Position and delimitation of Hordeum
Species concepts - delimitation and determination of species
Previous taxonomic studies
Morphology and terminology
Distribution
Ecology
Biology, reproduction, life forms, and dispersal
Genome relationships in Hordeum
Protein relationships in Hordeum
Variation in chromosome numbers and karyotypes
Genetic resources in Hordeum
Hordeum L. belongs to the tribe Triticeae of the family Poaceae (Gramineae). The tribe includes a number of important cereal crops, such as wheat (Triticum spp.), rye (Secale cereale), barley (Hordeum vulgare), and the artificially synthesized triticale (Triticosecale). In addition to these cereals many important forage grass species are referred to this tribe. Altogether the Triticeae comprises around 350 species (Dewey 1982, 1984, Löve 1984); the taxonomic delimitation of the group is still not satisfactorily resolved and there is still much disagreement among botanists and cytogeneticists concerning generic concepts.
Hordeum has generally been considered a well defined, easily recognized and monophyletic plant group characterized by three one-flowered spikelets at each rachis node, the two lateral ones being pedicellate, often rudimentary or sterile, and the central one sessile (rarely pedicellate). All the wild species were earlier considered to be fairly closely related to cultivated barley and to constitute a genetic resource for breeding purposes, even though rather strong sterility barriers were found to operate. In the light of more recent research, however, especially on the basis of genomic relationships, it has been claimed that Hordeum in its traditional circumscription comprises different groups of species being more distantly related. As a consequence Hordeum has been divided into two units, Hordeum sensu stricto, which includes only the two species H. vulgare and H. bulbosum (cf. Dewey 1984), and Critesion Raf., which comprises all the remaining Hordeum taxa (cf. Löve 1984). However, this concept of generic delimitation is not generally agreed upon and most researchers still maintain Hordeum in the traditional sense. Moreover, the genomic differentiation is such that if a subdivision is made, four or perhaps five genera should be recognized. In this treatment we maintain Hordeum in the traditional sense. It comprises 32 species and altogether 45 taxa.
The closest relatives of Hordeum in the Triticeae are probably the monotypic, annual genus Taeniatherum Nevski (Frederiksen 1986) distributed in the Mediterranean area; the perennial Psathyrostachys Nevski with 8 species in Central and Southwest Asia (Baden 1991); and the monotypic European, also perennial, genus Hordelymus (Jessen) Jessen (Bothmer and Jacobsen 1989b). These genera together with Hordeum constitute subtribe Hordeineae.
The subgeneric delimitation of Hordeum has also been the subject of much debate. Cultivated barley and its wild forms ("spontaneum" and "agriocrithon", see under H. vulgare) were first placed in one section (Sect. Crithe Doell, or Sect. Cerealia Ands.), and all other annuals in another section (Sect. Hordeastrum Doell). In the latter section the single uniting factor was the criterion of annual nature (Nevski 1941). The long-awned, perennial, American species were treated in Sect. Critesion (Raf.) Nevski, the short-awned perennial South American species in Sect. Anisolepis Nevski, the European, Asiatic and North American perennial species in Sect. Stenostachys Nevski, and finally H. bulbosum in Sect. Bulbohordeum Nevski. Based on morphology, Bothmer and Jacobsen (1985) recognized four sections, viz. Sect. Hordeum, Sect. Anisolepis, Sect. Stenostachys, and Sect. Critesion. For convenience, these sections are maintained in the present treatment, even though newer cytogenetic and biochemical data show that relationships within the genus are not completely reflected in the morphology.
Most species of Hordeum are biologically, and usually also morphologically, discrete entities. With a few exceptions the isolation barriers (usually as hybrid sterility) are very strict between the species and there is little or no genetic exchange in nature, even where two taxa have sympatric distribution. There are a number of reports on natural, sterile Hordeum hybrids (e.g. H. jubatum X H. brachyantherum in North America, H. lechleri with H. parodii, H. tetraploidum, and H. fuegianum, respectively, in South America, and H. jubatum with H. secalinum in Europe). Some species may be difficult to distinguish morphologically; however, at least one or a few "key characters" must differ between species. For an unambiguous determination of the species it is important to use a combination of several morphological characters. In this presentation we recommend the use of keys, descriptions of the individual species and illustrations. Some characters, for example, the brittle rachis at maturity, are common to most species while other characters are diagnostic for one or a few species. Appreciation of the differentiating sets of characters is not easy.
