Download Linear Dominance Relationship among Four Class

Plant Cell Physiol. 44(1): 70–75 (2003)
JSPP © 2003
Linear Dominance Relationship among Four Class-II S Haplotypes in Pollen
is Determined by the Expression of SP11 in Brassica Self-Incompatibility
Tomohiro Kakizaki 1, Yoshinobu Takada 1, Akiko Ito
Akira Isogai 3 and Masao Watanabe 1, 5
1, 4
, Go Suzuki 2, Hiroshi Shiba 3, Seiji Takayama 3,
1
Faculty of Agriculture, Iwate University, Morioka, 020-8550 Japan
Division of Natural Science, Osaka Kyoiku University, Kashiwara, 582-8582 Japan
3
Graduate School of Biological Sciences, Nara Institute of Science and Technology, Ikoma, 630-0101 Japan
2
;
phenotype, usually a mutant phenotype. By using recent molecular techniques, two of Mendel’s genes have been identified
(Bhattacharyya et al. 1990, Lester et al. 1997). In the case of
the recessive allele on the R (rugosus) locus, there was a transposon-like insertion in a gene encoding a starch-branching
enzyme, resulting in a wrinkled-seed character (Bhattacharyya
et al. 1990). To date, dominant/recessive alleles have been isolated and characterized for many genes related to several phenomena in various plant species (Glazebrook 1999, Szymanski
et al. 2000, Theisen 2001).
The biological phenomena regulated by multiple alleles at
a single locus are not frequently observed. The major histocompatibility complex (MHC) in mammals and self-incompatibility (SI) in plants are two good examples; both are involved
in distinguishing self and non-self (Bateman 1955, Parham et
al. 1995). In the case of MHC, two parental alleles are co-dominantly expressed, as it is generally assumed that most mammalian genes are transcribed from both alleles. In contrast, in the
sporophytic SI, the phenotypes of heterozygotes are influenced
by dominance relationships between alleles: when self-pollen
is rejected at the stigma surface, SI phenotypes of both pollen
and stigma are determined by dominant S alleles in the heterozygotes. The dominant-recessive allelic interactions of the SI
phenotype are complex, and include linear dominance relationships in Brassica and Ipomoea species, which possess the sporophytic SI system (Hatakeyama et al. 1998, Kowyama et al.
1994, Thompson and Taylor 1966). In the case of Brassica SI
system, both dominant and recessive alleles at the S locus
encode functional proteins in the pollen and stigma, respectively (Shiba et al. 2002, Takayama et al. 2000, Watanabe et al.
1994, Yamakawa et al. 1995). However, in the case of a twoallele locus (e.g. Mendel’s genes), the recessive allele encodes
a mutated protein, as described above (Bhattacharyya et al.
1990, Lester et al. 1997). This characteristic of recessive S alleles in the multiallelic S locus is apparently different from that
of the two-allele locus.
To date, three polymorphic SI genes have been identified
at the S locus of Brassica species. The allele is therefore considered as a haplotype. The SRK (S receptor kinase) gene and
SP11/SCR (S locus protein 11/S locus cysteine-rich protein)
gene determine the S specificity of the stigma (Takasaki et al.
Self-incompatibility (SI) prevents self-fertilization by
rejecting pollen from plants with the same S phenotype.
The Brassica SI system is controlled sporophytically by
multiple alleles at the single locus, S, and dominance relationships among S haplotypes are observed in both stigma
and pollen. We have identified previously five different
class-II S haplotypes in Brassica campestris. Here, we performed test-crosses between S heterozygotes and their
respective parental S homozygotes for four of these class-II
S haplotypes, and observed a linear dominance relationship on the pollen side. To determine how this relationship
is controlled, we performed RNA gel blot analyses for six S
heterozygotes and their respective parental S homozygotes
using the corresponding SP11 clone as a probe. In all six S
heterozygotes, SP11 derived from a dominant haplotype
was predominantly expressed, and SP11 derived from a
recessive haplotype was repressed. Thus, the linear dominance relationship of the SI phenotype on the pollen side is
regulated by the expression of SP11.
Keywords: Brassica campestris (syn. rapa) — Linear dominance relationship — Monoallelic expression — S multiple
alleles — Self-incompatibility — SP11.
