Copyright  1999 by the Genetics Society of America
Genome Mapping in Capsicum and the Evolution of Genome Structure
in the Solanaceae
Kevin D. Livingstone,* Vincent K. Lackney,* James R. Blauth,*,1 Rik van Wijk
and Molly Kyle Jahn*
*Department of Plant Breeding, Cornell University, Ithaca, New York 14853 and 
Keygene, n.v., 6708 PW Wageningen, The Netherlands
Manuscript received December 11, 1998
Accepted for publication April 7, 1999
ABSTRACT
We have created a genetic map of Capsicum (pepper) from an interspecific F2 population consisting
of 11 large (76.2­192.3 cM) and 2 small (19.1 and 12.5 cM) linkage groups that cover a total of 1245.7
cM. Many of the markers are tomato probes that were chosen to cover the tomato genome, allowing
comparison of this pepper map to the genetic map of tomato. Hybridization of all tomato-derived probes
included in this study to positions throughout the pepper map suggests that no major losses have occurred
during the divergence of these genomes. Comparison of the pepper and tomato genetic maps showed
that 18 homeologous linkage blocks cover 98.1% of the tomato genome and 95.0% of the pepper genome.
Through these maps and the potato map, we determined the number and types of rearrangements that
differentiate these species and reconstructed a hypothetical progenitor genome. We conclude there have
been 30 breaks as part of 5 translocations, 10 paracentric inversions, 2 pericentric inversions, and 4
disassociations or associations of genomic regions that differentiate tomato, potato, and pepper, as well
as an additional reciprocal translocation, nonreciprocal translocation, and a duplication or deletion that
differentiate the two pepper mapping parents.
THE field of comparative plant genomics was precipi- linkage blocks between related genomes, even when
tated in 1988 by two studies in the Solanaceae relat- comparing species that vary widely in DNA content and
ing the genetic maps of tomato and potato (Bonierbale karyotype morphology (Gebhardt et al. 1991; Tanks-
et al. 1988) and tomato and pepper (Tanksley et al. ley et al. 1992; Weeden et al. 1992; Menancio-Hautea
1988), each of which was constructed using common et al. 1993; Kowalski et al. 1994; Bennetzen and Free-
restriction fragment length polymorphism (RFLP) ling 1997; Cheung et al. 1997; Bennetzen et al. 1998;
probes. The first study found that the tomato and potato Gale and Devos 1998a,b; Lagercrantz 1998).
genomes differed only by paracentric inversions, and There are other previously published and unpub-
further studies (Gebhardt et al. 1991; Tanksley et al. lished genetic maps of Capsicum based on either inter-
1992) showed that five inversions differentiated these specific Capsicum annuum C. chinense populations
species. The tomato-pepper study also suggested that (Tanksley 1984; Tanksley et al. 1988; Prince et al.
pepper had maintained genomic content similar to to- 1993; Kim et al. 1998a), intraspecific C. annuum doubled-
mato, as defined by the presence of pepper sequences haploid populations (Lefebvre et al. 1995, 1997; Lefeb-
complementary to all tomato cDNAs tested, but that the vre and Palloix 1996; Caranta et al. 1997a,b), other
pepper genome was rearranged substantially, with many interspecific crosses (Zhang 1997; Y. Zhang, unpub-
pepper chromosomes containing three to four distinct lished results), or an intraspecific C. annuum F2 popula-
tomato segments. A later, more detailed comparison of tion (Massoudi 1995). To date, however, there is no
pepper and tomato concluded that pepper had lost map of Capsicum that achieves the goal of completely
regions homologous with the tomato genome and failed delineating and saturating the pepper chromosomes.
to change the perception that the homeologous linkage To answer questions remaining from these earlier
blocks in the pepper genome were fragmented substan- studies of Capsicum, a complete genetic map with 12
tially (Prince et al. 1993). As a result, the pepper-tomato linkage groups anchored in and completely represent-
comparison remains the frequently cited exception to ing the tomato genome is required. Toward this end,
numerous studies that have shown conservation of large we have constructed a molecular map of Capsicum using
randomly amplified polymorphic DNA (RAPD), iso-
zyme, amplified fragment length polymorphism
Corresponding author: Molly Jahn, Department of Plant Breeding, (AFLP), and RFLP analyses with tomato- and pepper-
252 Emerson Hall, Cornell University, Ithaca, NY 14853.
derived probes, which has allowed us to reexamine ques-E-mail: mmk9@cornell.edu
tions of genome structure and karyotypic evolution in1
Present address: Division of Biological Sciences, Alfred University,
Alfred, NY 14802. pepper, tomato, and potato.
Genetics 152: 1183­1202 (July 1999)
1184 K. D. Livingstone et al.
MATERIALS AND METHODS Genetic map construction: The genotypes of the RFLPs
and RAPDs were scored independently to obtain a consensus
Population construction, DNA extractions, and cytological genotype. If a probe produced multiple segregating bands,
examination: The F2 mapping population of 75 plants was then each band was initially scored as a dominant band. Some
developed by self-pollinating one F1 hybrid plant of C. annuum of these genotypes were subsequently converted to codomi-
cv. "NuMex RNaky" (Nakayama and Matta 1985) C. chi- nant pairs if two dominant bands, one from each parent,
nense PI 159234, obtained from S. Tanksley (Cornell Univer- mapped to the same position.
sity, Ithaca, NY). The parents and F1 and F2 plants were grown The initial RFLP data were then merged with isozyme,
in the greenhouse at Cornell University, and DNA was ex- RAPD, and AFLP marker genotypes. A test of departure from
tracted from harvested leaf tissue following the procedure of expected Mendelian ratios was conducted where possible;
Prince et al. (1997). Immature F1 flower buds were collected however, a number of the AFLP genotypes included A, B, H,
and fixed in Carnoy's solution for cytological examination. and C ( B or H) or D ( A or H) calls precluding this analysis.
