Download A Fine Physical Map of Arabidopsis thaliana Chromosome 5

DNA RESEARCH 4, 371-378 (1997)
A Fine Physical Map of Arabidopsis thaliana Chromosome 5:
Construction of a Sequence-ready Contig Map
Hirokazu KOTANI,1'* Shusei SATO,1 Masanobu FUKAMI, 2 Tsutomu HOSOUCHI,1 Naomi NAKAZAKI,1
Satomi OKUMURA,1 Tsuyuko WADA, 1 You-Guang Liu,3 Daisuke SHIBATA,3 and Satoshi TABATA1
Kazusa DNA Research Institute, 1532-3 Yana, Kisarazu, Chiba 292, Japan,1 Chiba Prefectural Agricultural
Experimental Station, Midori-ku, Chiba 266, Japan,2 and Mitsui Plant Biotechnology Research Institute,
TCI D-21, Sengen 2-1-6, Tsukuba, Ibaraki 305, Japan3
(Received 25 November 1997)
Abstract
A fine physical map of Arabidopsis thaliana chromosome 5 was constructed by ordering the clones from
YAC, PI, TAC and BAC libraries of the genome using the sequences of a variety of genetic and EST
markers and terminal sequences of clones. The markers used were 88 genetic markers, 13 EST markers, 87
YAC end probes, 100 YAC subclone end probes, and 390 end probes of PI, TAC and BAC clones. The
entire genome of chromosome 5, except for the centromeric and telomeric regions, was covered by two large
contigs 11.6 Mb and 14.2 Mb long separated by the centromeric region. The minimum tiling path of the
chromosome was constituted by a total of 430 PI, TAC and BAC clones. The map information is available
at the Web site http://www.kazusa.or.jp/arabi/.
Key words: Arabidopsis thaliana chromosome 5; physical map; contig map
accurate physical map as well as a sequence-ready contig map which covers the entire chromosome is essential
Arabidopsis thaliana has been adopted as an excel- to proceed with the sequencing project. In this paper, a
lent model organism for genetic, developmental and fine physical map of the entire chromosome 5 was conmetabolic studies of higher plants due to its short life structed by ordering the clones from YAC, PI, TAC and
cycle. This plant has recently been targeted for se- BAC libraries using the information on the sequences of
quencing of its entire genome because of its smaller various genetic and EST (expression sequence tag) markgenome size (approximately 120 Mb) and its lower fre- ers, terminal sequences of clones and subclones.
quency of repetitive sequences. Highly and moderately
repetitive DNA sequences have each been estimated to
2. Materials and Methods
share around 10% of the total genome.1'2 Although
3
4
genetic linkage and recombinant inbred (RI) maps
2.1. Libraries
(http://nasc.nott.ac.uk/new_ri_map.html) have been reFive kinds of libraries constructed from the genome
ported, the construction of accurate physical maps of
of
A. thaliana ecotype Columbia were used for the conthe chromosomes should be highly advantageous not only
of the map: CIC YAC12 from Arabidopsis
struction
for the genomic sequencing, but also for map-based gene
cloning.5"7 Based on this view, yeast artificial chromo- Biological Resource Center at Ohio State University,
some (YAC)-based physical maps of chromosomes 28 and IGF BAC (Mozo, T. unpublished, http://194.94.225.1
and TAMU
49 of A. thaliana have recently been constructed. We /private_workgroups/pg_101/bac.html),
13
BAC
libraries
from
Dr.
Ian
Bancroft
at
John Innes
have focused our attention on sequencing chromosome 5,
14
and
TAC
(Liu,
Y.-G.,
manuscript
in
Centre,
and
PI
consistent with the international agreement of the Ara10
preparation)
libraries
from
Mitsui
Plant
Biotechnology
bidopsis Genome Initiative. Even though the progress
of YAC ordering, which consists of 31 contigs of chro- Research Institute. The genomic coverage of these limosome 5, has been reported,11 the construction of an braries has been estimated to be equivalent to 3-10 times
the genomic size.
1.
