Journal of Heredity Advance Access originally published online on October 26, 2005
Journal of Heredity 2005 96(6):654-662; doi:10.1093/jhered/esi125
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Characterization and Molecular Mapping of Genes Determining Semidwarfism in Barley
From the USDA-Agricultural Research Service, P.O. Box 5677, SU Station, Fargo, ND 58105 (Dahleen), and the Department of Plant Sciences, North Dakota State University, Fargo, ND 58105 (Vander Wal and Franckowiak)
Address correspondence to L. S. Dahleen at the address above, or email: dahleenl{at}fargo.ars.usda.gov.
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Abstract |
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The semidwarf trait is desired in cereal breeding programs for increased lodging resistance. We characterized 27 brachytic (brh) semidwarf mutants in barley (Hordeum vulgare L.) and located the genes on barley chromosome linkage maps. All brachytic genes were transferred into the two-rowed cultivar Bowman by backcrossing four to seven times and selecting for semidwarf plants. The brachytic lines were evaluated for 10 phenotypic traits: plant height, awn, peduncle, and rachis internode length, leaf length and width, lodging, grain yield, number of kernels per spike, and kernel weight. We intercrossed the lines to determine which mutants were at independent loci and which were alleles at the same locus. F2 populations from 18 brh semidwarfs were constructed for genetic mapping using simple sequence repeat (SSR) markers. The brachytic semidwarf near-isogenic lines were significantly shorter than their normal counterparts and most had lower yields (16/27); shorter awns (26/27), peduncles (26/27), and rachis internodes (24/27); and reduced kernel weight (22/27). Twelve of the lines had shorter penultimate leaves and 15 had reduced lodging. Four lines had increased kernels per spike, while one had fewer kernels per spike. Allelism tests and mapping comparisons indicated that the 27 semidwarfs comprise 18 independent genetic loci. SSR mapping placed these loci in five of the seven barley chromosomes. Knowledge of the effects and locations of these brachytic semidwarf genes will help barley breeders select appropriate lines for barley improvement.
Barley semidwarf mutants have been investigated for decades with the goal of developing short-statured cultivars. The semidwarf trait is desirable because of reduced lodging and the potential for increased grain yield. Most semidwarf mutants have reduced grain yield, but higher yielding progeny have been identified from crosses between semidwarfs and high-yielding cultivars. Semidwarf barley cultivars have been successfully used around the world. Scientists in China have released more than 360 dwarf cultivars since 1950, with an average 4.7-fold yield increase over landraces and older cultivars (Zhang and Zhang 2003). Most European cultivars are semidwarf, and dwarf cultivars are common in Japan and Korea. The sdw1 (semidwarf 1) gene has been used in feed barley cultivars in the United States, western Canada, and Australia, but sdw1 appears to have negative pleiotropic effects on yield and malting quality (Hellewell et al. 2000). The denso allele at the same locus has been used successfully in most European malting barley cultivars. Implementing the use of semidwarf malting barley cultivars in the United States could potentially increase yield and save farmers space, time, and money (Hellewell et al. 2000).
Barley genotypes included in the semidwarf collection have been characterized as reduced height mutants, which are viable as homozygotes. Many semidwarf mutants have pleiotropic effects on traits other than culm length. Within the semidwarf collection, other traits affected include culm thickness, awn length, rachis internode length and number, kernel shape, leaf blade shape and size, coleoptile length and shape, tiller number, coiling of plant parts, and male fertility (Franckowiak 1986). However, the expression of these traits can be affected by environmental factors such as moisture, temperature, and photoperiod. Several of these mutants are insensitive to gibberellic acid (GA). Tests were conducted in early backcross generations to determine which mutants displayed a normal response to the GA hormone. Those that did not show a marked increase in elongation of the first leaf were classified as GA insensitive. This indicates an abnormal hormone response and may aid in characterizing these height mutants (Franckowiak and Pecio 1991).