The buds were transferred to a 70% ethanol solution and The markers were also divided into classes on the basis of a
then squashed with gentle heating in a 2% acetocarmine:45% subjective measure of the certainty with which the genotype
acetic acid solution. Metaphase I and anaphase I in pollen was ascertained. These classifications were used to find the
mother cells were then observed by light microscopy. RFLP markers that could be unambiguously read and whose
Molecular markers: RFLP: Pepper, tomato, and tobacco deviations from the expected Mendelian frequencies were P
DNA fragments were used as probes for RFLP. Three types 0.01 for dominant markers and P 0.001 for codominant
of tomato clones described in Tanksley et al. (1992) were markers. The more distorted markers were excluded from
supplied by S. Tanksley: tomato random genomic DNA (TG), the initial framework construction phase to protect against
tomato whole-leaf cDNA (CD), and tomato leaf epidermal mapping errors stemming from either pseudolinkages con-
joining independent chromosomal regions or incorrect esti-cDNA (CT). Pepper leaf epidermal cDNA (PC) and pepper
mates of map distances (Lorieux et al. 1995; Cloutier et al.random genomic (PG) DNA clones, described by Prince et
1997).al. (1993) and Blauth (1994), were either supplied by S.
The MAPMAKER/EXP v3.0b program (Lincoln et al. 1993)Tanksley or generated in our lab. In addition to these, other
was used for map construction. The subset of markers definedclones used as probes included the following: the tomato genes
above was divided into linkage groups using the "group" com-Prf, supplied by G. Martin (Boyce Thompson Institute, Ithaca,
mand (parameters: LOD 3, 20 cM), and then arrangedNY), and Sw-5, supplied by S. Tanksley; four pepper genomic
into a framework map using the "order" command (parame-clones (UB) from U. Bonas (Martin Luther University, Dom-
ters: LOD 3 for linkage, 20 cM, initial group size of 3,platzl, Germany); and the tobacco N cDNA (pN18C) provided
LOD 3 vs. alternative orders). The resultant orders for eachby B. Baker (U.S. Department of Agriculture, Albany, CA).
group were checked by multiple iterations of this process afterSurvey filters were prepared to assess polymorphism be-
scrambling the marker input order. When multiple markerstween parental DNA digested with 12 different restriction
cosegregated, codominant markers were given preference forenzymes: DraI, EcoRI, EcoRV, HindIII, BstNI, TaqI, XbaI, BamHI,
inclusion in the framework. Framework orders were checkedBglII, BclI, SacI, and StuI. Mapping filter sets for each of the
by manual examination of the "LOD table," the "ripple" com-12 restriction enzymes were also prepared, including both
mand (parameters: 3 markers, reporting alternative orders ifparents and all 75 F2 progeny. All filters were prehybridized
LOD 3 compared to the set framework), and finally byfor at least 4 hr in 70 ml of hybridization buffer before use.
checking the pairwise linkages between all framework markersThe cloned inserts used as probes were amplified by PCR and
from different linkage groups.then purified on Sephadex G50 spin columns equilibrated
AFLP markers were added to the linkage groups via thewith Tris-EDTA to reduce background signal. These products
"assign" command (parameter values LOD 3 and 20were then radiolabeled using a protocol modified from Fein-
cM), and they were added to the chromosomal frameworksberg and Vogelstein (1983) as follows. The amounts of the
using the "build" command if the placement of a marker intofollowing reagents were doubled to increase the signal
a particular interval was significantly better (LOD 3) thanstrength when using heterologous probes: cloned DNA (200
all alternative placements. This addition procedure was thenng instead of 100 ng DNA), labeling solution (22 l instead
repeated for the remaining initial RFLP markers and theof 11 l), Klenow enzyme (8 units instead of 4 units), and
skewed markers. The resultant orders for each linkage group[32
P]dCTP (0.1 mCi instead of 0.05 mCi). After a 90-min incu-
were then checked again by manual examination of the LOD
bation at 37 , the labeled clones were purified on Sephadex
table and the ripple command, as described above. Finally,
G50 spin columns in 1% SDS and 25 mm EDTA spun at 2500
the positions for all remaining markers were determined using
rpm for 8 min. The clones were denatured by heating at
the "try" command. Markers were given either a position be-
100 for 10 min and then added to the hybridization buffer.
tween framework markers if 2 LOD 3 for the interval
Hybridization was carried out overnight at 65 . Filters were
and all other placements were unlikely (LOD 1), or they
washed with one low-stringency (2 SSC, 0.1% SDS) wash were added into haplotype groups. Haplotype groups con-
and two moderate-stringency (1 SSC, 0.1% SDS) washes at sisted of markers that were separated from framework markers
65 and placed on Kodak XAR-5 film for 3­12 days, depending by 5 cM and placement on either side of the framework
on signal strength. marker was equally likely. These markers were assigned posi-
Isozyme analysis: The procedures of Loaiza-Figueroa et al. tions with the framework marker(s), but they are differenti-
(1989) were carried out in the laboratory of N. Weeden (New ated on the map (see Figure 1 legend). Some markers were
York State Agricultural Experiment Station, Geneva, NY) to placed beyond the framework ends of the linkage groups if
analyze Idh-1, Gpi-1, Gpi-2, 6-Pgdh, Pgm-1, Pgm-2, and Tk. they mapped to the end of a linkage group (2 LOD 3)
PCR-based markers: RAPD markers were generated following and all alternative locations within the group were unlikely
the procedures of Prince et al. (1995). RAPD 10-mer primers (LOD 1). Pairwise linkages with the terminal framework
were obtained from the National Science Foundation/Depart- markers were checked to ensure correct placement. These
ment of Energy/U.S. Department of Agriculture Plant Science markers were added to the map; however, they were not con-
Center at Cornell University and from Gilroy Foods (Gilroy, sidered framework markers for further linkage group exten-
CA). AFLP markers were generated by Keygene n.v. (Wagen- sion. All mapping was done without reference to the order of
ingen, The Netherlands) using the procedure of Vos et al. markers on the tomato map, and all distances were computed
using the Kosambi mapping function (Kosambi 1944).(1995).
1185Genome Evolution in the Solanaceae
Construction of the synteny map: A second genetic map pected single-locus Mendelian ratios. Slightly more than
was constructed to maximize the number of tomato-derived half of the tested subset (337 50.7%) showed devia-
markers for comparative analysis. For this map, all nontomato
tion from the expected ratios (P 0.01); 81 of thesemarkers were removed, and positions for the remaining to-
(12.2%) were severely distorted (P 0.001), with Pmato-derived markers were estimated by reducing the strin-
gency for addition to haplotype groups ( 8 cM) or placement values as low as 2.69 10 25
. Two common causes of
between framework loci (LOD 1.5). Other markers that misclassified segregation distortion (residual heterozy-
mapped into several contiguous intervals were placed at their gosity and comigrating RFLP or PCR fragments) were
most likely positions. The tomato map of Pillen et al. (1996)
ruled out because (1) all F2 plants came from only onewas then reduced to only the markers in common between
F1 individual that could carry only one allele from eachthe two maps.
parent; and (2) within a distorted region, all RFLP and
AFLP markers were distorted and comigration of multi-
RESULTS ple independent markers is extremely unlikely.
