Identification and Physical Localization of Useful Genes and Markers to a Major Gene-Rich Region on Wheat Group 1S Chromosomes

Corresponding author: Kulvinder S. Gill, Department of Agronomy, 362H Plant Science, P.O. Box 830915, University of Nebraska, Lincoln, NE 68583-0915., kgill1{at}unl.edu (E-mail)

Communicating editor: J. A. BIRCHLER

	ABSTRACT

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

The short arm of Triticeae homeologous group 1 chromosomes is known to contain many agronomically important genes. The objectives of this study were to physically localize gene-containing regions of the group 1 short arm, enrich these regions with markers, and study the distribution of genes and recombination. We focused on the major gene-rich region ("1S0.8 region") and identified 75 useful genes along with 93 RFLP markers by comparing 35 different maps of Poaceae species. The RFLP markers were tested by gel blot DNA analysis of wheat group 1 nullisomic-tetrasomic lines, ditelosomic lines, and four single-break deletion lines for chromosome arm 1BS. Seventy-three of the 93 markers mapped to group 1 and detected 91 loci on chromosome 1B. Fifty-one of these markers mapped to two major gene-rich regions physically encompassing 14% of the short arm. Forty-one marker loci mapped to the 1S0.8 region and 10 to 1S0.5 region. Two cDNA markers mapped in the centromeric region and the remaining 24 loci were on the long arm. About 82% of short arm recombination was observed in the 1S0.8 region and 17% in the 1S0.5 region. Less than 1% recombination was observed for the remaining 85% of the physical arm length.

COMMON wheat (Triticum aestivum L. em Thell, 2n = 42, AABBDD) has a large genome, 16 million kb/haploid cell. The wheat genome is 35 times larger than that of rice and 110 times that of Arabidopsis (BENNETT and SMITH 1976 ). The gene-containing fraction of the wheat genome should therefore be <2.7%. Since only a small fraction of the wheat genome is expected to represent genes, identification and marking of the gene-containing regions is invaluable for their characterization.

A strategy to identify and preferentially map the gene-containing regions of the wheat genome was proposed (GILL and GILL 1994 ) and demonstrated (GILL et al. 1996A , GILL et al. 1996B ). The strategy involved physical mapping of protein, DNA, and morphological markers on single-break chromosome deletion lines. The physical maps thus generated were compared with various genetic linkage maps of Triticeae via common markers. A total of 436 deletion lines involving all 21 wheat chromosomes was isolated using the gametocidal chromosome of T. cylindricum (ENDO and GILL 1996 ) and used to generate composite maps of all wheat chromosomes (WERNER et al. 1992 ; GILL et al. 1993 , GILL et al. 1996A , GILL et al. 1996B ; KOTA et al. 1993 ; DELANEY et al. 1995A , DELANEY et al. 1995B ; MICKELSON-YOUNG et al. 1995 ; WENG et al. 2000 ). The resulting composite maps revealed the distribution of genes and recombination on the chromosomes. High-density composite maps have revealed that >85% of the wheat genes are present in gene-rich regions, physically spanning only 5–10% of the chromosomal region (GILL et al. 1996A , GILL et al. 1996B ). The gene-rich regions are interspersed with blocks of repetitive DNA sequences visualized as regions of low gene density. About two to four major gene-rich regions were observed per chromosome arm. Gene-rich regions were mainly observed in the distal regions of chromosomes.

Division of higher organism genomes into gene-rich and gene-poor compartments may be a common feature (see SUMNER et al. 1993 for review). Among animal systems, gene distribution in the human genome is best studied. The conclusion based on the in situ hybridization of a random pool of mRNA (YUNIS et al. 1977 ) or with the G + C-richest isochore H3 (SACCONE et al. 1992 ), and by DNAase hypersensitivity (WEINTRAUB and GROUDINE 1976 ; ELGIN 1988 ), was that genes in the human genome are localized in R-bands and are more concentrated in T-bands, which are terminal R-bands (SUMNER et al. 1993 ). In all well-studied higher organisms, a major part of the genome is composed of repetitive DNA, most of which is made up of transposons (HAKE and WALBOT 1980 ; MOUCHIROUD et al. 1991 ; SUMNER et al. 1993 ; CARELS et al. 1995 ; BARAKAT et al. 1997 , BARAKAT et al. 1999 ). A partial sequence of the region near the Adh-F gene of maize showed that genes are present in clusters and are interspersed with long stretches of repeat units of retrotransposons (BENNETZEN et al. 1998 ). This gene-rich region is also conserved in sorghum, where homologues of the maize genes were present in a colinear order (BENNETZEN et al. 1998 ).

In wheat and many other organisms, a strong correlation was observed between the distribution of genes and recombination (THURIAUX 1977 ; CIVARDI et al. 1994 ; ZHANG et al. 1994 ; GILL et al. 1996A , GILL et al. 1996B ; BUSCHGES et al. 1997 ; KUNZEL et al. 2000 ). The actual ratio of physical to genetic distance for the regions around genes of most plants ranges from 14 kb/cM in maize (BROWN and SUNDARESAN 1991 ) to 90 kb/cM in tomato (GANAL et al. 1989 ), which is significantly smaller than the estimates made from total genome size and length of genetic linkage maps. These results clearly show that recombination is unevenly distributed along chromosomal lengths of most organisms and gene-containing regions are its preferred sites. This pattern of gene distribution and its relationship with that of recombination appears to be similar in vertebrates, where the genomes are organized into large domains of uniform (G + C) content (BERNARDI 1993 ). Most genes and chiasmata are found in regions richest in (G + C) content (IKEMURA and WADA 1991 ). This explains why gene-rich regions are higher in recombination.