A specific group of semidwarfs, called brachytic (brh) semidwarfs, has been characterized mainly through breeding trials. Characteristic traits include a short seedling leaf, reduced culm length, and short awns, and some brh lines show semicompact spikes, short anthers, and round kernels (Franckowiak 1999). Most were classified as insensitive to GA treatment, possibly because the mutation changed the balance between growth-promoting and growth-inhibiting hormones (Franckowiak and Pecio 1991). The first brachytic mutant identified was a spontaneous mutant found in the cultivar Himalaya, controlled by a single recessive gene, brh1 (Powers 1936). Several alleles have since been discovered at the same locus as brh1 (Franckowiak 1999). The brh1 locus has been placed on the molecular marker map linked to restriction fragment length polymorphism (RFLP) marker MWG2074B in the short arm of barley chromosome 7H (Li et al. 2001). The second brachytic locus, brh2, was identified by Tsuchiya (1980) and was located in the short arm of chromosome 4H.
A set of near-isogenic brachytic lines was developed by backcrossing 27 brachytic semidwarf mutants identified in various collections to the cultivar Bowman (PI 483237) to determine if inheritance was monogenic and to isolate the genes in a common genetic background (Franckowiak 1994a). Bowman was bred for North Dakota and is a two-rowed spring barley with high tolerance to heat stress (Franckowiak et al. 1985). It produces a relatively short plant in the greenhouse and does not have a recognized gene for strong photoperiod response or reduced height. Phenotypic traits include barbed lemmas, small sterile lateral spikelets, short glume awns, narrow leaves, semismooth awns, and long rachilla hairs (Franckowiak and Pecio 1991). There is a clear phenotype distinction between Bowman plants and brachytic mutants at almost all stages of development in most environments.
The Bowman near-isogenic brachytic lines provide ideal material for testing differences between brachytic mutants and for mapping their genes. Polymerase chain reaction (PCR)-based simple sequence repeat (SSR) markers (Ramsay et al. 2000) can be used to compare Bowman to the isogenic lines, with most of the polymorphisms associated with the brachytic loci. The objectives of this study were to characterize and map 27 new brachytic mutant alleles using SSR markers and near-isogenic lines backcrossed to Bowman barley.
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Materials and Methods |
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Mapping Population Development
A set of brachytic semidwarf mutant lines were selected from various barley collections based on phenotype and backcrossed four to seven times to Bowman (Table 1). In each F2, plants were selected that expressed the semidwarf trait and resembled the recurrent parent. Homozygous backcrossed lines, BCnF2 populations, and BCnF2-derived F3 lines were developed for mapping with molecular markers. Fifty BCnF2 seeds were sown for each semidwarf line in one of two greenhouses, along with the homozygous semidwarf parent and Bowman. The first greenhouse was maintained at 21°C–26°C with a 16 h day/8 h night cycle supplied by sodium halide lights. The second greenhouse was maintained at 16°C–24°C with a 14 h day/10 h night cycle. The greenhouse used depended on available space. Each plant was scored as either normal height or semidwarf. The semidwarf plants were at least 7 cm shorter than the normal height plants, although the difference depended on the brachytic gene. Plants were grown to maturity and harvested. Twelve BCnF3 seeds were sown for each BCnF2 plant to identify heterozygous lines. Parent and BCnF2 seeds were sown, one per 15 cm clay pot, in a soilless potting mix supplemented with a slow release fertilizer (14-14-14). The BCnF3 seeds were sown with six seeds per 15 cm clay pot and rated for plant height at the three- to four-leaf stage and again at maturity. Plants were treated with Marathon (Imidaclorprid) systemic insecticide at approximately the two- to three-leaf stage.
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Trait Analysis
Brachytic near-isogenic lines and Bowman were planted in a field near Christchurch (Leeston), New Zealand, and near Aberdeen, ID, in 2002 and 2003 for agronomic analysis. Height (cm) and lodging (1–9 scale) were measured at Christchurch only in both years at the hard-dough stage. Peduncle (cm) and awn length (cm), and the number of kernels per spike were measured in all four environments. Leaf length (cm) and width (mm) were measured on the penultimate leaf blade in all environments except 2002 Christchurch. Rachis internode length (mm) was measured in all environments except 2003 Aberdeen. Kernel weight (mg; based on the weight of 100 kernels) was measured in all environments except 2002 Aberdeen. Yield (g/m) was measured at Christchurch in 2002 and Aberdeen in 2003. Plots were sown in an augmented block design with Bowman repeated across blocks. Each plot was a 2 m row with rows spaced 60 cm apart. The seedling rate was approximately 20 seeds per meter of row. Data were analyzed by analysis of variance (ANOVA) using SAS software (SAS Institute 2002) and least squares means were compared using the general linear model procedure. Trait means of the semidwarf near-isogenic lines were compared to Bowman means using least significant difference values.
