THE ROLE OF Aegilops SPECIES IN THE ORIGIN AND IMPROVEMENT OF COMMON WHEAT Roman Pra

Some Aegilops species participated in wheat evolution playing a major role in wheat domestication and therefore the genus Aegilops represents a big part of the additional gene pool determining important traits of wheat. Breeders have been using these genes for many years to produce improved cultivars. Wide crosses between its wild relatives are sources of desirable characteristics for genetic improvement of common wheat. Triticum aestivum evolution and methods for transfer of alien material into wheat, briefly reviewed in this article, include incorporation of the whole genomes, single chromosomes, small chromosomal segments, single genes and cytoplasm substitution in wheat.

An example of the transfer of beneficial traits from Aegilops species to cultivated wheat is the translocation from Ae. ventricosa introduced in France to the winter variety VPM1, conferring resistance -owing to the genes Pch1 and Pch2 -to eyespot, caused by Pseudocercosporella herpotrichoides [26].In Great Britain an enzyme marker of the eyespot resistance gene was developed and the Rendezvous variety was produced, which is found in the lineage of many British, French, German and Swiss winter wheats as well as in Australian and North American wheats.In addition to resistance to Pseudocercosporella herpotrichoides, a translocation from Ae. ventricosa was also found to occur in these varieties, on chromosome 2B, containing a group of three rust resistance genes: Lr 37, Yr 17 and Sr 38 [36].

The role of Aegilops species in the evolution of common wheat
Both selection by man and natural cross-breeding between primitive wheats and wild grasses of the genus Aegilops occurring as weeds in wheat crops have played a significant role in the evolution of wheat.Some researchers estimate that hexaploid wheats evolved over 10,000 years [37].The donor of the A genome for common wheat is probably the diploid wheat T. urartu [38].The origin of the B genome is still a matter of controversy.H u a n g et al. [39] believe it to be similar to the S genome of Aegilops species belonging to the Sitopsis section.The S genome of Ae. speltoides is most similar to the B genome of polyploid wheats.This can be seen in the fact that the brittle rachis gene Br 3 has the same position on the short arm of chromosome 3S in Ae. speltoides [40] and on the short arm of chromosome 3B in the tetraploid wheat T. durum [41,42].The locus of another brittle rachis gene, Br 2 , was localized on the short arm of chromosome 3A in T. durum [42].The B genome, which originated in Ae. speltoides, probably underwent a secondary modification in wheat [43].Tetraploid wheats (AABB) emerged as the result of chance pollination of Ae. speltoides with T. urartu pollen.Later, the number of chromosomes in the resulting hybrid must have doubled spontaneously.DNA analysis by H a i d e r [44] revealed high similarity of the S genome of Ae. speltoides to the B genome of tetraploid and hexaploid wheat.Hexaploid wheats are presumed to have arisen from chance pollination of the tetraploid wheat T. dicoccoides with pollen of the diploid goatgrass Ae. squarrosa (Ae.tauschii) (DD), followed by spontaneous doubling of the number of chromosomes or the pairing of unreduced gametes in the resulting hybrid.Thus, they are natural amphiploids.The similarity between the D genomes of wheat and Ae.squarrosa can be seen in the position of the Br 1 brittle rachis gene on the short arm of chromosome 3D of T. aestivum and of the gene Br t on the short arm of chromosome 3D in Ae. squarrosa (Ae.tauschii) [41,42].

