* Institute of Molecular and Cellular Biosciences, the University of Tokyo, Bunkyo-ku, Tokyo, Japan
Hokuriku National Agricultural Experimental Station, Joetsu, Japan
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Abstract |
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Key Words: Oryza sativa indica and japonica rice Oryza rufipogon SINE insertion polymorphism polyphyletic origin
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Introduction |
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The origin of O. sativa has been questioned. Perennial type O. rufipogon is considered to be a possible progenitor, because the high genetic variability in the perennial population would provide higher evolutionary potential than that in the annual population, and because some wild-cultivated hybrid plants have been shown to form a bridge that connects the perennial type of O. rufipogon with O. sativa in various traits (Oka 1964, 1974). Annual type O. rufipogon is also considered to be a possible progenitor of O. sativa (Chang 1976), because annual strains have high seed productivity and certain other characters similar to O. sativa. Some O. rufipogon strains have been shown to be capable of evolving into both the indica and japonica types of O. sativa (Oka 1974; Oka and Morishima 1982), which supports the idea that the two ecotype strains have been derived monophyletically by domestication. Biochemical and molecular studies, however, show that the indica and japonica strains are closer in some characters or loci to different O. rufipogon strains than they are to each other (Second 1982; Morishima 1986; Dally and Second 1990; Wang, Second, and Tanksley 1992; Mochizuki et al. 1993; Hirano et al. 1994), which may support the idea that the two ecotype strains originated diphyletically. Note, however, that the number of genetic markers or O. sativa and O. rufipogon strains used in these studies are not sufficient to discuss the origin of the two ecotype strains.
Short interspersed elements (SINEs) are retroelements found in eukaryotic genomes (see Maraia 1995). SINEs range from 70 to 500 bp, and each has an internal promoter for RNA polymerase III (pol III). Many SINEs appear to be related to tRNAs, whereas a few, such as the primate Alu and rodent B1 family elements, are related to 7SL RNA. SINEs have been used as markers for phylogenetic studies owing to their character: The probability of independent retroposition at the same chromosome site is virtually nil, and a SINE insertion is irreversible (for a review, see Shedlock and Okada 2000). The insertion polymorphism of SINEs has been used to infer the phylogenetic relationship among species of primates (Bailey and Shen 1993, 1997; Hamdi et al. 1999), other animals (Murata et al. 1993; Shimamura et al. 1997; Nikaido, Rooney, and Okada 1999), and plants (Mochizuki et al. 1993; Tatout et al. 1999). Although SINEs are useful for phylogenetic studies, most published studies have been limited to an analysis of interspecies relationships. This mainly reflects the fact that most of the identified SINEs are fixed at particular loci in the population of a given species. Some Alu members, however, show insertion polymorphism in humans (Batzer et al. 1994; Roy et al. 1999), and several members of the salmon SmaI family show intraspecific polymorphism in chum salmon (Takasaki et al. 1997). These polymorphic members must have retroposed recently in the evolutionary time scale, and therefore they are not fixed in the human and salmon populations.
Here, we report the identification of members of a subfamily of p-SINE1, the first plant SINE identified in O. sativa and its related rice species (Umeda, Ohtsubo, and Ohtsubo 1991; Mochizuki et al. 1992, 1993; Motohashi et al. 1997). We show that these p-SINE1 members have been recently amplified in the O. sativa and O. rufipogon populations. A phylogenetic tree of the various O. sativa and O. rufipogon strains was constructed from "bar codes" based on the presence or absence of p-SINE1 members at particular loci in each strain. In this tree, the ecotypes of O. sativa or O. rufipogon strains are clearly distinguished. The O. sativa japonica strains and some perennial O. rufipogon strains appear to constitute one group. Most O. sativa indica strains and the annual O. rufipogon strains are separated but appear to constitute another group. This indicates that the japonica and indica strains are descended from different ancestors. The phylogenetic tree also suggests that temperate japonica strains originated from a common source and that a few indica strains originated by recent domestication in the annual O. rufipogon population. We also show that two types of chloroplast DNA are distributed in the rice strains tested and discuss the origin of the maternal source of O. sativa.
