**1. Introduction**

The tribe *Triticeae Dumort* belongs to the subfamily *Pooideae* of the grass family *Poaceae* (*Gramineae*). About 500 taxa are included in this tribe. The number and designation of genera, species and subspecies depend upon the taxonomic criterion [1,2]. All species are considered to have a monophyletic origin, that is, they have a common ancestor, which is theoretically estimated to diverge from the other *Poaceae* 25 million years ago (MYA) [3,4]. Among the about 360 species in the tribe, 80 are diploids, the majority are allopolyploids derived from interspecific or intergeneric hybrids, most likely with progenitor species repeatedly involved in different hybridization events and increasing polyploidy levels. Only a few species are considered autopolyploids, which originated mainly from intraspecific hybridization followed by chromosome doubling [5]. All species have a basic haploid chromosome number of *x* = 7; diploid species have 2*n* = 14 chromosomes, and polyploids possess multiples of 14 chromosomes, the tetraploids 2*n* = 4*x* = 28, and the hexaploids 2*n* = 6*x* = 42. *Elymus* shows the most complex series and the highest level (12*x*) of ploidy [2].

Some species are self-pollinated, and others are cross-pollinated. About 75% of *Triticeae* species are perennials that grow in Temperate and Artic regions, mainly in the Northern Hemisphere, while the annuals spread through the Eastern Mediterranean and Central Asiatic regions [2].

The tribe is the subject of many research areas such as archaeology, genetics, plant breeding and evolutionary biology, but the main interest is due to its global economic significance, as it includes grain crops such as wheat (*Triticum*), barley (*Hordeum*) and rye (*Secale*), as well as a considerable number of grasses used for animal feed or rangeland protection. Given the enormous capacity for interspecific hybridization among most of the *Triticeae* taxa, wild species represent an accessible source of genetic variability that can be used to improve crops. The taxonomy of the tribe is complex, and has varied over time according to the taxonomic criteria and methodologies used [1]. Probably, interspecific hybridization and a large number of allopolyploid species are the key factors in the appearance of inconsistencies between di fferent phylogenetic trees. However, the role of the wild species as potential donors of useful agronomic traits to be introgressed into their cultivated relatives, represents an additional incentive in resolving the supposed evolutionary relationships among them.

With regards to the divergence of di fferent genera there is a common consent that *Psathyrostachys* and *Hordeum* diverged early on from the rest of the *Triticeae*. *Aegilops* and *Triticum* are closely related genera with a more recent origin. The estimates of the divergent times sugges<sup>t</sup> that *Hordeum* diverged 11 MYA, *Secale* 7 MYA and the *Aegilops-Triticum* complex 2.5–4.5 MYA [4]. *Hordeum* originated in western Eurasia, and later extended over The Northern Hemisphere, South Africa and South America. It contains about 33 species. Four genomes have been described H, I, Xa and Xu, which are present in diploid (2*x*), tetraploid (4*x*) and hexaploid (6*x*) taxa [6]. The H genome is present in barley, *H. vulgare*, and *H. bulbosum*, Xu in *H. murinum*, Xa in *H. marinum*, and the remaining species share variants of the I genome. Barley, used to feed livestock, and malted for beer or whisky (also whiskey) production, is the economically most important species in the genus, with a world production of about 147.40 million metric tons in 2017 (http://www.fao.org/faostat/es/#data/QC). It ranks the fourth in both quantity produced and in area of cultivation of cereal crops in the world. The barley genome has a size of 5.1 Gb, and contains 30,400 genes [7]. Its chromosomes are designated 1H to 7H according to the homoeologous relationships relative to the wheat chromosomes. The taxonomy of the genus *Secale* has been a matter of disagreement. The about 15 species initially recognized were reduced to three, *S. strictum*, *S. sylvestre* and *S. cereale*. This *S. strictum*, the perennial species of the genus, is considered the ancestral taxon. The other two species are annual, and *S. sylvestre* diverged first from *S. strictum*, while *S. cereale* is the younges<sup>t</sup> species of the group, and includes also *S. vavilovi* [8]. Rye (*S. cereale*) is the sixth most important cereal in production with a total of 13.73 million metric tons in 2017 (http://www.fao.org/faostat/es/#data/QC). Rye also has a large genome (8.1 Gb, nearly 50% larger than the barley genome) with 31,000 detected genes [9]. Chromosomes of rye are designated 1R to 7R, according to the homoeologous relationships relative to wheat chromosomes.