Two major gene-rich regions at fraction length (FL) 0.8 (1S0.8 region) and FL 0.5 (1S0.5 region), were identified on the short arm of homeologous group 1 chromosomes (GILL et al. 1996B ). The 1S0.8 region is one of the largest gene-rich regions of wheat. On chromosome 1B, the region is present in the middle satellite part of the chromosome and is bracketed by the breakpoints of deletions 1BS-4 (FL 0.54) and 1BS-19 (FL 0.31). This region is only 23% of the satellite. Fourteen agronomically important genes, including genes conferring resistance to diseases [leaf rust (Lr, Lr21), stem rust (Sr33), powdery mildew (Pm3)], preharvest sprouting (Qphs.cnl), fertility restoration gene (Rf3), and seed storage proteins, and 11 DNA markers were also localized to the gene-rich region (GILL et al. 1996B ).

Gene synteny is conserved among living organisms and the extent of conservation is proportional to the evolutionary distances involved. Wheat belongs to the grass family Poaceae (Gramineae) that includes other major cereal crops such as barley (Hordeum vulgare), oat (Avena sativa), rye (Secale cereale), maize (Zea mays), and rice (Oryza sativa). Gene synteny is conserved among the genomes of the tribe Triticeae (HART 1987 ). Conserved linkage blocks exist even among genomes of wheat, rice, and maize (AHN et al. 1993 ; AHN and TANKSLEY 1993 ; BENNETZEN and FREELING 1993 ; VAN DEYNZE et al. 1995 ; GALLEGO et al. 1998 ). The number of restriction fragment length polymorphism (RFLP) markers mapped on one or more of the Triticeae species is >2800. As RFLP markers can be used across maps, markers from different maps can be selected by comparative mapping and can be used on deletion lines to enrich a particular region in the wheat genome.

The objectives of this study were to identify and physically localize useful genes to the wheat homeologous group 1 short arm, enrich the gene containing regions with markers, and study the relationship between distribution of genes and recombination.

	MATERIALS AND METHODS

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

Plant material:
Various chromosome, arm, and subarm aneuploid stocks were used to physically map DNA markers to their respective chromosomal regions. Wheat homeologous group 1 nullisomic-tetrasomic lines (missing a pair of chromosomes, the deficiency of which is compensated for by a pair of homeologous chromosomes) and ditelosomic lines (missing a pair of chromosome arms; SEARS 1954 ) were used to assign DNA restriction fragments to their respective chromosomal arms. Four single-break deletion lines with their breakpoints flanking two previously known gene-rich regions of wheat homeologous group 1 short arm were used for subarm localization of DNA markers. Among these, breakpoints of deletions 1BS-4 and 1BS-19 bracket the 1S0.8 region (Fig 1; GILL et al. 1996B ). Between these, 1BS-4 is the smaller deletion with only 46% of the satellite region deleted compared to 69% in 1BS-19 (ENDO and GILL 1996 ). The breakpoints of deletion lines 1BS-9 and 1BS-20 flank the 1S0.5 region. In addition to the satellite, the deletion line 1BS-9 has 16% (FL 0.84) of the short arm missing compared to 28% in 1BS-20.

View larger version (46K): In this window In a new window Download PPT slide   Figure 1. Physical map of short arm of chromosome 1B of wheat in comparison with consensus genetic linkage map of Triticeae (VAN DEYNZE et al. 1995 ) and genetic linkage map of T. aestivum (VAN DEYNZE et al. 1995 ). Markers common between physical map and consensus genetic linkage map of Triticeae are represented in boldface type and markers common between physical map and genetic linkage map of wheat are underlined. Some common markers are joined by lines. Fraction breakpoints and the corresponding line numbers are indicated to the left of each chromosome. Asterisk represents fraction length for satellite. C, centromere.

Comparative mapping:
Eleven markers that were previously mapped in the 1S0.8 region (GILL et al. 1996B ) were used for comparative mapping across Poaceae maps to identify agronomically important genes and additional markers present in the gene-rich region. The published Poaceae maps and Graingenes database were compared with each other and with the consensus physical map of wheat (CHAO et al. 1989 ; LAGUDAH and APPELS 1991 ; KOHLER et al. 1992 ; WANG et al. 1992 ; LAURIE et al. 1995 ; BEZANT et al. 1996 ; GILL et al. 1996B ; DEVOS et al. 1998 ; KORZUN et al. 1998 ; WARD et al. 1998 ). A total of 11 wheat, 11 barley, 6 rye, 3 rice, 2 oat, and 2 Triticeae consensus maps were used for the comparative mapping. In the first phase of comparative mapping, markers present in the 1S0.8 region in the existing physical map were used as anchor markers on genetic linkage maps. All the markers on any genetic linkage map, present in between two anchor markers, were selected. In the second phase of comparative mapping, the markers selected in the first phase were used as anchor markers on other genetic linkage maps to select more markers. Some markers that were not flanked by two anchor markers but were tightly linked to one of the anchor marker were also included.