A few taxa are "critical" in the sense that they show intricate biological and morphological patterns of variation. Taxonomically this has made it necessary to subdivide the species into two or more subspecies. The traditional concept of subspecies is retained here, i.e. that they occupy different, but overlapping geographical areas, and that the "typical" representatives of each subspecies differ in morphology. There are often transitional forms between the subspecies in areas where their distributions overlap because of incomplete sterility barriers. Hence hybridization and gene transfer from one subspecies to another is not only theoretically possible, but common. Such is the case with the diploid, South American H. patagonicum, in which five subspecies have been recognized (Bothmer et al. 1986a, 1988c) and with the Asiatic, polyploid complex H. brevisubulatum sensu lato, which also has five subspecies (Landström et al. 1984). Another situation exists in e.g. H. bulbosum of which a diploid and a tetraploid cytotype are known. Based on this criterion the two cytotypes should deserve taxonomic recognition (Baum & Bailey 1985 a, b). However, because there is no single morphological trait (or combination of characters) which can unambiguously distinguish the two cytological forms, they are not recognized as distinct taxa here (Jørgensen 1982). The situation is somewhat similar in the North American - East Asian H. brachyantherum. The diploid form has been described as a separate species, H. californicum, with a restricted distribution in California, USA (Covas 1949). The characters used to separate the diploid from the tetraploid (e.g. appearance of the lateral spikelets) have been shown to be very complicated, and the two are maintained as subspecies.
Some comprehensive reviews of the genus Hordeum have been published earlier. The first treatment was made by Linnaeus (1753) in his Species Plantarum. In this he recognized 8 species, 5 of which are to be referred to cultivated barley, Hordeum vulgare, according to modern taxonomic understanding. The most thorough treatment was made by the Russian taxonomist, Nevski, who made the first modern attempt at a monograph (1941) including all species known at that time. Trofimovskaya (1972) treated most of the species and Bothmer and Jacobsen (1985) reviewed all species in a rather condensed way. The Canadian botanists Bowden (cf. 1962) and Baum and Bailey (cf. 1989 a, b) in a series of papers treated many species of the genus. The more general treatments or overviews by Nevski (1941), Trofimovskaya (1972), Tzvelev (1976), Parodi and Nicora (1978), and Bothmer and Jacobsen (1985) are not cited among the references for each species.
The diagnostic character of the genus Hordeum is the possession of three 1-flowered spikelets at each rachis node. Of the spikelets the lateral ones are pedicellate (except in some forms of H. vulgare). Most wild species of Hordeum resemble each other in size and general appearance, while H. vulgare is a much coarser plant and the proportions in its spike may deviate considerably. The descriptions given below may not always be applicable to a number of cultivated forms of H. vulgare. H. bulbosum and some forms of H. murinum are also fairly large plants, but they fall within the general description of the wild species.
The plants are tufted annuals or perennials. Only H. brevisubulatum and H. guatemalense have short rhizomes (these two species also develop sterile shoots, especially in cultivation). The lower leaf sheaths are usually hairy even if the upper ones are glabrous. Only H. intercedens has hairy upper leaf sheaths. The nodes are glabrous to hairy. The culms are mostly erect, in a few cases nodding or even de- or procumbent. Auricles are absent in most species, but very prominent in some. The leaves are flat or more or less involute, and more or less hairy on the abaxial as well as on the adaxial side, especially over the veins.
The spikes are identically built, varying in the shape, size, and colour of the various parts. The rachis is flat with shorter or longer hairs or bristles on the edges, usually longer ones upwards towards the spikelets. At each node there are three 1-flowered spikelets, a so-called triplet. The central spikelet usually has a well developed rachilla, while in most species the rachilla is lacking in the lateral spikelets. Each group of three spikelets is inserted alternately and distichously on either side of the rachis.
The central spikelet is sessile in most species, the glabrous to hairy lemma extends into an awn, the palea is glabrous to hairy, more or less bifid in the apex; the central spikelet is subtended by two glumes that are setaceous to more or less flat in the basal part.
The lateral spikelets are pedicellate, on a curved or straight pedicel, subtended by two glumes that in some species are unequal in size and shape. The lateral florets are rarely both female and male fertile, usually being staminate or completely sterile. In some cases the lemma is reduced to such a degree that it can only be characterized as a rudiment (the palea then lacking). According to species, the lemma extends into a shorter or longer awn.
The anthers also vary greatly in size, the longest ones being found in outcrossing species, the smaller ones in self-pollinating species, usually basifixed, yellow or with spotted pigmentation. The ovary is hairy and has two long or short, feathery stigmas. The ripe caryopsis is usually tightly enclosed in the lemma and palea. At maturity the rachis becomes fragile and shatters, dehiscing the three spikelets just above each node as a unit. H. bogdanii has (in most cases) a tough rachis at maturity and its spikelets shatter independently, also the lateral ones when occasionally seed-setting. Most cultivated forms of H. vulgare have a tough rachis at maturity.