The wheat-*Aegilops* complex consists of three genera, *Amblyopirum*, *Aegilops* and *Triticum*, with one, 10 and two diploid species each, respectively. Based on the genome divergence, these diploid species were classified in seven groups: T-group (*A. muticum*); S-group (*Ae. speltoides*, *Ae. bicornis*, *Ae. longissima*, *Ae. sharonensis*, and *Ae. searsii*); A-group (*T. monococcum* and *T. urartu*); D-group (*Ae. tauschii*); C-group (*Ae. caudata*); M-group (*Ae. comosa* and *Ae. uniaristata*); U-group (*Ae. umbellulata*) [2]. In addition to the diploids, the *Aegilops* genus contains 10 allotetraploid species: *Ae. biuncialis* (UUMM), *Ae. geniculata* (MMUU), *Ae. neglecta* (UUMM), *Ae. columnaris* (UUMM), *Ae triuncialis* (UUCC), *Ae. kotschyi* (SSUU), *Ae. peregrina* (SSUU), *Ae. cylindrica* (CCDD), *Ae. crassa* (DDMM), and *Ae. ventricosa* (DDNN), and four allohexaploids: *Ae. recta* (UUMMNN), *Ae. vavilovi* (DDMMSS), *Ae. crassa* (DDDDMM), and *Ae. juvenalis* (DDMMUU).

The genus *Triticum* contains two tetraploid species, *T. turgidum* (AABB) and *T. timopheevii* (AAGG), the allohexaploid *T. aestivum* (AABBDD) and the autoallohexaploid *T. zhukovskyi* (AAGGA m A m). *T. turgidum* and *T. aestivum* constitute the Emmer lineage, and *T. timopheevii* and *T. zhukovskyi* constitute the Timopheevii lineage of polyploid wheats. *Triticum* is the most important genus of the tribe *Triticeae*

for its agricultural value. Its ranks the second after corn in grain production, contributing about 20% of the total calories consumed by humans.

The world production of wheat reached 771.72 million metric tons in 2017 (http://www.fao.org/ faostat/es/#data/QC), most of which is bread wheat, *T. aestivum*. Several studies on the divergence time of the diploid genomes of the wheat-*Aegilops* complex agree in showing the A and S genomes as the basal branches of the group, while the D genome diverged later [10–12]. Feldman and Levy [2] suggested a reticulate evolution in the group, in which the primitive diploid species diverged theoretically 2.5–3.0 MYA, and the more recent ones 2.5 MYA. The three ploidy levels of the wheat group contain cultivated species. One diploid species, *T. monococcum*, and the two tetraploids, were domesticated with the birth of agriculture about 10,000 years ago, while *T. aestivum* and *T. zhukovskyi* are considered to be originated under the cultivation of *T. turgidum* and *T. timopheevii*, respectively. Wild tetraploid wheat, *T. turgidum* ssp. *dicoccoides* (AABB) is believed to have originated within the past few hundred thousand years [4] from the hybridization of wild diploid einkorn wheat, *T. urartu* (AA), with a close relative of *Ae. speltoides* (SS, where S is closely related to B) [13–15]. The hexaploid *T. aestivum* (AABBDD) originated from a second hybridization event between *T. turgidum* and the wild diploid progenitor of the D genome, *Ae. tauschii* [16,17]. *T. timopheevii* originated 0.4 MYA [4,12], its A-genome was derived from *T. urartu* [13], while the G-genome originated from the S-genome of *Ae. speltoides* [15,18–23]. The hexaploid wheat *T. zhukovskyi* originated from the hybridization of *T*. *timopheevii* and *T. monococcum* [13,24]. Bread wheat has a large genome (17 Gb), whose reference sequence has been identified with an estimated coverage of 94%, giving access to 107,891 high-confidence genes [25,26]. A 10.5-Gb genome assembly composed of 14 pseudomolecule sequences representing the 14 chromosomes of wild emmer wheat (genome size estimated to be 12 Gb) was also reported [27]. Other wheat-relative genome sequences, including those of *T. urartu* (4.94 Gb) and *Ae. tauschii* (4.5 Gb), have been published [28,29].