Abbreviations: MHC, major histocompatibility complex; NOR,
nucleolus organizer region; SCR, S locus cysteine-rich protein; SI,
self-incompatibility; SLG, S locus glycoprotein; SP11, S locus protein
11; SRK, S receptor kinase.
Introduction
The laws of inheritance were originally established by
Gregor Mendel in breeding experiments with the garden pea
(Mendel 1866). Based on these laws, in heterozygous plants
with a dominant allele and a recessive allele at the same
locus, the character of the dominant allele appears as a phenotype, whereas the character of the recessive allele disappears.
Not surprisingly, in homozygous plants with two recessive
alleles, the character of the recessive allele appears as a
4
5
Current address: Iwate Biotechnology Research Center, Kitakami, 024-0003 Japan.
Corresponding author: E-mail, [email protected]; Fax, +81-(0)19-621-6177.
70
Linear dominance relationship in S haplotypes
71
Fig. 1 Test pollination for determination of dominance relationships among four class-II S haplotypes and RNA gel blot analysis of six S heterozygotes possessing class-II S haplotypes. (A) Pollen grains from each S heterozygote were used to pollinate its parental S homozygotes to determine the dominance relationships in pollen. +, Compatible; –, incompatible. (B) One microgram of poly(A)+ RNA isolated from anthers of each
plant was loaded in each lane. Each blot was hybridized with digoxigenin (DIG)-labeled probes indicated above each panel. Each blot was reprobed with the vascular H+-ATPase genomic fragment from B. campestris (V-ATP), and the results are presented below each panel. 29, S29
homozygote, 40, S40 homozygote; 44, S44 homozygote, 60, S60 homozygote; 29/40, S29S40 heterozygote; 29/44, S29S44 heterozygote; 29/60, S29S60
heterozygote; 40/44, S40S44 heterozygote; 40/60, S40S60 heterozygote; 44/60, S44S60 heterozygote.
2000) and the pollen (Schopfer et al. 1999, Shiba et al. 2001,
Shiba et al. 2002, Suzuki et al. 1999, Takayama et al. 2000),
respectively. The SLG (S locus glycoprotein) enhances the SI
recognition reaction (Takasaki et al. 2000), perhaps by stabilizing SRK (Dixit et al. 2000). Recent biochemical analysis has
suggested that SP11/SCR functions as a sole ligand to activate
72
Linear dominance relationship in S haplotypes
its cognate SRK specifically (Takayama et al. 2001). Based on
the sequence diversity of the SI genes, S haplotypes are
classified into class I and class II; the amino acid sequence
similarity of SLG and SRK is about 65% between classes and
80–90% within classes (Watanabe et al. 2001). Interestingly,
class-I S haplotypes are dominant over class-II ones in the
dominance relationships on the pollen side (Hatakeyama et al.
1998, Nasrallah and Nasrallah 1993, Thompson and Taylor
1966). Recently, RNA gel blot and in situ hybridization experiments of SP11 in the S heterozygotes having a pair of class-I
and class-II S haplotypes have shown that the expression of the
class-II SP11 was suppressed in the S heterozygote, suggesting
that the dominance relationships between class-I and class-II S
haplotypes on the pollen side are determined by the expression
level of SP11 (Shiba et al. 2002). Similar results were obtained
in another cruciferous SI species, Arabidopsis lyrata (Kusaba
et al. 2002). In the case of stigma SI phenotype, the crosspollination experiments using SRK-introduced transgenic
Brassica species showed that the dominance relationships are
determined by SRK itself, and not as a result of its relative
transcription level (Hatakeyama et al. 2001).
In this study, we determined the dominance relationships
among four class-II S haplotypes (S29, S40, S44 and S60) by using
test pollination, and found a linear dominance relationship
among them on the pollen side. We surveyed the expression of
SP11 in six S heterozygotes with different combinations of
these four S haplotypes, as well as in their respective parental S
homozygotes. We found that the linear dominance relationship
of the SI phenotype on the pollen side was regulated by the
expression of SP11.