The distorted regions (0.01 P 0.001) includedCytology of meiosis in (C. annuum NuMex RNaky
the middle of pepper linkage group (P)1 between TG70C. chinense PI 159234) F1 plants: Cytological examination
and A211, distorted in favor of C. annuum homozygotesof meiotic chromosome spreads from pollen mother
over C. chinense homozygotes; the middle of P3 betweencells of C. annuum C. chinense F1 revealed multivalents
TG74 and TG290a, distorted in favor of C. chinense ho-and bridges extending across the metaphase plate at
mozygotes over C. annuum homozygotes; the bottom oflate anaphase I (M. Cadle, unpublished results). These
P6 near CT109, distorted in favor of heterozygotes overdata are consistent with the presence of at least one
C. annuum homozygotes; and the middle of P11 betweenreciprocal translocation between these species, as de-
CT70 and CD127a, distorted in favor of C. annuum ho-scribed previously by Tanksley (1984), Kumar et al.
mozygotes over C. chinense homozygotes. Severely dis-(1987), and Lanteri and Pickersgill (1993).
torted regions (P 0.001) included the upper endMarker genotyping and analysis: RFLP: A total of 399
of P2 down to CT128a, with an excess of C. chinensetomato probes selected to represent the tomato genome
homozygotes over C. annuum homozygotes; the upperwere assayed for polymorphism (270 TG, 89 CT, 33
end of P3 at CT220, with an excess of heterozygotesCD, and 7 other tomato cDNAs). Furthermore, 184 PG
over C. chinense homozygotes; the upper end of P11 atclones, 4 PC clones, 4 other pepper genomic (UB)
CD127d and CD186d, again with an excess of heterozy-clones, and pN18C were also tested. All tomato clones
gotes over C. chinense homozygotes; all of P7, distorted intested hybridized to pepper genomic DNA, and 203 TG,
favor of C. chinense homozygotes, almost to the complete58 CT, 28 CD, 7 other tomato cDNA, 2 PC, 3 UB, pN18C,
exclusion of C. annuum alleles in some regions; and theand 43 PG clones were used as probes. The lower per-
upper end of P12 down to A3, with an excess of C.centage of PG clones used (23 vs. 75% for TG, 65% for
chinense homozygotes over C. annuum homozygotes. TheCT, and 85% for CD) resulted from the number of PG
regions corresponding to P1, P2, P3, P6, P11, and P12clones (74 40.2%) that produced a smear of unresolv-
were also distorted in either one or both of the tomatoable bands. Some survey autoradiograms are available
populations of de Vicente and Tanksley (1993) orfrom the Solgenes database2
(Paul et al. 1994). The
Bernacchi and Tanksley (1997), and markers fromprobes produced 460 segregating RFLP; 227 (49.3%)
P7 and P12 were also distorted in the earlier pepperwere codominant.
population of Prince et al. (1993) and the potato popu-Isozymes: Genotypes were obtained for all seven iso-
lation of Tanksley et al. (1992).zymes.
Genetic map construction: A genetic map consistingPCR-based markers: From the 116 RAPD primers tested,
of 11 large (76.2­192.3 cM) and 2 small (19.1 and 12.559 produced 75 reproducible polymorphic bands (OPR,
cM) linkage groups covering 1245.7 cM was constructedR, U, OPO, OPA, Q, and OPE markers). In addition,
from the genotypic data (Figure 1). Although 2N 2X20 primer combinations were used in AFLP. These reac-
24 for these species, the reciprocal translocation intions yielded 465 segregating bands (A markers), of
the parents would cause pseudolinkage between mark-which 340 could be scored as codominant by a proprie-
ers near the interchange breakpoints on the chromo-tary algorithm. The primer sequences, fragment sizes,
somes involved (Burnham 1991). P1 contains Idh-1 andand parental lines showing amplification for all PCR-
Pgm-2, which are described by Tanksley (1984) as beingbased markers are available from Solgenes.3
near the exchange breakpoint in a similar interspecificSegregation distortion: Of the 1007 markers gener-
cross; therefore, we propose that this linkage groupated, 665 could be tested for deviation from their ex-
represents the two pepper chromosomes involved in
this rearrangement. The two small linkage groups in
our map remained unlinked despite the use of clones2
Go to http://probe.nalusda.gov:8300/ and choose "databases,"
then "browse" from the options of the Solgenes database, and look from the corresponding regions of the tomato genome.
for "image" class objects with "ACF" in the title.
Of the 1007 marker genotypes generated, 6773
Go to http://probe.nalusda.gov:8300/ and choose "databases,"
(67.2%) were either given positions in the LOD 3 frame-then "browse" from the options of the Solgenes database, and look
for the marker under its name in the "locus" objects list. work or placed in framework intervals at 2 LOD
1186 K. D. Livingstone et al.
Figure 1.--A genetic map of Capsicum. Markers in boldfaced type at tick marks are framework markers ordered at LOD
3, and multiple markers at a tick mark cosegregated. Markers listed in plain type after framework markers were closely linked
to the framework markers ( 5 cM), but placed equivalently on either side of the framework position at LOD 2 when compared
to other positions in the linkage group. Markers in parentheses placed between framework positions at 2 LOD 3. Marker
types and designations are as follows: tomato genomic RFLP (TG); tomato cDNA RFLP (CD, CT, Sw5, and Prf); pepper genomic
RFLP (PG and UB); pepper cDNA RFLP (PC); tobacco cDNA RFLP (pN18C); AFLP (A); RAPD (OP, U, R, Q); and isozyme
(Gpi-2, Idh-1, and Pgm-2). Lowercase letters at the end of the marker names indicate that the marker is one of at least two
segregating loci detected by a single assay. Distances between framework positions in centimorgans (Kosambi) are to the left of
each chromosome.
1187Genome Evolution in the Solanaceae
Figure 1.--Continued.
3, while 5 markers (1 isozyme, 1 TG, 1 CT, and 2 AFLP) this classification placed equally well into a small num-
ber (3­5) of contiguous intervals in the framework areasremained unlinked. The remaining 325 markers group-
ed (LOD 3) with the linkage groups but did not place with high marker densities. There were, however, 29
markers in this group that placed in a greater numberwell within the frameworks (multiple equivalent LODs).
