10400957

Keywords

Aegilops tauschii, allozymes, DNA sequences, Genetic variation, Histone H1, molecular phylogeny

Introduction

Aegilops tauschii Coss. (syn. Aegilops squarrosa auct. non L.) is a diploid, mostly self-pollinating goat-grass (genome DD, 2n = 14) which donated its genome D to common wheat, Triticum aestivum L. (genome AABBDD, 2n = 42). Ae. tauschii is very important wild relative of common wheat, a donor of agriculturally important genes for its improvement (Kimber and Feldman 1987; Kilian et al. 2011). So, since genetic variability of Ae. tauschii is an important natural resource, it has been studied by researches throughout the world since the middle of the previous century. Genetic methods used started from rather simple allozyme technique and up to nowadays methods such as DArT, AFLP, etc. Modern genetic methods revealed rather detailed picture of Ae. tauschii genetic differentiation, but they do not explain how all this was formed in the course of the species evolution, i.e. these studies revealed Ae. tauschii population genetic structure but not phylogeny. Phylogenetic study was necessary for understanding of Ae. tauschii evolutionary history.

It should be mentioned that intraspecies phylogeny is essentially differs from interspecies one. So, in a simple general example of a species presented by one big and practically panmictic population no intraspecies phylogeny could be found. Phylogenetic study will not form “a tree” in this case; a rake-like structure will be formed instead. Of course, it is not a case of Ae. tauschii. This species is mostly selfpollinating, it is presented by many local populations, and here we could find very interesting picture of intraspecies divergence (Dudnikov 2021). Nevertheless occasional cross-pollination sometimes happens in Ae. tauschii and has an important impact on the species evolution (Dudnikov 2017, 2021). Therefore phylogenies of different parts of Ae. tauschii genome could differ.

The usage of molecular-genetic methods (AFLP, SSR, DArT, single nucleotide polymorphisms etc.) providing many genetic markers “scattered” through genome permits to obtain the picture of Ae. tauschii population genetic structure. Here recombination occurring in the course of Ae. tauschii evolution is being involved. And as it could be expected, different methods gives completely the same picture of Ae. tauschii population genetic structure (Lubbers 1991, Pestsova et al. 2000; Saeidi et al. 2008; Takumi et al. 2008, Mizuno et al. 2010, Sohail et al. 2012, Matsuoka et al. 2013, Wang et al. 2013, Su et al. 2020, Zhou et al. 2021). In contrast, the study of Ae. tauschii intraspecies phylogeny needs genetic system without recombination. For this purpose non-coding chloroplast DNA sequences were used (Dudnikov 2019). The other study used DNA sequences of nuclear gene Got2 (Dudnikov 2017, 2021). (Probability of intragenic recombination seems to be negligible in the case of mostly self-pollinating species Ae. tauschii.) As it could be expected, the two different methods give different pictures of Ae. tauschii intraspecies divergency (Dudnikov 2021). Also the general picture of Ae. tauschii molecular phylogeny obtained with molecular-genetic systems with practically no recombination – differ from the picture of the species population genetic structure obtained using molecular genetic systems with recombination being involved. So, population structure presents two sublineages, western and eastern (to say nothing of Ae. tauschii from Henan, China), in TauL1 gene-pool of the species; and two sublineages, western and eastern, in TauL2 gene-pool (Zhou et al. 2021); while molecular phylogeny presents several major lineages (plus some relicts) within TauL2; and only one major lineage and several relicts in TauL1 (Dudnikov 2021).

Ae. tauschii molecular phylogeny based on non-coding cpDNA sequences turned out to be relatively less accurate and reliable in comparison with phylogenetic picture based on DNA sequences of nuclear gene Got2 (Dudnikov 2019, 2021), and it could be due to the relatively lower mutation rate in cpDNA in comparison with nuclear DNA (Saitou 2018). It would be interesting to compare “Got2” phylogenetic tree with other tree(s) based on DNA sequences of nuclear gene(s) located in different parts of Ae. tauschii genome. But unfortunately each such a study needs sequencing of more than 300000 b.p. and is rather laborious.