Results
Determination of dominance relationships among class-II S
haplotypes
In B. campestris (syn. rapa), only five class-II S
haplotypes have been identified. We chose four of these five S
haplotypes, S29, S40, S44 and S60 (Hatakeyama et al. 1998,
Hatakeyama et al. 2001, Shiba et al. 2002, Takasaki et al.
1999), to study the dominance relationships on the pollen side
among class-II S haplotypes, because the SP11 genes of these
four S haplotypes had been well characterized (Shiba et al.
2002). Pollen grains from an S heterozygote were used to pollinate its parental S homozygotes to determine the dominance
relationships between the pair of S haplotypes on the pollen
side (Fig. 1A). All the S heterozygous plants tested were selfincompatible (data not shown). On the pollen side, the S44 haplotype was dominant over S29, S40 and S60; the S60 haplotype
was dominant over S29 and S40; the S40 haplotype was dominant over S29 (Fig. 1A). Thus, a linear dominance relationship
(S44>S60>S40>S29) was observed in the pollen. In this linear relationship, S44 is always dominant over the other three S haplotypes, and S29 is always recessive to the others. However, S40
and S60 are dominant in some cases, but recessive in other
cases: the dominance relationships for these two S haplotypes
are thus affected by the other S haplotype present in an S heterozygote.
Expression of SP11 in S heterozygotes carrying class-II S haplotypes
These four class-II S haplotypes studied here (S29, S40, S44
and S60) had been shown to be genetically recessive to class-I S
haplotypes on the pollen side (Hatakeyama et al. 1998,
Hatakeyama et al. 2001). However, there was no investigation
for the expression of S29-SP11 or S44-SP11 in anthers of class-I
and class-II S heterozygotes. We performed RNA gel blot analysis in two different combinations of class-I and class-II S haplotypes; S9S29 and S9S44 (Fig. 2A, C). Transcripts of S29-SP11
and S44-SP11 were not detected in anthers of the S9S29 and S9S44
heterozygotes, respectively, whereas S9-SP11 was normally
expressed in both heterozygotes, and both S29-SP11 and S44SP11 were normally expressed in homozygotes. In addition, the
same phenomenon was also observed in two other combinations of class-I and class-II S haplotypes, S9S40 and S9S60 (Fig.
2B, D), showing that expression of the four class-II SP11s in
anthers of class-I and class-II S heterozygotes was suppressed
at the mRNA level without exception; these results were consistent with the previous report of two other S heterozygotes
(S52S60 and S35S40; Shiba et al. 2002).
In order to determine what mechanisms regulate the linear dominance relationship among the four class-II S haplotypes (S29, S40, S44 and S60) on the pollen side, we surveyed
SP11 expression in all six combinations of S heterozygotes by
using RNA gel blot analysis (Fig. 1B). We carefully determined the washing conditions to reduce cross-hybridization
between S29-SP11, S40-SP11, S44-SP11 and S60-SP11 (see
Materials and Methods), because sequence similarity of SP11
within class II is much higher than that between class I and
class II (Shiba et al. 2002).
In all three S heterozygotes with the S44 haplotype (S29S44,
40 44
S S and S44S60), S44-SP11 was expressed, but the expression
of SP11 of the other haplotypes was dramatically suppressed
(Fig. 1B), in agreement with the dominance of S44 over S29, S40
and S60 in pollen (Fig. 1A). Similarly, in two S heterozygotes,
S29S60 and S40S60, only S60-SP11 was expressed (Fig. 1B), consistent with the dominance of S60 over S40 and S29 in pollen
(Fig. 1A). In the S29S40 plant, S40-SP11 was expressed, but not
S29-SP11 (Fig. 1B). Thus, the linear dominance relationship
among the class-II S haplotypes was perfectly correlated with
the expression of the SP11 genes in anthers, as demonstrated in
the case of S heterozygotes having class-I and class-II S haplotypes (in this study; also see Shiba et al. 2002).
Discussion
We showed previously that SP11 of the class-I S haplotype
was predominantly expressed, and that SP11 of the class-II S
haplotype was suppressed at the mRNA level in each of two S
Linear dominance relationship in S haplotypes
73
Fig. 2 RNA gel blot analysis of four S heterozygotes each possessing a class-I and a class-II S haplotypes. One microgram of poly(A)+ RNA
isolated from anthers of each plant was loaded in each lane. Each blot was hybridized with DIG-labeled probes indicated above each panel (A–D).