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Materials and Methods |
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Polymerase Chain Reaction
The polymerase chain reaction (PCR) analysis was done with Ex Taq DNA polymerase (Takara), as described elsewhere (Motohashi et al. 1997). The presence or absence of each p-SINE1 member was determined by identifying one unique PCR fragment with or without a p-SINE1 member after electrophoresis in the agarose gel. When the fragments differed in size or when two or more bands were present, the presence or absence of p-SINE1 in the fragments was confirmed by Southern hybridization or by direct sequencing of the PCR products (Mochizuki et al. 1993; Motohashi et al. 1997). Primer sequences will be provided upon request.
Adaptor-ligation basedPCR (ADL-PCR) (Spertini, Beliveau, and Bellemare 1999) was performed with Ex Taq DNA polymerase (Takara) as follows: The total DNA of O. sativa cv. IR36 or C5924 was digested with EcoRI, HindIII, BamHI, XbaI, NheI or SpeI (New England Biolabs), none of which cut the p-SINE1 sequence. T4 DNA ligase (New England Biolabs) was used to ligate the digested DNA with the oligonucleotide adaptor. PCR first was performed with a ligated sample as the template and with primers that hybridize to the adaptor and the p-SINE1 sequence to obtain fragments with the proximal portion of p-SINE1 and its flanking sequence. PCR then was accomplished with primers that hybridize to the adaptor and a different portion of the p-SINE1 sequence (see fig. 1 for primers used). Fragments that included the entire p-SINE1 sequence were obtained by an ADL-PCR with primers that hybridize to the flanking sequence of each identified member and the adaptor. Two pairs of primers [P1 and P2; P1(RA) and P2(RA) (see fig. 1)] were used to isolate general p-SINE1 members and RA subfamily members, respectively.
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Cloning and DNA Sequencing
In this study, PCR products were cloned into the pGEM-T Easy Vector plasmid (Promega), according to the supplier's instructions. DNA sequencing was done with a BigDye Terminator kit (PE Biosystem) and an ABI PRISM DNA sequencing system. Nucleotide sequence data reported are available in the DDBJ/EMBL/GenBank databases under the accession numbers AB086069AB086091.
Computer Analysis
Primary nucleotide sequences were analyzed with the GENETYX-Mac 10.1 system program. Nucleotide sequence searches of the DDBJ/Genbank/EMBL databases were done with the program BLAST (Altschul et al. 1990) and a Smith-Waterman search (Smith and Waterman 1981). Multiple sequences were aligned by use of the program CLUSTAL W (version 1.7).
To construct the phylogenetic tree for the various rice strains, the presence or absence of the p-SINE1 members at particular loci in the strains was organized into a data matrix, such that the presence of a p-SINE1 member at a given locus was coded 1, and its absence at the same locus was coded 0. Some strains generated two PCR-amplified fragments with or without a p-SINE1 member, indicative of both the presence and the absence of the member. Such a case was coded 1, the presence state. The Neighbor-Joining method was used with the computer program PAUP* 4.0b8 (Swofford 1998).
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Results and Discussion |
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Note that three members (r210, r215, and r216) were isolated by IPCR based on the sequences of transcripts in suspension-cultured cells of O. sativa cv. C5924 (see Materials and Methods). This indicates that some members with the common mutations are transcribed and supports the speculation that the six p-SINE1 members have recently been amplified.
Recently Amplified p-SINE1 Members Forming a Subfamily
To ascertain whether members other than the six with the three diagnostic mutations are present in O. sativa, we used ADL-PCR to isolate p-SINE1 members with mutations in the pol III promoter and obtained 16 members (r51r66; table 1). Except for two members, r64 and r65, these members carried the same three mutations as those in the six p-SINE1 members identified above (fig. 1B), suggesting that these and the six members form a subfamily. Two members (r64 and r65) did not have the third diagnostic mutation in the distal end region of p-SINE1 (fig. 1B), suggesting that they are not subfamily members. A computer-aided homology search of the databases further identified seven members (named r501r507) that have the three diagnostic mutations (table 1 and fig. 1B). Alignment of all members with three diagnostic mutations showed that they are highly homologous but divided into several groups, the members of which carry an additional diagnostic mutation(s) (fig. 1B).
To determine whether the newly identified 23 members have been recently amplified or not, their presence or absence at their respective loci in the rice strains was investigated. Twenty members were absent from the four rice species other than O. sativa and O. rufipogon and showed insertion polymorphism in O. sativa and O. rufipogon (table 1). One member, r63, which had a retrotransposon insertion within the p-SINE1 sequence, however, was present not only in O. sativa and O. rufipogon but also in two of the other four species (table 1), as was one (r34) of the six members identified earlier. Two members, r64 and r65, which were considered not to be subfamily members because of lack of a third diagnostic mutation in the distal end region of p-SINE1, were present in all the rice species (table 1), as expected. These findings indicate that p-SINE1 members that carry all three diagnostic mutations have been amplified in recent evolutionary time. We therefore named them RA (recently amplified) subfamily members.
