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Genetics and Molecular Biology |
2Laboratory of Ecology and Genetics, Graduate School of Environmental Earth Science, Hokkaido University, Sapporo, Hokkaido 060-0810, Japan; 3Mukogaoka, Ebetsu-city, Hokkaido 067-0075, Japan
Received for publication March 23, 2004. Accepted for publication November 17, 2004.
ABSTRACT
Abandonment of sexual reproduction is a well-known characteristic in aquatic plants, while the causes, levels, and consequences of sterility are often unknown. Utricularia australis f. australis (Lentibulariaceae) is a free-floating, sterile bladderwort distributed widely in temperate and tropical regions. Experimental crosses in cultivated conditions, AFLP analysis, and cpDNA haplotypes of natural populations clearly demonstrated that U. australis f. australis originates from the asymmetric hybridization between two parental taxa: U. australis f. tenuicaulis (mostly as female) and U. macrorhiza (mostly as male). No post-F1 hybrids were detected using the additive patterns of AFLP bands combined with the observation of extensive sterility in U. australis f. australis. Recurrent hybridizations and subsequent perpetuation by asexual reproduction were demonstrated by the unique, but monomorphic, AFLP genotypes observed in each U. australis f. australis population. Hybrids and parental species did not coexist, implying the superiority of the hybrid U. australis f. australis in certain environmental conditions. It remains unclear whether populations of U. australis f. australis are maintained by colonizing propagules or as relicts of past hybridization events.
Key Words: AFLP • asymmetric crossability • clonal reproduction • cpDNA haplotypes • F1 dominance • free-floating aquatic plant • hybrid sterility • hybrid vigor
Of the angiosperms with diverse flowering systems, many combine both sexual and asexual reproduction. The relative importance of both reproductive modes, however, may vary among species as well as among populations within species (Eckert, 2002
). In the aquatic environment, sexual reproduction is rather difficult for the great majority of angiosperms due to limited flowering opportunity; clonal reproduction, therefore, plays an essential role in their recruitment (Grace, 1993
). Moreover, several forms of clonal offspring, such as turions, winter buds, and shoot fragments, are highly effective and economical in the aquatic environment, reducing the selective value of sexual reproduction (Grace, 1993
; Les and Philbrick, 1993
).
In the aquatic angiosperm Elodea canadensis (Canada pondweed), the loss of sexual reproduction combined with the high vagility of its clonal offspring has been observed, with only female plants being distributed in northern Europe (Sculthorpe, 1967
; Hutchinson, 1975
). Similar examples, that is, the presence of a single mating type in a population or region, are observed in several other species: dioecious Hydrilla verticillata (Verkleij et al., 1983
), and heterostylous Pontederia rotundifolia (Barrett, 1977
). Thus, extensive clonal reproduction, high dispersal ability of vegetative propagules, and rare-to-sporadic sexual reproduction represent life-history traits typical of aquatic angiosperms (Les and Philbrick, 1993
).
The limitation and/or absence of sexual reproduction results from both biotic and abiotic factors (reviewed in Barrett et al., 1993
; Eckert, 2002
). These factors include the accumulation of sterile genes, meiotic irregularities associated with hybridization and changes in ploidy level, environmental suppression of seed maturation, and dominance of a single clone in a self-incompatible species. Thus, investigations of the mechanisms underlying sterility and its relationship to clonal reproduction are essential to understand the ecological traits and evolutionary processes of aquatic plants.