Many studies carried out in order to identify the diploid progenitors of the allopolyploid species in the wheat-*Aegilops* complex were based in the genome analysis developed by Kihara [30–33]. This method assumed that the genetic architecture of the different genomes present in a given allopolyploid is preserved as in their diploid progenitors, making possible their identification through the analysis of meiotic pairing in interspecific crosses. A high frequency of bivalent pairing at metaphase I between the chromosomes of the diploid and polyploid species identified the homology of such genomes. Meiotic pairing also has implications on the possibility of transferring genes of agronomic interest from wild species to cultivated ones, especially to common wheat. Homologous recombination can be used in the transfer of genes from species of the primary and secondary gene pool, which share homologous genomes with common wheat. After direct hybridization and homologous recombination, useful genes can be selected in the offspring of the hybrids and in subsequent backcrosses [34]. In the case of species belonging to the tertiary gene pool, genomes are more differentiated relative to those of wheat, and any gene transfer to be achieved needs the occurrence of a recombination between homoeologous chromosomes. This became effective after the discovery of the *Ph1* gene that suppresses recombination between homoeologous chromosomes in wheat [35–39]. In the absence of *Ph1*, recombination is possible between the homoeologous chromosomes of wheat or between those of wheat and other species. Alternatively, *Ph* suppressors present in *Ae. speltoides* can be used to induce homoeologous recombination. Different genes have been transferred from the *Aegilops* species via such homoeologous recombination [40]. On the other hand, meiotic recombination appears also to be the foci of current research projects because of the importance of extending their occurrence to all genomic regions, especially to those that are usually restricted. In this review, I will summarize all of the features of meiotic recombination with implications on breeding-related programs, especially those concerning polyploid wheats.

### **2. Chromosome Structure in Triticeae**

All species of the tribe *Triticeae* are assumed to have evolved from a common ancestor. In the species divergence, chromosomes could adopt di fferent evolutionary paths, which can be established after unraveling the content and order of the genes present in the homoeologous linkage groups. In this task, bread wheat has played a central role.

Hexaploid wheat, *T. aestivum*, is the first allopolyploid in which all 21 chromosomes were identified according to its genomes of origin (A, B or D) and homoeologous groups. Such a chromosome classification was later used as a reference in the identification of the homoeologous relationships of chromosomes from other genomes of the tribe. Aneuploid sets of monosomics, nullisomis, telocentrics, trisomics and tetrasomics, as well as the 42 nullisomic-tetrasomic combinations obtained by Sears in cv. Chinese Spring [41,42], were indispensable materials used for this purpose. Unpaired chromosomes in the crosses of 21 monosomics of bread wheat and tetraploid wheat AABB were allocated to the D genome [41]. Chromosomes of the A and B genomes were identified in crosses between 13 ditelocentric lines and a synthetic tetraploid AADD [43]. Six telocentrics that formed a heteromorphic bivalent with a normal chromosome in the AABDD hybrids were assigned to the A genome, and the seven telocentrics that appeared as univalents were assigned to the B genome. The remaining chromosome, which belonged to group 4 [41], was determined to be 4A. Further studies demonstrated the initial misclassification of the chromosomes 4A and 4B, and they were reassigned as 4B and 4A, respectively [44].