Hordeum, like most other genera in the Triticeae, occurs in temperate areas on both the northern as well as on the southern hemisphere. It reaches subtropical areas in central South America and arctic areas in North America and Central Asia and is found from sea level up to more than 4500 m in the Andes and the Himalayas.
Centres of diversity for Hordeum, based on areas containing the highest number of species, are found in four areas of the world, viz. in Southwest Asia, (where cultivated barley evolved as a crop in ancient times in "the Fertile Crescent"), Central Asia, western North America, and southern South America. The last mentioned area also contains the highest number of native species, i.e. 17.
Whereas most species have comparatively restricted distribution areas, a few species, e.g. H. brevisubulatum, H. bulbosum, and H. brachyantherum, are very widespread. Some species, e.g., H. erectifolium (central Argentina), H. guatemalense (northern Guatemala), and H. arizonicum (southern USA and northern Mexico) are known only from one or a few locations. Some species, e.g., H. murinum, H. marinum, and H. jubatum, have become established as weeds in many parts of the world.
The majority of the Hordeum species are confined to grassland habitats. The species may be annual or perennial. In some of the perennial ones stressful and thus limiting climatic factors allow only a short lifespan of the individual plant, which thus approaches an annual life cycle.
The annual habitats are found where the summer rainfall does not permit a permanent vegetation cover. This occurs in areas where the rainfall is naturally low, possibly in combination with especially sunny conditions, or in habitats that are naturally moist during the winter season only (e.g. salt marshes).
The Mediterranean is an area commonly associated with the annual habitat, where e.g. H. vulgare subsp. spontaneum, H. murinum, and H. marinum are native. All three species are winter as well as summer annual types, the latter one occurring in drier areas where it flowers and ripens in the early spring before the summer drought. Other annual species are found in central and western North America which also has a Mediterranean climate, H. pusillum, H. intercedens, and H. depressum being found in ditches, along rivers, and, especially the latter two, along vernal pools with an often somewhat saline soil. H. arizonicum is perennial, often short-lived, adapted to river beds and saline areas that suffer severe drying up in summer. In cultivation it is likewise rather short-lived, failing to produce real tufts (where the true annual species may produce strong (annual), leafy tufts).
Fig. 1. Moist meadow with H. roshevitzii, USSR, Altai, northeast of Ust-Kan (August 25, 1990)
In South America, e.g. in the province of Buenos Aires, the annual H. euclaston grows in habitats similar to e.g. H. pusillum habitats, but also in grazed fields (not necessarily saline), the perennial H. flexuosum and H. stenostachys occupying more humid sites in the same field.
Generally the annual species occur at lower altitudes, but in inland pampas, prairies, and steppe areas they may reach an elevation of ca. 1000 m or more. The perennial Hordeum species are naturally found in closed, perennial grasslands. The European (-North African) H. secalinum grows along the seashore as well as in inland meadows. Through Asia H. brevisubulatum sensu lato, H. bogdanii, and H. roshevitzii are found in meadows and in grasslands along rivers more or less influenced by salt at altitudes of 1000 to more than 4000 m (Fig. 1). H. bulbosum occurs in the Mediterranean area as well as in Southwestern Asia, its perenniality in these dry areas being accomplished by its bulbous, basal stem internodes (Fig. 2).
In North America the perennials H. jubatum and H. brachyantherum are found in seashore and lowland meadows. The latter species may occur at higher altitudes and even in alpine meadows at 4000 m. H. jubatum is often found in more saline and drier areas (Fig. 3). The two species rarely occur together. But when they do they may occasionally hybridize and form hybrid swarms. The diploid cytotype of H. brachyantherum, subsp. californicum, is often found in alkaline soils or on serpentine.
In South America the perennial species are also found from sea level up to about 4000 m. Especially in the southern part of South America the species are found at low altitude, although when going inland to the Andes some of them may be found also at higher elevations.
On Tierra del Fuego H. lechleri, H. fuegianum, and H. pubiflorum occur in seashore meadows and grasslands in river estuaries, both fresh and salty. Further north these species go up into the mountains. H. pubiflorum is sometimes encountered in open Nothofagus forest meadows.
Characteristic Hordeum habitats in southern South America are more or less salty pans, hillsides, and river beds. In areas with stagnant water in winter and salt pans in summer, the subspecies of H. patagonicum are very common, and usually also H. lechleri and H. halophilum are found nearby. The latter two species also occur with H. parodii and H. tetraploidum in richer meadows.
