TY - JOUR
AU - Nishio, Takeshi
AB - Abstract There are several pairs of similar class I S haplotypes between Brassica oleracea and Brassica rapa. The similar S halotypes in these interspecific pairs have been reported to have the same recognition specificities. In the present study, three interspecific pairs showing a high sequence similarity were found in class II S haplotypes, i.e. between BoS-2b (B. oleracea S-2b) and BrS-44 (B. rapa S-44), between BoS-5 and BrS-40, and between BoS-15 and BrS-60. By pollination tests using interspecific hybrids between B. oleracea and B. rapa, BoS-5 and BoS-2b were revealed to have slightly and completely different recognition specificities from those of BrS-40 and BrS-44, respectively. The recognition reaction between SP11 and SRK of BoS-15 was suggested to be incomplete. The regions of class II SP11 and SRK important for self-recognition specificity and the diversification of class II S haplotypes are discussed herein. Introduction Many flowering plants have outbreeding systems preventing autogamy and promoting allogamy. One outbreeding system is self-incompatibility, in which the pistils inhibit pollen germination or pollen tube growth after self-pollination. In Brassicaceae, the molecular mechanism of self-incompatibility has been studied intensively, and recognition molecules encoded by multiple alleles in the S locus have been elucidated. The recognition molecule in the stigma is the S locus receptor kinase (SRK) (Stein et al. 1991), and that in the pollen is a low molecular weight cysteine-rich protein, S locus protein 11(SP11)/S locus cysteine-rich protein (SCR) (SP11 hereafter) (Schopfer et al. 1999, Suzuki et al. 1999), which interacts directly with SRK as a ligand (Kachroo et al. 2001, Takayama et al. 2001). S locus glycoprotein (SLG), the S locus-specific stigma molecule first identified (Nasrallah and Wallace 1967), has an amino acid sequence similar to that of the extracellular domain of SRK, but its function in self-incompatibility is unclear. The genes for these three molecules are closely linked in the S locus and transmitted to progeny as S haplotypes. The number of S haplotypes in Brassica oleracea has been reported to be 50 (Ockendon 2000), and in Brassica rapa >100 (Nou et al. 1993). S haplotypes are divided into two classes, class I and class II, on the basis of nucleotide sequence identities of SLG and the S domain of SRK (Nasrallah et al. 1991). The identities of the deduced amino acid sequences of SLG and the S domain of SRK are <70% between the classes and >72% within the classes. The sequence similarity of SLG, SRK and SP11 between class II S haplotypes tends to be higher than that between class I S haplotypes. Only three class II S haplotypes have been identified among the many S haplotypes analyzed in B. oleracea (Okazaki et al. 1999), while seven S haplotypes have been reported to be class II in B. rapa (Nishio et al. 1996, Takasaki et al. 1999). Class I S haplotypes are generally dominant over class II S haplotypes in the pollen, and the expression of SP11 of class II S haplotypes is suppressed in class I/class II heterozygotes (Kusaba et al. 2002, Shiba et al. 2002). The self-incompatibility of class II S haplotypes is generally weaker than that of class I S haplotypes (Nasrallah et al. 1991). Nucleotide sequence analyses of SRK, SP11 and SLG of many S haplotypes have revealed that B. oleracea, B. rapa and Raphanus sativus L. have similar S haplotypes, with >89.5% amino acid identity of both SRK and SP11 (Sato et al. 2002, Okamoto et al. 2004). Interspecific or intergeneric pairs of S haplotypes probably evolved from common ancestral S haplotypes. Five interspecific pairs of class I S haplotypes and one interspecific pair of class II S haplotypes between B. oleracea and B. rapa, and an intergeneric pair between B. rapa and R. sativus have been shown to possess the same recognition specificity (Sato et al. 2003, Sato et al. 