Previously the studies of allozymes geographic occurrence through Ae. tauschii range revealed that each allele of each essentially polymorphic enzyme-encoding locus studied has its personal very special geographic pattern of occurrence which distinctly corresponds to environmental conditions, both on geographic map (Dudnikov 2012a, 2014a) and in the space of climatic parameters on the plot of principal component analysis (Dudnikov 2014b). Also it was pointed out that the time span during which seeds retain their germination capacity is in line with allozyme allelic constitution of enzyme-encoding genes in Ae. tauschii (Dudnikov 2003a). These mean that allozimes in Ae. tauschii are involved in adaptive processes of some kind. Enzyme encoding genes studies in Fundulus heteroclitus, Drosophila melanogaster and Colias spp. butterflies showed that sometimes substitution of a single aminoacid leading to the origin of new allozyme could have an essential adaptive value changing considerably the fitness of organism (Chambers 1988, Powers et al. 1991, Watt 1992, Eanes et al. 1996). But it seemed very unlikely that each such substitution could be adaptive and therefore could be the reason of total correspondence of allozyme variation in Ae. tauschii with ecological conditions through the species range. Explanation of spatial patterns of allozyme variation in Ae. tauschii has come from the study of Ae. tauschii intraspecies phylogeny based on DNA sequences of enzyme-encoding gene Got2. It was shown that the shape of Ae. tauschii phylogenetic tree is mostly formed by natural selection. Its branches present the species lineages which essentially differ from each other in their ecological “preferences”. The tree is a result of competition between different lineages through evolutionary history of Ae. tauschii (Dudnikov 2021). Also, investigation of Got2 DNA sequences revealed that in the case of Ae. tauschii the species age is relatively small in comparison with enzyme gene mutation rate, and the probability of the same allozyme (i.e. enzyme with particular electrophoretic mobility) to originate more than once as a result of two or more independent mutations in the course of Ae. tauschii evolution is very low. So, it was pointed out that Got2 enzyme-encoding gene allozyme variation with two alleles, Got2¹⁰⁰ and Got2¹⁰⁵, is due to a single unique mutation, the substitution of GA by AT in positions 2415–2416 which led to replacement of gluetamic acid by isoleucine (Dudnikov 2017). This means that in Ae. tauschii allozymes are good and reliable phylogenetic markers, and each allozyme marks its own specific point of intraspecies divergence in the course of Ae. tauschii evolutionary history, i.e. a specific part of the phylogenetic tree.

Therefore in Ae. tauschii each essentially polymorphic allozymes encoding locus in fact presents a phylogenetic tree. It is a low resolution tree, as usual having just two or three branches, but it is a reliable one. And we have a set of different independent trees of such kind which could be compared with the detailed molecular phylogenetic tree obtained previously using DNA sequences of Got2 gene.

Histone H1 proteins in Ae. tauschii are being encoded by three different loci (Dudnikov et al. 2002). And as well as in the case of allozymes, geographic patterns of histone H1 electrophoretic variants occurrences turned out to be distinctly adaptive (Dudnikov 2012b). Histone H1 encoding genes were not sequenced in Ae. tauschii, but the data obtained on Pisum sativum L. (Zaytseva et al. 2012) indicate that Histone H1 electrophoretic allele variants could be good phylogenetic markers the same as allozymes.

Comparison of previously obtained detailed Ae. tauschii philogenetic tree based on Got2 DNA sequences with a set of low resolution phylogenies revealed by proteins electriphoretic polymorphisms could help to understand peculiarities of Ae. tauschii evolution and the role of cross-pollination in it. The result of such comparison is presented below.

Material and methods

114 Ae. tauschii accessions were used for construction of molecular phylogenetic tree based on Got2 DNA sequences, 57 of ssp. tauschii and 57 of ssp. strangulata (Suppl. material 1: Table 1s); and all of them except for AL8/78 of ssp. strangulata were used for electrophoretic analysis of proteins polymorphism. The sources of the plant material are as follows: (1) N.I. Vavilov All-Russian Institute of Plant Genetic Recourses (VIR), (‘‘k’’); (2) Kyoto University (‘‘KU’’); (3) IPK Gatersleben (‘‘AE’’) and (4) the collection of Dudnikov (1998) (‘‘t’’). Ae. tauschii subdivision into subsp. tauschii and subsp. strangulata was considered according to Eig (1929), Hammer (1980), Jaaska (1980, 1981), Dudnikov (2021) and Zhou (2021), which means that TauL1 gene-pool belongs to subsp. tauschii while TauL2 and TauL3 gene-pools belong to subsp. strangulata. Subspecies identification was performed according to Dudnikov (2000).