Allelism Testing
Near-isogenic brachytic semidwarf lines were intercrossed in a half-diallel in the second greenhouse described above. Spikes of the female parents were emasculated prior to anthesis and covered with glassine bags. Approximately 2 to 7 days later, when stigmas were receptive, spikes from the male parents containing dehiscing anthers were collected and pollen was applied to the females. Hybrid seeds were harvested and sown in greenhouse 2, described above, with three to five seeds per 15 cm clay pot. Plants from each cross were rated for plant height. Data were reported when at least nine hybrid seeds were recovered from each cross combination.
Molecular Marker Testing
Leaf tissue was harvested from young parent and BCnF2 plants grown in the greenhouse and the DNA extracted using the method of Dahleen et al. (2003). The DNA was then resuspended in 200 µl of modified TE (10 mM Tris-Cl, pH 7.4, and 0.1 mM EDTA). SSR markers (Ramsay et al. 2000) were screened against the semidwarf near-isogenic lines and Bowman to identify polymorphisms. We identified potential chromosome arm locations for many of the semidwarfs based on linkage drag with mapped morphological markers. For these, we started screening SSRs from that chromosome and usually found linkage to the semidwarf gene. When we didn't find linkage, we expanded our search to SSRs across the genome to identify polymorphisms. For example, brh7.w was suspected to be located in chromosome 7HS from linkage drag with the red stem base trait (ant1 locus; Franckowiak 1994b). None of the 20 SSRs screened for chromosome 7H were polymorphic, so another 62 SSRs were tested to identify the three used to map brh7.w to the short arm of chromosome 5H.
The PCR methods used are described in Dahleen et al. (2003). Amplified fragments were separated by gel electrophoresis using 4% superfine resolution (SFR) agarose (Amresco, Solon, OH) in 1x TAE (40 mM Tris-acetate and 1 mM EDTA). Alternatively, acrylamide gel electrophoresis was used as described by Wang et al. (2003). The gels were stained with ethidium bromide and photographed under ultraviolet (UV) light. Markers that detected polymorphisms between Bowman and a semidwarf near-isogenic line were tested on the corresponding BCnF2 population. Occasionally, pooled DNA extracted from at least nine BCnF2:3 plants was used for marker analysis when sufficient BCnF2 DNA was not available. A chi-square goodness-of-fit test was performed to determine whether the height segregation of each population fit the 3:1 ratio expected with a recessive, single-gene trait and the SSR marker data fit a 1:2:1 ratio expected for a codominant marker. SSR and height segregation data were entered into the MapMaker software (Lander et al. 1987; Lincoln et al. 1992) to test linkage between the markers and the semidwarf trait.
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Results |
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Trait Evaluation
As expected, all 27 brh backcross-derived lines were significantly shorter than Bowman (Table 2). The average height for the semidwarf lines was 64.8 cm, compared to 87.9 cm for Bowman. Allelic mutants tended to be similar for height. All but one semidwarf (brh.n) also had significantly shorter awns, and all but one (brh7.w) had shorter peduncles. Rachis internode length was shorter than Bowman in all but seven semidwarfs. Fifteen lines had shorter leaves; all lines were similar to Bowman for leaf width. Surprisingly only 15 of the dwarf lines had reduced lodging, a trait that often is improved by decreasing height. All brh1 and brh3 alleles reduced lodging, but lines with either brh6 allele had lodging scores similar to Bowman.