The number of these markers from each linkage group of intervals all along the length of a particular chromo-
some. A hallmark of these loci was moderate pairwisecould be a function of the length of the linkage group
(r2
0.77, P 8.4 10 5
). Only groups 1 and 4 deviated linkage with a framework locus (LOD  3, 15­20 cM),
but no linkage to the flanking framework markers.significantly toward more of these loci than expected
(data not shown). The majority of the markers that fit The 677 markers across 1245.7 cM provide an average
1188 K. D. Livingstone et al.
Figure 1.--Continued.
marker density of 1 marker per 1.8 cM; however, the allowed Tanksley et al. (1992) to show that the clus-
ters represented regions of suppressed recombinationmean distance between framework positions is 9.0 cM.
There is great variability in these densities because many around tomato centromeres. Pepper centromeres have
been mapped using C banding (Moscone et al. 1993);markers showed pronounced clustering (Figure 1). One
region of marker clustering occurs on each of the large however, pepper lacks both the classical map and dele-
tion studies to correlate our map with these data. Thus,linkage groups and includes 44­66% of the markers in
that linkage group. Overall, 54% of the markers are while all the clusters on our map contain markers linked
to centromeres in tomato, an observation also made forlocated in these clusters. This figure may be an overesti-
mate, however, as some of the AFLP markers may be several of the linkage groups of the map in Prince
et al. (1993), we can only presume that these regionsallelic pairs.
The nonrandom distribution of markers within link- correspond to the centromeric regions of each of the
linkage groups.age groups is similar to tomato, where cytogenetic data
1189Genome Evolution in the Solanaceae
Genome content: Most probes used (66%) produced Comparative map of pepper and tomato: The probes
used detected 308 loci on the tomato map of Pillen et2­6 bands; 21% gave 6­10 bands, and 12% revealed
segments of the genome that had been duplicated ex- al. (1996) and 352 loci on our augmented pepper map
(Figure 2). We then defined homologous segments con-tensively ( 10 bands) but still provided distinguishable
polymorphisms. To examine the relative copy number taining common markers from contiguous regions of
the genetic maps of both species. Breaks in homeologyof sequences detected by hybridization, we compared
a subset of 30 pepper survey blots with tomato survey were not declared if the intervening markers not from
the contiguous region of the other species were eitherblots from the Tanksley laboratory using the same
probe-enzyme combinations. Five of the tomato blots from probes detecting multiple segregating loci or from
more than one different chromosome.also included a lane with DNA from our C. annuum
parent. In 2 of these 5 control comparisons, our surveys There were only four regions in pepper and one re-
gion in tomato where homeology was either difficult toshowed more bands than the Tanksley surveys (6 vs. 2
and 9 vs. 3). In the other three cases, results were more assign or not apparent: the top of P4, which included
markers from throughout the tomato genome; the topsimilar (3 vs. 1, 5 vs. 4, and 11 vs. 10), although in every
case the larger number came from our laboratory. This of P5, which is duplicated in and represented only by
dominant markers from the C. chinense parent; the toplimited sample suggests that some differences observed
between tomato and pepper in the copy number of of P7, which contains a large number of markers that
are spread throughout the tomato genome and someprobes may result from specific laboratory procedures.
When all 30 comparisons between pepper and tomato loci that were uniquely duplicated in pepper; the bot-
tom of P7, which contained markers from different to-were considered, 14 showed more bands for a given
probe in pepper than tomato, and 16 were approxi- mato chromosomes; and the top of tomato chromosome
(T)7, which is represented in the pepper (all probesmately similar.
In our study, 43 clones (6 pepper genomic DNA, and hybridized) but appears to be scattered throughout the
pepper genome. It is impossible to tell whether these37 tomato probes, 17 cDNA, and 20 genomic clones)
detected multiple segregating loci in pepper. Seven of regions are the result of novel associations of markers
in one of the genera or the disassociation of a group ofthe 37 tomato clones also detected multiple segregating
loci in the tomato (Pillen et al. 1996), but the duplica- markers in another. Overall, 98% of the tomato genome
and 95% of the pepper genome were included in de-tions in each species appeared to be distinct. The major-
ity (93%) of the pepper duplications appeared to be fined regions of homeology.
Within homeologous segments, 30% of the lociunlinked duplications of single loci. There was only one
set of multiple linked loci that revealed a duplication mapped in only one genome, perhaps because no corre-
sponding homolog was present in the other genus orin the Capsicum genome: CD42, CD44, CT205, TG51,
TG174, TG215, and TG314 produced loci on the middle the homolog was not segregating. We cannot distinguish
between these two alternatives because nonsegregatingof P1 in C. annuum and the top of P2 and P5 in C.
chinense. The frequency of tandemly duplicated loci sep- bands were detected by most probes in at least one of
the populations, but we can resolve two classes of loci.arable by recombination within intervals 10 cM was
0.87%. Some loci appear to be uniquely duplicated in one
Figure 2.--Homeologous relationships between the genetic maps of Capsicum and tomato. The genetic map of tomato was
modified from the map of Pillen et al. (1996): only the markers in common between the two maps are presented, and the
orientation of tomato chromosome 8 is reversed. For the tomato map, markers in plain type at tick marks are framework loci
ordered at LOD 3, markers in parentheses are placed in intervals at LOD 3, and positions of underlined loci were
approximated from other maps. The pepper map is based on Figure 1, but all markers except those in common to the two maps
have been removed. Markers in bold represent framework markers ordered at LOD 3. Markers in plain type listed with the
framework markers may be up to 8 cM from the framework marker, based on pairwise linkage estimates. Pepper markers
enclosed in parentheses are placed at 1.5 LOD 3, and underlined markers are placed at their maximum likelihood position
(LOD 1.5). When a chromosome is homeologous to two chromosomes from the other species, one side of the chromosome
has been widened out. Marker types and designations are as follows: tomato genomic RFLP (TG); tomato cDNA RFLP (CD and
CT); pepper cDNA RFLP (PC); cloned genes [Pto ( CD186), Fen ( CD127), and Prf]; and isozymes (Idh-1, Pgm). Numbers in
square brackets after locus names indicate the nonhomeologous chromosome in the other species where a map position was
obtained for that particular probe. An asterisk after a locus name denotes a locus mapped uniquely in one species from a probe
that produced multiple segregating loci, with the other loci mapping to syntenous positions; e.g., if a probe produced two
fragments in tomato and one fragment in pepper that mapped to a syntenous position, the second locus would be marked with
an asterisk. A dagger indicates that a homolog groups with the syntenous linkage group, but a definitive position cannot be
assigned. The markers that grouped (LOD 3) but did not place well within the linkage group frameworks for each of the
linkage groups are as follows (annotations are the same as above): P3­TG16b*; P4­CD55, CD64c*, CD64d*, CD64g*,
CT205c *, TG503a [5], TG503b [5]; P7­CD39d*, CT32a [9], CT129a*, TG47 [11], TG220b*, TG418; the two unlinked markers
are CT182 [11] and TG214 [3].