An extreme biotope for a Hordeum species is on the sandy beaches at the Atlantic coast in southernmost Argentina (mainly Tierra del Fuego) where H. patagonicum subsp. magellanicum occurs.
In southern South America where more than one (sometimes several) species often occur in the same locality, hybrids are often found. Only occasionally are hybrids reported from other areas of the world, primarily because different species do not often occur together as they do in South America.
In central and northern Argentina H. halophilum and H. lechleri are found at higher altitudes. H. comosum, which has a well-developed root system, occurs on the dry, stony hillsides, with sparse vegetation, often with other tuft grasses and bushes. Higher up in the Andes and further north in Argentina and Bolivia, H. halophilum and H. muticum are met with at altitudes up to 4000 m in the puna steppes (Fig. 4) or in marshy meadows and regularly submerged alpine grasslands. The latter two habitats are also common to the Central American H. guatemalense.
Hordeum species are annual or perennial, the majority being perennial. The former include winter as well as summer annuals. Inbreeding (self-fertilization) predominates in the annual species although some may occasionally be cross-pollinated. For example, H. vulgare subsp. spontaneum and sometimes subsp. vulgare show rather open flowering which promotes out-breeding. There may, however, be variation in the degree of outcrossing even within populations. The inbreeders are not obligate selfers and this is reflected in considerable morphological and biochemical variation within populations.
Most of the perennial taxa have a versatile reproductive system without any specialization. Some, like, for example H. patagonicum, are mainly inbreeders with small anthers and stigmas and flowers which mostly do not open.
Two species are almost obligate outbreeders, namely H. bulbosum and H. brevisubulatum. Both have a two-locus self-incompatiblity system which largely prevents self-fertilization (Lundqvist 1962, Bothmer 1979), but a small degree of self-fertilization occurs, usually 2-3%. Some species are mainly outbreeders, viz. H, secalinum and H. tetraploidum, even though differentiation has not gone so far that self-incompatibility has been developed. They have the morphology of outbreeders with large pollen-rich anthers which hang out freely, large stigmas, and open flowers; a certain protandry is also obvious.
There seem to be two major trends of differentiation regarding seed dispersal. One evolutionary line is towards wind dispersal. These species have small, light seeds, very long, light, and slender awns, and glumes which bend outwards to around 90° and thus serve as an elegant flying and tumbling apparatus. Examples are H. jubatum, H. lechleri, H. procerum, and H. comosum. The other evolutionary trend is towards zoochory, i.e. dispersal by animals. This is found mainly in H. vulgare (including both subspecies), H. murinum, and H. bulbosum. These species have large, heavy seeds. The awns and rachis nodes are densely covered with stiff, straight hairs which attach to the fur of animals or the clothes of humans.
The basic concept of genome relationships is that like (homologous) chromosomes pair completely at meiosis; similar, but not identical (homoeologous) chromosomes pair to a certain extent, but not completely; and dissimilar (non-homologous) chromosomes do not pair at all. The pairing behaviour of the genomes of two species is normally analyzed at meiotic metaphase I in their mutual hybrid, and usually reported as the average number of chiasmata per cell. There are several sources of error in the determination of meiotic pairing, but providing an adequate number of cells and hybrid combinations have been analyzed, valid conclusions may be drawn. There have been attempts to make a taxonomic delimitation strictly based on genomes, but the system has not up to now become widely accepted (cf. Löve 1984).
Fig. 5. Average meiotic pairing between different diploid species in Hordeum. The letters I, X, Y and H refer to the genomic designations (cf. Bothmer et al. 1986a). No diploid hybrids with H. murinum were available for meiotic analysis
In Hordeum, the pattern of relationship is complicated due to the presence of several genomes (Bothmer et al 1987b). At the diploid level, four "basic" genomes occur. In their mutual hybrid, H. vulgare and H. bulbosum usually show very high meiotic pairing (up to 7 ring bivalents, Lange 1971, Kasha and Sadasivaiah 1971, Bothmer et al. 1983, Thomas and Pickering 1988). The two species share the genome named I, which is not present in any of the other species of Hordeum (Fig. 5; Bothmer et al. 1986a). The tetraploid cytotype of H. bulbosum forms a high frequency of tri- and quadrivalents, indicating it is a true autotetraploid with the genomic designation II (Jørgensen 1982).