Got2 DNA sequences of Ae. tauschii accession AL8/78 of Armenian origin (Jia et al. 2013) were obtained from GenBank (AOCO010130377, AOCO010130378). Got2 DNA sequences of all the other 113 accessions were obtained as described in Dudnikov (2021) and the nucleotide sequences were deposited in the DDBJ/EMBL/ GenBank database (http://www.ncbi.nlm.nih.gov/, accession numbers KX773890 to KX773948 and MT051581 to MT051634).

Phylogenetic analysis was conducted using MEGA version 6 (Tamura et al. 2013). Maximum likelihood (ML) method was used. Inversion and indels were treated as fifth character state (Simmons and Ochoterena 2000). Statistical bootstrap support of nodes was calculated with 1000 replicates.

Twelve enzyme systems were used for allozyme electrophoretic analysis: aconitate hydratase (ACO, EC 4.2.1.3), acid phosphatase (ACPH, EC 3.1.3.2), adenylate kinase (AK, EC 2.7.4.3), catalase (CAT, EC 1.11.1.6), esterase (EST, EC 3.1.1.2), fructose-1,6-diphosphatase (FDP, EC 3.1.3.11), glutamatic-oxaloacetatic transaminase (GOT, EC 2.6.1.1), glucosephosphate isomerase (GPI, EC 5.3.1.9), malate dehydrogenase (MDH, EC 1.1.1.37), NADH diaphorase (NADHD, EC 1.6.4.3), and phosphoglucomutase (PGM, EC 2.7.5.1). Enzymes extraction, electrophoresis and staining were carried out as in Dudnikov (2014b). Polymorphism of eight essentially polymorphic in Ae. tauschii allozyme-encoding loci, Acph1, Got1, Got2, Got3, Est2, Ak, Fdp, Cat2, and nine low polymorphic loci, Aco1, Aco2, Acph4, Gpi, Mdh1, Mdh2, Ndhd1, Ndhd2, Pgm, were considered in the study. Allele Est2^null was considered together with Est2¹⁰⁰ which electrophoretic band is often of low intensity.

Histone H1 proteins extraction, electrophoresis and staining were carried out as in Dudnikov (2012b).

Result

Ae. tauschii ML molecular phylogenetic tree obtained is displayed on Fig. 1. The data on proteins electrophoretic polymorphism are presented in Fig. 1 and Suppl. material 2: Table 2s.

As expected, Got2 allozyme variation perfectly corresponded to molecular phylogenetic tree based on DNA sequences of the same very locus Got2: Ae. tauschii accessions from clades “A – I” had Got2¹⁰⁵ allozyme allele; and accessions from clades “J - M” had Got2¹⁰⁰ allele (Fig. 1, Table 1). It is known that Acph1 loci allozyme variation perfectly corresponds to Ae. tauschii subdivision into subsp. tauschii (TauL1 gene-pool) and subsp. strangulata (TauL2 + TauL3 gene-pools) (Dudnikov 1998, 2000, Kirby et al. 2005). So, accessions from clades “A - H” had Acph1⁹⁵ allozyme allele, and accessions from clades “I - M” had Acph1¹⁰⁰ allele (Fig. 1, Table 1).

All allozyme and histone H1 encoding loci considered which were essentially polymorphic in Ae. tauschii subsp. strangulata (Got1, Got3, Est2, Ak, Hst2, Hst3) had distinctly uneven distribution of occurrences of their alleles among Ae. tauschii subsp. strangulata clades of Got2 DNA tree, “A - H”, with each allele being predominant or common in some clades and rare or absent in other. So, Got1⁹⁵ and Got3¹²⁵ predominantly occured in clade “C”. Est2⁸⁴ predominantly occured in clades “E” and “H”. Ak⁹² was rather common in clades “C” and “F”. Hst2¹⁰²⁶ was predominant in clade “F”. Hst2⁹⁸⁸ was rather common in clade “D” and was found in this clade only. Hst3⁹⁷⁷ was rather common in clade “F” (Fig. 1, Table 1).