2004). Sequence analysis of SP11 alleles of class II S haplotypes showed that the deduced amino acid sequences of S-40, S-44 and S-60 in B. rapa are highly similar to those of S-5, S-2b and S-15 in B. oleracea, respectively (Shiba et al. 2002, Sato et al. 2003). In the present study, we determined the nucleotide sequences of the S locus genes in multiple class II S haplotypes, revealing the number of different class II S haplotypes in B. rapa to be only four. The recognition specificities of three interspecific pairs of class II S haplotypes between B. oleracea and B. rapa were also investigated by pollination tests using interspecific hybrid plants. In this study, S-n haplotypes in B. rapa and B. oleracea were described as BrS-n and BoS-n, respectively, and SP11, SRK and SLG in BrS-n and BoS-n were denoted as BrSP11-n, BoSP11-n, BrSRK-n, BoSRK-n, BrSLG-n and BoSLG-n, respectively. Results Nucleotide sequences of SP11 and SRK alleles in class II S haplotypes Although S-31, S-39 and Turkish lines of S-35 in B. rapa have been reported to be class II S haplotypes (Nishio et al. 1996), the nucleotide sequences of the S locus genes of these S haplotypes have not been determined. Nucleotide sequences of the second exon of the SP11 alleles in BrS-31, BrS-39 and a Turkish line 7-12T of BrS-35, which encode the full length of the mature SP11 proteins, were identical to those of BrSP11-29, BrSP11-40 and BrSP11-60 (Shiba et al. 2002), respectively. Sequences of approximately 1 kb PCR products amplified with the primer pair PS-3 and PS-21 (Nishio et al. 1996) from BrS-31, BrS-39 and 7-12T of BrS-35, which correspond to about 80% of the coding regions of SLG and the S domain of SRK, were the same as those of BrSRK-29 (Hatakeyama et al. 1998), BrSLG-40 (Hatakeyama et al. 1998) and BrSRK-60 (Fukai et al. 2003), respectively. Although we were unable to perform pollination tests with S-31 and S-39 homozygotes because of abnormal growth, probably due to inbreeding depression, 7-12T of S-35 was incompatible with S-60 homozygotes. These results suggest that there are only four class II S haplotypes in B. rapa, i.e. S-29, S-40, S-44 and S-60. The S domains of BrSRK-40 and BrSRK-44 were amplified by reverse transcription–PCR (RT–PCR) and the nucleotide sequences were determined. BrSRK-40 (accession number AB201306) showed 97.2% nucleotide sequence identity and 94.8% deduced amino acid identity to BoSRK-5 (Cabrillac et al. 1999). BrSRK-44 (accession number AB201307) showed 97.5% nucleotide sequence identity and 96.6% deduced amino acid identity to BoSRK-2b (Kusaba et al. 2000) (Table 1). The comparison of the deduced amino acid sequences between BrSRK-40 and BoSRK-5 and between BrSRK-44 and BoSRK-2b revealed that both pairs have two different amino acids in HV II (hypervariable region II) (Fig. 1A, B). It has been reported that BoSP11-2b and BoSP11-5 are highly similar to BrSP11-44 and BrSP11-40, respectively (Shiba et al. 2002). These results suggest that there are three interspecific pairs showing the high sequence similarity, including the previously reported interspecific pair between BoS-15 and BrS-60 (Sato et al. 2003), among class II S haplotypes (Table 1). Recognition specificity of the interspecific pairs of class II S haplotypes Interspecific hybrid plants have been successfully used for the investigation of recognition specificities between B. oleracea and B. rapa (Sato et al. 2003, Sato et al. 2004). Therefore, the recognition specificities of the pair BoS-2b and BrS-44 and those of BoS-5 and BrS-40 were investigated using interspecific hybrid plants obtained by crossing of BoS-2b, BoS-5 and BoS-15 homozygotes with BrS-52 homozygotes. The stigmas of the interspecific hybrid of BoS-2b/BrS-52 were compatible with the pollen grains of BrS-44 homozygotes, but incompatible with those of the BoS-2b homozygote (Fig. 2A). The pollen grains of both BoS-5 and BrS-40 were incompatible with the stigmas of BoS-5/BrS-52 (Fig. 2B). Although BrS-40 homozygotes were completely self-incompatible, the incompatibility of the BoS-5/BrS-52 stigmas with the pollen of the BrS-40 homozygotes was significantly weaker than that with the BoS-5 pollen. These results indicate that the interspecific pair BoS-5 and BrS-40 have slightly different recognition specificities, and that BoS-2b has a completely different specificity from BrS-44. Using interspecific hybrids of BrS-60/BoS-32, we have previously revealed the same recognition specificity of BoS-15 and BrS-60 (Sato et al. 2003). In the pollination tests using an interspecific hybrid of BoS-15/BrS-52, the pollen grains of the BrS-60 homozygotes were incompatible with the stigmas of BoS-15/BrS-52 (Fig. 2C). Weakness of self-incompatibility of BoS-15 The pollen grains of the BoS-15 homozygotes exhibited significantly weaker incompatibility with BoS-15/BrS-52 stigmas than those of the BrS-60 homozygotes (Fig. 2C). Self-incompatibility of the BoS-15 homozygotes was also significantly weaker than that of the BrS-60 homozygotes (Fig. 3). However, the pollen grains of both the BoS-15 and BrS-60 homozygotes were completely incompatible with the stigmas of BrS-60/BoS-18 (Fig. 4). These results suggest that both SP11 and SRK of BoS-15 are completely functional but that the recognition reaction between BoSP11-15 and BoSRK-15 is incomplete. Discussion Regions important for recognition specificity of SP11 and SRK in class II S haplotypes The amino acid sequence of SP11 was divided into six regions on the basis of conserved cysteine residues (Sato et al. 2003). It has been shown that region III and region V of SP11 of class I S haplotypes are conserved between interspecific pairs having the same recognition specificity (Sato et al. 2003), suggesting the importance of these regions for the recognition specificity of SP11. The importance of regions III and V has been demonstrated by a study using chimeric SP11 sequences (Sato et al. 2004). Three amino acid substitutions in region V were found between BoSP11-2b and BrSP11-44, which have different recognition specificities (Fig. 5). Between BoSP11-5 and BrSP11-40, which are slightly different in specificity, there are two amino acid substitutions in region V. No substitutions in region V were found between BoSP11-15 and BrSP11-60, both of which induced incompatibility with the stigmas of the BrS-60/BoS-18 interspecific hybrid. The interspecific pairs of class II S haplotypes have as many amino acid substitutions in region IV as the class I S haplotype pairs. Therefore, region V is likely to be important for the recognition specificity of SP11s in class II S haplotypes. Comparison of the amino acid sequences of SRKs from different accessions having BoS-2 (Miege et al. 2001) has suggested an important role for HV I and HV II for the recognition function. The amino acid sequence identity between BoSRK-2b and BrSRK-44 was found to be 96.6% (Table 1). This identity was the highest among interspecific pairs of either class I or class II S haplotypes, but the recognition specificity was different. There were two substitutions (both leucine to phenylalanine) in HV II and no substitutions in HV I and HV III (Fig. 1). Between BoSRK-5 and BrSRK-40, whose specificities are slightly different from each other, two amino acid substitutions (leucine to valine and threonine to serine) were found in HV II, but none in HV I and HV III. Therefore, it seems likely that HV II is important for the recognition specificity in these S haplotypes. The self-incompatible reaction of BoS-15 was found to be incomplete. Our previous study indicated that the pollen grains of transgenic plants expressing RsSP11-6 (SP11 of R. sativus S-6) were partially incompatible with the stigmas of BrS-52, while those expressing chimeric RsSP11-6 exchanged with regions III and V of BrSP11-52 were completely incompatible with BrS-52, suggesting that the incomplete interaction between SP11 and