Its hexaploid constitution confers upon bread wheat the ability of tolerating the loss of complete chromosomes, as well as the addition of chromosomes from related species without drastically a ffecting the viability of the plant. This ability and the crossability of wheat with di fferent species of genera *Aegilops, Haynaldia, Secale, Thinopyrum, Elymus, Leymus, Elytrigia, Roegneria* or *Hordeum* have permitted to develop wheat-alien addition and substitution lines. Sets of wheat-alien additions are derived from backcrosses of interspecific hybrids, or synthetic allopolyploids, with wheat. Such lines contain one chromosome (monosomic addition) or one chromosome pair (disomic addition) from a given specie added to the entire chromosome complement of common wheat. Additions from more than 20 related species have been reported in bread wheat [45]. Once a complete set of wheat-alien additions is obtained, the added chromosomes are assigned to homoeologous groups based on their genetic affinity to wheat chromosomes. In wheat-alien substitution lines a pair of alien homologues are substituted for a pair of wheat chromosomes. These lines are usually more stable than addition lines, but their production requires the use of wheat-alien additions. The standard method to obtain alien substitutions is to cross a disomic addition with a wheat monosomic of the same homoeologous group of the alien chromosome, and to select the disomic substitution in the o ffspring of the double monosomic obtained in the cross. In the case where the homoeologous relationships of the addition lines were not established, it is possible to cross a wheat-alien addition with seven monosomics. Among the substitutions obtained, only one involving homoeologous chromosomes will produce genetic compensating and fertile plants, thus identifying the homoeologous group of the alien chromosome. The ability of an alien chromosome to compensate for the absence of a wheat chromosome resembles the nullisomic-tetrasomic compensation test used by Sears [42] in the identification of the homoeologous chromosomes of wheat, and is the most e fficient method of identifying the homoeology of alien chromosomes to wheat. Telocentrics produced through a mis-division of the added chromosomes have also been recovered, and these increase the richness of cytogenetic stocks available in wheat.

Once the homoeologous relationships of chromosomes from di fferent genomes are identified, the level of synteny that they share can be assessed using di fferent comparative analysis. Meiotic pairing [46], physical location of low copy DNA probes [47], genetic maps [48,49] and genome sequencing [50] are di fferent approaches used to study whether collinearity of homoeologous chromosomes is preserved or broken down by rearrangements produced during genome di fferentiation.

### *2.1. Durum and Bread Wheats*

Meiotic pairings have been used to study the chromosome structure of bread wheat genomes [46]. The wheat chromosome arms that paired at metaphase I in wheat × rye hybrids lacking either the *Ph1* or *Ph2* were identified by C-banding. In most cases associations occurred between homoeologous arms, but some associations were produced between chromosome arms of di fferent homoeologous groups.

The 4AL arm was paired with 7AS and 7DS, 5AL with 4BL and 4DL, and 7BS with 5BL and 5DL. In addition, infrequent associations of 4AL-4DS, 4AS-4BL and 4AS-4DL were also observed. Such results indicated normal homoeology for all wheat chromosome arms except 4AS, 4AL, 5AL and 7BS. The arms 4AL, 5AL and 7BS are involved in a cyclic translocation and chromosome 4A in a pericentric inversion produced in the evolution of wheat. Meiotic pairing between chromosomes of tetraploid wheat *T. turgidum* and *T. aestivum* suggested the following sequence of chromosome rearrangements [51]. The arms 4AL and 5AL were involved in a reciprocal translocation, T(4AL-5AL)1 [52], produced during the evolution of the A genome, which was transmitted from *T. urartu* to *T. turgidum.* This and other chromosome rearrangements are described according to the standard nomenclature [53]. A second reciprocal translocation, T(4AL-7BS)2, and the pericentric inversion of chromosome 4A, Inv(4AS.4AL)1, occurred at the tetraploid stage. All of these chromosome rearrangements were transmitted to *T. aestivum*.

Di fferentiation of the chromosome structure of wheat genomes was also addressed by physical mapping. More than 60 full-length cDNAs were used as fluorescence in situ hybridization (FISH) probes, whose position was identified in the arms of the 21 chromosomes of hexaploid wheat [47]. Markers were selected to produce three di fferent signals per chromosome arm located in proximal, intercalary and distal positions, respectively. Most of these probes hybridized to all of the three wheat homoeologs. The order and relative positions of the markers was similar in all chromosome arms, except in chromosome arms 2AS, 4AS, 4AL, 4BL, 6AS and 7BS. Such exceptions are the result of the evolutionary rearrangements of 4A, 5AL and 7BS, as indicated above, or the chromosome rearrangements which appeared in Chinese Spring and other cultivars.