Each blot was reprobed with V-ATP, and the results are presented below each panel. 9, S9 homozygote; 29, S29 homozygote; 40, S40 homozygote,
44, S44 homozygote, 60, S60 homozygote; 9/29, S9S29 heterozygote; 9/40, S9S40 heterozygote; 9/44, S9S44 heterozygote, 9/60, S9S60 heterozygote.
heterozygotes that carried a class-I and a class-II S haplotype
(S52S60 and S35S40; Shiba et al. 2002). In the present study, we
analyzed an additional four such S heterozygotes (S9S29, S9S40,
S9S44 and S9S60), and showed that the transcripts of all four
class-II SP11 were dramatically reduced in their respective S
heterozygotes. These results suggested that the correlation
between the sequence diversity of class-I/class-II and dominance/recessiveness in pollen SI phenotype was due to the
difference in the amounts of transcripts of class-I SP11 and
class-II SP11 in the S heterozygotes. The suppression of classII SP11 must have resulted in the recessive SI phenotype of the
class-II S haplotype on the pollen side. From this viewpoint,
one can infer that the general dominance relationships in the
pollen SI phenotype are also regulated by the expression of
SP11 genes at the mRNA level, although that is not the case for
the expression of SRK in the stigma SI phenotype (Hatakeyama
et al. 2001). To clarify the hypothesis, we performed RNA gel
blot analysis for S heterozygotes of four class-II S haplotypes,
which showed a linear dominance relationship. Our results
clearly supported the hypothesis that in all six combinations of
the S heterozygous plants, the SP11 of the dominant S haplotype was predominantly expressed, while transcripts of the
recessive SP11 were not detected in anthers. This is the first
report demonstrating that the linear dominance relationships in
pollen are regulated by the suppression of recessive S haplotypes.
In the linear dominance relationship in pollen
(S44>S60>S40>S29) examined in this study, S44 was dominant
over all the three other S haplotypes, and S29 was recessive to
all the other three S haplotypes. Interestingly, S40 and S60 can be
both dominant and recessive depending on the other partner S
haplotype in a heterozygote. This phenomenon is one of the
characteristics of multiallelic locus. In the locus with only two
alleles, dominant and recessive alleles are generally fixed. It is
apparent that the dominant allele is able to become a recessive
allele by mutations (e.g. nucleotide substitution and transposon
insertion); however, these events must be accompanied by
alteration of genomic DNA sequences and are not easily
reversible. In the multiallelic S locus, the dominance relationships for some haplotypes (e.g. S40 and S60) can change without alteration of genomic DNA sequences, and thus they are
apparently a reversible epigenetic phenomenon. This reversible characteristic of the dominance relationships in the SI system is similar to the nucleolar dominance in Crepis hybrids, in
which loss of secondary constriction is observed in underdominant (suppressed) chromosomes because of the difference of
NOR (nucleolus organizer region) activity (Pikaard 2000;
discussed in Shiba et al. 2002). It is noteworthy that monoallelic expression in the mammal immune system showed a
reversible epigenetic phenomenon (Rada and Ferguson-Smith
2002). In the immune system, only one of the two alleles of the
antigen receptor is completely rearranged and expressed in B
cells, whereas the other one is silenced. Recent examinations
using the FISH technique showed that the silenced nonrearranged allele was localized to the heterochromatin, whereas
the active rearranged allele remained dissociated from the
heterochromatin (Hesslein et al. 2001, Skok et al. 2001). The
relationship between subnuclear localization and monoallelic
expression is one of the most important factors to determine the
mechanisms of the dominance/recessiveness in the plant SI
system.