Figure 1.Figure 1. Maximum Likelyhood phylogenetic tree of Aegilops tauschii based on Got2 DNA sequences. Indels were treated as fifth character state. Bootstrap values for 1000 replicates are displayed. Designations before an accession name are as follows: "t" – subsp. tauschii, and Acph1¹⁰⁰ allele; "s" – subsp. strangulata, and Acph1⁹⁵ allele; "GF" – Got2¹⁰⁵ allele (it is peculiar to subsp. strangulata and the most ancient relict gene-pool of subsp. tauschii (Dudnikov 2017)), "GS" – Got2¹⁰⁰ allele. After an accession name the country of its origin is mentioned: TY – Turkey, NO – North Ossetia, DG – Dagestan, GE – Georgia, AR – Armenia, AZ – Azerbaijan, CI – Continental Iran, WI – Western Precaspian Iran, EI – Eastern Precaspian Iran, TN – Turkmenistan, AF – Afghanistan, PA – Pakistan, IN – India, UZ – Uzbekistan, TJ – Tajikistan, KZ – Kazakhstan, KI – Kirgizstan. Continuing on the next page.

Figure 2.Figure 1. Continuing from the previous page. The subdivision of Precaspian Iran into ‘‘Western’’ and ‘‘Eastern’’ was made according to Dudnikov and Kawahara (2006), with an approximate dividing line going between the towns of Chalus and Babolser, along the 52 meridian. Allelic constitution of essentially polymorphic loci considered other then Acph1 and Got2 is displayed to the right side at each accession, with the most common alleles “100” or “1000” being shown as “.”. Occurrences of rare allele of low-polymorphic allozyme loci are displayed as follows: “α” – Aco1¹⁰⁷, “β” – Aco2¹¹⁰ , “γ” – Aco2⁹⁰, “δ” – Acph4¹¹³, “ε” – Gpi⁴⁵, “η” – Mdh1¹¹³, “λ” – Mdh2⁹⁰, “μ” – Nadhd1⁸⁸, “ν” – Nadhd2⁹² , “φ” – Pgm¹¹⁵.

Similarly, in Ae. tauschii subsp. tauschii allele Fdp⁸⁶ was found predominantly in clade “M” (Fig. 1, Table 1). In contrast, essentially polymorphic in Ae. tauschii subsp. tauschii Cat2 allozyme encoding locus displayed quite different pattern of its alleles occurrences. Cat2¹⁴⁰ and Cat2³⁵ occured sporadically through different clades of subsp. tauschii on Got2 DNA based phylogenetic tree (Fig. 1, Table 1).

Also, while considering Ae. tauschii subsp. tauschii it is interestin to outline that most of rare allozyme alleles found in subsp. tauschii belonged to one small relict lineage “M”: three out of four accessions from this lineage presented on the tree had different extremely rare allozyme alleles Acph4¹¹³, Aco2¹¹⁰, Mdh1¹¹³, Nadhd1⁸⁸ (Fig. 1).

Among all the loci considered the mentioned above Hst3 was the only one essentially polymorphic in both subsp. tauschii and subsp. strangulata with its allele Hst3⁹⁷⁷ being presented in both subspecies with the frequency of about 10%.

Discussion

Previously, a comparison of based on nuclear gene Got2 DNA sequences and cp-DNA non-coding sequences molecular phylogenies of Ae. tauschii revealed great differences between them indicating effects of cross-pollination in the species evolution and relatively low accuracy of cpDNA based phylogeny as well (Dudnikov 2021).

In the case of different nuclear-based phylogenies being compared, as in the present study, the effects of cross-pollination in Ae. tauschii evolution are also obvious, but nevertheless, different nuclear genome based phylogenies correspond rather satisfactory to each other. According to the data we have, Got2¹⁰⁵ allele originated not long before the origin of Ae. tauschii subsp. tauschii and Acph1⁹⁵ originated then at a time of Ae. tauschii subsp. tauschii appearance. Soon after subsp. tauschii segregation, Got1⁹⁵ and Est2⁸⁴ alleles originated in containing the lineage “C” and the lineages “E + H” parts of the tree, respectively. Later on, Got3¹²⁵ originated also in “C” part of the tree; while Hst2¹⁰²⁶ and Hst2⁹⁸⁸ – in “F” and “D” parts, respectively (Fig. 1). Fdp⁸⁶ originated not recently in the course of Ae. tauschii subsp. tauschii evolutionary history and corresponds to relict lineage “M” of the subspecies (Fig. 1, Table 1).