*
t
Introduction
Communicated by Mituru Takanami
To whom correspondence should be addressed. Tel. +81-43852-3920, Fax. +81-438-52-3921, E-mail: [email protected]
The nucleotide sequence data of MUB10-Sp6 will appear in
the DDBJ, EMBL and GenBank nucleotide sequence databases
under accession number AB008800.
2.2. DNA markers and PCR primers
RFLP (restriction fragment length polymorphism)
markers, expression sequence tags (EST) markers,
A Fine Physical Map of Arabidopsis thaliana Chromosome 5
372
[Vol. 4,
Table 1. DNA markers used in this work.
Categoly
RFLP markers
EST Markers
CAPS Markers
SSLP Markers
Cloned Genes
Markers
g3715, m447, m217, g3837, m224, pCIT1243, tt4,
g5962, pCIT718, g4560, g4111, g6843, KG-8, KG-10,
GRF3, m423, m442, cral, m331, m435, g4130, m558,
g3844, g2455, m211, pCITdllO, g2368, CD3-42
1, mi97, miP5-3, mil74, mi322, mi438, mil38,
mi90, mi433, mi219, mil25, mil37, mil94, mi83, mi61,
miP5-8, mi69, mi70, mil84, mi335, mi323
T04154, T04657, T13673, T88208, T13672, T21894,
T14190, T04366, T04492, R65089, T22529, T21228
T20526
CTR1, PAI2, ASA1, PAT1, CHS1, NIT4, PHYC,
DFR, 17C2, 10A10, EG7F2, ASB2, LYF3
nga225, ngal51, ngalO6, ngal39, S0262, ngal58
pCA72, nga76, S0191, ngal29, CDPK9, nga249
HANKA
PDC1 (U71121), PDC2 (U71122), UBQ3 (L5363),15
GLU1 (Y09667), AGL15 (U22528), GDH1 (U37771),
ASP2 (U15033),16 TSB1 (M23872),17 AGL8 (U33473),
GAS1 (U03773).18 BEL1 (U39944),19 CER3 (X95962)20
PAP1 (U48448)
cleaved amplified polymorphic sequence (CAPS) markers, simple sequence length polymorphism (SSLP) and
genes used for designation of polymerase chain reaction
(PCR) primers and their sources are given in Table 1.
Resouces
Arabidopsis Biological Resource
Center (Columbus, Ohaio)
Mitsui Plant Biotechnology
Research Institute (Tsukuba, Ibaraki)
http://genome-www.stanford.edu
/Arabidopsis/EST2CIC.html
http://genome-www.stanford.edu
/Arabidopsis/maps/C APS_Chr5.html
http://cbil.humgen.upenn.edu/~atgc/
genetic-mapping/gen_maps.html
Sequence Data are derived from the
DDBJ, EMBL and GenBank.
Accession numbers are indicated in
parentheses
probes, we isolated 109 YAC clones, 1130 PI clones, 748
TAC clones, and 130 BAC clones. By ordering the overlapping clones using PCR products which were amplified
with primers designed from the end sequences of isolated
clones, the physical map of chromosome 5 of A. thaliana
was
finally constructed (Fig. 1). As discussed in sec2.3. Screening and clone analysis
tion
3.3, we tentatively postulated the gap sizes to be
To construct a physical map by clone ordering, PCR
0.4
Mb,
and in Fig. 1, the physical distance of the chroscreening of DNA pools was done to identify positive
mosome
is indicated by the number in of megabase pairs
clones harbored in YAC, PI and TAC libraries. If posifrom
the
end of contig 1 containing the top marker of
tive clones were not selected in the PI and TAC libraries,
chromosome
5. YAC clones formed 11 contigs, and 9
the IGF and TAMU BAC libraries were screened. End seout
of
10
gaps
of the YAC contigs were closed by assigquences of positive clones were determined by amplification with cassette-ligated PCR21 followed by sequencing ment of PI, TAC and BAC clones. Finally, the physical
with dye terminator cycle sequencing kit FS or dRho- map consisted of two contigs covering 11.6 Mb (contig