As stated above, RA subfamily members have two mutations in the A-box and B-box sequences of the internal pol III promoter. These members have another mutation in the distal end region, which is thought to be important for priming reverse transcription and integration into the target site. All mutations that occurred in p-SINE1 may have had a positive influence on the transcription and retroposition of p-SINE1, leading to the beneficial amplification of RA subfamily members in the O. sativa and O. rufipogon populations.
Phylogenetic Analysis of O. sativa Strains Based on p-SINE1 Insertion Polymorphism
We collected 101 strains of O. sativa and O. rufipogon. O. sativa strains have been classified morphologically into indica and japonica (fig. 2). Except for seven strains, the O. rufipogon strains have been classified into two ecotypes, annual and perennial (fig. 2). Of the exceptional strains, five have been classified as an intermediate type and two as the annual type based on one classifier or as the perennial type based on another (fig. 2).
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Phylogenetic Analysis of O. rufipogon Strains
O. rufipogon strains are divided among all four groups on the tree (fig. 3). The five O. rufipogon intermediate-type strains examined are in group II or IV, whereas the two O. rufipogon strains, whose ecotype identification is inconsistent among different classifiers, also are in groups II and IV (fig. 3). This is significant because O. rufipogon shows remarkably high intraspecific variation (Morishima, Sano, and Oka 1992). Interestingly, all the annual O. rufipogon strains, except for one strain (W2004 in group IV), are present in group II, whereas the perennial strains are in each of the other three groups, I, III, and IV (fig. 3). This finding supports the speculation that the annual strains are derived from the primitive perennial strain (Morishima, Sano, and Oka 1992). The annual O. rufipogon strains have been referred to as an independent species, Oryza nivara (Sharma and Shastry 1965), whose classification is still accepted by some rice geneticists. Because annual type strains appear to form a distinct group in the O. rufipogon population (fig. 3), differentiation into the annual type should be considered an intraspecific variation, as reported previously (Oka 1988).
The insertion of SINE is thought to be irreversible. Therefore, it is reasonable that the ancestral state of the species with the AA genome would have had no insertion of any p-SINE1 member. The perennial strains of group IV have only a few p-SINE1 members at particular loci (fig. 2), which suggests that these strains may represent the progenitor of the other perennial strains as well as of the annual strains. In the phylogenetic tree, the hypothetical ancestor with no p-SINE1 members at the respective loci has been placed with the strains of group IV (fig. 3).
Polyphyletic Origin of O. sativa
The phylogenetic tree shows the japonica strains of O. sativa and six perennial strains of O. rufipogon are in group I (fig. 3), indicating that the japonica and perennial strains of this group originated from a common source, probably O. rufipogon of the perennial type. Note that five of the six perennial O. rufipogon strains in this group are from China (fig. 2).
The indica strains of O. sativa and annual strains of O. rufipogon are both in group II (fig. 3). Most indica strains are clearly distinct from the annual strains, indicating that both types of strains are originated from another common source. When we consider the fact that the O. sativa cultivars are essentially perennial plants (Morishima, Sano, and Oka 1992), the source is most likely O. rufipogon of the perennial type. However, a few indica strains, including those from Assam (India) and Nepal, are clustered with the annual strains (fig. 3). This suggests that these indica strains may have originated in the annual O. rufipogon population by recent domestication. These findings show that the O. sativa strains originated polyphyletically.
Relationship Between O. rufipogon and Other Wild Rice Species with the AA Genome
The presence or absence of all the p-SINE1 members at particular loci in the four strains belonging to the other four wild rice species with the AA genome (O. glumaepatula, O. meridionalis, O. longistaminata, and O. barthii ) was also investigated by PCR. These strains carry only some of the p-SINE1 members at the corresponding loci (fig. 2), and are clustered together with the perennial strains of O. rufipogon of group IV and with the hypothetical ancestor (fig. 3).