The annual species H. marinum shows, despite morphological similarities to some of the other Hordeum species, no chromosomal homologies to the other species and appears to have a separate genome, preliminarily called "X" (Fig. 5; Bothmer et al. 1986a, 1987b). This genome is common to the two diploid forms, subsp. marinum and subsp. gussoneanum (Bothmer et al, 1989c). The cytogenetic behaviour of the tetraploid cytotype of H. marinum subsp. gussoneanum is debated. It forms almost exclusively bivalents at meiosis, which should indicate an alloploid nature. Data from, for example, isoenzyme patterns and the presence of only one satellited chromosome pair in the karyotype also agree with the hypothesis that two unrelated genomes are represented in the tetraploid (Jørgensen 1982, 1986, Jaaska and Jaaska 1986, Jaaska 1992, Linde-Laursen et al. 1989b). However, the hybrid between the di- and tetraploid forms of H. marinum has full meiotic pairing. It forms almost exclusively trivalents, which indicates a very high degree of homology among the chromosomes (Bothmer et al. 1989c). Contrary to the other evidence, this suggests an autoploid nature of H. marinum, 4x, combined with a very strong genetic regulation for bivalent pairing. Further support for an autoploid origin is gained from the demonstration of a chromosome pair, morphologically similar to the satellited chromosome pair, having an inactive nucleolus organizer region (Linde-Laursen et al. 1992b). One chromosome of each of the two pairs forms a bivalent in H. marinum subsp. gussoneanum, 4x x Secale cereale-hybrids with up to seven Hordeum ring bivalents. Thus, the tetraploid H. marinum has most probably originated as a hybrid between two biotypes of diploid H. marinum.
As deduced from studies of polyploid interspecific hybrids, the diploid form of H. murinum (subsp. glaucum) has yet another genome, preliminarily called "Y" (Bothmer et al. 1987b). There is no chromosomal homology among the polyploids of the H. murinum complex (subsp. murinum, 4x, and subsp. leporinum, 4x and 6x), and other Hordeum species (Rajhathy and Morrison 1962, Bothmer et al. 1988b, c). Like the tetraploid H. marinum, the polyploids of H. murinum also behave as alloploids, i.e. exclusively forming bivalents. However, there are also some cytogenetic indications that H. murinum, 4x and 6x, are also of an autoploid origin, but have very strong diploidizing mechanisms (Rajhathy and Morrison 1962, Bothmer et al. 1988b).
All the remaining Hordeum diploids have intermediate to high meiotic pairing in their hybrids (3-7 bivalents and 5-14 chiasmata/cell) which shows that they all have a common genome, named H (Dewey 1984, Löve 1984, Bothmer et al. 1986a). There is some differentiation between the Old and the New World diploids (Fig. 5). All the 11 South American diploid species, despite large morphologic differentiation, have more or less complete pairing in their mutual hybrids indicating little genomic differentiation. The North American annual diploids, H. intercedens and H. pusillum, are both closely related to the South American diploid species and show no genomic differentiation relative to these (Bothmer et al. 1985b, 1986a). The perennial, diploid H. brachyantherum subsp. californicum, native to western North America, is more closely related to the Asiatic diploids, H. bogdanii, H. roshevitzii, and H. brevisubulatum subsp. brevisubulatum than to the South American taxa.
The genome pattern is much more complicated at the polyploid levels (4x and 6x). The polyploids (4x and 6x) of the outbreeding Asiatic H. brevisubulatum complex, with its five subspecies, are autoploids, based on the H genome (Dewey 1979, Landström et al. 1984). Most other polyploid taxa of Hordeum are of a segmental alloploid type with an intricate pattern of relationships based on the H genome. The American tetraploids, viz. H. jubatum, H. brachyantherum, H. guatemalense, H. tetraploidum, and H. fuegianum are genomically very similar (Bothmer et al. 1987b, 1988b, 1989a). They behave as true alloploids with two unrelated genomes. However, a relatively high pairing in intergeneric hybrids, in particular with S. cereale, shows that there is a high degree of homoeology between the Hordeum chromosomes and, thus, that the two genomes are closely related. This very strong genetic mechanism for non-pairing among homoeologous chromosomes has been demonstrated especially in H. jubatum (Wagenaar 1960, Gupta and Fedak 1985).