damine dye terminator cycle sequencing kit (Perkin- 1) and 14.2 Mb (contig 2) of the chromosome 5 genome,
Elmer-ABI, Foster City, CA). The primers designed from respectively. Since the identity of the overlapping regions
the end sequences of positive clones were used to confirm among YAC clones was confirmed using PCR products
the overlap between clones and also to select clones in amplified with the primers designed from the end regions
libraries for genome walking. YAC subclones were pre- of the corresponding PI, TAC or BAC clones, we assume
pared as follows; DNA fragments in YAC clones were iso- the estimation error for the contig sizes to be less than
lated by PFG electrophoresis (CHEF Mapper, Bio-Rad, 5%. The total size of the two contigs becomes approxiCA), digested with Bglll or EcoT22I (TAKARA, Kyoto) mately 25.8 Mb. As described below, the genetic distance
and ligated into pUCH8. After transformation, the se- between PDC3 and nga76 in contigl is 71.56 cM and the
quences of YAC subclones were determined. Sequence physical distance is 11.0 Mb, so that contig 1 could cover
data of ends and subclones were subjected to homology a region of about 75 cM. Also, the genetic distance besearch by the BLAST and FASTA software (GCG, Madi- tween PHYC (74.35 cM) and CD3-42 (135.21 cM) corresponds to 13.4 Mb, so that contig 2 could cover about
son, WI)
64 cM. Therefore, the 25.8-Mb region of the two contigs
cover a minimum of 139 cM which corresponds to more
3. Results and Discussion
than 95% of chromosome 5 (140.23 cM). A minimal tiling
path is constituted by 430 bacterial clones, as shown in
3.1. Construction of physical map
Fig. 1. These clones should be suitable for the genomic
Using the PCR primers from 88 genetically mapped sequencing of chromosome 5 22 ' 23 as well as for positional
markers, 13 EST markers, 87 YAC end probes, 100 YAC cloning of genes. As a result of a BLAST search of the
subclone probes, and 390 of PI, TAC and BAC end
3
i hi
12
10
I
;!
II 11
14
20
22
24
Figure 1. The physical map of A. thaliana chromosome 5. The chromosome is covered by two large contigs (contig 1; blue bar, contig 2; green bar) of clones split by a gap
presumably containing the centromere. The scale on the abscissa indicates the distance in megabase pairs from the end of contigl containing the top genetic marker of
chromosome 5. Eighty-five genetic markers and 13 EST markers (vertically black letters) and 87 YAC end markers (vertically red letters) were assigned on the map by the
PCR method using the clones from YAC, P I , TAC and BAC libraries. PDC3 and CERX (vertically green letters) are described in the text. Name and size of CIC YAC clones
are indicated in wide open boxes and the chimeric YAC clones are shown by yellow boxes. Bacterial clones constituting the minimum tiling path are shown by open boxes
(PI and TAC clones) and closed boxes (IGF and TAMU BAC clones) below the wide YAC boxes. The names of bacterial clones are indicated at the right side of boxes as PI
(M—), TAC (K—), IGF BAC (F—) and TAMU BAC (T—). The red striped box shows the gap region. The vertically blue letters show the accession numbers of A. thaliana
genes mapped on chromosome 5 by BLAST search using the end sequences of bacterial clones and subclone sequences of YAC clones.
26
No. 6]
H. Kotani et al.
Table 2. Genes of Arabidopsis thaliana mapped on chromosome 5.
Accession
No.