Utricularia australis R. Br. (Lentibulariaceae) is a free-floating, aquatic plant widely distributed in temperate and tropical regions, except North and South America (Taylor, 1989
). In spite of its cosmopolitan distribution, almost complete sterility is recognized in this species (Taylor, 1989
). A fertile group, however, has been observed only in Japan (Komiya and Shibata, 1980
; Taylor, 1989
). The fertile and sterile groups in Japan were first recognized as two different species, fertile U. tenuicaulis Miki (Miki, 1935
) and sterile U. japonica Makino (Makino, 1914
). Fertile U. tenuicaulis morphologically differs from sterile U. japonica in having a solid-core peduncle, short, quadrified absorptive bladder hairs, and small oblong turions (Miki, 1935
). These two species, however, are now both regarded as U. australis and are referred to as fertile U. australis f. tenuicaulis, and sterile U. australis f. australis (Komiya and Shibata, 1980
; Taylor, 1989
).
Several studies on U. australis (often treated by different names) have focused on taxonomical classification (Tamura, 1953
; Taylor, 1989
; Kadono, 1994
), geographical distribution (Komiya and Shibata, 1980
), and ecological traits (Yamamoto and Kadono, 1990
; Araki, 2000
; Araki and Kadono, 2003
). A recent report of Komiya et al. (1997)
determined the distribution of a closely related fertile taxon in Japan, U. macrorhiza Le Conte. Misidentification of U. macrorhiza as U. australis seems probable, because a detailed comparison of morphological traits is required to discriminate between the two (Komiya et al., 1997
).
In the present study, we aim to reveal the causes, levels, and consequences of sterility in U. australis f. australis, taking into consideration two closely related fertile taxa, U. australis f. tenuicaulis and U. macrorhiza. We examined (1) the potential ability of sexual reproduction and crossability under cultivation, (2) the maternal lineages of this sterile taxon by analyzing two regions of cpDNA, and (3) the genetic relationship among three taxa by amplified fragment length polymorphism (AFLP) analysis.
MATERIALS AND METHODS
Sampling of plant materials
The distribution ranges in Japan of the three bladderworts, U. australis f. australis, U. australis f. tenuicaulis, and U. macrorhiza, are rather uncertain, mainly due to limited information. Because several studies on the northern island of Japan, Hokkaido, revealed the distribution pattern (Komiya et al., 1997
) and ecological traits (Araki, 2000
) of these bladderworts, our plant materials were collected mainly from this region (Table 1, Fig. 1).
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Pollen germination and experimental crosses
Pollen germination was examined for 20, 28, and 26 flowers of cultivated U. australis f. tenuicaulis, U. australis f. australis, and U. macrorhiza, respectively. Pollen grains were collected from the anther of each flower and cultivated in 5% sucrose solution at 25°C for 1 h according to Araki (2000)
. The number of pollen grains counted for each flower was 383.9 ± 17.6 (mean ± SE). The pollen germination rate, based on the number of germinated and ungerminated pollen grains, was recorded for each flower.
Experimental crosses were conducted for the 26 cultivated populations. In all populations, scapes developed above the water surface from mid-June to late August, and approximately 5–10 flowers were observed on each scape. Scapes were covered with cellophane paper to exclude unintentional pollination from outside of the following experimental treatments: (1) self-pollination with their own pollen grains, (2) cross-pollination with different populations of the same taxon, and (3) cross-pollination with different taxa. Different treatments were often applied to different flowers on the same scape because of the limited number of flowers. Mature fruits were collected prior to dehiscence from mid-July to late-September, and the number of seeds per fruit was counted under a stereomicroscope. As a control for experimental crosses, 17, 87, and 51 flowers for each of U. australis f. tenuicaulis, U. australis f. australis, and U. macrorhiza, respectively, were kept covered without any treatment. These covered flowers produced no seeds, demonstrating the dependence on experimental pollination for seed production.
DNA extraction
Total genomic DNA was isolated from about 50 mg of tissue from each of the 128 frozen stems according to a CTAB (hexadecyltrimethylammonium bromide) miniprep procedure (Stewart and Via, 1993
).