Sporadical patterns of Cat2¹⁴⁰ and Cat2³⁵ occurrence through Ae. tauschii subsp. tauschii branches of the molecular phyloginetic tree indicate that (1) these alleles originated long ago, probably in some lineage(s) being extinct now; and that (2) different lineages of subsp. tauschii, all except lineage “K” being relicts now with fragmentary ranges and practically no contacts with each other, in ancient times had good opportunities to exchange their genetic material. (Occurrence of rare allozyme allele Mdh1¹¹³ in clade “I” and clade “M” al well, also gives evidence of genetic exchanges between these relict clades in the past (Fig. 1, 2))

Example of genetic exchange between subsp. tauschii and subs. strangulata is displayed by the patterns of Hst3977 occurrence through the tree. This allele was found in clades “F”, “D” of subsp. strangulata and in clade “K” of subsp. “tauschii” (Fig. 1, Table 1). Accession KU-2109 belonging to relict clade “L” of Ae. tauschii subsp. tauschii presents another example of genetic exchange between the two subspecies. This accession was collected in western pre-caspian Iran, the region where Ae. tauschii subsp. tauschii is very rare (Dudnikov and Kawahara 2006) and it has alleles Got1⁹⁵ and Hst1¹⁰⁴³ which besides this particular accession of subsp. tauschii were found in subsp. strangulata only (Suppl. material 1: Table 1s; Suppl. material 2: Table 2s).

Of course, both between subspecies and within subspecies genetic exchanges mentioned should have taken place at some concrete geographic regions. And it should be outlined that occurring sporadically on the phylogenetic tree Cat2¹⁴⁰, Cat2³⁵ and Hst3⁹⁷⁷ have distinct non-random patterns of occurrence through the range on geographic map. Cat2¹⁴⁰ and Cat2³⁵ were found only in the eastern part of the range (Dudnikov 2012a), while Hst3⁹⁷⁷ occur in the western part of the range and was never found in the east (Dudnikov 2012b). In fact, being involved in rather wide genetic exchange within TauL1, Cat2 elecrtophoretic polymorphism more correctly brings to light position of clade “I” than Got2 DNA sequences do. Occurrence of Cat2¹⁴⁰ indicates that clade “I” belong to TauL1, while Got2 DNA sequences data mistakenly put clade “I” of subsp. tauschii (TauL1) together with clades of subsp. strangulata TauL2 (Fig. 1)

Occurrence of several extremely rare allozymes in one clade “M” displays that this phylogenetic lineage of Ae. tauschii subsp. tauschii that in ancient times was presented by one large “wealthy” population, nowadays exist as a set of small isolated local populations which managed to survive in competition with other younger and more successful lineages of this subspecies. In isolated population of small size the impact of genetic drift increases, purifying natural selection becomes not effective, therefore such a population becomes a trap for slightly deleterious alleles, which hardly could be found in large population (Saitou 2018). Examples of alleles or traits found in small isolated populations of Ae. tauschii and which slightly deleterious effect is obvious, could be mentioned. So, not only extremely rare allozymes Aco2¹¹⁰ and Nadhd1⁸⁸ were found in accession k-1954 from the relict clade “M” of Ae. tauschii subsp. tauschii (Fig. 1), but also an extremely rare allele vrn-D2a which determines a very rare extremely spring type of growth habit in k-1954 (Dudnikov 2003b). (This effect is known to be a result of deletion in Vrn-D2 locus (Kippes et al. 2016)). Also, the plants from relict small isolated population t-9¹-s of Ae. tauschii subsp. strangulata, gene-pool TauL3, have extremely rare allozymes Nadhd2⁹² and Mdh2⁹⁰ (Dudnikov 1998), (Fig. 1). And as well, the seeds of these plants were found to retain their germination capacity during a time span which is about three times shorter than usual for Ae. tauschii (Dudnikov 2003a).