X94248
X77199
U73526
U03990
U40566
X71787
U02565
X92393
AF014806
Y14199
Z68495
M55551
AF001415
U1651
Z49268
Z86095
M84698
Z15058
U33014
X70990
L23985
X99923
X79195
AB005889
U88087
U91414
S69727
U75194
U39782
L19354
D89342
U24177
U87794
U12126
D17582
U78866
X83380
D13044
X52629
U29699
Z34294
D21138
L16789
Z22596
X97323
S77849
U11254
Y08966
J04737
X90458
Z49859
U33757
X16432
X06477
Z18242
D86122
M84701
X99097
U18411
L29261
L40358
Y13180
Clone'
MJE20T7
MHD9T7
MNC9SP6
MAN10SP6
MJP2SP6
MEO23T7
MYB9SP6
C7A7ET3F
MZH1T7
K18J7L
K21P8R
K21N7L
F2A6SP6
K6E24L
K15A21L
MQE23SP6
K14P17R
K19B10R
K13O21L
K13O21R
K17E15L
K20K6L
F12J1SP6
MJG5T7
C6D8BG7A
C11F1LET6H
MZD3T7
MKH4T7
MHK7T7
MPK23SP6
K11D4R
K3J11L
MSN3T7
MNI3T7
MWB16T7
K22K2R
MIC6T7
C11F10BG5B
MIM11T7
MPM10T7
MRK3T7
MRB17T7
K5P14
MTE17
MZI11SP6
MYN21T7
K16J12
MPL14
MNB21SP6
MZF3T7
MOM7T7
MTFi3T7
C9A1E12D
MVE14SP6
K22G18L
MVF19SP6
MQB2T7
MZL20SP6
K11D18L
MPA24T7
MUB2SP6
K1L20L
Map position
(Mb)