The North American annual tetraploid H. depressum, has previously been considered a pure alloploid with the H genome in combination with an unrelated genome (Bothmer et al. 1988b, Bothmer and Jacobsen 1989b). It may, however, be a segmental alloploid or even an autoploid, but with a very strong diploidizing mechanism, similar to the one found in H. marinum and H. murinum. This is confirmed by results from Secale sp. x H. depressum hybrids that show a very high pairing between the two H. depressum genomes (Petersen 1991a, b). The nature of the two tetraploid perennials, H. secalinum (Europe) and H. capense (southern Africa), is still not clear. In hybrids, they behave as alloploids having one H genome together with a hitherto unidentified second genome (Bothmer et al 1988b). The American hexaploids H. procerum, H. lechleri, H. parodii (all South America) and H. arizonicum (North America), are all segmental alloploids with different variants of the H genome (Bothmer et al. 1989 a, b).
In a study of some isoenzyme systems in Hordeum, Jørgensen (1986) proposed the relationships among the various species. The relationships were inferred from the electrophoresis of the six enzymes, glutamate oxaloacetate transaminase (Got), phosphogluconate dehydrogenase (6-Pgd), malate dehydrogenase (Mdh), isocitric acid dehydrogenase (Idh), and alfa- and beta-amylase. These systems were chosen among 21 different enzymes, because they revealed a high level of interspecific variation and a minimum of intraspecific variation making them suitable as markers for studying taxonomic relations among species. Eleven loci were scored for in the selected systems revealing altogether 153 different alleles. A numerical treatment of the electrophoretic data was carried out using a maximum likelihood (furthest neighbour) and a Wagner network algorithm. The former method gives a phenetic clustering, the latter depicts phylogeny. In all, 427 populations representing 40 taxa of the genus were studied. For a more detailed description of protein relationships in Hordeum see Jørgensen (1986).
Diploids
The numerical treatment of the electrophoretic data revealed that the Hordeum species fall into three groups (Jørgensen 1986):
1. The H. vulgare group, comprising the three species H. vulgare sensu lato, H. bulbosum, and H. murinum sensu lato. The only discrepancy between the two different data analyses was that in the Wagner networks, H. murinum was more closely related to the H. pubiflorum group (see below) than to the H. vulgare group. H. vulgare subsp. vulgare and subsp. spontaneum, were not distinguished by the enzyme characters used in this survey. Likewise, the two tetraploid cytotypes of H. murinum, subsp. murinum and subsp. leporinum, could not be separated. A thorough analysis of seed proteins in the H. murinum aggregate was carried out by Booth and Richards (1978).Polyploids2. The monotypic H. marinum sensu lato group. The subspecies marinum and gussoneanum had very distinct isoenzymes.
3. The H. pubiflorum group consisting of all the remaining Hordeum species. H. pubiflorum and H. stenostachys held a central position in the group as the majority of evolutionary lines seemed connected to these species. The diploids in this group could be divided into four subgroups:
A. The first subgroup consisted of only one species, viz. H. muticum. Perhaps not surprisingly, H. muticum deviates enzymatically as its distribution area is separated from that of the other Hordeum species.B. H. chilense from Chile and H. roshevitzii from Central Asia made up the second subgroup. This unexpected relationship was reflected also in the high frequency of bivalents at meiosis in hybrids between the two species.
C. Together with the South American diploids (except H. muticum and H. chilense), H. pusillum and H. intercedens from North America constituted the third subgroup. This relationship is consistent with data from the interspecific crosses carried out by Bothmer et al. (1985b, 1986a).
D. The fourth subgroup included close relationship between H. bogdanii and H. brevisubulatum from Asia and H. brachyantherum from North America. This group may reflect some phytogeographical connection between the continents still evident from the presence of the tetraploids H. jubatum and H. brachyantherum, both in Asia and North America.
Polyploids have been of great importance for speciation in Hordeum. Generally, a comparison between enzymes of intraspecific cytotypes revealed that the phenotype of a diploid could be distinguished in the polyploids. In addition, extra electrophoretic bands, not found in the diploid, were nearly always present. This suggests an alloploid nature of these polyploids (Jørgensen 1986). The alloploid nature of many polyploids was also reflected in the frequent occurrence of fixed heterozygotic phenotypes. For instance, in the majority of the polyploids of the H. pubiflorum group, a Got allele appeared which was found only in H. marinum among the diploid Hordeum taxa. In the polyploids, this allele was expressed as part of a three-banded fixed heterozygotic pattern that was almost the sole phenotype in these polyploids. The other allele showing fixed heterozygosity in this pattern was contributed by one of the diploid species of the H. pubiflorum group. Got is a dimer enzyme and the third band was hence a hybrid band. In the hexaploids H. lechleri and H. procerum, the intensity of the three bands in the Got phenotype suggested that the gene of the marinum allele was found in one dose; the gene of the other allele in two doses. In the tetraploids with this pattern the two alleles had equal intensity.