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The majority of brh genes significantly reduced grain yield, but 11 lines had yields similar to Bowman. These included four of the five brh1 alleles, both brh6 alleles, and genes for brh4, brh7, and brh8. Three of the higher yielding lines had an increased number of kernels per spike. Only one line, brh.u, had significantly fewer kernels per spike. More than 80% (22/27) of the semidwarfs had significantly reduced kernel weight. The five without reduced kernel weight included ert-t.55 and its allele brh3.g, plus brh7.w, brh.ac, and brh.v. With few exceptions, the allelic Bowman near-isogenic lines were phenotypically similar to each other. The two brh2 near-isogenic lines did not differ for any of the traits; the brh6 alleles differed only for rachis internode length. Two brh1 allelic pairs differed for peduncle length and one pair differed for rachis internode length. More differences were observed among the ert-t (brh3) near-isogenic lines. While these four lines did not differ for lodging, yield, awn length, and leaf width, one or two allelic pairs were significantly different for the remaining traits. For example, brh3.y had significantly shorter leaves than brh3.g, brh3.i, and ert-t.
Allelism Tests
Examination of progeny from crosses between semidwarf lines were used to determine allelism between the lines. If all the resultant progeny were dwarf, then the two lines contain the same semidwarf locus. If the progeny were tall, the two lines contain different semidwarf loci (Table 3). Progeny from allelism crosses identified brh.z and brh.aa as alleles of brh1, ari-l.3 as an allele of brh2, and brh.g, brh.i, and brh.y as alleles of brh3. The new brh3 semidwarfs were identified as alleles of the previously named locus ert-t (Lundqvist and Franckowiak 1997). The brh.r and brh.s semidwarfs were allelic to each other and the brh6 locus. Most of the mutants found to be allelic had similar near-isogenic line phenotypes. For example, lines with the ert-t (brh3) alleles have slightly twisted or coiled awn tips. Only four of the parent pair allelic relationships could not be determined, brh.n and brh.p, brh.u and brh.ab, brh.p and brh.ac, and brh6 and brh.ac. All four pairs are probably independent loci based on morphology. The remaining semidwarfs were not allelic as determined by progeny of crosses (Table 3) or map position (Table 2 and Figure 1).
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Mapping
Backcrossing the brh genes into Bowman limited most SSR marker polymorphisms to regions surrounding the semidwarf genes. Because SSR markers do not give complete coverage of the barley genome, one of the 18 lines, brh.u, did not show any polymorphism compared to Bowman and could not be mapped. Single SSR markers were linked to 3 of the semidwarf genes, while two or more markers were linked to 11 semidwarf genes. As expected, brh1.z mapped to the short arm of chromosome 7H (Figure 1e), where brh1 was mapped by Li et al. (2001). None of the new brh loci mapped near this locus. The only new gene that mapped to chromosome 7H was brh.v, located on the long arm. The brh2 locus was mapped near the centromere in the long arm of 4H using morphological markers (Hang and Tsuchiya 1980). The ari-l.3 allele of brh2 was located in the same region using SSR markers (Figure 1c). The brh5.m locus mapped to chromosome 4H, near ari-l.3, but all of the 15 plants from allelism crosses between the two semidwarfs were tall, indicating they are likely independent loci. A new semidwarf, brh.k, also mapped to this region, but the allelism crosses again produced only tall progeny.
The brh3.y allele of the previously identified brachytic mutant ert-t.55 (Tsuchiya 1976) was located at the end of the short arm of chromosome 2H (Figure 1a). The brh4.j locus was also placed in the short arm of chromosome 2H, proximal to the centromere. A new gene located in chromosome 2H was brh.l, which was linked to SSR markers near the centromere and was not allelic to ert-t.55 or brh4.j (Table 2). The gene brh8.ad was located near the centromere in chromosome 3H (Figure 1b). A new gene, brh.q, also was placed in chromosome 3H, but in the long arm.