0.3
0.6
0.9
1.9
2.2
3.0
3.43.7
3.8
3.9
4.5
5.4
5.5
5.9
5.9
6.9
7.2
7.2
7.4
7.5
7.6
7.9
9.5
9.9
10.0
12.3
12.7
14.4
15.2
15.4
15.7
17.6
18.7
19.0
19.7
19.9
20.0
20.3
20.9
21.0
21.1
21.2
21.3
21.5
21.6
21.8
22.0
22.2
22.3
23.0
23.1
2X2
23.5
23.9
24.0
24.1
24.3
24.7
25.3
25.4
25.5
25.6
a) See Fig. 1 legend. C— show YAC subclones
Score
Description
1095 A. thaliana mRNA for ferritin.
1121 A. thaliana hsc70-1 gene.
3000 A. thaliana B' regulatory subunlt of PP2A (AtB'alpha) mRNA
""36ro""""A7th^liar«Columbi7gamm
2346 A. thaliana ubiquiBn activating enzyme 2 (UBA2) gene
1264 A. thaliana AAP2 mRNA (or amino ackJ permease.
1076 A. thaliana Columbia 14-3-3-like protein 1 (AMI) mRNA
1517 A. thaliana mRNA for KNAT4 homeobox protein
1885 A. thaliana alpha-gjucosidase 1 (Aglui) gene
791 A. thaliana mRNA for MAP3K delta-1 protein kinase
2303 A. thaliana CHLH gene.
385
A. thaliana transcription factor (AGL2) mRNA
3332 A. thaliana 14-3-3-like protein GF14j>hi (GRF5)
510 A. thaliana syntaxln homologue mRNA
825 A. thaliana P2 mRNA for zeta-crystallin-like protein
512 A. thaliana mRNA for peptkfyl-prolyl cis-trans Isomerase
2487 A. thaliana alpha-5 tubulin (TUA5) gene
1276 A.thaliana of bcb gene encoding blue copper-binding protein
2592
A. thaliana polyubiquitin (ubq4) gene
1865
582
1051
2224
1275
1539
2878
915
710
778
1315
2170
774
2147
1428
690
2624
515
1209
3332
584
736
956
2500
1191
1312
711
676
2591
2704
2926
2716
A. thaliana gene for sucrose synthase
A. thaliana protein kinase (TOUSLED) mRNA
A. thaliana mRNA for male sterility 2-like protein
A. thaliana TGG2 gene for myrosinase.
A. thaliana mRNA for ATMYB4
A. thaliana LON protease homolog (LON_ARA) mRNA
A. thaliana heteromeric acetyl-CoA carboxylase biotin carboxylase subunit (CAC2) gene
A. thaliana light-regulated glutamine synthetase isoenzyme
A. thaliana germin-like protein (GLP6) mRNA
A. thaliana lysine and histidine specific transporter mRNA
A. thaliana ubkjuitin conjugating enzyme (UBC4) gene
A. thaliana DNA for luminal binding protein
A. thaliana 3-ketoacyl-acyl carrier protein synthase I JKAS I) mRNA
A. thaliana transcription factor inhibitor I kappa B homologjnimiJ gene
A. thaliana clone SRP-54B signal recognition particle 54 kDa subunit (Srp-54) gene
A. thaliana mRNA for ERD1 protein
A. thaliana putative arginine-aspartate-rtch RNA binding protein genes
A.thaliana mRNA for gibberellin 20-oxidase
A. thaliana rd29A gene and rd29B gene
A.thaliana gene for USB small nuclear RNA (snRNA)
A. thaliana light-dependent NADPH:protochlorophyllide oxidoreductase A (PorA) mRNA
A. thaliana (C1A) myosin heavy chain mRNA
A. thaliana katC mRNA for heavy chain of kinesirvlike protein
A. thaliana small Ras-like GTP-binding protein (Ran-1) mRNA
A. thaliana protein phosphatase mRNA
A.thaliana mRNA for outward rectifying potassium channel KCO1
HSP81 -3=heat-shock Protein [Arabidopsis thaliana=thale-cress, Genomic, 3094 ntj.
A. thaliana Columbia eootype metallothioneiri (MT1 b) gene
A. thaliana gene encoding ABI2 protein
A. thaliana ATPase gene
A. thaliana mRNA for cytochrome P450
A.thaliana mRNA for copper transporterprotein
1174
A"thaiiana ubiquran1 conjugating enzyme i E ^ i i i c ^ g e m
923
1266
2931
1226
2196
658
567
3266
1368
745
A. thaliana EF-1 alpha-A4 (NAEEFTU 4) gene
A. thaliana U2 RNA gene (U2.7)
A. thaliana calnexin homolog
A. thaliana mRNA for Mei2-like protein
A. thaliana bete-3 tubulin (TUB3) gene
A. thaliana mRNA for peroxkjase ATP15a
A. thaliana IAA9 (IAA9) gene
A. thaliana 1 -amino-1 -cyclopropanecarboxylate synthase (ACS5) mRNA
A. thaliana calmodulin-binding protein mRNA
A. thaliana mRNA for proteasome subunit proSc
375
A Fine Physical Map of Arabidopsis thaliana Chromosome 5
[Vol. 4,
the order of genetic markers well coincides with that of
the physical map, but the ratio of physical and genetic
distances between markers varied significantly along the
chromosome. Within the range of this resolution, relatively cold spots of recombination are seen in the middle region of each contig (nga249 to g4560 and mi69 to
LYF3). This pattern resembles that of chromosome 4
of A. thaliana, but contrasts with that of tomato and
wheat chromosomes in which recombination is strongly
suppressed over large intervals at the centromere; rather,
maximum recombination occur in the proximal regions.9
The average values observed for contigs 1 and 2 are 154
Kb/cM and 209 Kb/cM, respectively. This difference
may reflect the number and distribution of hot spots
in each contig. In the classic genetic map,3 CER3 was
mapped near the LYF3 marker which was mapped to
the 24-Mb position of the physical map. However, the
cloned gene (Accession No. X95962) reported as CER322
was mapped to the 0.5-Mb position of the physical map.
According to the sequence data of one of the YAC subclones derived from CIC2B9, the sequence was identical
to that of X95962. It is likely that the cloned CER3 gene
may be one of the unmapped eceriferum genes in addition
to CER1-8 : This gene is indicated as CERX in Fig. 1.