The four strains in the tree appear to be closely related (see fig. 3). This is due to the use of RA-subfamily p-SINE1 members, which are specifically present in strains of the O. rufipogonO. sativa population, but not in those of the other species. Therefore, to analyze the relationships among the strains of the other species in more detail, p-SINE1 members showing insertion polymorphism in one or more of the other species have to be used. In fact, the non-RA polymorphic p-SINE1 members identified in this study (see table 1) proved to be useful for the phylogenetic study of all the rice species with the AA genome, which showed that the O. sativa and O. rufipogon strains appear as one of several major branches of the phylogenetic tree (Cheng et al. 2002).
Analysis of the Maternal Source of the Rice Strains Investigated
Previous RFLP analysis indicated that there are overlaps in variation in the chloroplast DNA of O. sativa and O. rufipogon (Murata et al. 1993). It is reported that indica strains carry chloroplasts whose genome has a 69-bp deletion at the ORF100 locus, whereas japonica strains do not (Kanno et al. 1993; Kaneda et al. 1996). To clarify the variation in chloroplast DNA in the rice strains used in this study, the presence or absence of a deletion in chloroplast DNA was investigated by PCR with a pair of primers hybridizing to the sequences flanking ORF100. O. rufipogon strains of each of the four groups have chloroplast DNA with or without the deletion (see fig. 3 for strains [asterisk] with deleted chloroplast DNA). All four strains of the other wild rice species with the AA genome had chloroplast DNA without deletion (fig. 3). This suggests that chloroplast DNA deletion occurred after O. rufipogon diverged from its ancestral rice species.
As for O. sativa, 63% of the indica strains had chloroplast DNA with deletion, but the rest had the chloroplast DNA without deletion (fig. 3), suggesting that the indica strains have a polyphyletic maternal source. All the japonica strains, however, had chloroplast DNA without deletion (fig. 3), suggesting that japonica strains have a monophyletic maternal source. This finding is interesting but inconsistent, considering that some japonica strains have been derived by hybridization with indica strains in the course of variety improvement. The combination of cytoplasm carrying the deleted chloroplast DNA with the japonica-type nucleus may be restricted during natural selection by a mechanism as yet unknown. Moreover, nuclear substitution in japonica strains by indica strains may be frequent during variety improvement, whereas nuclear substitution in indica strains by japonica strains is rare. This rare form of nuclear substitution would lead to the production of japonica strains carrying chroloplast DNA without deletion. This theory may be supported by distorted segregation in indicajaponica hybrids, in which the segregation ratios usually deviate from the mendelian ratio owing to an increase in the number of genes derived from the indica parent (Oka 1988).
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Acknowledgements |
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Footnotes |
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E-mail: eohtsubo{at}ims.u-tokyo.ac.jp.
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Literature Cited |
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![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol 215:403-410.[CrossRef][ISI][Medline]
Bailey, A. D., and C. K. J. Shen. 1993. Sequential insertion of Alu family repeats into specific genomic sites of higher primates. Proc. Natl. Acad. Sci. USA 90:7205-7209.[Abstract]
Bailey, A. D., and 1997. Molecular origin of the mosaic sequence arrangements of higher primate a-globin duplication units. Proc. Natl. Acad. Sci. USA 94:5177-5182.
Batzer, M. A., M. Stoneking, M. Alegria-Hartman, et al. (11 co-authors) 1994. African origin of human-specific polymorphic Alu insertions. Proc. Natl. Acad. Sci. USA 91:12288-12292.
Chang, T.-T. 1976. The origin, evolution, cultivation, disseminationand diversification of Asian and African rice. Euphytica 25:425-441.[CrossRef][ISI]
Cheng, C., S. Tsuchimoto, H. Ohtsubo, and E. Ohtsubo. 2002. Evolutionary relationships among rice species with AA genome based on SINE insertion analysis. Genes Genet. Syst 77:323-334.[CrossRef][ISI][Medline]
Dally, A. M., and G. Second. 1990. Chloroplast DNA diversity in wild and cultivated species of rice (Genus Oryza, section Oryza): cladistic-mutation and genetic-distance analysis. Theor. Appl. Genet 80:209-222.[ISI]
Glaszmann, J. C. 1987. Isozymes and classification of Asian rice varieties. Theor. Appl. Genet 74:21-30.[ISI]
Hamada, M., N. Takasaki, J. D. Reist, A. L. Decicco, A. Goto, and N. Okada. 1998. Detection of the ongoing sorting of ancestrally polymorphic SINEs toward fixation or loss in populations of two species of charr during speciation. Genetics 150:301-311.