The mechanism for the suppression of the recessive SP11
is unknown. An enhancer imbalance model, selective hypermethylation model, and chromosome pairing model have been
proposed to explain the suppression of expression of class-II
SP11 in the S heterozygotes having class-I and class-II S haplotypes (Kusaba et al. 2002, Shiba et al. 2002). The linear dominance relationship observed here might be regulated by the
74
Linear dominance relationship in S haplotypes
same mechanism as observed in S heterozygotes possessing
class-I and class-II S haplotypes, and thus these three models
are possible hypotheses to explain dominance relationships. In
addition, we propose another possibility; the expression of
SP11 is regulated by subnuclear localization of the S locus as in
the case of the monoallelic expression in the mammal immune
system (Hesslein et al. 2001, Skok et al. 2001) described
above. In the report of Shiba et al. (2001), S8-SP11 was introduced into S52S60 heterozygotes of B. campestris, and it functioned as the pollen SI determinant with the S8 specificity,
even though S8 is recessive to S52 in pollen (T. Kakizaki, T.
Nakanowatari, and M. Watanabe, unpublished results from a
pollination test). If the dominance relationships among class-I
S haplotypes in pollen are also controlled by SP11 expression,
S8-SP11 should be suppressed in these transgenic plants. However, the S8-SP11 transgene was normally expressed in the
transgenic plants and conferred the pollen S8 function. This
result can be explained by the position effect of the transgene;
the genomic location of the integrated T-DNA with S8-SP11
might be distant from the S locus, and thus not silenced. This
explanation fits the subnuclear localization model. Determination of the subnuclear localization of the recessive SP11 region
in the tapetum cells of the S heterozygotes is a challenging
topic for research that should be considered in the future.
Materials and Methods
Plant materials and determination of dominance relationships among
class-II S haplotypes
The S homozygotes of B. campestris used in this study included
one class-I S haplotype, S9, and four class-II S haplotypes, S29, S40, S44
and S60 (Hatakeyama et al. 2001, Nou et al. 1993, Takasaki et al.
1999). Within class-II S haplotypes, the dominance relationships
among S29, S40 and S44 had been determined (Hatakeyama et al. 1998),
but the dominance relationships of S60 to the other three class-II S haplotypes had not. To test this, three S heterozygous lines, S29S60, S40S60
and S44S60, were generated. Test-crosses for the determination of the
dominance relationships were performed with these S heterozygous
lines and their parental S homozygous lines (Hatakeyama et al. 1998).
Three or more flowers were used for each test cross, and observations
were generally replicated four or five times. The compatibility of each
test cross was also examined as described by Hatakeyama et al. (1998).
mRNA isolation and RNA gel blot analysis
Isolation of poly(A)+ RNA, electrophoresis of denaturated RNA
samples and blotting to a nylon membrane (Roche, Mannheim, Germany) were performed as described by Watanabe et al. (1994). One
microgram of poly(A)+ was loaded onto an agarose gel. Digoxigneinlabeled probes for S29-SP11, S40-SP11, S44-SP11 and S60-SP11 were
prepared by using PCR with the PCR DIG Labeling Mix (Roche)
using SP11–60-F3 (Shiba et al. 2002) and NotI-dT primer (Watanabe
et al. 2000). After hybridization of each probe, membranes were
washed three times in 0.05´SSC, 0.1% SDS at 75°C for 20 min.
Detection of hybridized probe was carried out as described by Matsuda
et al. (1996) with a slight modification. CDP-Star (Tropix, Bedford,
MA, USA) was used as the chemiluminescent substrate. A DNA fragment encoding vacuolar H+-ATPase (V-ATP) of B. campestris (Takasaki et al. 2000) was used as a control probe. For the control probe, the
procedure of the hybridization and detection of hybridized probes was
performed as described above, except that the membranes were
washed three times in 0.1´ SSC, 0.1% SDS at 65°C for 20 min.
Acknowledgments
This work was supported in part by a Grant-in-Aid for Special
Research on Priority Areas (B) (11238201) and for Scientific Research
(B) (11460001, 14360002) to M.W. from the Ministry of Education,
Culture, Sports, Science and Technology of Japan and by a Grant from
Intelligent Cosmos Academic Foundation to M.W. The authors thank
Dr. Yukihiro Ito (National Institute of Genetics), Dr. Tsuyoshi Yamazaki
(Tokai University), Dr. Katsunori Hatakeyama (National Institute of
Vegetable and Tea Science), Dr. Masami Morimatsu (Iwate University), Dr. Atsushi Higashitani (Tohoku University) for their valuable
discussions. The authors are also grateful to Miss Ayako Chiba, Eri
Abe, Misako Shinkai and Rina Kikuta (Iwate University) for technical
assistance.