Of course, some of alleles which are slightly deleterious for Ae. tauschii in wild nature could be useful from applied point of view in Triticum aestivum L. breeding programs. So, the usage of vrn-D2 allele from k-1954 accession (E1 genetic line) of Ae. tauschii gave an opportunity to create a very special genetic line of T. aestivum, a synthetic vrn2-null . This line is being of spring growth habit as a result of having non-functional vrn-D2, vrn-A2 and vrn-B2 loci (Kippes et al. 2016).

Conclusion

Comparison of the high-resolution phylogenetic tree based on Got2 DNA sequences with a set of low-resolution trees based on allozymes and histone H1 electrophoretic proteins polymorphism leads to the following conclusions.

(1) Since Ae. tauschii is a self-pollinating species, there is a correspondance between different phylogenetic trees, each based on a single locus genetic variation. At the same time, these different trees markedly differs, indicating that cross-pollination do exist in Ae. tauschii and plays an important role in the species evolution.

(2) The study displays an example of evolutionary history of a phylogenetic lineage of Ae. tauschii subsp. tauschii. The lineage “M” in previous time occupied a vast area. Than it was forced out by younger and more successful lineages. A set of small completely isolated populations of lineage “M” managed to survive in different local refugiums; and each these small independent populations became “a trap" for unique genetic variation.

Acknowledgements

The work was supported by the Siberian Branch of the Russian Academy of Science (grant number FWNR-2022-0019).

References

Chambers GK (1988) The Drosophila alcohol dehydrogenase gene-enzyme system. Advances in Genetics 25: 39–107.

Dudnikov AJ (1998) Allozyme variation in Transcaucasian populations of Aegilops squarrosa. Heredity 80: 248–258.

Dudnikov AJ (2000) Multivariate analysis of genetic variation in Aegilops tauschii from the world germplasm collection. Genetic Resources and Crop Evolution 47: 185–190. https://doi.org/10.1023/A:1008722919064

Dudnikov AJ, Gorel FL, Berdnikov VA (2002) Chromosomal location of histone H1 genes in common wheat. Cereal Research Communications 30: 55–61.

Dudnikov AJ (2003a) Germination capacity is in line with the allelic constitution of enzyme-encoding genes in Aegilops tauschii. Cereal Research Communications 31: 403– 406. https://doi.org/10.1007/BF03543371

Dudnikov AJ (2003b) Allozymes and growth habit of Aegilops tauschii: genetic control and linkage patterns. Euphytica 129: 89–97. https://doi.org/10.1023/A:1021558628874

Dudnikov AJ, Kawahara T (2006) Aegilops tauschii: genetic variation in Iran. Genetic Resources and Crop Evolution 53: 579–586. https://doi.org/10.1007/s10722-004-2681-3

Dudnikov AJ (2012a) Spatial patterns of adenylate kinase, catalase, endopeptidase and fructose-1,6-diphosphatase encoding genes allelic variation in Aegilops tauschii Coss. Genetic Resources and Crop Evolution 59: 1–8. https://doi.org/10.1007/s10722-011-9659-8

Dudnikov AJ (2012b) Geographic patterns of histone H1 encoding genes allelic variation in Aegilops tauschii Coss. (Poaceae). Molecular Biology Reports 39: 2355–2363. https://doi.org/10.1007/s11033-011-0986-9

Dudnikov AJ (2014a) Geographic patterns of Got1, Got2, Got3 and Est2 enzyme-encoding genes allelic variation in Aegilops tauschii Coss. Genetic Resources and Crop Evolution 61: 143–149. https://doi.org/10.1007/s10722-013-0020-2

Dudnikov AJ (2014b) Aegilops tauschii Coss.: allelic variation of enzyme-encoding genes and ecological differentiation of the species. Genetic Resources and Crop Evolution 61: 1329–1344. http://dx.doi.org/10.1007/s10722-014-0115-4

Dudnikov AJ (2017) Polymorphism of Got2 DNA sequences sheds light on Aegilops tauschii Coss. intraspecies divergence and origin of Triticum aestivum L. Genetic Resources and Crop Evolution 64: 1623–1640. https://doi.org/10.1007/s10722-016-0461-5