Probes:
The cDNA and genomic DNA probes used to construct the physical map were derived from wheat (CS, KSU, WG, PSR, NOR, TAM), barley (ABC, ABG, BCD, MWG, and cMWG), oat (CDO), and rice (RZ). The RFLP probes were described by the following authors. BCD, CDO, WG: HEUN et al. 1991 ; RZ: CAUSSE et al. 1994 ; KSU: GILL et al. 1991B ; MWG and cMWG: GRANER et al. 1991 ; ABC, ABG: KLEINHOFS et al. 1993 ; PSR: SHARP et al. 1989 ; and TAM: DEVEY and HART 1993 . LRK10 was kindly supplied by Dr. C. Feuillet, University of Zurich.

DNA analysis:
Genomic DNA from various plant materials was isolated following a method described elsewhere (ANDERSON et al. 1992 ). For each sample, 15 µg of genomic DNA was digested with a restriction enzyme and electrophoretically separated on 0.8% agarose gel as previously described (GILL et al. 1993 ). Two restriction enzymes (EcoRI and HindIII) were used for physical mapping. Southern blotting onto nylon membrane (Micron Separations Inc., Westborough, MA), DNA immobilization, and hybridization were performed following manufacturer's recommendations.

Probe preparation, hybridization, and autoradiography:
Approximately 30 ng of probe DNA was labeled with 30 µCi of [³²P]dCTP in a 15-µl reaction volume, following random primer labeling technique (FEINBERG and VOGELSTEIN 1983 ). Hybridization was performed in 35 x 300-mm glass bottles containing 10 ml of hybridization buffer (5% dextran sulfate, 6x SSPE, 5% Denhardt's solution, 0.5% SDS), incubated at 65° for 16–18 hr in a hybridization rotisserie oven (Hybaid, Inc.). Blots were washed at 65° in 2x SSPE, 0.5% SDS for 30–50 min and exposed for 3–7 days at -80°.

	RESULTS

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

Comparative mapping:
A total of 195 markers were identified for the 1S0.8 region by comparing 35 different maps of Poaceae. Seventy-five of these were useful genes, 93 were RFLPs, 15 were simple sequence repeats, 7 were sequence-tagged sites, and 5 were amplified fragment length polymorphism markers. Among the agronomically important genes were several resistance genes including 6 leaf rust (Lr), 5 yellow rust (Yr), 4 stem rust (Sr), 1 barley rust (Pa), and 10 powdery mildew (Mla, Mlk, Mlnn, Mlra, Pm) genes, and a suppressor of powdery mildew (Su-Pm); genes for seed storage proteins such as gliadin (Gli), glutenin (Glu), triticin (Tri), and Hordein (Hor); and some other interesting genes such as preharvest sprouting resistance (Qphs.cnl), the restorer for cytoplasmic male sterility (Vi and Rf), and a tiller-inhibitor gene (Tin) (Table 1). Of the 93 RFLPs, 3 were wheat cDNA (PSR and Nor), 16 were wheat genomic (PSR, WG, TAM, and LRK), 22 were barley cDNA (ABC, BCD, and cMWG), 31 were barley genomic (ABG and MWG), 4 were PstI genomic clones from T. tauschii (KSU), 15 were oat cDNA (CDO) and 2 were rice cDNA clones (RZ). A total of 42 (45%) probes were cDNA and 51 (55%) probes were genomic.

Physical mapping:
The 93 putative RFLP probes for the gene-rich regions were physically mapped by gel blot DNA analysis of wheat homeologous group 1 nullisomic-tetrasomic lines, ditelosomic lines, and the deletion lines 1BS-4, 1BS-19, 1BS-9, and 1BS-20. Restriction enzymes EcoRI and HindIII were used for the analysis. Of the 93 RFLP probes, 73 mapped on wheat homeologous group 1. Twenty-eight of 73 probes were specific to group 1 and 45 detected bands on other chromosome groups also. These 73 probes detected 223 loci on group 1 (Table 2). Three probes detected fragments for only one of the three homeologous group 1 chromosomes, 8 detected fragments for two and the remaining probes detected fragments for all three homeologous chromosomes (Table 2).

Seventy-three group 1 probes detected 91 loci on chromosome 1B. Of the 73 group 1 probes, 39 mapped in the 1S0.8 region and detected 41 marker loci on chromosome 1B (Fig 1). These 39 probes detected 121 loci on three homeologous chromosomes. Three probes detected fragments for only one of the three homeologous group 1 chromosomes, 6 detected fragments for two, and 33 probes detected fragments for all three homeologous chromosomes. Three marker loci (Xbcd98, Xcdo99, and Xcdo580b) showed 1B specific fragment band missing in 1BS-4 and 1BS-19, mapping them distal to the breakpoint of 1BS-4. Seven markers mapped just proximal to the breakpoint of 1BS-19 and detected 20 loci on the three homeologous chromosomes. One marker detected fragments for one of the homeologous groups and six markers detected fragments for all three homeologous chromosomes. Ten markers mapped in the 1S0.5 region and detected 32 loci on the three homeologous chromosomes. All 10 markers detected fragments for all three homeologous chromosomes. Four markers mapped proximal to the breakpoint of 1BS-20. For two marker loci (Xbcd1072 and Xpsr161) the B fragment band was present in both of the ditelosomic lines, mapping them in the centromere. The remaining 24 marker loci mapped to the long arm.