References
Bateman, A.J. (1955) Self-incompatibility systems in angiosperms. III. Cruciferae. Heredity 9: 52–68.
Bhattacharyya, M.K., Smith, A.M., Ellis, T.H.N., Hedley, C. and Martin, C.
(1990) The wrinkled-seed character of pea described by Mendel is caused by
a transposon-like insertion in a gene encoding starch-branching enzyme. Cell
60: 115–122.
Dixit, R., Nasrallah, M.E. and Nasrallah, J.B (2000) Post-transcriptional maturation of the S receptor kinase of Brassica correlates with co-expression of the
S-locus glycoprotein in the stigmas of two Brassica strains and in transgenic
tobacco plants. Plant Physiol. 124: 297–311.
Glazebrook, J. (1999) Genes controlling expression of defense responses in Arabidopsis. Curr. Opin. Plant Biol. 2: 280–286.
Hatakeyama, K., Takasaki, T., Suzuki, G., Nishio, T., Watanabe, M., Isogai, A.
and Hinata, K. (2001) The S receptor kinase gene determines dominance relationships in stigma expression of self-incompatibility in Brassica. Plant J. 26:
69–76.
Hatakeyama, K., Watanabe, M., Takasaki, T., Ojima, K. and Hinata, K. (1998)
Dominance relationships between S-alleles in self-incompatible Brassica
campestris. Heredity 79: 241–247.
Hesslein, D.G.T., Fields, P.E. and Schatz, D.G. (2001) Location, location, location: the cell biology of immunoglobulin allelic control. Nature Immunol. 2:
825–826.
Kowyama, Y., Takahashi, H., Muraoka, K., Tani, T., Hara, K. and Shiotani, I
(1994) Number, frequency and dominance relationships of S-alleles in diploid Ipomoea trifida. Heredity 73: 275–283.
Kusaba, M., Tung, C.-W., Nasrallah, M.E. and Nasrallah, J.B. (2002) Monoallelic expression and dominance interactions in anthers of self-incompatible
Arabidopsis lyrata. Plant Physiol. 128: 17–20.
Lester, D.R., Ross, J.J., Davies, P.J. and Reid, J.B. (1997) Mendel’s stem length
gene (Le) encodes a gibberellin 3b-hydroxylase. Plant Cell 9: 1435–1443.
Matsuda, N., Tsuchiya, T., Kishitani, S., Tanaka, Y. and Toriyama, K. (1996)
Partial male sterility in transgenic tobacco carrying antisense and sense PAL
cDNA under the control of a tapetum-specific promoter. Plant Cell Physiol.
37: 215–222.
Mendel, G.J. (1866) Versuche uber Pflanzen-Hybriden. Verh. Naturforsch. Ver.
Brunn. 4: 3–47.
Nasrallah, J.B. and Nasrallah, M.E. (1993) Pollen-stigma signaling in the sporophytic self-incompatibility response. Plant Cell 5: 1325–1335.
Nou, I.S., Watanabe, M., Isogai, A. and Hinata, K. (1993) Comparison of S-alleles and S-glycoproteins between two wild populations of Brassica campestris in Turkey and Japan. Sex. Plant Reprod. 6: 79–86.
Parham, P., Adams, E.J. and Arnett, K.K. (1995) The origin of HLA-A, B, C
polymorphism. Immunol. Rev. 143: 141–180.
Pikaard, C.S. (2000) The epigenetics of nucleolar dominance. Trends Genet. 16:
495–500.
Rada, C. and Ferguson-Smith, A.C. (2002) Epigenetics: monoallelic expression
Linear dominance relationship in S haplotypes
in the immune system. Curr. Biol. 12: 108–110.
Schopfer, C.R., Nasrallah, M.E. and Nasrallah, J.B. (1999) The male determinant of self-incompatibility in Brassica. Science 286: 1697–1700.
Shiba, H., Iwano, M., Entani, T., Ishimoto, K., Shimosato, H., Che, F.-S., Satta,
Y., Ito, A., Takada, Y., Watanabe, M., Isogai, A. and Takayama, S. (2002) The
dominance of alleles controlling self-incompatibility in Brassica pollen is
regulated at the RNA level. Plant Cell 14: 491–504.