A genetic map of wheat chromosomes, which was based on the arm location of 800 restriction fragment length polymorphism (RFLP) markers using aneuploidy stocks, confirmed the chromosome rearrangements detected with chromosome pairing [48]. Construction of linkage maps involving homoeologous group 4, 5 and 7 chromosomes revealed the presence of a paracentric inversion on chromosome arm 4AL, Inv(4AL.4AL)1 [49,54]. The use of the deletion stocks of wheat [55] allowed us to establish the distribution of di fferent RFLPs markers along the wheat group 4 chromosomes, and a more precise identification of rearranged segments on chromosome 4A, as well as a pericentric inversion on chromosome 4B [56]. Using nulli-tetrasomic and ditelosomic lines and the deletion set of wheat group 4 chromosomes, the distribution of 1,918 expressed sequence tag (EST) loci along di fferent bins of chromosomes 4A, 4B and 4D, was reported [57]. In addition to the identification of inversions Inv(4AS.4AL) and Inv(4AL.4AL)1 and the translocated segments from 5AL and 7BS, another pericentric inversion, Inv(4AS.4AL)2, was detected on chromosome 4A. Comparison of genome sequences of *Ae. tauschii* and wild *T. turgidum* ssp. *dicoccoides* was employed to identify the breakpoints in the rearrangements of chromosome 4A, 5A and 7B [52]. The breakpoints harboring the pericentric inversion Inv(4AS.4AL)1 were located in sequences containing satellite DNA, while those of reciprocal translocations T(4AL-5AL) and T(4AL-7BS) were situated in non-repeated DNA sequences. The breakpoints of the paracentric inversion Inv(4AL.4AL)1 overlapped with the breakpoints of Inv(4AS.4AL)1 and translocation T(4AL-7BS), which suggested that these three rearrangements occurred simultaneously. The breakpoints of pericentric inversion Inv(4AS.4AL)2 were not identified.

The shotgun sequence obtained from individual chromosome arms of Chinese Spring provided a map of 551 homoeologous genes, which denoted the presence of pericentric inversions in at least 10 of the 21 chromosomes [58]. It is likely that some of such rearrangements occurred during the production of the aneuploid lines used in the study. A mapping population of 445 recombinant inbred lines (RILs) obtained from the cross of durum wheat cv. 'Langdon' x wild emmer was developed

and genotyped with single nucleotide polymorphism (SNP) markers to construct a high-density map of 2,650 segregating markers. An alignment of SNP markers in *T. turgidum* compared to that in *Brachypodium distachyon*, rice and sorghum, revealed the presence of 15 structural chromosome rearrangements, in addition to the already known rearrangements [59].

Intra-chromosomal translocations of short segments, a reciprocal translocation between 3B and 6B, a non-reciprocal translocation of a short 6BS segmen<sup>t</sup> to 7BL, and three large and one small paracentric inversions, were discovered. Genetic diversity in the rearranged chromosome 4A showed that the rearrangements could occur in the primitive tetraploid wheat.

Minor chromosome rearrangements due to gene locus deletion or gene locus duplication were detected in a sample of 3,159 Chinese Spring A- and D-genome gene loci. Such microsynteny perturbations occurred at both the diploid and polyploid levels, and showed a non-random distribution. Their occurrence correlated positively with the distance of the locus from the centromere [10].

Comparative studies revealed significant macro-collinearity between cereal genomes supporting that rice, sorghum and *Triticeae* originated from a common ancestor with a basic number of x = 12 chromosomes [60]. Rice maintains this chromosome number, but a reduction to x = 10 and x = 7 occurred in the divergence of sorghum and the ancestor of *Triticeae*, respectively. Comparison of the genome of *Ae. tauschii* with the rice and sorghum genomes revealed di fferent chromosome rearrangements produced in the evolution of sorghum and *Triticeae*, and that reduction of the chromosome number was mainly produced by insertion of an entire chromosome in a break produced in the pericentromeric region of another chromosome. In some instance, the inserted chromosome underwent telomeres fusion accompanied with a break in the pericentromeric region [61]. Of 50 rearrangements detected, 40 were assigned to the *Ae. tauschii* lineage, while two and eight occurred in the evolution of rice and sorghum, respectively. This result suggested a more accelerated evolution of the large genome of the *Triticeae* species.