SRK may be related to weak incompatibility (Sato et al. 2004). There were three amino acid substitutions in regions II, III and IV between BoSP11-15 and BrSP11-60 (Fig. 5). The weakness of the self-incompatibility of BoS-15 may suggest the involvement of regions II, III or IV of SP11 in the recognition specificity. One amino acid substitution (arginine to threonine) in HV I and four (threonine to serine, alanine to threonine, tyrosine to phenylalanine and methionine to leucine) in HV II between BoSRK-15 and BrSRK-60 can be responsible for the incomplete interaction of BoSRK-15 with BoSP11-15. Diversification of class II S haplotypes Between RsS-6 (R. sativus S-6) and BoS-18, a class-I S haplotype with the same recognition specificity, the amino acid identities of SP11 and SRK are 70.9 and 88.3%, respectively (Sato et al. 2004). RsS-6 is also partially incompatible with BrS-52. The amino acid identities of SP11 and SRK between RsS-6 and BrS-52 are 69.1 and 86.6%, respectively. The identities of SP11 and SRK between BoS-2b and BrS-44, whose recognition specificities differ, are higher, 87.3 and 96.6%, respectively, suggesting that the generation of a new class II S haplotype has occurred with a smaller number of mutations of recognition molecules. Class II S haplotypes may have diverged more recently than class I S haplotypes as indicated by the higher nucleotide sequence identities between different class II S haplotypes in a species than those of class I S haplotypes. The findings of different recognition specificities between BoS-2b and BrS-44 in the interspecific pair, and slightly different specificities between BoS-5 and BrS-40, suggest that alteration of recognition specificities of class II S haplotypes occurred after speciation. A hypothesis for the generation of a new S haplotype has been presented by Chookajorn et al. (2004). In the model, new S haplotypes evolve via self-incompatible intermediates, and the intermediates gradually acquire new recognition specificity, resulting in a weakening of incompatibility with the original S haplotype. In class II S haplotypes, acquisition of new recognition specificity might result in the loss of the original recognition specificity in a shorter time because of the weakness of self-incompatibility. Since self-compatibility caused by disruptive mutations in class II S haplotypes can be masked by dominant S haplotypes in S heterozygotes, the weakly incompatible BoS-15 could perhaps have been maintained in B. oleracea populations under selection pressure for self-incompatibility. If the weakening of self-incompatibility is one step in the process of the generation of a new S haplotype, BoS-15 might be in the process of generating a new S haplotype. Materials and Methods Plant materials Homozygotes of S-29, S-31, S-35 (7-12T), S-39, S-40, S-44 and S-60 in B. rapa L. (Nishio et al. 1996) and homozygotes of S-2b, S-5 and S-15 in B. oleracea L. (Kusaba et al. 2000, Ockendon 2000) were used. Interspecific hybrids between B. oleracea and B. rapa were raised by ovary culture according to Inomata (1977). Sequence analysis of S locus genes of class II S haplotypes Class II SP11 alleles were amplified from genomic DNAs of BrS-31, BrS-35 and BrS-39 by PCR using the primer pair 60-F (5′-AACAAATATACACTACTTATGTTTCATA-3′) and 40-R (5′-ATACTGCATAGAGTAACCGTATCTGG-3′). SLG and SRK alleles of these S haplotypes were amplified using PS-3 and PS-21 (Nishio et al. 1996). The PCR products were cloned into the pGEM-T Easy Vector (Promega, Madison, WI, USA). The clones were sequenced with ABI Prism 310 Genetic Analyzer (ABI, Foster City, CA, USA) Total RNA was isolated from stigmas of flower buds of BrS-40 and BrS-44 homozygotes with ISOGEN (Nippongene, Japan). First-strand cDNA was synthesized using primer PK8-4 (Okamoto et al. 2004) with a First-Strand cDNA Synthesis Kit (Amersham, Piscataway, NJ, USA). DNA fragments of the S domain of SRK were amplified using primer pair