Shiba, H., Takayama, S., Iwano, M., Shimosato, H., Funato, M., Nakagawa, T.,
Che, F.S., Suzuki, G., Watanabe, M., Hinata, K. and Isogai, A. (2001) A pollen coat protein, SP11/SCR, determines the pollen S-specificity in the selfincompatibility of Brassica species. Plant Physiol. 125: 2095–2103.
Skok, J.A., Brown, K.E., Azuara, V., Caparros, M.-L., Baxter, J., Takacs, K.,
Dillon, N., Gray, D., Perry, R.P., Merkenschlager, M. and Fisher, A.G. (2001)
Nonequivalent nuclear location of immunoglobulin alleles in B lymphocytes.
Nature Immunol. 2: 848–854.
Suzuki, G., Kai, N., Hirose, T., Fukui, K., Nishio, T., Takayama, S., Isogai, A.,
Watanabe, M. and Hinata, K. (1999) Genomic organization of the S locus:
identification and characterization of genes in SLG/SRK region of S9 haplotype of Brassica campestris (syn. rapa). Genetics 152: 391–400.
Szymanski, D.B., Lloyd, A.M. and Marks, M.D. (2000) Progress in the molecular genetic analysis of trichome initiation and morphogenesis in Arabidopsis.
Trends Plant Sci. 5: 214–219.
Takasaki, T., Hatakeyama, K., Suzuki, G., Watanabe, M., Isogai, A. and Hinata,
K. (2000) The S receptor kinase determines self-incompatibility in Brassica
stigma. Nature 403: 913–916.
Takasaki, T., Hatakeyama, K., Watanabe, M., Toriyama, K., Isogai, A. and
Hinata, K. (1999) Introduction of SLG (S locus glycoprotein) alters the phenotype of endogenous S haplotype, but confers no new S haplotype specifi-
75
city in Brassica rapa L. Plant Mol. Biol. 40: 659–668.
Takayama, S., Shiba, H., Iwano, M., Shimosato, H., Che, F.-S., Kai, N., Watanabe, M., Suzuki, G., Hinata, K. and Isogai, A. (2000) The pollen determinant
of self-incompatibility in Brassica campestris. Proc. Natl. Acad. Sci. USA 97:
1920–1925.
Takayama, S., Shimosato, H., Shiba, H., Funato, M., Che, F.-S., Watanabe, M.,
Iwano, M. and Isogai, A. (2001) Direct ligand-receptor complex interaction
controls Brassica self-incompatibility. Nature 413: 534–538.
Theisen, G. (2001) Development of floral organ identity: stories from the
MADS house. Curr. Opin. Plant Biol. 4: 75–85.
Thompson, K.F. and Taylor, J.P. (1966) Non-linear dominance relationships
between S alleles. Heredity 21: 345–362.
Watanabe, M., Hatakeyama, K., Takada, Y. and Hinata, K. (2001) Molecular
aspect of self-incompatibility in Brassica species. Plant Cell Physiol. 42:
560–565.
Watanabe, M., Ito, A., Takada, Y., Ninomiya, C., Kakizaki, T., Takahata, Y,
Hatakeyama, K., Hinata, K., Suzuki, G., Takasaki, T., Satta, Y., Shiba, H.,
Takayama, S. and Isogai, A. (2000) Highly divergent sequences of the pollen
self-incompatibility (S) gene in class I S haplotypes of Brassica campestris
(syn. rapa) L. FEBS Lett. 473: 139–144.
Watanabe, M., Takasaki, T., Toriyama, K., Yamakawa, S., Isogai, A., Suzuki, A.
and Hinata, K. (1994) A high degree of homology exists between the protein
encoded by SLG and the S receptor domain encoded by SRK in self-incompatible Brassica campestris L. Plant Cell Physiol. 35: 1221–1229.
Yamakawa, S., Watanabe, M., Hinata, K., Suzuki, A. and Isogai, A. (1995) The
sequence of S-receptor kinase (SRK) involved in self-incompatibility and
their homologies to S-locus glycoproteins of Brassica campestris. Biosci.
Biotech. Biochem. 59: 161–162.
(Received September 9, 2002; Accepted November 8, 2002)