The final numbered semidwarf genes mapped were brh6.r and brh7.w, which linked to SSR loci on the short arm of chromosome 5H. Five new genes—brh.n, brh.o, brh.p, brh.ab, and brh.ac—were located in this region. These seven semidwarf genes were linked to SSR markers Bmag0387 and HvLEU, with brh7.w, brh.n, and brh.ab toward the centromere and the remainder toward the telomere. Allelism tests indicated there are at least six separate loci (Table 3). The brh.p line crossed to brh.ac did not produce seedlings because dormancy prevented germination. The phenotypic differences between the brh.p and brh.ac near-isogenic lines indicated that they are unlikely to be alleles at the same locus.
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Discussion |
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The mapping and allelism data indicate that there are at least two clusters of semidwarf genes, in chromosome 4HL near the centromere and in chromosome 5HS. The chromosome 4H cluster contains three loci—brh2, brh5, and the new semidwarf brh.k. Map comparisons indicate the cluster is located in the region defined by barley bins five through seven. This region has been associated with height quantitative trait loci (QTLs) in several mapping populations, including Steptoe x Morex (Hayes et al. 1993), Harrington x Morex (Marquez-Cedillo et al. 2001), and Gobernadora x CMB643 (Zhu et al. 1999). The semidwarf loci cluster on chromosome 5H includes the brh6 and brh7 loci plus five new loci in barley bins two through four. Tinker et al. (1996) identified a height QTL from the Harrington x TR306 mapping population that was located in this region, with Harrington contributing to reduced height.
The use of near-isogenic lines backcrossed four to seven times to a common parent greatly facilitated this study. The original dwarfs were identified in various collections around the world and represent diverse genetic backgrounds. The background effects of each genotype would have confounded phenotypic comparisons of the original dwarfs. The repeated backcrossing to a locally adapted cultivar minimized these differences. The near-isogenic lines also simplified molecular mapping. The number of markers screened depended on the semidwarf and previous knowledge of potential locations based on linkage drag with morphological markers. The fewest markers (12) were tested on the brh2 parent versus Bowman, as we knew the gene was located on chromosome 4HL. The most markers (145) were tested on the brh.u parent versus Bowman, while most semidwarf parents were tested with 90–100 SSR markers. For those semidwarfs tested for many SSRs, almost all SSR polymorphisms observed (95–100%) were linked to a semidwarf gene.
In these field trials of near-isogenic semidwarf alleles, many lines have obvious problems that will affect breeding for reduced height. Seventeen of the 27 lines had significantly reduced yield, and 12 lines did not have reduced lodging. Besides plant height, lodging scores could be affected by factors such as anchorage provided by adventitious roots, plant weight, and spike weight (kernel per spike, kernel weight, and seed set). Seven of the semidwarfs, including brh.ab, brh7.w, brh8.ad, and four of the brh1 alleles had both significantly reduced lodging and yields comparable to Bowman. Of these, only brh7.w did not show a significant reduction in kernel weight. The malting quality of these lines needs to be evaluated to determine whether any of them are suitable for breeding a semidwarf malting barley cultivar for the United States. The characterization and mapping of these lines, however, provides breeders with information to select the most appropriate semidwarf genes to incorporate into barley cultivars to reduce height.
In summary, the results from this project make a substantial expansion of the characterization of brachytic semidwarf mutants beyond the two original loci identified as having the brachytic phenotype. Prior to the molecular mapping studies, six new loci were identified based on linkage drag and phenotype. The map position was found for one of the six new loci, and chromosome position information was confirmed for four of the five new loci. The sixth, brh7, was located in a different chromosome than indicated by linkage drag. Ten new loci were identified based on molecular markers and allelism tests, and nine of these were placed on a barley linkage map. We suggest these 10 loci be designated as brh9 to brh18, as listed in Table 1.
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Acknowledgments |
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We thank Bill Morgan, who crossed the brachytic dwarfs for allelism tests, and Shipra Mittal and Rachel McArthur for assisting with some of the DNA extractions and SSR markers. We also thank Dr. An Hang and Kathy Satterfield of the USDA-Agricultural Research Service, National Small Grains Research Facility, Aberdeen, ID, for assistance in the collection of morphological data.
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Footnotes |
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Corresponding Editor: Susan Gabay-Laughnan
Received March 13, 2005
Accepted August 15, 2005
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