PK7-2 (Okamoto et al. 2004) and PK8-4, and PCR products were cloned into the pGEM-T Easy Vector (Promega). The nucleotide sequences of three clones for each SRK allele were determined. Pollination test Pollination tests were conducted as described by Sato et al. (2004). Self-incompatibility was evaluated using indices based on the number of pollen tubes penetrating stigma papilla cells. The indices are as follows: 1, no or few germinating pollen grains observed on a stigma with no pollen tube penetrating a papilla cell; 2, >30 germinating pollen grains on a stigma and <5 pollen tubes penetrating papilla cells; 3, between six and 29 pollen tubes penetrating papilla cells; 4, 30–100 pollen tubes penetrating papilla cells; 5, >100 pollen tubes penetrating papilla cells. Acknowledgments This work was supported in part by a Grant-in-Aid for Fundamental Research (No. 16380002) from the Ministry of Education, Science, Sports and Culture, Japan. The nucleotide sequences reported in this paper have been submitted to GenBank under accession numbers AB201306 and AB201307. 1 Present address: Kofu Higashi High School, Sakaori 1-17-1, Kofu, Yamanashi, 400-0805 Japan. View largeDownload slide Fig. 1 Comparison of the deduced amino acid sequences of SRK. (A) Comparison between BoSRK-2b and BrSRK-44. Boxes show hypervariable (HV) regions. (B) Comparison between BoSRK-5 and BrSRK-40. View largeDownload slide Fig. 1 Comparison of the deduced amino acid sequences of SRK. (A) Comparison between BoSRK-2b and BrSRK-44. Boxes show hypervariable (HV) regions. (B) Comparison between BoSRK-5 and BrSRK-40. View largeDownload slide Fig. 2 Incompatibility of the stigmas of the interspecific hybrids, BoS-2b/BrS-52, BoS-5/BrS-52 and BoS-15/BrS-52. The pollen grains of four S haplotypes in B. rapa and three S haplotypes in B. oleracea were used to pollinate the stigmas of each interspecific hybrid. Fourteen to 32 stigmas were used for each pollination test. Bars show standard errors of the indices. (A) Incompatibility of the stigmas of BoS-2b/BrS-52. Asterisks represent significant differences from an incompatible control, BoS-2b, at 1%. (B) Incompatibility of the stigmas of BoS-5/BrS-52. Asterisks represent significant differences from an incompatible control, BoS-5, at 1%. (C) Incompatibility of the stigmas of BoS-15/BrS-52. Asterisks represent significant differences from an incompatible control, BoS-15, at 1%. View largeDownload slide Fig. 2 Incompatibility of the stigmas of the interspecific hybrids, BoS-2b/BrS-52, BoS-5/BrS-52 and BoS-15/BrS-52. The pollen grains of four S haplotypes in B. rapa and three S haplotypes in B. oleracea were used to pollinate the stigmas of each interspecific hybrid. Fourteen to 32 stigmas were used for each pollination test. Bars show standard errors of the indices. (A) Incompatibility of the stigmas of BoS-2b/BrS-52. Asterisks represent significant differences from an incompatible control, BoS-2b, at 1%. (B) Incompatibility of the stigmas of BoS-5/BrS-52. Asterisks represent significant differences from an incompatible control, BoS-5, at 1%. (C) Incompatibility of the stigmas of BoS-15/BrS-52. Asterisks represent significant differences from an incompatible control, BoS-15, at 1%. View largeDownload slide Fig. 3 Self-incompatibility of BrS-60 and BoS-15 homozygotes. Twenty-one stigmas for BrS-60 and 41 stigmas for BoS-15 were used for the pollination test. Bars show standard errors of the indices. An asterisk represents a significant difference from BrS-60, at 1%. View largeDownload slide Fig. 3 Self-incompatibility of BrS-60 and BoS-15 homozygotes. Twenty-one stigmas for BrS-60 and 41 stigmas for BoS-15 were used for the pollination test. Bars show standard errors of the indices. An asterisk represents a significant difference from BrS-60, at 1%. View largeDownload slide Fig. 4 Incompatibility of the stigmas of an interspecific hybrid, BrS-60/BoS-18. The pollen grains of BrS-60, BoS-15 and