Hamdi, H., H. Nishio, R. Zielinski, and A. Dugaiczyk. 1999. Origin and phylogenetic distribution of Alu DNA repeats: irreversible events in the evolution of primates. J. Mol. Biol 289:861-871.[CrossRef][ISI][Medline]
Hirano, H.-Y., K. Mochizuki, M. Umeda, H. Ohtsubo, E. Ohtsubo, and Y. Sano. 1994. Retrotransposition of a plant SINE into the wx locus during evolution of rice. J. Mol. Evol 38:132-137.[CrossRef][ISI][Medline]
Kaneda, C., M. Umikawa, M. R. Singh, C. Nakamura, and N. Mori. 1996. Genetic diversity and subspecies differentiation in local rice cultivars from Manipur state of India. Breed. Sci 46:159-166.[ISI]
Kanno, A., N. Watanabe, I. Nakamura, and A. Hirai. 1993. Variations in chloroplast DNA from rice (Oryza sativa): differences between deletions mediated by short direct-repeat sequences within a single species. Theor. Appl. Genet 86:579-584.[ISI]
Kato, S., H. Kosaka, and S. Hara. 1928. On the affinity of rice varieties as shown by fertility of hybrid plants (in Japanese). Bull. Sci. Fac. Agric. Kyushu Univ 3:132-147.
Khush, G. S. 1997. Origin, dispersal, cultivation and variation of rice. Plant Mol. Biol 35:25-34.[CrossRef][ISI][Medline]
Maraia, R. J. 1995. The impact of short interspersed elements (SINEs) on the host genome. Springer-Verlag, New York.
Matsuo, T. 1952. Genealogical studies on cultivated rice (in Japanese). Bull. Natl. Inst. Agric. Sci. Jpn 3:1-111.
Mochizuki, K., H. Ohtsubo, H. Hirano, Y. Sano, and E. Ohtsubo. 1993. Classification and relationships of rice strains with AA genome by identification of transposable elements at nine loci. Jpn. J. Genet 68:205-217.[Medline]
Mochizuki, K., M. Umeda, H. Ohtsubo, and E. Ohtsubo. 1992. Characterization of a plant SINE, p-SINE1, in rice genomes. Jpn. J. Genet 67:155-166.[Medline]
Morinaga, T. 1954. Classification of rice varieties on the basis of affinity. Pp. 114 in Reports of the 5th Meeting of the International Rice Commission's Working Party on Rice Breeding. Ministry of Agriculture and Forestry, Tokyo.
Morishima, H. 1986. Wild progenitors of cultivated rice and their population dynamics. Pp. 314 in Rice genetics. International Rice Research Institute, Manila.
Morishima, H., H. I. Oka, and W.-T. Chang. 1961. Directions of differentiation in populations of wild rice, Oryza perennis and O. sativa F. spontanea. Evolution 15:326-339.[ISI]
Morishima, H., Y. Sano, and H. I. Oka. 1984. Differentiation of perennial and annual types due to habitat conditions in the wild rice Oryza perennis. Plant Syst. Evol 144:119-135.[ISI]
Morishima, H. 1992. Evolutionary studies in cultivated rice and its wild relatives. Oxford Surveys Evol. Biol 8:135-184.
Motohashi, R., K. Mochizuki, H. Ohtsubo, and E. Ohtsubo. 1997. Structures and distribution of p-SINE1 members in rice genomes. Theor. Appl. Genet 95:359-368.[CrossRef][ISI]
Murata, S., N. Takasaki, M. Saitoh, and N. Okada. 1993. Determination of the phylogenetic relationships among pacific salmonids by using short interspersed elements (SINEs) as temporal landmarks of evolution. Proc. Natl. Acad. Sci. USA 90:6995-6999.[Abstract]
Nikaido, M., A. P. Rooney, and N. Okada. 1999. Phylogenetic relationships among cetartiodactyls based on insertions of short and long interspersed elements: hippopotamuses are the closest extant relatives of whales. Proc. Natl. Acad. Sci. USA 96:10261-10266.
Ohtsubo, H., M. Umeda, and E. Ohtsubo. 1991. Organization of DNA sequences highly repeated in tandem in rice genomes. Jpn. J. Genet 66:241-254.[Medline]
Oka, H. I. 1958. Intervarietal variation and classification of cultivated rice. Indian J. Genet. Plant Breed 18:79-89.