1190 K. D. Livingstone et al.
Figure 2.
1191Genome Evolution in the Solanaceae
Figure 2.--Continued.
genus (a probe reveals a pair of loci that map to synten- appear to be uniquely duplicated, while 67 loci (21.8%)
lack a counterpart in the homeologous pepper segment.ous positions and an additional locus in one species);
some loci are represented only once on each map not In pepper, 40 loci (11.4%) appear to be uniquely dupli-
cated, and 70 loci (19.9%) lack a counterpart on thein homeologous segments. In tomato, 11 loci (3.6%)
1192 K. D. Livingstone et al.
Figure 2.--Continued.
1193Genome Evolution in the Solanaceae
Figure 2.--Continued.
1194 K. D. Livingstone et al.
Figure 2.--Continued.
1195Genome Evolution in the Solanaceae
homeologous tomato segment. When all 660 loci are sented by 18 homeologous segments with unique rela-
tionships in each genus. The majority of these segmentsconsidered, 51 loci (7.7%) are uniquely duplicated on
1 map, and 137 loci (20.8%) lack a homolog in the maintain strict syntenic order throughout, while a few
maintain locus content but have undergone paracentrichomeologous segment of the other genome. This is
comparable to the percentage of markers (20­40%) inversions within the segment. Despite the number of
rearrangements, chromosomes from both genera ap-without meaningful synteny in comparisons among the
grasses (Bennetzen and Freeling 1997). pear to contain at most only two conserved segments.
Genome structure in the Solanaceae: The pepper-To provide a concise representation of synteny be-
tween tomato and pepper, we modified Figure 2 as tomato comparative map can be used with the phylog-
eny of Capsicum, Lycopersicon, and Solanum (Spoonerfollows to create Figure 3: all marker names were omit-
ted, indicators for markers with no homologs mapped et al. 1993) and the tomato-potato comparative map
(Tanksley et al. 1992) to identify conserved linkagein the homeologous region were omitted, the positions
of the tomato centromeres and the regions of sup- blocks, to reconstruct portions of the genome of the
most recent ancestor of these species, and, in somepressed recombination on the pepper linkage groups
were added, and the lines connecting pairs of loci were cases, to determine in which lineage rearrangements
occurred. Where pepper and tomato/potato differ, thechanged to dashed if one of the loci in a pair was not
mapped at framework stringency, was inferred from an- number of ad hoc hypotheses is the same using either
condition as the ancestral state, so only two alternativeother map, or was duplicated such that orthology was
suspect. arrangements can be presented. We assumed that para-
centric and pericentric inversions and translocationsFigures 2 and 3 show that the tomato and pepper
genomes share large linkage blocks that have under- were the prominent mechanisms of structural change,
and we did not equate nonsyntenous markers withgone various typical rearrangements during speciation4
.
Four pairs of chromosomes show conservation of con- breaks because no simple way exists to explain these
loci concordantly with these typical chromosomal re-tent of entire chromosomes: T2-P2, T6-P6, T7-P7, and
T10-P10. Both marker locus content and overall struc- arrangements.
A1: The ancestral homeologs of chromosome 1 (A1)ture in the T6-P6 pair appears to have been maintained
completely. Two of the other pairs show paracentric in tomato and potato are identical (Figure 4). The pep-
per species differ by a reciprocal translocation with A8inversions, a small part of the lower end of T2/P2, and
the lower arm of T10/P10. The T2-P2 pair also includes and the small linkage block found on P1 in C. annuum
and P2 and P5 in C. chinense, but not found in tomato/the region at the top of P2, which is unique to C. chinense,
and three markers (TG205, CT140, and CT176) that potato. We conclude that A1 was most like tomato/
potato, with at least two breaks in the pepper lineages,map to nonsyntenous positions. The T7-P7 pair main-
tains a common core, but differs in the position of one to create the A1-A8 translocation and the other to
account for the position of the duplicated region in C.TG183 and unique linkages at both ends of P7 and one
end of T7, as mentioned previously. annuum.
A2: The tomato/potato A2 homeologs are identical,The rest of the genome appears to have been con-
served in linkage blocks corresponding to chromosome while pepper and tomato/potato differ by a paracentric
inversion. The pepper species also differ in the distalarms rearranged by nonreciprocal translocations as well
as pericentric and paracentric inversions. The complex- region of P2; therefore, at least two breaks differentiate
the pepper and tomato/potato lineages, with at leastity of the rearrangements ranges from a single nonrecip-
rocal translocation, in the case of the T4-P4, to multiple one more break in one of the pepper lineages.
A3: The tomato/potato homeologs are identical tonested translocations and inversions seen in the T9-P9-
T12 comparison. The rearrangements must also have each other and to a segment of pepper, but at least two
breaks must have occurred in one of these lineages toincluded multiple pericentric inversions in the P12-T11-
P11-T5 chromosomes. The T1-P1-T8 comparison is account for the differences between pepper and to-
mato/potato.unique because of the major translocation within Capsi-
cum, but it also appears to conserve whole arms as link- A4: The tomato/potato A4 homeologs and most of
pepper A4 occur as a single linkage block. The segmentage blocks. The possible exception is the upper arm of
T1, although the observed lack of synteny could be attached to tomato/potato A4 is attached to the A5
homolog in pepper in a reversed telomere-centromerecaused by mapping artifacts arising from the transloca-
tion within pepper. Finally, Figure 3 illustrates the align- orientation and is distinct in the two pepper species: C.
chinense has an additional linkage block not found inment of tomato centromeres with the regions of sup-
pressed recombination in pepper. C. annuum. As a result, we infer at least one break with
a reversal of orientation between tomato/potato andThe pepper and tomato genomes can then be repre-
pepper, as well as a break in one of the Capsicum spe-
cies.