Twelve of the 1S0.8 region probes (CDO388, CDO580, CMWG645, MWG835, MWG837, MWG913, MWG938, MWG2021, MWG2048, MWG2056, PSR381, PSR688) detected a second locus on chromosome 1B and two probes (KSUD14, MWG2148) detected three loci each on the same chromosome. All three loci for KSUD14 were present in the 1S0.8 region, whereas two loci for MWG2148 were present on chromosome 1BL. A second locus for probe CDO580 was present distal to the breakpoint of 1BS-4 and a second locus of MWG913 was present proximal to the breakpoint of 1BS-20. Two of 1S0.5 region probes (BCD762, CDO127) detected a second locus on the same chromosome. A second locus of BCD762 was present on the long arm, whereas a second locus of CDO127 was present just proximal to the breakpoint of 1BS-19.

All the three markers that mapped distal to the breakpoint of 1BS-4 were cDNA. Among the 41 marker loci mapped to the 1S0.8 region, 12 were cDNA and 29 were genomic. Of the 14 1S0.8 region markers, which had more than one locus on chromosome 1B, 3 were cDNA and 11 were genomic clones. Four marker loci of the 7 that mapped just proximal to the breakpoint of 1BS-19 were cDNA and 3 were genomic. Of the 10 marker loci that mapped to the 1S0.5 region, 6 were cDNA and 4 were genomic. Two marker loci of four that mapped proximal to the breakpoint of 1BS-20 were cDNA and 2 were genomic. Both markers present at the centromere were cDNA. Eight of the 24 loci that mapped to the long arm were cDNA and 16 were genomic DNA clones.

Distribution of genes/markers:
Physical mapping revealed that the distribution of markers on the chromosomes was not uniform (Fig 1). Seventy-eight percent (51/65) of the marker loci present on the 1BS arm were present in two major gene-rich regions. Deletion lines 1BS-4 and 1BS-19 bracket 6% of the total arm (23% of satellite) and 41 marker loci mapped in this small region. The region encompassed by 1S0.5 region was 8% of chromosome 1BS and 10 marker loci were located in this region. Only 14 markers mapped in the remaining 86% of the arm. Two cDNA marker loci (Xbcd1072 and Xpsr161) were present at the centromere of 1B chromosome.

Genetic vs. physical maps:
The genetic linkage map of chromosome 1B in the Synthetic x Opata population and the consensus genetic linkage map of Triticeae homeologous group 1 (VAN DEYNZE et al. 1995 ) were used for a comparison with the physical map. The consensus genetic linkage map of Triticeae homeologous group 1 was constructed using the mapping information from >13 different genetic linkage maps of wheat, T. tauschii, T. monococcum, barley, and oat. Of the markers present on the physical map, 30 were common with the consensus map and 21 with the genetic linkage map of T. aestivum (Fig 1). The consensus genetic linkage map for the Triticeae showed higher marker density around the centromere. The trend was similar for the genetic linkage maps of T. aestivum. The order of markers was fairly consistent between the consensus genetic linkage map and physical map, but there were a few inconsistencies between physical and genetic linkage maps of T. aestivum. Most of these inconsistencies were for the markers that were mapped at LOD < 3.0 (Fig 1, probes in parentheses). This means that accuracy in mapping these probes was lower compared to other probes. There are some markers for which there were two loci in the physical map and there was only one locus in the genetic linkage map of T. aestivum, which may have affected the accuracy of the genetic map. For example, probe CDO580 detected two loci (Xcdo580a and Xcdo580b) on the physical map, whereas it detected only one locus on genetic linkage maps. Two marker loci (Xbcd98 and Xcdo99) mapped on the distal end on the physical map, whereas, on all genetic maps these loci are present in the proximal regions (Fig 1). We do not have any valid explanation for this inconsistency. Upon comparison with the physical map, it became apparent that the markers present in the 1S0.8 region were scattered within a 45-cM distance on the consensus genetic linkage map and within a 25-cM distance on the genetic linkage map for T. aestivum. The 1S0.8 region, which is only 6% of the total chromosome arm, showed 82% of the arm's recombination. About 17% of recombination occurred in the 1S0.5 region, which is physically 8% of the 1BS arm. Less than 1% of the short arm's recombination occurred in the remaining 86% of the arm.