Physical
map
Rl map
Figure 2. The alignment of the physical and RI maps of chromosome 5 and the ratio of the physical (kb) and genetic (cM)
scales along the RI map. Fifty-three out of 54 markers which
have been mapped on the RI map were assigned on the physical
map according to Fig. 1. The gray boxes separated by an open
box at the left represent two contigs and the gap consisting the
physical map (Mb) and the shaded box at the middle shows
the RI map (cM). The ratio of the physical scale (kb) to the
genetic scale (cM) was calculated from the physical and genetic
distances. The average values for contigs 1 and 2 are indicated
by vertical broken lines.
end sequences used for contig construction, 62 genes indicated in Table 2 were mapped on chromosome 5, as
shown in Fig. 1.
3.2. Comparison of genetic and physical maps
A comparison of genetic and physical maps is shown
in Fig. 2. Fifty-four of the genetic distances have been
derived from up to 100 lines of a recombinant inbred mapping population.4 Therefore, the two maps can be compared directly. Except for the markers mi90 and GRF3,
In the RI map, PDC1 has been assigned as the top
marker of chromosome 5. Using the sequence of the
PDC1 gene registered in DNA databases (Accession No.
U71121), we isolated two YAC clones (CIC11D9 and
CIC6A9) and several PI and TAC clones. However,
clones CIC11D9 and CIC6A9 have already been mapped
on contig IV of chromosome 4.9 A PI clone, MJO17, containing the PDC1 gene also has the ATH1 gene24 which
is used as a characterization marker of chromosome 4
and has also been mapped on CIC11D9 and CIC6A9.9
Therefore, we concluded that the PDC1 gene is located
on chromosome 4 near the ATH1 locus. In a BLAST
search of the end sequences of PI and TAC clones, the
end sequence (Accession No. AB008800) of the Sp6 side
of MUB10, which is mapped on the left end of CIC2B9,
has a high similarity for the PDC1 gene. So, we concluded the top end (0 cM) of the RI map of chromosome
5 was the Sp6 side of MUB10 and is termed PDC3 (see
Fig. 1). STL has been assigned as the bottom marker
of the chromosome 5 RI map,4 but we did not succeed
so far in isolating clones containing the STL marker because of the lack of a suitable probe. It is necessary to fill
in the gap presumably encompassing the centromere and
the telomeric 5-cM region between CD3-42 and STL for
the complete coverage of the genetic map of chromosome
5.
3.3. Comparison of cytogenetic and physical maps
Due to the lack of suitable genetic markers, the centromere was not mapped on the physical map in the
present study. It seems likely, however, that the cen-
No. 6]
H. Kotani et al.
tromeric region of chromosome 5 should be positiond in
the gap region between contigs 1 and 2, because any end
sequences of mapped clones did not contain the sequences
similar to the tandemly repeated 180-bp sequence contained in plasmid pALl. 25 This repeated DNA sequence
is present in arrays of over 50 kb, has been shown to
locate in the heterochromatin moiety surrounding the
centromere26'27 and to hybridize equally to both sides
of the centromere on all five chromosome pairs.28 Thus,
we assume that the centromere is present in the gap between the two contigs. So far now, this gap could not be
closed due to the absence of YACs containing end probes
of contigs in the YAC library. Such repetitive sequences
in yeast cells have been reported to be unstable,12'28 and
this may account for the difficulty isolating YAC clones
covering the centromere.
The genetic distance between nga76 and PHYC containing the gap is only 2.8 cM and 1.3 Mb of that region
has already been covered. Since the average value estimated from the two contigs is 0.18 Mb/cM, we assume
that the gap region is a few hundred kilo bases unless recombination is strongly suppressed at the gap. The physical distances of telomeres to the ends of contigs have also
not been estimated. For the construction of the complete
physical map, we have been continuing genomic walking
using various libraries.
Acknowledgments: We are grateful to Drs. S. Choi
and R. Wing of Texas A & M University, T. Altman of
Max-Plank Institute and I. Bancroft of John Innes Centre for providing the TAMU and IGF BAC libraries. We
thank E. Mitsui for her excellent technical assistance and
Dr. T. Hashimoto (Nara Institute of Science and Technology) for providing unpublished informations about the
ordering of mi69-mi70 region. This work was supported
by the Kazusa DNA Research Institute Foundation. We
also thank M. Takanami for his support and encouragement to perform this work.
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