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CELL BIOLOGY & MOLECULAR GENETICS

Identification of RFLP Markers Linked to the Barley Aluminum Tolerance Gene Alp

^a USDA-ARS, U.S. Plant, Soil and Nutrition Lab., Tower Road, Ithaca, NY 14853 USA
^b Dep. of Plant Breeding, Cornell Univ., Ithaca, NY 14853 USA

dfg3{at}cornell.edu

	ABSTRACT

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Aluminum (Al) toxicity limits crop productivity in acidic soils. As with many crops, natural genetic variation for Al tolerance has been found in barley (Hordeum vulgare L.). Al tolerance can be evaluated by replicated field trials, by soil bioassays in pots, or by solution culture methods. To date, alternative marker-assisted methods of Al tolerance selection in barley have not been developed. The goal of this study was to identify molecular markers for Alp, a gene in the barley cv Dayton that confers a high level of Al tolerance. An F₂ mapping population was generated from a cross between Dayton and the more aluminum-sensitive cv Harlan Hybrid. Al tolerance in this population was scored by hematoxylin staining, and was confirmed to segregate in a monogenic fashion. Restriction fragment length polymorphism (RFLP) mapping of Alp was undertaken, and it was localized to the long arm of chromosome 4H, 2.1 cM proximal to the marker Xbcd1117 and 2.1 cM distal to the markers Xwg464 and Xcdo1395. These markers can be used for marker-assisted selection of Al tolerance in barley without the need for field trials, soil bioassays, or solution culture analysis. Further, the linkage between Xcdo1395 and Alp is interesting because this marker is also linked to the wheat (Triticum aestivum L.) Al tolerance gene Alt_BH located on the long arm of chromosome 4D. This result is suggestive of the possibility that Al tolerance in barley and wheat may be due to the action of orthologous loci.

Abbreviations: cM, centimorgan • C, complete staining • N, no staining • P, partial staining • RFLP, restriction fragment length polymorphism

	INTRODUCTION

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ALUMINUM TOXICITY limits crop growth and productivity on acidic soils, which represent approximately 12% of the world's cultivated lands (von UexKüll and Mutert, 1995). The predominant form of Al that is found in acid soils is Al³⁺. This ion is highly toxic to plant roots (Kinraide, 1991), resulting in a poorly developed root system and thus susceptibility to drought stress and nutrient deficiencies (Foy, 1988; Kochian, 1995). While liming of soil can ameliorate some Al toxicity, it is expensive, ineffective in the subsoil, and in some cases heavy lime application may have a deleterious effect on soil structure (Rao et al., 1993).

Another strategy for improving crop productivity on Al-toxic acidic soils is to select for cultivars with increased Al tolerance. Natural variation for Al tolerance in crops is well documented (Foy, 1988). Among the small grains, barley is the most Al-sensitive species, while rye (Secale cereale L.) appears to possess the highest degree of Al tolerance (Foy, 1983). Further, genotypic variation for Al tolerance within these species also exists (DeSousa, 1998; Foy et al., 1965; Lafever et al., 1977; Reid et al., 1969) and in some instances has been used to improve crop productivity in acid soils. While genotypic variation for Al tolerance exists in barley, production of this crop on acidic soils is more limited than its more Al-tolerant relatives because of a generally high level of Al sensitivity in the species as a whole.

The inheritance of Al tolerance in barley has been reported to be controlled by a single gene (Minella and Sorrells, 1992; Reid et al., 1971). While barley cultivars exhibit a range of variation for Al tolerance (Foy et al., 1965; Reid et al., 1969, 1971), in many instances this appears to be due to the action of a single locus, with different alleles conferring different degrees of Al tolerance (Minella and Sorrells, 1992). Interestingly, Minella and Sorrells (1992) also reported that Al tolerance segregation ratios, while monogenic, shifted from dominant to recessive as Al concentrations increased, suggesting that Al tolerance is a gene dosage-dependent trait in barley. Future barley Al tolerance improvement might rely upon either undiscovered Al tolerance genes that confer higher Al tolerance or unique genes that could be pyramided to obtain an additive enhancement of the trait. An alternative strategy for improving barley Al tolerance would be to introduce Al tolerance genes from more Al-tolerant relatives into barley.

The barley cv Dayton is considered to possess a high level of Al tolerance, which is conferred by a single gene, designated Alp (Minella and Sorrells, 1992; Reid, 1971). Trisomic analysis revealed that Alp was located on chromosome 4H (Minella and Sorrells, 1997). In wheat, aneuploid studies suggest that a gene (or genes) essential for normal Al tolerance expression is on the long arm of wheat chromosome 4D (Aniol and Gustafson, 1984), and major Al tolerance genes have been mapped to this chromosome arm as well (Luo and Dvorak, 1996; Riede and Anderson, 1996). Given the significant degree of synteny between Triticum and barley (e.g., Namuth et al., 1994; Van Deynze et al., 1995), one possibility that emerges is that orthologous loci may play a role in determining Al tolerance variation in wheat and barley.