	DISCUSSION

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

The grass family Poaceae includes major crop plants such as wheat, barley, oat, rice, and maize. Triticeae is one of the tribes containing >15 genera and 300 species including wheat and barley. Gene order and synteny are highly conserved among the species of Triticeae and moderately conserved among various tribes of the family (FEUILLET and KELLER 1999 ). There are now >2800 DNA markers present on one or more of the Triticeae genetic maps and the number is more than double for the Poaceae family (GrainGenes, http://wheat.pw.usda.gov/; Barley database, http://barleygenomics.wsu.edu/; RiceGenes, http://ars-genome-cornell.edu/rice/; Oryzabase, http://shigen.nig.ac.jp/rice/oryzabase/; MaizeDB, http://nucleus.agron.missouri.edu/). Since a majority of the markers are RFLPs, many of which can be used across the family, comparative mapping can be a very powerful approach for targeted mapping and cross-referencing of any chromosomal region of interest. In this study, comparative mapping identified 195 markers for the target region (the 1S0.8 region), which is only about 1/1119th of the wheat genome. About 56% (41/73) of the putative gene-rich region probes, selected by comparative mapping, mapped in the target region. The reason for 44% of the probes mapping outside the target region is that during the comparative mapping we were inclusive rather than exclusive in the selection of markers since eliminating false positives was relatively easy. Further, a group of three markers is present just distal to the breakpoint of 1BS-4 and a group of seven markers is present just proximal to the breakpoint of the 1BS-19. As there is no reason for the deletion line to have a break exactly at the end of the gene-rich region, it is likely that these markers are part of the 1S0.8 region. Furthermore, genetic linkage maps were used for comparative mapping. On average, only 18% of the wheat group 1 arm recombination occurs proximal to the 1S0.8 region. Therefore, many of the 1S0.5 region probes and even some of the long arm probes appeared to be linked to the 1S0.8 region probes and, thus, were selected.

Recently, it has been demonstrated that genes in cereals are present in clusters encompassing physically small chromosomal regions (GILL et al. 1993 , GILL et al. 1996A , GILL et al. 1996B ; CIVARDI et al. 1994 ; DESCENZO et al. 1996 ; WEI et al. 1999 ). Gene-containing regions of wheat are the best defined and account for 5–10% of the genome (GILL et al. 1996A , GILL et al. 1996B ). In this study we have not only confirmed these observations but have also precisely marked the gene-containing regions and revealed the distribution of genes on the wheat homeologous chromosome group 1 short arm. The 1S0.8 region is physically 6% of chromosome arm 1BS but contains 63% (41/65) of short arm markers. The 1S0.5 region is 8% of the chromosome arm and contains 15% (10/65) of the markers. Marker density in the 1S0.8 region is more than five times as compared to the 1S0.5 region. Most of the group 1 short arm specific markers and genes are present in the two gene-rich regions, which physically encompass only 14% of the arm. The gene-containing regions of barley, maize, and rice were estimated to be 12%, 17%, and 24% of their total genome size, respectively (CARELS et al. 1995 ; BARAKAT et al. 1997 ). All the recent studies on gene cloning and structural genome analyses support these observations (ROGOWSKY et al. 1993 ; DUNFORD et al. 1995 ; KILIAN et al. 1997 ; WEI et al. 1999 ).

Distribution of markers in this study most likely depicts distribution of wheat genes. Thirty-two of the 73 group 1 probes are cDNA and 38 of the 41 genomic clones were generated using PstI, which is known to cut preferentially in the gene-containing regions (BURR et al. 1988 ). Distribution of cDNA and genomic clones was similar along the chromosome length. Highly conserved genes and multicopy gene families may not be proportionally represented in this study. Sequences representing high copy number gene families are less likely to be included in our study as they will be eliminated as "bad probes" during the initial search for probes that can be mapped. Twelve of the 73 markers, however, detected >15 bands, suggesting that these represent multigene families. The distribution of these markers was similar to that of the single/few copy probes. Most of the markers in this study were selected from genetic linkage maps and thus have been selected for their ability to detect polymorphism. Centromeric regions in most organisms are recombination poor (GILL et al. 1996B ; PUECHBERTY et al. 1999 ). The genes present around the centromeric region are, therefore, more likely to be conserved and are less likely to be represented in our study.

Organization of genes in clusters encompassing physically small chromosomal regions seems to be true for all wheat chromosomes and perhaps for the whole Poaceae family. High-density mapping revealed that the organization of genes for group 5 is similar to that of group 1 (GILL et al. 1996A ; FARIS et al. 2000 ). It was shown that markers on chromosome 5L were present in five gene-rich regions, of which three were major regions and two were minor. The region between FL 0.75 and 0.79 was 4% of 5L arm, but contained 55% (77/139) of the markers. The estimated size of the region is 20 Mb, which makes at least one marker every 260 kb (GILL et al. 1996A ; FARIS et al. 2000 ). Distribution of genes in barley showed a striking similarity to that of wheat (KUNZEL et al. 2000 ). In maize 70% of the genome consists of repetitive DNA, which is made up of transposons (HAKE and WALBOT 1980 ). Detailed studies on genome organization revealed that maize genes are present in clusters and are interspersed by long stretches of repeat units of retrotransposons (BENNETZEN et al. 1998 ). The Sh2/A1 region of maize is also conserved in sorghum and rice but lacks numerous retrotransposons present in maize (BENNETZEN et al. 1998 ). By molecular clock criteria sorghum and rice have undergone 50 million years of independent evolution, but still the colinearity of gene-rich regions has been maintained (BENNETZEN et al. 1998 ). Arabidopsis lacks abundant transposons and repeat DNA in intergenic regions, but distribution of genes in Arabidopsis still is not completely uniform (SCHMIDT et al. 1995 ).