BoS-2b were used to pollinate the stigmas of BrS-60/BoS-18. Eleven to 23 stigmas were used for each pollination test. Bars show standard errors of the indices. View largeDownload slide Fig. 4 Incompatibility of the stigmas of an interspecific hybrid, BrS-60/BoS-18. The pollen grains of BrS-60, BoS-15 and BoS-2b were used to pollinate the stigmas of BrS-60/BoS-18. Eleven to 23 stigmas were used for each pollination test. Bars show standard errors of the indices. View largeDownload slide Fig. 5 Comparison of the deduced amino acid sequences of SP11s between three interspecific pairs of class II S haplotypes. White and gray boxes show the conserved cysteine residues and different amino acids between interspecific pairs, respectively. The amino acid sequence of SP11 was divided into six regions on the basis of conserved cysteine residues (Sato et al. 2003). I, region I; II, region II; III, region III; IV, region IV; V, region V; and VI, region VI View largeDownload slide Fig. 5 Comparison of the deduced amino acid sequences of SP11s between three interspecific pairs of class II S haplotypes. White and gray boxes show the conserved cysteine residues and different amino acids between interspecific pairs, respectively. The amino acid sequence of SP11 was divided into six regions on the basis of conserved cysteine residues (Sato et al. 2003). I, region I; II, region II; III, region III; IV, region IV; V, region V; and VI, region VI Table 1 Amino acid identities of SP11 and the S domain of SRK between three class II S haplotypes in B. oleracea and four class-II S haplotypes in B. rapa   BrS-44  BoS-5  BrS-40  BoS-15  BrS-60  BrS-29    SRK/SP11  SRK/SP11  SRK/SP11  SRK/SP11  SRK/SP11  SRK/SP11  BoS-2b  96.6/87.3*  93.9/66.7  93.4/63.5  86.0/57.6  88.0/57.6  94.6/69.8  BrS-44    92.6/61.9  92.4/58.7  85.3/54.5  86.2/56.9  93.6/61.9  BoS-5      94.8/93.7*  88.2/56.1  88.9/56.1  93.6/63.5  BrS-40        85.5/54.5  87.7/53.0  92.6/65.1  BoS-15          95.8/95.5*  86.2/57.6  BrS-60            88.5/56.1    BrS-44  BoS-5  BrS-40  BoS-15  BrS-60  BrS-29    SRK/SP11  SRK/SP11  SRK/SP11  SRK/SP11  SRK/SP11  SRK/SP11  BoS-2b  96.6/87.3*  93.9/66.7  93.4/63.5  86.0/57.6  88.0/57.6  94.6/69.8  BrS-44    92.6/61.9  92.4/58.7  85.3/54.5  86.2/56.9  93.6/61.9  BoS-5      94.8/93.7*  88.2/56.1  88.9/56.1  93.6/63.5  BrS-40        85.5/54.5  87.7/53.0  92.6/65.1  BoS-15          95.8/95.5*  86.2/57.6  BrS-60            88.5/56.1  Asterisks show amino acid identities between S haplotypes in interspecific pairs. The amino acid sequence of BoSRK-2b is from Kusaba et al. (2000). BoSRK-5 and BoSRK-15 are from Cabrillac et al. (1999). BrSRK-29 and BrSRK-60 are from Hatakeyama et al. (1998) and Fukai et al. (2003), respectively. BoSP11-2b, BoSP11-5, BrSP11-29, BrSP11-40, BrSP11-44 and BrSP11-60 are from Shiba et al. (2002). BoSP11-15 is from Sato et al. (2003). View Large Abbreviations HV hypervariable region RT–PCR reverse transcription–PCR SLG S locus glycoprotein SP11 S locus protein 11 SRK S locus receptor kinase References Cabrillac, D., Delorme, V., Garin, J., Ruffio-Chable, V., Giranton, J.-L., Dumas, C., Gaude, T. and Cock, J.M. ( 1999) The S15 self-incompatibility haplotype in Brassica oleracea includes three S gene family members expressed in stigmas. Plant Cell  11: 971–986. Google Scholar Chookajorn, T., Kachroo, A., Ripoll, D.R., Clark, A.G. and Nasrallah, J.B. ( 2004) Specificity determinants and diversification of the Brassica self-incompatibility pollen ligand. Proc. Natl Acad. 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TI - Interspecific Pairs of Class II S Haplotypes Having Different Recognition Specificities between Brassica oleracea and Brassica rapa
JF - Plant and Cell Physiology
DO - 10.1093/pcp/pci250
DA - 2006-03-01
UR - https://www.deepdyve.com/lp/oxford-university-press/interspecific-pairs-of-class-ii-s-haplotypes-having-different-3klPn8ZuW4
SP - 340
EP - 345
VL - 47
IS - 3
DP - DeepDyve
ER -