As for many traits, linked markers for barley Al tolerance genes may serve a number of functions. First, they could be used for marker-assisted selection of Al tolerance in the crop. Second, they could be employed to identify potentially unique barley Al tolerance genes from different germplasm sources without extensive test crossing, as has been done for unique disease resistance loci that confer indistinguishable resistance phenotypes (Abbott et al., 1992; Garvin et al., 1997). Third, such markers provide the basic tools for addressing questions regarding the uniqueness or orthology of Al tolerance loci found in different, but related grain crops by comparative mapping. In this study, we sought to identify molecular markers for the barley Alp gene that can be used as a resource for these purposes.

	Materials and methods

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Plant Materials
The barley cultivars used to produce the mapping population for this study were Dayton, a highly Al-tolerant six-rowed winter barley that harbors the Al tolerance gene Alp (Reid, 1971), and Harlan Hybrid, a moderately Al-sensitive six-rowed spring barley (Minella and Sorrells, 1992). The two parents were crossed and a single F₁ plant was selfed to generate an F₂ progeny, from which 48 plants were randomly chosen as the mapping population. After Al tolerance evaluation, the F₂ plants were selfed to produce F₃ families for progeny testing to obtain complete F₂ genotypes for Alp.

Analysis of Al Tolerance
Seedlings were grown hydroponically as described previously (Minella and Sorrells, 1992) with some modifications. Briefly, barley seeds were sown on moist filter paper in petri dishes, and placed in the dark at 4°C for 5 days. The seeds were then moved to room temperature for 1 d, and the following day the emerging seedlings were individually placed in gridded plastic cups suspended on a plastic lid over 8 L of continuously aerated nutrient solution. The nutrient solution consisted of 4 mM CaCl₂, 6.5 mM KNO₃, 2.5 mM MgCl₂, 0.1 mM (NH₄)₂SO₄, and 0.4 mM NH₄NO₃, pH 4.0. After 72 h of growth at room temperature, the solution was replaced with the same nutrient solution also containing 50 µM AlCl₃, and the seedlings were grown for an additional 24 h.

The hematoxylin method was used to evaluate Al tolerance (Polle et al., 1978). This method was chosen because it is has proven to be an accurate indicator of Al tolerance, and has been successfully used for inheritance studies as well as Al tolerance selection in cereals (e.g., Carver et al., 1993; Delhaize et al., 1993; Johnson et al., 1997; Minella and Sorrells, 1992; Riede and Anderson, 1996; Wheeler et al., 1993). After growing the seedlings for 24 h in the nutrient solution containing 50 µM AlCl₃, the roots were washed with deionized water for 1 h, and were then immersed in a solution of 0.2% (w/v) hematoxylin, 0.02% (w/v) KIO₃ for 15 min, followed by 1 h of rinsing in deionized water. The seedlings were rated for Al tolerance on the basis of the relative degree of staining of the root by the hematoxylin, which is inversely correlated with Al tolerance.

RFLP Analysis
DNA was isolated from leaf tissue of parents and the mapping population according to the method described by Riede and Anderson (1996). For the mapping population, DNA was obtained by extraction of bulked leaf tissue from approximately 12 F₃ progeny of each individual F₂ plant in order to reconstitute the F₂ genotype. Survey membranes of parental DNA were prepared by digesting 20-µg aliquots of DNA with 20 units of each of the following restriction endonucleases: BamHI, DraI, EcoRI, EcoRV, HindIII, PstI, SstI, XbaI, and XhoI for approximately 16 h. The digested DNA was then separated on 0.8% (w/v) agarose gels with 0.5x TBE electrophoresis buffer, and was then transferred to Hybond N+ membrane (Amersham, Arlington Heights, IL) following the manufacturer's recommendations. These parental survey filters were hybridized with a set of wheat, barley, and oat (Avena sativa L.) genomic and cDNA clones that either have been mapped to barley chromosome 4H (Graner et al., 1991; Heun et al., 1991; Kleinhofs et al., 1993; Langridge et al., 1995) or to the wheat group 4 chromosomes (Nelson et al., 1995; Riede and Anderson, 1996). The clones were radiolabeled with 32-P by the method of Feinberg and Vogelstein (1984), and hybridization to the parental filters was conducted overnight at 65°C as described previously (Bernatsky and Tanksley, 1986). The following day, the filters were sequentially washed at 65°C for 20 min with 2x SSC, 1x SSC, and 0.5x SSC (1x SSC: 0.15 M NaCl, 0.015 M sodium citrate, pH 7.0), containing 0.1% (w/v) SDS. The filters were then placed against X-ray film to obtain autoradiographs. On the basis of the results of the parental survey hybridizations, the appropriate DNA filters for the mapping population were generated and used to obtain segregation data for the RFLP probes that detected parental polymorphisms.