Methods and techniques of gene transfer from Aegilops species to common wheat
Some Aegilops species occurring as weeds in wheat crops or on unploughed land between fields can spontaneously cross breed with common wheat [45].The effectiveness of such spontaneous cross-breedings is similar to that of artificial ones.Seed setting in hybrids takes place more often when the maternal form is Aegilops and the paternal form is wheat [46,45,3].Most easily cross-bred with wheat are Aegilops species containing the D genome, which has the highest homology to the D genome of wheat [3].
Failures in cross-breeding of wheat with many Aegilops species are due to low homology or lack of homology between their genomes and those of wheat, and to an improper number of chromosomes in the endosperm.Underdevelopment of the endosperm leads to the death of the embryos in the early stage of development.Embryos can be isolated and grown on artificial media in vitro.Sterility in F 1 hybrids of distant forms is due to disturbances in the meiosis process [47], which results in a lack of functional gametes.Backcrossing with wheat or colchicination is necessary to obtain kernels [48].
Difficulties in obtaining F 1 intergeneric hybrids also result from the genetic barrier posed by the group of Kr genes in common wheat.The system controlling the capacity for intergeneric cross-breeding of T. aestivum with rye includes four dominant genes, Kr1, Kr2, Kr3 and Kr4, of which Kr1 produces the strongest effect and Kr3 the weakest.In their dominant form, these genes inhibit seed-setting ability in the F 1 generation [49,50,51].There are, however, varieties of wheat, e.g.Chinese Spring with the genotype kr1 kr1 kr2 kr2, which are distinguished by adequate ability to cross breed with rye [52].
To overcome barriers to cross-breeding, various methods and techniques are used for transferring genes from Aegilops species to wheat.These include the following: -adding the entire genome of the Aegilops species to wheat genomes, i.e. obtaining amphiploids, and from these, via backcrossing with wheat, addition and substitution lines; -one of the recombination methods, i.e. crossover resulting from homologous or homeologous pairing of chromosomes; -translocations induced by ionizing radiation, caused by gametocidal chromosomes, or resulting from somaclonal variation; -obtaining alloplasmic forms of wheat with the cytoplasm of Aegilops species; -transferring single genes to wheat via genetic engineering methods.Chromosome doubling using colchicin in F 1 hybrids makes it possible to obtain amphiploids [53], and from these, via backcrossing with wheat, addition and substitution lines [54,55].Amphiploids can also arise spontaneously via pairing of unreduced male and female gametes formed by intergeneric or interspecific F 1 hybrids [56].
By backcrossing amphiploids with wheat and carrying out selection for 43-chromosome plants, addition lines can be produced.One Aegilops chromosome is added to the complete set of wheat chromosomes, and following pollination of plants with 43 chromosomes, forms arise that have two Aegilops chromosomes.Although addition lines have not found wide application in practice due to disturbances in meiotic divisions leading to the loss of the added chromosome and to low fertility, they are used to identify foreign chromosomes and as initial forms for transferring foreign genetic material to wheat [55,57].
Addition lines are used to obtain substitution lines.These are more stable than addition lines and have more genotypic variation.Substitution lines were obtained in which Aegilops chromosomes were substituted in place of wheat chromosomes [6,58,59,60].Owing to the foreign chromosomes, these lines are resistant to fungal pathogens, nematodes, and insects.
The simplest method for transferring foreign genes to wheat is recombination resulting from homologous pairing of chromosomes, usually chromosome D of Aegilops and chromosome D of wheat [3].The species Ae. squarrosa (D), Ae. ventricosa (UnD), and Ae.cylindrica (CD) contain D genomes that are homologous to that of wheat [2].In this case, gene transfer can take place on the basis of a simple crossing over.
Recombination resulting from homeologous pairing of chromosomes occurs exclusively via inactivation of the Ph genes of the homologous pairing system in common wheat.Suppression of homeologous pairing is controlled by the group of dominant Ph genes -Ph1 on chromosome 5 BL and Ph2 on chromosome 3DS, as well as other unidentified genes on chromosomes 3AS, 4D, 5A, 5B, and 5D.Of these, Ph1 exhibits the strongest effect [61].The gene Ph1 occurs both in common wheat T. aestivum and in tetraploid wheat T. durum, but is not present in diploid species of wheat or in the Aegilops species from which tetraploid wheats with AABB and AAGG genomes were produced.This gene must have appeared at the tetraploid level in the development of hexaploid wheat.The absence of the Ph1 gene in the goatgrass Ae. speltoides indicates that it emerged as the recessive mutation ph, enabling pairing of chromosomes of diploid wheat (AA) with chromosomes of Ae. speltoides (SS), or as a translocation of a segment of an extra chromosome of the goatgrass Ae. mutica with a wheat chromosome [62].
In the absence of dominant Ph genes (nullisomy 2n = 40: ph ph, monosomy 2n = 41: Ph ph) or in the case of a recessive mutation (disomy 2n = 42: ph ph), there occurs homeologous pairing of chromosomes of foreign species with wheat chromosomes in F 1 hybrids.The effect of the recessive ph allele is manifested only in interspecific and intergeneric hybrids; it does not affect the pairing of chromosomes of the A, B and D genomes in common wheat [63].During homeologous pairing reciprocal translocations take place, which constitute the main mechanism by which a chromosome fragment from a foreign species is incorporated in the wheat genome, and the transfer of foreign genes sought in T. aestivum breeding occurs.Thus, the system of recessive ph genes enabling homeologous pairing is exploited in the introgression of foreign genes into common wheat.For this reason work has been undertaken to obtain recessive ph ph genotypes in T. aestivum wheat [52].S e a r s [64] obtained the world's first complete sets of 21 monosomic lines (2n = 41) and 21 nullisomic lines (2n = 40) in the Chinese Spring variety.This allowed the heterozygous genotypes Ph1ph1 (mono-5B) and Ph2ph2 (mono-3D) and the homozygous genotypes ph1ph1 (nulli-5B) and ph2 ph2 (nulli-3D) to be used in breeding.Subsequent monosomic series of wheat were obtained in the cultivars 'Drabant', 'Jara', 'Favorit' and others [52].