Dudnikov AJ (2019) Aegilops tauschii Coss. chloroplast genome phylogeny. Journal of Plant Biochemistry and Biotechnology 28: 245–252. https://doi.org/10.1007/s13562-018-0469-3

Dudnikov AJ (2021) Aegilops tauschii Coss. molecular phylogeny: nuclear gene Got2 versus chloroplast DNA data. Genetic Resources and Crop Evolution 68: 2469–2482. https://link.springer.com/article/10.1007/s10722-021-01143-2

Eanes WF, Kirchner M, Yoon J, Biermann CH, Wang IN, McCartney MA, Verrelli BC (1996) Historical selection, amino acid polymorphism and lineage-specific divergence at the G6pd locus in Drosophila melanogaster and D. simulanss. Genetics 144: 1027–1041. https://doi.org/10.1093/genetics/144.3.1027

Eig A (1929) Monographisch-kritische Übersicht der Gattung Aegilops. Repertorium Speciorum Novarum Regni Vegetabilis. Beihefte 55: 1–228.

Hammer K (1980) Vorarbeiten zur monographischen Darstellung von Wildpflanzensortimenten: Aegilops L. Kulturpflanze 28: 33–180.

Jaaska V (1980) Electrophoretic survey of seedling esterases in wheats in relation to their phylogeny. Theoretical and Applied Genetics 56: 273–284. https://doi.org/10.1007/BF00282570

Jaaska V (1981) Aspartate aminotransferase and alcohol dehydrogenase enzymes: intraspecific differentiation in Aegilops tauschii and the origin of the D genome polyploids in the wheat group. Plant Systematics and Evolution 137: 259–273.

Jia J, Zhao S, Kong X, Li Y, Zhao G, He W, Appels R, Pfeifer M, Tao Y, Zhang X, Jing R, Zhang C, Ma Y, Gao L, Gao C, Spannagl M, Mayer KFX, Li D, Pan S, Zheng F, Hu Q, Xia X, Li J, Liang Q, Chen J, Wicker T, Gou C, Kuang H, He G, Luo Y, Keller B, Xia Q, Lu P, Wang J, Zou H, Zhang R, Xu J, Gao J, Middleton C, Quan Z, Liu G, Wang J, International Wheat Genome Sequencing Consortium, Yang H, Liu X, He Z, Mao L, Wang J (2013) Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation. Nature 496: 91–95. https://doi.org/10.1038/nature12028

Kilian B, Mammen K, Millet E, Sharma R, Graner A, Salamini F, Hammer K, Ozkan H (2011) Aegilops. In: Kole C (Ed.) Wild crop relatives: genomic and breeding resources. Cereals. Springer, Berlin, 1–76.

Kimber G, Feldman M (1987) Wild wheat. An introduction. Special report 353. College of Agricultural University of Missouri, Columbia, 1–142.

Kirby J, Vinh HT, Reader SM, Dudnikov AJ (2005) Genetic mapping of the Acph1 locus in Aegilops tauschii. Plant Breeding 124: 523–524.

Kippes N, Chen A, Zhang X, Lukaszewski AJ, Dubcovsky J (2016) Development and characterization of a spring hexaploid wheat line with no functional VRN2 genes. Theoretical and Applied Genetics 129: 1417–1428. https://doi.org/10.1007/s00122-016-2713-3

Lubbers EL, Gill KS, Cox TS, Gill BS (1991) Variation of molecular markers among geographically diverse accessions of Triticum tauschii. Genome 34: 354–361. https://doi.org/10.1139/g91-057

Matsuoka Y, Nasuda S, Ashida Y, Nitta M, Tsujimoto H, Takumi S, Kawahara T (2013) Genetic Basis for Spontaneous Hybrid Genome Doubling during Allopolyploid Speciation of Common Wheat Shown by Natural Variation Analyses of the Paternal Species. PLOS ONE 8: e68310. https://doi.org/10.1371/journal.pone.0068310

Mizuno N, Yamasaki M, Matsuoka Y, Kawahara T, Takumi S (2010) Population structure of wild wheat D-genome progenitor Aegilops tauschii Coss.: implications for intraspecific lineage diversification and evolution of common wheat. Molecular Ecology 19: 999– 1013. https://doi.org/10.1111/j.1365-294x.2010.04537.x