The 45 taxa of Hordeum are basically diploid (2n = 2x = 14), tetraploid (2n = 4x = 28) or hexaploid (2n = 6x = 42) with a basic number of x = 7. However, 7 diploid or tetraploid taxa include a cytotype at the nearest higher ploidy level. In a few cases, plants with aneuploid chromosome numbers, due to elimination or duplication of chromosomes, have been observed (Linde-Laursen et al. 1980, 1986b, 1990a).
The karyotypes are symmetrical with chromosomes of approximately the same size and centromeres located at median or submedian positions. The lengths of the chromosomes at somatic metaphase are variously reported to be from about 5 to about 12 mm, seldom longer (the variation can partly be ascribed to differences in cytological technique). Some of the chromosomes, especially the satellite (SAT) chromosomes, are morphologically so characteristic that in some cases they can be used as markers for species identification (Rajhathy et al. 1964).
Most diploid Hordeum species have karyotypes comprising four pairs of metacentrics, one pair of submetacentrics, and two pairs of SAT-chromosomes, but some taxa, e.g. H. marinum and H. muticum, have only one SAT-chromosome pair. In contrast, H. brevisubulatum subsp. brevisubulatum and some populations of the diploid cytotype of subsp. violaceum have three SAT-chromosome pairs.
Among the tetraploids, cytotypes occur with one, two, three or four SAT-chromosome pairs. Among the hexaploids, the number of SAT-chromosome pairs may be two, four, five or six. The existence of tetraploid cytotypes with one, and a hexaploid cytotype with two SAT-chromosome pairs suggests nucleolar dominance.
Populations with visibly rearranged chromosomes have only been observed in H. vulgare (translocations, inversions), H. procerum (translocation), H. brevisubulatum subsp. violaceum, 2x (translocation), and H. brachyantherum, 4x (translocation) (Linde-Laursen et al. 1980, 1986a, 1990a, Konishi and Linde-Laursen 1988).
During the last 15 years, the knowledge of the karyotypes of the genus has increased substantially through the application of Giemsa C- or N-banding to the chromosome complements of all 52 cytotypes recognized in the genus (cf. Bothmer et al. 1987b). All inbreeders have shown banding pattern polymorphism differentiating populations, whereas no polymorphism was detected within populations and plants except in single plants of cultivated barley and H. bogdanii. Except for a population of H. secalinum from southern Spain and the two South American species, H. tetraploidum and H. parodii, that are considered more or less allogamous (Bothmer et al. 1986c), all outbreeding material has shown intrapopulational and intraplant banding pattern polymorphism. In some diploid, and to a lesser extent in polyploid inbreeders, banding patterns allow identification of homologues among populations. The number of visible bands per chromosome varies from 0 to 15, but the variation within a species is lower. Most bands are small, but they may vary in size from very small to large (>10% of the arm length). The most heavily banded chromosomes have been found in a population of H. murinum subsp. leporinum, 6x (Linde-Laursen et al. 1989b). In the majority of the species, the bands tend to be randomly disposed. However, in H. bulbosum nearly all bands are centromeric (Linde-Laursen et al. 1990b), and the karyotype of H. vulgare is distinguished by having mostly centromeric and juxtacentromeric bands (Linde-Laursen 1981). Most taxa of H. brevisubulatum have conspicuous telomeric bands (Fig. 6) in addition to a low number of intercalary and centromeric bands (Linde-Laursen et al. 1980). Bands are normally present on one or both sides of the nucleolar constrictions of the SAT-chromosomes.
Consideration of C-banding patterns and chromosome morphology indicates that all diploid Hordeum species of the Americas except H. muticum and H. cordobense have similar karyotypes. This questions the biological relevance of referring them to three different sections. The tetraploid American Hordeum species, with the exception of H. depressum, have similar or rather similar C-banded karyotypes suggesting a common origin. The marker chromosomes of the constituent genomes show great similarity with the Asiatic H. roshevitzii and North American H. brachyantherum subsp. californicum suggesting an alloploid origin based on these two diploid taxa. The American hexaploids are alloploids. Except for H. brachyantherum, 6x, all combine genomes similar to those found in most American tetraploids plus a genome of an American diploid species. H. brachyantherum, 6x may combine genomes similar to those of H. depressum and H. brachyantherum subsp. californicum (Rajhathy and Symko 1966, Linde-Laursen et al. 1986a, 1990a, 1992a, Baum and Bailey 1989a).