Uneven distribution of recombination along chromosome length appears to a be the rule in all organisms (DVORAK and CHEN 1984 ; GANAL et al. 1989 ; GILL et al. 1993 , GILL et al. 1996A , GILL et al. 1996B ; CHOUDHURI and MESSING 1995 ; UMEHARA et al. 1995 ; CAI et al. 1997 ; TRANQUILLI et al. 1999 ; FARIS et al. 2000 ; KUNZEL et al. 2000 ; SPIELMEYER et al. 2000 ). In this study, 99% of the recombination occurred in the distal 60% of the arm. Recombination in the distal 25% of the arm was five times higher as compared to the rest of the arm. Recombination near the centromere was negligible. Because of the nonrandom distribution of recombination along the chromosomal length, base pair per centimorgan estimates would differ among regions. The predicted estimate for 1-cM genetic distance in rice is 273 kb. However, comparisons of actual physical distances with the genetic distances reveal that this estimate may vary from 120 kb to 1 Mb (UMEHARA et al. 1995 ). Cytogenetic and genetic linkage maps of Drosophila melanogaster revealed widespread variation in the rates of recombination among different chromosomal regions (LINDSLEY and SANDLER 1977 ). In wheat it has been shown that the distal one-third of any arm shows 8–15 times the recombination compared to the proximal one-third (HOHMANN et al. 1995 ; GILL et al. 1996A , GILL et al. 1996B ). Heterochromatic regions of the genome are devoid of recombination. Centromeric regions were highly suppressed in recombination in many organisms (TANKSLEY et al. 1992 ; MCKEE and HANDEL 1993 ; LAURENT et al. 1998 ; PUECHBERTY et al. 1999 ).

As reported previously, a strong correlation was also observed between the distribution of genes and recombination (GILL et al. 1996A , GILL et al. 1996B ; KUNZEL et al. 2000 ). Of the total short arm recombination, 82% occurred in the 1S0.8 region and 17% in the 1S0.5 region. Almost all of the short arm recombination occurred in 14% of the short arm corresponding to the two gene-rich regions and no recombination was observed in the remaining 86%. A high correlation of recombination with genes or gene-rich regions has been observed in a wide range of organisms. The base pair per centimorgan estimate for the chromosomal region around the cyst nematode-resistant gene in sugar beet was 30 kb/cM compared to 677 kb/cM for the whole genome (CAI et al. 1997 ). Recombination in the A1 locus (12–25 kb/cM) and Bronze 1 locus (14 kb/cM) was comparable and was two orders of magnitude higher than the estimation from the overall maize genome (BROWN and SUNDARESAN 1991 ).

In barley, the base pair per centimorgan estimates for the chromosomal regions around the Mlo and Rar1 loci (both resistant genes in different chromosomal regions) were 50 kb/cM (BUSCHGES et al. 1997 ; LAHAYE et al. 1998 ). Hot spots of recombination correspond to 4.9% of the total barley genome and contain 47.3% of the total number of mapped markers (KUNZEL et al. 2000 ). Based on the genome size and RFLP linkage map length, the predicted size of tomato chromosomal region per centimorgan is 550 kb (GANAL et al. 1989 ). However, estimates for regions around various disease resistance genes range from 43 to 90 kb (GANAL et al. 1989 ; SEGAL et al. 1992 ; ZHANG et al. 1994 ). All these genes showing a higher level of recombination probably are part of some gene-rich regions. The bp/cM estimates from high-density composite maps of wheat homeologous groups 1 and 5 range from 118 kb for the gene-rich regions to 22 Mb for the gene-poor regions (GILL et al. 1996A , GILL et al. 1996B ). In this study, for the 1S0.8 region, the base pair per centimorgan estimate was 365 kb in comparison to the whole 1BS arm, where it was 5 Mb/cM. The base pair per centimorgan estimates for the regions around genes are comparable among various crop plants with the average of 100 kb/cM. However, the upper limit for such estimates depends upon the genome size. Therefore, the sizes of gene-poor compartments of the genome will determine the upper limit for base pair per centimorgan estimates. The rice genome is 35 times smaller than that of wheat and the upper limit in rice is 1 Mb/cM compared to 22 Mb/cM in wheat. The total length of linkage maps is fairly constant among eukaryotes and the average frequency of crossing over per unit of DNA decreases by several levels of magnitude from lower to higher eukaryotes (THURIAUX 1977 ). These relationships have profound evolutionary implications. Intragenic recombination can result in the creation of chimeric alleles (CHOUDHURI and MESSING 1995 ). Thus the evolutionary advantage of creating genetic diversity in a population may have fostered a mechanism that preferentially selected genes as sites of recombination.