Linkage Analysis
Linkage analysis was conducted with the Linkage-1 (Suiter et al., 1983) and Mapmaker (Lander et al., 1987) programs.

	Results

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Inheritance of Al Tolerance
In pilot studies, significant differences in root hematoxylin staining in Dayton and Harlan Hybrid were obtained when the seedlings were grown in nutrient solution containing 50 µM AlCl₃. At this Al concentration, the roots of the Al-tolerant Dayton showed no staining, while the roots of Harlan Hybrid seedlings exhibited violet staining in the terminal 5 to 7 mm of the root, particularly in a 1 to 2 mm zone near the tip (Fig. 1) . Al-induced root growth inhibition was also examined in the two cultivars in these studies, and revealed that Harlan Hybrid exhibited more pronounced Al-induced inhibition of root elongation than Dayton. After 1 d of growth in 50 µM Al, mean elongation of the longest root of Harlan Hybrid plants was 5.5 mm vs. 13.5 mm for Dayton (n = 4; P < 0.005). This can be attributed to differential Al tolerance rather than differential growth rates, because the initial root lengths of these plants were not different (60.25 vs. 64.25 mm for Harlan Hybrid and Dayton, respectively; P > 0.6). Thus differences in hematoxylin staining intensity in these two lines were negatively associated with Al tolerance, as expected. Further, since hematoxylin staining reflects the amount of Al present in the root, these results indicate that the mechanism of Al tolerance acting in Dayton is Al exclusion from the root apex, which is the site of Al phytotoxicity (Kochian, 1995).

View larger version (71K): [in this window] [in a new window]   Fig. 1 Differential hematoxylin staining of root tips of the barley cvs Dayton, Harlan Hybrid, and their F1 hybrid. Dayton; F1 Hybrid; Harlan Hybrid

Identification of RFLP Markers Linked to Alp
Forty-four barley, wheat, and oat clones were hybridized to the parental filters, and 20 were found to reveal polymorphisms between the parents that were deemed suitable for segregation analysis in the mapping population. Among this group of polymorphic markers, 14 have been mapped previously to barley chromosome 4H, while the remaining clones have been mapped to the group 4 chromosomes of wheat. Fourteen of the 20 probes detected single copy sequences in the barley genome, while the hybridization patterns for the six others were suggestive of two different loci.

Alp exhibited tight linkage (2.1 cM, standard error 1.4 cM) to three codominant RFLP markers on chromosome 4H: Xbcd1117, Xwg464, and Xcdo1395. The order of these loci was determined to be Xbcd1117—Alp—Xwg464/Xcdo1395 (Fig. 2) . No recombinants between Xwg464 and Xcdo1395 were detected, so their relative order could not be determined. To our knowledge, neither Xcdo1395 nor Xbcd1117 have been mapped in barley. However, Xwg464 has been mapped to the long arm of barley chromosome 4H, as has Xabg472 (Kleinhofs et al., 1993), another RFLP marker that segregated in our population and maps to a location approximately 30 cM from Alp (Fig. 2). Since Alp resides between Xwg464 and Xabg472, by inference it is also located on the long arm of barley chromosome 4H. On the basis of the order of Alp, Xbcd1117, Xwg464, and Xcdo1395 relative to Xabg472, we determined that Alp is proximal to Xbcd1117 and distal to Xwg464 and Xcdo1395. The marker Xbcd1230, which exhibits tight linkage to a major wheat Al tolerance gene (Alt_BH) located on chromosome arm 4DL (Riede and Anderson, 1996), mapped to a position on the long arm of barley chromosome 4H, 3.3 cM distal to Xabg472 and approximately 33 cM from Alp (Fig. 2).

View larger version (12K): [in this window] [in a new window]   Fig. 2 Linkage relationships between Alp and RFLP markers on the long arm of chromosome 4H. C denotes the orientation of the loci relative to the centromere

	Discussion

TOP NOTES ABSTRACT INTRODUCTION Materials and methods Results Discussion REFERENCES

Traditionally, selection for Al tolerance has relied upon field evaluations, soil bioassays, or solution culture methods (Carver and Ownby, 1995). In barley, a significant positive correlation between rankings obtained in solution culture and soil has been reported (Reid et al., 1971). The molecular markers for a major barley Al tolerance gene (Alp) that we have identified provide an alternative means of selecting for Al tolerance that will reduce the dependence on extensive field testing, soil bioassays, or solution culture. With three markers that are all tightly linked to Alp, there is an increased likelihood that one of them will reveal a useful polymorphism for marker-assisted selection of Alp in a given cross between Dayton and an Al-sensitive target cultivar. Further, since two of the three pairwise combinations of markers flank Alp, simultaneous selection of polymorphic flanking markers (Xbcd1117 with either Xcdo1395 or Xwg464) would make accidental selection of recombinant individuals highly improbable.