A5: The potato and tomato homeologs of A5 are4
A more exhaustive description of the differences between the
tomato and pepper genomes is also available (Livingstone 1999). identical for one arm, but differ by a paracentric inver-
1196 K. D. Livingstone et al.
Figure 3.--Comparative ge-
nome structure of pepper and
tomato. The genetic maps of
Figure 2 [pepper chromo-
somes (P), gray bars; tomato
chromosomes (T), white bars]
have been reduced to only
markers that map to homeolo-
gous segments of the genome.
These points are connected by
solid lines, except where either
a clone produced multiple seg-
regating loci in one or both of
the species with loci mapping
to nonsyntenous positions,
making the assignment of para-
logous pairs questionable, or
one or both of the marker(s)
mapped at LOD 2 or was
mapped in a different popula-
tion. These marker pairs are
connected by dashed lines.
The positions of the tomato
centromeres are indicated by
shaded bars or points on the
tomato chromosomes. The re-
gions of suppressed recombi-
nation on the pepper chromo-
somes are indicated by white
circles or bars. The locations of
pepper linkage groups A and
B are indicated by bars next to
tomato chromosomes 8 and 3.
sion for the other. The noninverted arm of the A5 ho- A8: This chromosome is identical in tomato/potato,
but is part of a reciprocal translocation pepper. Themeolog is also conserved in pepper, while the other
arm is attached to the A11 homeolog. The orientation other difference between pepper and tomato/potato is
the small piece distal to the centromere in tomato/of this arm in pepper and potato is superficially similar;
however, CD64 homologs occur in different linkage potato that is unlinked in pepper. At least one break
occurred in one of the pepper species, and another mayblocks of pepper and tomato/potato, indicating that
the inversions are independent and that a pericentric have occurred in either the tomato/potato or pepper
lineage.inversion occurred early in either the tomato/potato
or pepper lineage. We conclude that there was an early A9: The tomato and potato homeologs of this chro-
mosome differ by a paracentric inversion. Tomato andpericentric inversion followed by independent paracen-
tric inversions in the potato and pepper lineages. pepper also differ by a similar paracentric inversion;
however, the positions of the breakpoints are different.A6: The structure of this homeolog is maintained in
all three species. These data are consistent with either tomato or pepper
being closest to the ancestral condition, as both config-A7: The structure is conserved, except for the unique
distal linkage blocks. urations require two breaks and two new telomeres.
1197Genome Evolution in the Solanaceae
lineage and a series of at least four breaks to account
for the position and arrangements of the G block.
A10: The potato/pepper and tomato homeologs dif-
fer by one paracentric inversion, indicating the paracen-
tric inversion and break has occurred in the tomato
lineage.
A11: The tomato and potato homeologs differ by a
paracentric inversion. The corresponding pepper arm is
similar to that of potato, although attached to a different
chromosome. We presume the pepper/potato orienta-
tion of this arm is ancestral. The position of TG104/
TG105 also differs in tomato/potato and pepper. We
conclude that one break and a paracentric inversion
occurred in the tomato lineage, and another three
breaks and a pericentric inversion occurred in either the
tomato/potato or pepper lineage that moved TG104/
TG105 and changed the attached linkage blocks.
A12: One arm of the A12 homeolog has been con-
served in pepper, tomato, and potato. Tomato and po-
tato differ by a paracentric inversion of the other arm
that requires one break in either tomato or potato to
account for the inversion and at least one break in either
the tomato/potato or pepper lineages to change the
attached blocks.Figure 4.--Overview of genome structure within the Sola-
naceae. The genetic maps of the 12 chromosomes of tomato, In total, we conclude that there have been at least 2
potato, pepper (P), and an inferred configuration for their breaks in the tomato genome, 2 breaks in the potato
most recent common ancestor (A) are represented, along with genome, 1 break in either the tomato or potato genome,
the deviations from this common ancestor within each species.
1 break in the pepper genome that differentiates it fromWhite regions are conserved between the three species and
tomato/potato, and another 5 breaks to account fordefine the ancestral condition. Other white regions are con-
served between pepper and either potato or tomato, but not the differences between the 2 pepper species. Nineteen
both, indicating a derived condition in the nonidentical spe- other breaks must have occurred in either the pepper
cies. Gray regions in the ancestral genome denote areas where lineage or in the common ancestor of tomato/potato.
the ancestral condition cannot be defined. Gray regions in
These breaks were part of 5 translocations, 10 paracen-the other genomes show actual or potential differences be-
tric inversions, 2 pericentric inversions, and 4 disassocia-tween that species and the proposed ancestral genome. Inver-
sions are indicated by white arrows within gray bars. An upward tions or associations of genomic regions that produced
direction is defined as the ancestral condition, except for the observed genome variation among genera. An addi-
areas on A2, A9, and A12, where orientation could not be tional reciprocal translocation, nonreciprocal transloca-
determined on the basis of parsimony. On these segments,
tion, and a duplication or deletion differentiates thethe arrows in the A genome are double headed, and the
two pepper mapping parents.direction of the arrows in potato, tomato, and pepper indicate
relative orientation only. Rearranged segments are identified
by a letter to the right of the segment. In the ancestral genome,
DISCUSSIONall possibilities for a region are indicated (an X indicates
absent), and the region present in potato/tomato is under-
The Capsicum genetic map: The variability betweenlined. Asterisks denote areas unique to pepper (the extensions
our mapping parents maximized intralocus polymor-at the ends of P7) and differences that have occurred between
Capsicum species (the extensions in C. chinense at the ends phism, but also included major structural rear-
of P2 and P5 and the reciprocal translocation between P1 and rangements. As a result, we have defined more precisely
P8 in one species). Regions marked with a dagger denote the differences between the genomic structures of C.
linkage blocks unique to tomato/potato. The curved arrows
annuum and C. chinense, knowledge that is important toto the left of A11 homeologs indicate possible movements
plant breeders because C. chinense is a significant sourcewithin the linkage blocks.
of characters for C. annuum breeding. The major recip-
rocal translocation reduced this map to 11 large linkage
groups; however, through comparative mapping, we
Furthermore, the location and arrangement of linkage could establish the locus order for two of the four link-
block G is distinct in all three species; therefore, we age blocks of the two chromosomes involved. The
cannot ascertain the ancestral position or orientation marker order for the other two blocks will require intra-
of G, but all scenarios require at least four breaks. In specific populations genotyped with those markers.