The haploid wheat chromosome complement is 235 µm in length (GILL et al. 1991A ), containing 16 million kb of DNA (BENNETT and SMITH 1976 ). The 1S0.8 region is flanked by the breakpoints of deletions 1BS-4 and 1BS-19 and is present in the middle of the chromosome 1BS satellite. The 1BS satellite is 1 µm in length, comprising about 68 Mb of DNA (calculated by dividing 16 million kb, the genome size, by the total chromosome size of 235 µm). The gene-rich region is 23% of the satellite (between FL 0.31 and 0.54 of the satellite; ENDO and GILL 1996 ). The gene-rich region should, therefore, be 15 Mb in size. In this study, we have identified 41 markers for this region with an average distribution of a marker every 365 kb. The region syntenic to 1S0.8 region in barley is 20 cM (GrainGenes). The 1-cM region spanning the barley Mla cluster centered between markers bcd249.1 and mwg036 is 1 Mb (WEI et al. 1999 ). If the kilobase/centimorgan ratio is uniform within the region, the total size of the region will be 20 Mb. However, physical to genetic distance within the Mla region may vary over 10-fold, with 176 kb/cM being the most favorable ratio. These observations indicate that the gene and recombination distributions within the gene-rich region are not uniform. Recombination seems to occur only in the gene-containing regions; however, accuracy of the observation within the gene-rich regions has not been tested yet. If the relationship between the distribution of genes and that of recombination holds within the gene-rich region also, only a part of the 1S0.8 region should contain genes. The 1S0.8 region markers most likely mark only the gene-containing parts of the region. The current marker density should therefore be sufficient to construct a contiguous map of the gene-containing regions of the gene-rich region.

In conclusion, the comparative mapping-based enrichment of a gene-rich region with markers is a powerful technique. Comparative mapping combined with targeted physical mapping strategy physically localized 75 useful genes to the 1S0.8 region along with 41 markers, which should be adequate to construct a contiguous map for the region and eventually allow cloning of these genes. Most wheat genes are present in clusters. Many of these gene-rich regions have been bracketed by the breakpoints of single-break deletion lines, which are available for all wheat chromosomes. Therefore, the approach outlined in this study can be used to target any gene-rich region in the wheat genome.

	ACKNOWLEDGMENTS

Contribution no. 13066 from the Institute of Agricultural and Natural Resources (IANR), University of Nebraska, Lincoln. The research was supported by U.S. Department of Agriculture-National Research Initiative (USDA-NRI).

Manuscript received September 22, 2000; Accepted for publication January 10, 2001.

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				L. Reddy, T. L. Friesen, S. W. Meinhardt, S. Chao, and J. D. Faris Genomic Analysis of the Snn1 Locus on Wheat Chromosome Arm 1BS and the Identification of Candidate Genes The Plant Genome, July 1, 2008; 1(1): 55 - 66. [Abstract] [Full Text] [PDF]

				P. R. Bhat, A. Lukaszewski, X. Cui, J. Xu, J. T. Svensson, S. Wanamaker, J. G. Waines, and T. J. Close Mapping translocation breakpoints using a wheat microarray Nucleic Acids Res., May 14, 2007; 35(9): 2936 - 2943. [Abstract] [Full Text] [PDF]

				N. L. V. Lapitan, J. Peng, and V. Sharma A High-Density Map and PCR Markers for Russian Wheat Aphid Resistance Gene Dn7 on Chromosome 1RS/1BL Crop Sci., March 1, 2007; 47(2): 811 - 818. [Abstract] [Full Text] [PDF]

				A. Mohan, A. Goyal, R. Singh, H. S. Balyan, and P. K. Gupta Physical Mapping of Wheat and Rye Expressed Sequence Tag-Simple Sequence Repeats on Wheat Chromosomes Crop Sci., January 1, 2007; 47(Supplement_1): S-3 - S-13. [Abstract] [Full Text] [PDF]

				J. L. Alt, W. R. Fehr, G. A. Welke, and D. Sandhu Phenotypic and Molecular Analysis of Oleate Content in the Mutant Soybean Line M23 Crop Sci., August 26, 2005; 45(5): 1997 - 2000. [Abstract] [Full Text] [PDF]

				L. I. Khrustaleva, P. E. de Melo, A. W. van Heusden, and C. Kik The Integration of Recombination and Physical Maps in a Large-Genome Monocot Using Haploid Genome Analysis in a Trihybrid Allium Population Genetics, March 1, 2005; 169(3): 1673 - 1685. [Abstract] [Full Text] [PDF]

				D. Zhang, Q. Yang, W. Bao, Y. Zhang, B. Han, Y. Xue, and Z. Cheng Molecular Cytogenetic Characterization of the Antirrhinum majus Genome Genetics, January 1, 2005; 169(1): 325 - 335. [Abstract] [Full Text] [PDF]

				J. H. Peng, H. Zadeh, G. R. Lazo, J. P. Gustafson, S. Chao, O. D. Anderson, L. L. Qi, B. Echalier, B. S. Gill, M. Dilbirligi, et al. Chromosome Bin Map of Expressed Sequence Tags in Homoeologous Group 1 of Hexaploid Wheat and Homoeology With Rice and Arabidopsis Genetics, October 1, 2004; 168(2): 609 - 623. [Abstract] [Full Text] [PDF]

				E. J. Conley, V. Nduati, J. L. Gonzalez-Hernandez, A. Mesfin, M. Trudeau-Spanjers, S. Chao, G. R. Lazo, D. D. Hummel, O. D. Anderson, L. L. Qi, et al. A 2600-Locus Chromosome Bin Map of Wheat Homoeologous Group 2 Reveals Interstitial Gene-Rich Islands and Colinearity With Rice Genetics, October 1, 2004; 168(2): 625 - 637. [Abstract] [Full Text] [PDF]

				A. M. Linkiewicz, L. L. Qi, B. S. Gill, A. Ratnasiri, B. Echalier, S. Chao, G. R. Lazo, D. D. Hummel, O. D. Anderson, E. D. Akhunov, et al. A 2500-Locus Bin Map of Wheat Homoeologous Group 5 Provides Insights on Gene Distribution and Colinearity With Rice Genetics, October 1, 2004; 168(2): 665 - 676. [Abstract] [Full Text] [PDF]