Oka, H. I. 1964. Pattern of interspecific relationships and evolutionary dynamics in Oryza. Pp. 7190 in Rice genetics and cytogenetics. International Rice Research Institute, Elsevier, Amsterdam.
Oka, H. I. 1974. Experimental studies on the origin of cultivated rice. Genetics 78:475-486.
Oka, H. I. 1988. Origin of cultivated rice. Japan Sci. Soc. Press/Elsevier, Tokyo/Amsterdam.
Oka, H. I., and Morishima H. 1967. Variations in the breeding systems of a wild rice, Oryza perennis. Evolution 21:249-258.[ISI]
Oka, H. I., and 1982. Phylogenetic differentiation of cultivated rice. XXIII. Potentiality of wild progenitors to evolve the indica and japonica types of rice cultivars. Euphytica 31:41-50.[CrossRef][ISI]
Roy, A. M., M. L. Carroll, D. H. Kass, S. V. Nguyen, A.-H. Salem, M. A. Batzer, and P. L. Deininger. 1999. Recently integrated human Alu repeats: finding needles in the haystack. Genetica 107:149-161.[CrossRef][ISI][Medline]
Sano, Y., H. Morishima, and H. I. Oka. 1980. Intermediate perennial-annual populations of Oryza perennis found in Thailand and their evolutionary significance. Bot. Mag. (Tokyo) 93:291-305.[ISI]
Second, G. 1982. Origin of the genic diversity of cultivated rice (Oryza spp.): study of the polymorphism scored at 40 isozyme loci. Jpn. J. Genet 57:25-57.
Sharma, S. D., and S. V. S. Shastry. 1965. Taxonomic studies in genus Oryza L: III. O. rufipogon griff. sensu stricto and O. nivara Sharma et Shastry nom. nov.. Indian J. Genet. Plant Breed 25:157-167.[ISI]
Shedlock, A. M., and N. Okada. 2000. SINE insertions: powerful tools for molecular systematics. BioEssays 22:148-160.[CrossRef][ISI][Medline]
Shimamura, M., H. Yasue, K. Ohshima, H. Abe, H. Kato, T. Kishiro, M. Goto, I. Munechika, and N. Okada. 1997. Molecular evidence from retroposons that whales form a clad within even-toed ungulates. Nature 388:666-670.[CrossRef][ISI][Medline]
Smith, T. F., and M. S. Waterman. 1981. Identification of common molecular subsequences. J. Mol. Biol 147:195-197.[ISI][Medline]
Spertini, D., C. Beliveau, and G. Bellemare. 1999. Screening of transgenic plants by amplification of unknown genomic DNA flanking T-DNA. Biotechniques 27:308-314.[ISI][Medline]
Swofford, D. L. 1998. PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, Mass.
Takasaki, N., T. Yamaki, M. Hamada, L. Park, and N. Okada. 1997. The salmon SmaI family of short interspersed repetitive elements (SINEs): interspecific and intraspecific variation of the insertion of SINEs in the genomes of chum and pink salmon. Genetics 146:369-380.
Tatout, C., S. Warwick, A. Lenoir, and J. M. Deragon. 1999. SINE insertions as clade markers for wild crucifers species. Mol. Biol. Evol 16:1614-1621.
Tenzen, T., Y. Matsuda, H. Ohtsubo, and E. Ohtsubo. 1994. Transposition of Tnr1 in rice genomes to 5'-PuTAPy-3' sites, duplicating the TA sequence. Mol. Gen. Genet 245:441-448.[CrossRef][ISI][Medline]
Umeda, M., H. Ohtsubo, and E. Ohtsubo. 1991. Diversification of the rice Waxy gene by insertion of mobile DNA elements into introns. Jpn. J. Genet 66:569-586.[Medline]
Wang, Z. Y., and S. D. Tanksley. 1989. Restriction fragment length polymorphism in Oryza sativa L. Genome 32:1113-1118.[ISI]
Wang, Z. Y., G. Second, and S. D. Tanksley. 1992. Polymorphism and phylogenetic relationships among species in the genus Oryza as determined by analysis of nuclear RFLPs. Theor. Appl. Genet 83:565-581.[ISI]
Wu, C.-I. 1991. Inference of species phylogeny in relation to segregation of ancient polymorphism. Genetics 127:429-435.