Using induced homeologous pairing and crossing over, a number of wheat varieties with Aegilops genes have been obtained.One of the first was Compair [65], with resistance to yellow rust transferred from Ae. comosa.Resistance to rust was determined by the dominant gene transferred to chromosome 2D of wheat together with a fragment of chromosome 2M of Ae. comosa.
On chromosome 5S of the goatgrass Ae.Speltoides, Dvorak et al. [61] identified dominant Ph I suppressor genes which cause inactivation of the gene Ph1 on chromosome 5BL of common wheat.In the presence of these genes, and despite the presence of the Ph1 gene, synapsis takes place between homeologous chromosomes of foreign species and of T. aestivum.Similar genes were located in Ae. peregrina and Ae.kotschyi [66].Suppressor genes were successfully used to transfer genes of resistance to brown and yellow rust from Ae. umbellulata [14] and from Ae. triuncialis and Ae.geniculata [67] to common wheat.
If a foreign chromosome is not homeologous to wheat chromosomes and cannot pair with them in F 1 hybrids, genetic material from Aegilops can be introduced into wheat by means of translocations.It is then necessary to apply radiation methods in order to physically activate the chromosome [69].These methods involve irradiation of the anthers or kernels of F 1 hybrids and self-pollination.In both cases, in the F 2 generation translocations with a foreign chromosome must be identified [70,52].S e a r s [71] was the first to use ionizing radiation to induce chromosomal aberrations and to transfer the gene for resistance to brown rust (Puccinia recondita) from Ae. umbellulata to the Chinese Spring variety of wheat.
Gametocidal chromosomes can contribute to the transfer of foreign genes to wheat.It has been observed that certain foreign chromosomes added to wheat are not eliminated from its genome despite successive backcrossings.Gametes with such chromosomes were found to be fertile, while other gametes were incapable of fertilization.The presence of a gene or genes conferring the 'gametocidal' trait was observed on chromosome 3C of Ae. markgrafii and Ae.triuncialis [72], on chromosome 2C of Ae. cylindrica [73], on chromosome 4M of Ae. geniculata [74], on chromosomes 2S l and 4S l of Ae. longissima, on 2S sh and 4S sh of Ae. sharonensis [75], and on chromosomes 2S and 6S of Ae. speltoides [76].Gametocidal chromosomes introduced into wheat induced mutations involving structural changes in chromosomes such as deletions and translocations [77].
In vitro breeding conditions can also contribute to translocations between Aegilops and Triticum chromosomes.F e l d m a n [78] observed the presence of multivalents in meiosis, probably caused by translocations in hybrids of T. aestivum with the amphiploid T. turgidum-Ae.squarrosa, regenerated from callus obtained from an in vitro microspore culture.
Aegilops species can be used as donors of cytoplasmic genes.As a result of the transfer of the common wheat nucleus to the cytoplasm of Ae. caudata and Ae.ovata, in later generations of backcrossing hybrids there appeared male-sterile forms of wheat that could constitute starting material in heterosis breeding [79].Cytoplasm substitution can cause changes in grain yield, protein content and resistance to various biological and ecological stresses, due to diverse interactions between the nucleus and the cytoplasm [80].By cross-breeding the species Ae. caudata, Ae. columnaris, Ae. kotschyi, Ae. markgrafii, Ae. peregrina, Ae. umbellulata and Ae.triuncialis with alloplasmic wheat with a translocated 1BL/1RS chromosome, wheat haploids can be induced as the result of parthenogenesis [81].From these haploids it is possible to obtain double haploids, by colchicination or the use of other mutagens that double genetic material, thus substantially shortening the process of producing new varieties.
Recent years have seen the rapid development of genetic engineering techniques.Transgenic varieties of wheat have been obtained which are resistant to the herbicide glyphosate [82].One subject of current research is the risk of transfer of such transgenes from wheat to Aegilops species, which are often present as weeds in wheat crops [45].Genetic markers can be used to evaluate the scale of this phenomenon.Areas in which DNA markers have found wide application include evaluation of genetic similarity or distance, selection and identification of desired forms, confirmation of the effectiveness of cross-breeding, and identification of Aegilops genes determining important performance features [36,83,84,57,85,86,87,17,88].Using molecular techniques, Aegilops genes can be isolated and stored in artificial bacterial chromosomes and then transferred to wheat [89,90].

CONCLUSION
Transfer of Aegilops genes makes it possible to enrich wheat with valuable resistance and quality characteristics and to prevent genetic erosion of the species.The modifications and breeding lines obtained constitute starting material for new varieties which are more fertile, more resistant, and better suited to changing climate and soil conditions.
Handling Editor: Elżbieta Weryszko-Chmielewska This is an Open Access digital version of the article distributed under the terms of the Creative Commons Attribution 3.0 License (creativecommons.org/licenses/by/3.0/),which permits redistribution, commercial and non-commercial, provided that the article is properly cited.©The Author(s) 2013 Published by Polish Botanical Society