The similar C-banded karyotypes of H. secalinum and H. capense indicate a very close relationship (Linde-Laursen et al. 1986b). Although H. vulgare and H. bulbosum contain the same genome, named I (Bothmer et al. 1986a), the differences between their C-banded karyotypes (Fig. 7) indicate that they are not very closely related (e.g. Linde-Laursen 1981, Xu and Snape 1988, Linde-Laursen et al. 1990b). The C-banded karyotype of H. bulbosum (4x) supports the argument that it is an autopolyploid derivative of the diploid cytotype. A similar close correspondence is not observed among C-banded karyotypes of the autopolyploid H. brevisubulatum species complex (Linde-Laursen et al. 1980). The C-banded karyotype of H. marinum subsp. gussoneanum, 4x, and studies using in situ hybridization (Linde-Laursen et al. 1992b) support the idea that it is an autopolyploid derivative of diploid H. marinum. H. murinum, 4x, 6x contain the genome of H. murinum, 2x. The sources of the other genomes are so far unidentified. The C-banded karyotypes of the remaining taxa give no clear indications of the closer relationships.
The utilization of wild Hordeum species in barley breeding for the transfer of desirable genetic traits has not been as successful as, for example, in cultivated wheat. This has two main causes. (1) Barley is a diploid organism, which is much more sensitive to minor genetic imbalances than wheat, which has a buffering effect due to polyploidy (presence of four or six instead of two genomes). (2) Most wild Hordeum species are much more distantly related to cultivated barley than are Aegilops and Triticum species to bread wheat (Kimber and Feldman 1987).
The species of Hordeum can be divided into three categories based on their relation to cultivated barley and how accessible they are as gene donors to the crop species.
Primary genepool
This is defined as material so closely related to the crop species that there are no or very weak biological barriers for gene transfer. In barley, the primary genepool consists of landraces from various geographical regions, where they are still cultivated or have been used recently. However, landraces disappear rapidly and are no longer available from large regions, for example, northern and central Europe. Landraces are still used as food in Central and Southwestern Asia and parts of Northern Africa including Ethiopia. The progenitor of cultivated barley, i.e. H. vulgare subsp. spontaneum also belongs to the primary genepool. The major problem for the use of subsp. spontaneum in barley breeding is the presence of several non-desirable characters like shattering, uneven germination, stiff awns, shrunken seeds, and variation in vernalization requirements. Some generations of pre-breeding are needed to transfer the genetic material into an adapted barley genotype which can then be used in conventional breeding programmes. Several traits are of interest for transfer into barley germplasm, particularly disease-resistance genes (Fischbeck et al. 1976, Moseman et al. 1983, Lehmann and Bothmer 1988).
Secondary genepool
This comprises all wild or weedy forms that have a comparatively good crossability with the cultivated species, but in which certain sterility factors are operating. The single representative in Hordeum is the perennial, di- and tetraploid species, H. bulbosum, native to the Mediterranean region. It is obviously the closest relative of cultivated barley, apart from subsp. spontaneum, and shares the I genome with H. vulgare. H. bulbosum has been widely used in cereal breeding, because its chromosomes are normally eliminated in the young H. vulgare x H. bulbosum hybrid embryos during the first days of development, leaving one set (7) of barley chromosomes. The embryo develops into a haploid barley plant which can be chromosome-doubled through application of colchicine. It gives rise to a completely homozygous line of barley, which may be used directly in a breeding programme. Sometimes chromosome elimination does not take place, but the embryo develops into a true, stable hybrid (this is genotype/environment dependent). The chromosomal pairing during meiosis is often very high in the hybrids, but the fertility is extremely low (Lange 1971, Kasha and Sadasivaiah 1971, Bothmer et al. 1983, Xu and Snape 1988). Some time during later meiotic phases or during the development of the pollen, the normal developmental process fails, leading to formation of sterile gametes, but this process is not understood in detail. Several characters in H. bulbosum are of putative interest for transfer into cultivated barley, e.g. resistance to powdery mildew (Jones and Pickering 1978, Szigat and Pohler 1982, Gustafsson and Claësson 1988, Xu and Snape 1989).
Tertiary genepool
All other Hordeum species belong to the tertiary genepool of cultivated barley. This indicates that interspecific hybrids have to be established through embryo rescue techniques. The species possess genomes other than cultivated barley, and the hybrids with it are highly sterile. So far the germplasm of these wild species has not contributed to the progress of barley breeding. The development of new techniques, e.g. somatic hybridization and gene transformation, may make the genetic content of these taxa available for transfer in the future. Several of the wild species have been shown to contain interesting resistance genes (Orton 1979, Schooler 1980, Bothmer and Hagberg 1983, Bothmer 1992).