This map contains two small, unlinked groups: P(A),conclusion, we infer at least one break in the potato
1198 K. D. Livingstone et al.
which is homeologous to the telomeric region of T8, loci, whereas in the latter case, cross-hybridization would
not be expected, as demonstrated by Hulbert et al.and P(B), which is homeologous to the telomeric region
of T3. In the two other interspecific maps constructed (1990), Barakat et al. (1997), and Bennetzen et al.
(1998).in our lab using a C. frutescens BG 2814-6 C. chinense
PI 159234 F2 and a C. frutescens BG 2814-6 C. annuum Differences between the tomato and pepper genomes
with regard to the number of both homologous andRNaky F2, linkages are seen between TG176 on P(A)
and CT252 from the opposite end of T8, and between segregating loci detected by a probe were apparent, with
pepper generally showing a higher copy number. TheP(B) and the top end of P4 (Zhang 1997; Y. Zhang,
unpublished results). The linkages between P(B) and greater number of probes detecting multiple loci in
pepper relative to tomato could be a consequence ofP4 through TG132 are detectable in the C. annuum
C. chinense map; however, neither was strong enough the detection of more loci per probe in pepper, or
perhaps evidence of a higher degree of interspecific(LOD 2.5, 30 cM) in this population to assert
linkage. The absence of linkage between P(A) and polymorphism within Capsicum compared to the inter-
specific cross used to construct the tomato map. Regard-CT252 in our population is puzzling; this linkage is clear
when either parent is crossed to C. frutescens, but it less, these differences in copy number between the spe-
cies lacked the patterns that would be associated withdisappears when the C. annuum and C. chinense parents
are intercrossed. Perhaps C. annuum and C. chinense systematic duplications. Overall, our observations con-
cur with results from previous work in this system (Tank-differ in the location of P(A), and the strength of the
linkage in the C. frutescens parent is causing the associa- sley et al. 1988) and the grasses (Bennetzen and Free-
ling 1997) that have shown only limited species-specifiction in one of the other maps, or P(A) may be separated
enough from other detected markers in the linkage duplications and deletions. The absence of systemati-
cally duplicated or deleted genomic regions or individ-group in both C. annuum and C. chinense that no linkage
is apparent. There is support for both hypotheses: ual loci effectively rules out paleopolyploidy, duplica-
tion, or deletion as explanations for the differences inKumar et al. (1987) and Lanteri and Pickersgill
(1993) have both reported that at least two transloca- genome size between pepper and tomato.
Increases in the amount of repeated DNA have beentions differentiate these species, and Moscone et al.
(1993) observed heterochromatic segments at the telo- established as a cause of genome expansion in plants
(Flavell et al. 1974), and recent work in the Gramineaemeres of all C. annuum chromosomes.
Several Capsicum maps have related linkage groups has shown a pattern of increases in retroelements be-
tween the genes of large-genome species relative toto chromosomes through a series of primary trisomics
generated by Pochard (1977). Unfortunately, this se- smaller-genome species (SanMiguel et al. 1996; Chen
et al. 1997; Panstruga et al. 1998). A study of repetitiveries is no longer complete or available. Because of incon-
sistencies between markers and their chromosomal asso- DNA in the pepper genome by An et al. (1996) estimated
that 5% of the pepper genome was composed of ele-ciations among recently published maps (Lefebvre and
Palloix 1996; Caranta et al. 1997a,b; Lefebvre et al. ments with copy number 10,000, 26% with copy num-
ber 150, and 65% single-copy sequences. This estimate1997), and some significant differences in observed link-
ages between these maps and our map, we have not of the single-copy fraction of the pepper genome ap-
pears high in light of our results, unless some of theassigned our linkage groups to named chromosomes.
Moscone et al. (1993) have succeeded in differentiating single-copy sequences are also unique to pepper, but
these data do show a significant amount of both high-the pepper chromosomes using C banding, indicating
that fluorescent in situ hybridization could be used with and medium-copy-number sequences. Our observation
that a high percentage of pepper genomic DNA clonessingle-copy probes identified in this study to relate the
genetic map to Capsicum chromosomes. detected repeated sequences also points to repeated
sequences in the pepper genome. Moreover, retro-Genome size, structure, and evolution in the Solana-
ceae: Genome size and content: The 2C DNA content of transposons are well documented in Capsicum (Fla-
vell et al. 1992; Pozueta-Romero et al. 1995; K. Living-pepper is two- to fourfold greater than that of tomato
(Arumuganathan and Earle 1991). We observed that stone, unpublished results). The extra DNA in pepper
relative to tomato cannot all be accounted for by theall tomato clones tested hybridized to pepper DNA and
covered the pepper genetic map. Our results conflict blocks of constitutive heterochromatin (7% of the total
karyotypic length) seen exclusively at the telomeres ofwith Prince et al. (1993), who observed that clones from
regions of tomato chromosomes 1, 2, 6, and 9­12 failed C. annuum chromosomes (Moscone et al. 1993). There-
fore, it is probable that the retrotransposons inter-to hybridize with pepper DNA, perhaps because these
clones were either more diverged from their pepper spersed equally across both the gene-rich and gene-
poor regions of the genome, as seen in the Gramineaehomologs or representative of intergenic sequences
unique to tomato (Ganal et al. 1988). In the case of (Barakat et al. 1997), will account for differences in
nuclear DNA content between pepper and tomato.the former, perhaps different hybridization conditions
in our RFLP analysis revealed these more weakly related Conservation of linkages: Our comparison of the pepper
1199Genome Evolution in the Solanaceae
and tomato genomes demonstrates overwhelmingly the upper arms of T5 and T9 in pepper and potato and
those seen by Caccone et al. (1998) in mosquitoes.conservation of marker order from whole-tomato chro-
In the recent comparison of Arabidopsis and B. nigra,mosome arms, and even entire chromosomes, in pep-
Lagercrantz (1998) reported that interstitial telo-per. There were, however, seemingly random interrup-
meric repeats colocalized with rearrangement break-tions in synteny. These markers may have been what
points. Telomeric sequences have been mapped to theled Tanksley et al. (1988) to conclude that many of
centromeric regions of eight tomato chromosomesthe pepper chromosomes were comprised of many inde-
(Presting et al. 1996), and all but one of the transloca-pendent tomato segments.