Pestsova E, Korzun V, Goncharov NP, Hammer K, Ganal MW, Roder MS (2000) Microsatellite analysis of Aegilops tauschii germplasm. Theoretical and Applied Genetics 101: 100–106. https://doi.org/10.1007/s001220051456

Powers DA, Lauerman T, Crawford D, DiMichele L (1991) Genetic mechanisms for adapting to a changing environment. Annual Review of Genetics 25: 629–659. https://doi.org/10.1146/annurev.ge.25.120191.003213

Saeidi H, Tabatabaei BES, Rahimmalek M, Talebi-Badaf M, Rahiminejad MR (2008) Genetic diversity and gene-pool subdivisions of diploid D-genome Aegilops tauschii Coss. (Poaceae) in Iran as revealed by AFLP. Genetic Resources and Crop Evolution 55: 1231– 1238. http://dx.doi.org/10.1007%2Fs10722-008-9323-0

Saitou N (2018) Introduction to Evolutionary Genomics. Computational Biology. 2nd edition. Springer Nature Switzerland AG. https:/doi.org/10.1007/978-3-319-92642-1

Sohail Q, Shehzad T, Kilian A, Eltayeb AE, Tanaka H, Tsujimoto H (2012) Development of diversity array technology (DArT) markers for assessment of population structure and diversity in Aegilops tauschii. Breeding Science 62: 38–45. https://doi.org/10.1270%2Fjsbbs.62.38

Su Y, Su Y, Zhang C, Zhang D, Li S (2020) Genetic structure characteristic of Aegilops tauschii from different geographical populations and the origin of Chinese population. Journal of Agricultural Science and Technology 22(3): 851–862. http://dorl.net/dor/20.1001.1.16807073.2020.22.3.8.8

Takumi S, Mizuno N, Okumura Y, Kawahara T, Matsuoka Y (2008) Two major lineages of Aegilops tauschii Coss. revealed by nuclear DNA variation analysis. In: Appels R, Eastwood R, Lagudah E, Langridge P, Mackay M, McIntyre L, Sharp P (Eds) The 11th International Wheat Genetics Symposium proceedings. Sydney University Press, Sydney, Australia. http://hdl.handle.net/2123/3432

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution 30: 2725–2729. https://doi.org/10.1093/molbev/mst197

Wang J, Luo M, Chen Z, You F, Wei Y, Zheng Y, Dvorak J (2013) Aegilops tauschii single nucleotide polymorphisms shed light on the origins of wheat D-genome genetic diversity and pinpoint the geographic origin of hexaploid wheat. New Phytologist 198: 925–937. https://doi.org/10.1111/nph.12164

Watt WB (1992) Eggs, enzymes and evolution – natural genetic variants change insect fecundity. Proceedings of National Academy of Sciences USA 89, 10608–10612. https://doi.org/10.1073%2Fpnas.89.22.10608

Zaytseva OO, Bogdanova VS, Kosterin OE (2012) Phylogenetic reconstruction at the species and intraspecies levels in the genus Pisum (L.) (peas) using a histone H1 gene. Gene 504: 192–202. https://doi.org/10.1016/j.gene.2012.05.026

Zhou Y, Bai S, Li H, Sun G, Zhang D, Ma F, Zhao X, Nie F, Li J, Chen L, Lv L, Zhu L, Fan R, Ge Y, Shaheen A, Guo G, Zhang Z, Ma J, Liang H, Qiu X, Hu J, Sun T, Hou J, Xu H, Xue S, Jiang W, Huang J, Li S, Zou C, Song C (2021) Introgressing the Aegilops tauschii genome into wheat as a basis for cereal improvement. Nature Plants 7: 774–786. https://doi.org/10.1038/s41477-021-00934-w

Supplementary material 1

Table 1s. Ae. tauschii accessions Authors: Alexander J. Dudnikov Data type: table

Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.

Link: http://journal.asu.ru/biol/article/view/14436/12225

Supplementary material 2

Table 2s. Electrophoretic alleles variation of proteins encoding loci among lines of Ae. tauschii used for reconstruction of the species phylogeny on the base of Got2 DNA sequences

Authors: Alexander J. Dudnikov Data type: table

Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.

Link: http://journal.asu.ru/biol/article/view/14436/12226