				H. S. Randhawa, M. Dilbirligi, D. Sidhu, M. Erayman, D. Sandhu, S. Bondareva, S. Chao, G. R. Lazo, O. D. Anderson, Miftahudin, et al. Deletion Mapping of Homoeologous Group 6-Specific Wheat Expressed Sequence Tags Genetics, October 1, 2004; 168(2): 677 - 686. [Abstract] [Full Text] [PDF]

				K. G. Hossain, V. Kalavacharla, G. R. Lazo, J. Hegstad, M. J. Wentz, P. M. A. Kianian, K. Simons, S. Gehlhar, J. L. Rust, R. R. Syamala, et al. A Chromosome Bin Map of 2148 Expressed Sequence Tag Loci of Wheat Homoeologous Group 7 Genetics, October 1, 2004; 168(2): 687 - 699. [Abstract] [Full Text] [PDF]

				L. L. Qi, B. Echalier, S. Chao, G. R. Lazo, G. E. Butler, O. D. Anderson, E. D. Akhunov, J. Dvorak, A. M. Linkiewicz, A. Ratnasiri, et al. A Chromosome Bin Map of 16,000 Expressed Sequence Tag Loci and Distribution of Genes Among the Three Genomes of Polyploid Wheat Genetics, October 1, 2004; 168(2): 701 - 712. [Abstract] [Full Text] [PDF]

				B. S. Gill, R. Appels, A.-M. Botha-Oberholster, C. R. Buell, J. L. Bennetzen, B. Chalhoub, F. Chumley, J. Dvorak, M. Iwanaga, B. Keller, et al. A Workshop Report on Wheat Genome Sequencing: International Genome Research on Wheat Consortium Genetics, October 1, 2004; 168(2): 1087 - 1096. [Abstract] [Full Text] [PDF]

				K. G. Hossain, O. Riera-Lizarazu, V. Kalavacharla, M. I. Vales, S. S. Maan, and S. F. Kianian Radiation Hybrid Mapping of the Species Cytoplasm-Specific (scsae) Gene in Wheat Genetics, September 1, 2004; 168(1): 415 - 423. [Abstract] [Full Text] [PDF]

				M. Erayman, D. Sandhu, D. Sidhu, M. Dilbirligi, P. S. Baenziger, and K. S. Gill Demarcating the gene-rich regions of the wheat genome Nucleic Acids Res., July 7, 2004; 32(12): 3546 - 3565. [Abstract] [Full Text] [PDF]

				K. M. Haen, H. Lu, T. L. Friesen, and J. D. Faris Genomic Targeting and High-Resolution Mapping of the Tsn1 Gene in Wheat Crop Sci., May 1, 2004; 44(3): 951 - 962. [Abstract] [Full Text] [PDF]

				S. Tang, A. Heesacker, V. K. Kishore, A. Fernandez, E. S. Sadik, G. Cole, and S. J. Knapp Genetic Mapping of the Or5 Gene for Resistance to Orobanche Race E in Sunflower Crop Sci., May 1, 2003; 43(3): 1021 - 1028. [Abstract] [Full Text] [PDF]

				J. D. Faris, J. P. Fellers, S. A. Brooks, and B. S. Gill A Bacterial Artificial Chromosome Contig Spanning the Major Domestication Locus Q in Wheat and Identification of a Candidate Gene Genetics, May 1, 2003; 164(1): 311 - 321. [Abstract] [Full Text] [PDF]

				D. Sandhu, D. Sidhu, and K. S. Gill Identification of Expressed Sequence Markers for a Major Gene-Rich Region of Wheat Chromosome Group 1 Using RNA Fingerprinting-Differential Display Crop Sci., July 1, 2002; 42(4): 1285 - 1290. [Abstract] [Full Text] [PDF]

				E. C. Howell, G. C. Barker, G. H. Jones, M. J. Kearsey, G. J. King, E. P. Kop, C. D. Ryder, G. R. Teakle, J. G. Vicente, and S. J. Armstrong Integration of the Cytogenetic and Genetic Linkage Maps of Brassica oleracea Genetics, July 1, 2002; 161(3): 1225 - 1234. [Abstract] [Full Text] [PDF]

				J. King, I. P. Armstead, I. S. Donnison, H. M. Thomas, R. N. Jones, M. J. Kearsey, L. A. Roberts, A. Thomas, W. G. Morgan, and I. P. King Physical and Genetic Mapping in the Grasses Lolium perenne and Festuca pratensis Genetics, May 1, 2002; 161(1): 315 - 324. [Abstract] [Full Text] [PDF]

				D. Sandhu and K. S. Gill Gene-Containing Regions of Wheat and the Other Grass Genomes Plant Physiology, March 1, 2002; 128(3): 803 - 811. [Abstract] [Full Text] [PDF]

				C. FEUILLET and B. KELLER Comparative Genomics in the Grass Family: Molecular Characterization of Grass Genome Structure and Evolution Ann. Bot., January 1, 2002; 89(1): 3 - 10. [Abstract] [Full Text] [PDF]