tion breakpoints between tomato/potato and pepperOne observation emerging from other comparative
appear at the centromere or putative centromere of thestudies is that these rogue markers seem to be concen-
respective chromosome. Tomato telomeric sequencestrated in centromeric and telomeric regions (Moore et
appear at tomato centromeres, where we believe theal. 1997). This same result is manifest in our comparison
chromosomes have been truncated in pepper (T4 andat the centromeres of P1, P2, P4, P7, P12, T4, T5, T9,
T8); at the centromeres of T5, T9, T11, and T12, whichand T12, and the telomeres of P2, P4, P5, T3, T8, and
are breakpoints; and at the centromeres of T3 and T7,T11. This phenomenon may be a function of the con-
which may or may not be sites of rearrangement. Nocentration of breaks at these sites; however, the specific
telomeric sequences were mapped, however, to themechanisms that account for marker accumulation and
breakpoints that we concluded were unique to tomato,loss at these breakpoints remains unknown. Another
T10 and T11, although this may result from lack ofgeneral mechanism that could possibly explain the ap-
polymorphism or the pericentric inversion we believepearance of nonsyntenous markers is excision via in-
occurred on either T11/P11. These results, therefore,trachromosomal recombination of direct repeats, fol-
support both the observation that centromeres are im-lowed by integration at distant sites. This process has
portant sites for chromosomal rearrangement and thebeen shown to move transgenes to distant sites in the
hypothesis that interstitial telomeric repeats may be agenome of transformed tobacco (Peterhans et al.
critical if not a causal link between centromeres and1990). If retrotransposons, which have been associated
these events.
with duplications and rearrangements in the genome
Three interrelated lines of evidence imply that the
of Saccharomyces cerevisiae (Kim et al. 1998b), acted as
majority of the unplaced chromosomal rearrangements
direct repeats in this process, it is not difficult to see
probably occurred in the pepper lineage. (i) We have
how the present situation could have developed.
observed at least five differences between the parental
Genome rearrangement: Our estimate of the minimum
pepper species that are equal to the number of differ-
number of breaks that differentiate tomato and pepper
ences between potato and tomato (Tanksley et al.
(22) is 7 greater than that reported by Prince et al.
1992); therefore, propensity toward rearrangement may
(1993), but 10 less than that reported by Tanksley et
be an inherent property of the pepper genome, a trend
al. (1988). The probable cause of the differences in
noticed earlier by Lanteri and Pickersgill (1993).
these estimates is the extent of coverage of the tomato
(ii) The increase in the size of the pepper genome,
genome in each study. By looking at the entire tomato
without apparent increases in gene content, implicates
genome as it is represented in pepper, we have been expansion of heterochromatin in this genome. Hetero-
able to both see the larger patterns of genome reorgani- chromatin has been positively correlated with the
zation and refine the estimate of the overall number of amount of rearrangement in a genome (Prokofieva-
events that have occurred since divergence. Belgovskaya 1986). (iii) Retrotransposons probably
This study joins with others that begin to provide make up the bulk of the extra DNA in the pepper
glimpses into the complex nature and mechanisms of genome, and retroelements have been associated with
genome structural rearrangements. Similar to our re- chromosomal rearrangements in plants (Robbins et al.
sults, inversions were also a major contributor to the 1989; Belzile and Yoder 1994), yeast (Kim et al. 1998b),
extensive rearrangement of the Brassica nigra genome mosquitoes (Mathiopoulos et al. 1998), and Drosoph-
relative to Arabidopsis (Lagercrantz 1998). Clues to ila (Engels and Preston 1984; Lim 1988; Lyttle and
the biology underlying these rearrangements include Haymer 1992; Sheen et al. 1993; Eggleston et al. 1996;
this and other studies of intraspecific karyotype diversity Ladeveze et al. 1998; O'Hare et al. 1998).
(Gill et al. 1980; Badaeva et al. 1994) and comparative Segregation distortion factors: Many of the markers
mapping (Moore et al. 1997) that have shown transloca- in our population displayed significant deviations from
tion breakpoints to occur more frequently at centro- their expected Mendelian ratios. While this observation
meres. Although to the best of our knowledge no com- has been made in many interspecific plant populations
parable study has been done for inversions, the (e.g., Zamir and Tadmor 1986), comparisons of the
analogous localization of inversion breakpoints to re- amount and direction of distortion across different gen-
gions of the genome would make similar independent era are limited. We have identified regions that display
consistent segregation distortion both within a genusinversions more likely, such as those we observed in the
1200 K. D. Livingstone et al.
and across genera. Understanding of the loci control- comparisons available across three genera, now stands
as the broadest and most thoroughly characterized com-ling this behavior has important practical applications
for breeders and biological implications for the evolu- parative genetic system in dicotyledonous plants.
tion of these genera. The recent cloning of the Segrega- The authors acknowledge J. Prince, E. Radwanski, J. Jantz, M. Cadle,
tion distorter locus from Drosophila (Merrill et al. 1999) L. Landry, and G. Moriarty for their assistance. We thank Drs. S.
Tanksley for clones and access to unpublished data; B.-D. Kim, U.shows that molecular study of these loci is feasible. Loci
Bonas, M. Massoudi, K. Welch, A. Palloix, and V. Lefebvre for markerswith conserved distortion functionality apparent in mul-
and unpublished data; and N. Weeden for isozyme analyses. We thank
tiple genera would make appropriate initial targets for R. Grube, A. Matern, L. Landry, M. Sorrells, S. Tanksley, and two
molecular characterization in plants. anonymous reviewers for critical reading and suggestions that im-
Genome size, genetic length, and implications for proved the manuscript. K.D.L. and J.R.B. were supported in part by
a Department of Energy/National Science Foundation/United Statesrecombination: The lengths of the tomato and pepper
Department of Agriculture grant to the Research Training Groupgenetic maps are almost identical: 1275 cM in tomato
in Molecular Mechanisms of Plant Processes and in part by Marie
vs. 1246 cM in pepper. Figures 2 and 3 illustrate that
Lavallard. Financial and material support was provided by Seminis
most of the intervals between adjacent syntenous mark- Vegetable Seeds, the California Pepper Commission/California Pep-
ers are approximately equal in pepper and tomato de- per Improvement Foundation, Gilroy Foods, Mr. C. Werly, USDA
NRICGP awards 91-37300-6564 and 94-37300-0333, and BARD awardspite comparisons of dual interspecific maps. The simi-
IS-2389-94.lar lengths of the genetic maps, together with the
difference in DNA content, indicate that the average
recombination rate per unit of physical distance is not
the same in pepper and tomato. This is what would be LITERATURE CITED
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