When barley germplasm possesses intermediate alleles (e.g., moderately tolerant vs. moderately sensitive) of the Alp locus, single plant genotyping by the hematoxylin method becomes more challenging because differential staining among genotypes becomes much more quantitative (Minella and Sorrells, 1992). The markers identified here may be used to select for Al tolerance in such cases. However, the markers are likely to find their broadest practical utility if they can be successfully converted to a PCR-based format. In this case, marker-assisted Al tolerance selection may be conducted more rapidly than other available methods including hematoxylin staining, particularly if PCR-based markers are to be used for other traits as well. Furthermore, these markers can be used as genome landmarks to assess the potential uniqueness of Al tolerance genes in other germplasm. If linkage between such genes and the markers we have identified is not detected, then one could conclude that they are in fact unique loci.

Our results confirm that Al tolerance in barley cv Dayton is controlled by the action of a single gene, Alp (Reid, 1971; Minella and Sorrells, 1992). On the basis of the hematoxylin staining results, Alp appears to confer Al tolerance by an Al exclusion mechanism acting at the root apex, which has been shown to be the site of Al phytotoxicity (Kochian, 1995). Similar results have been reported in wheat (Delhaize et al., 1993; Riede and Anderson, 1996). We have determined that Alp, previously shown to reside on chromosome 4H (Minella and Sorrells, 1997), is on the long arm of this chromosome. Previously, Stolen and Anderson (1978) mapped a major gene (Pht) controlling acid soils tolerance to barley chromosome 4H. It therefore seems likely that Pht is the same as Alp, since Al toxicity is the main limiting factor in acid soils.

In wheat, major Al tolerance genes have also been mapped to the long arm of chromosome 4D (Luo and Dvorak, 1996; Riede and Anderson 1996), and the loss of this same chromosome arm results in the elimination of Al tolerance (Aniol and Gustafson, 1984). Since the group 4 chromosomes of wheat and barley exhibit significant synteny, these results provoke questions about the possibility that intraspecific Al tolerance differences in wheat and barley may in part be due to allelic variation at orthologous loci. In our study, the single copy marker Xcdo1395 was located 2.1 cM from Alp, whereas in wheat this marker is 11.3 cM from the Al tolerance gene Alt_BH, which resides on the long arm of chromosome 4D (Riede and Anderson, 1996). Though the two estimates are quantitatively different, this result tends to support the possibility that Alp and Alt_BH may be orthologous loci. Such a possibility is bolstered by the fact that both Alp and Alt_BH appear to confer Al tolerance by the same mechanism, namely excluding Al from the root apex, as indicated by hematoxylin staining (Riede and Anderson, 1996). In contrast, we found that Xbcd1230 (also a single copy locus) was only weakly linked to Alp (33 cM), while in wheat it is 1.1 cM from Alt_BH (Riede and Anderson, 1996). These results were not due to mislabeling of clones, since we confirmed their identity via linkage to Alt_BH in a subset of the wheat recombinant inbred population that was originally used to map this gene (Riede and Anderson, 1996). The observation that Xbcd1230 is not tightly linked to Alp as it is to Alt_BH in wheat, coupled with the fact that the relative positions of Xbcd1230 and Xcdo1395 are different with respect to Alp vs. Alt_BH (Riede and Anderson, 1996), suggests that this chromosome segment has been subject to structural rearrangements and/or duplication and deletion events in the two species. Therefore a more definitive conclusion cannot be reached regarding the potential orthology of Alt_BH and Alp with the comparative mapping data obtained in this study. Nonetheless, the potential orthology between wheat and barley Al tolerance genes merits further investigation, because if Alt_BH is orthologous to Alp and can be cloned, it may be possible to improve the low level of barley Al tolerance by the addition of this wheat gene. Indeed, if introduced into the barley genome in an unmodified form, the Alt_BH gene may simply function as a stronger allele of the existing multiallelic barley Alp.Stolen Andersen 1978

	NOTES

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Research supported by USDA-NRI grant 97-35100-4501 to L.V.K., D.F.G., and M.E.S.

Received for publication September 20, 1999.

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TOP NOTES ABSTRACT INTRODUCTION Materials and methods Results Discussion REFERENCES

 

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