Chloroplast DNA analysis
Two regions of cpDNA were amplified by universal primers: the trnT-trnL region by primers "a" and "b" (Taberlet et al., 1991
), and trnQ-trnS intergenic spacer region by the primer pair ccmp2 (Weising and Gardner, 1999
). PCR amplification was performed with the GeneAmp PCR system 9700 thermal cycler (Applied Biosystems, Foster City, California, USA). PCR product sizes were determined for all 128 samples using the ABI Prism 3100 automated sequencer (Applied Biosystems) and GENESCAN v3.7.1 analysis software (Applied Biosystems).
Four samples were selected from each haplotype and sequenced using the BigDye Terminator Cycle Sequencing kit (v3.1, Applied Biosystems) and the ABI Prism 3100 automated sequencer (Applied Biosystems) with its associated DNA sequencing analysis software v.3.7.
AFLP analysis
AFLP was performed for all 128 samples according to Vos et al. (1995)
with some modifications. Genomic DNA (
0.1 µg per sample) was digested with the restriction enzymes EcoRI and MseI at 37°C, 1.5 h. Double-stranded adaptors were ligated to the ends of the digested DNA fragments at 20°C, overnight. The resulting products were amplified using two steps: pre-amplification using primers with one additional (selective) base, and selective amplification using primers with three selective bases. Selective amplifications were conducted with the MseI-CAG primer in combinations with EcoRI-ACT (FAM), -ACG (VIC), and -AGC (NED) primers. The AFLP Amplification Core Mix (Applied Biosystems) and the GeneAmp PCR system 9700 thermal cycler (Applied Biosystems) were used for both amplifications. AFLP fragments were detected with the ABI Prism 3100 automated sequencer and GENESCAN analysis software.
Statistical analysis
The pollen germination ratio expressed as a percentage was transformed (x' = arcsin 
) prior to statistical analysis. The means of pollen germination rates and number of seeds produced were compared using one-way ANOVA. Significant differences (P < 0.05) were assessed with Tukey's honestly significant difference (HSD) test. All statistical analyses were performed using JMP 4.0 software (SAS Institute, Cary, North Carolina, USA).
The presence/absence data of AFLP segments (bands) were subjected to principal coordinates analysis (PCOA). Genetic similarity was estimated as Sij = 2Nij/(Ni + Nj), where Nij is the number of shared bands between plants i and j, Ni and Nj is the number of bands found in plants i and j, respectively (Dice, 1945
). Genetic similarity was transformed to dissimilarity using the formula Dij = 1 – Sij, and then subjected to PCOA. All calculations were performed with R Package 4.0 software (Casgrain and Legendre, 1999
).
RESULTS
Pollen germination and experimental crosses
We found that Utricularia australis f. australis had almost completely lost its male function: only 0.6% of its pollen grains germinated, whereas 54.3% of the pollen of U. australis f. tenuicaulis and 42.6% of U. macrorhiza germinated (Table 2). The pollen germination rate was significantly lower for U. australis f. australis, but not significantly different between U. australis f. tenuicaulis and U. macrorhiza. In addition to the nearly complete loss of male function, a defect in female function in U. australis f. australis was confirmed by experimental crosses: only a small number of seeds, 1.28 and 0.48 seeds, on average, were produced by crosses with fertile U. australis f. tenuicaulis and U. macrorhiza, respectively (Table 3). Moreover, both self- and cross-pollination in U. australis f. australis produced no seed, demonstrating complete sterility within the taxon (Table 3).
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CpDNA analysis
Two cpDNA lengths were observed at the trnT-trnL region: 404 and 412 bp (Table 4). Sequence analyses confirmed that these haplotypes differed by two indels (2 bp and 6 bp) together with one substitution (DDBJ accession numbers AB161189 for U. australis f. tenuicaulis and AB161188 for U. macrorhiza). Variation in cpDNA was also observed in the trnQ-trnS region; the two haplotypes of 175 and 181 bp (Table 4) differed by a 4-bp indel at one site (DDBJ accession numbers AB161191 for U. australis f. tenuicaulis and AB161190 for U. macrorhiza).
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AFLP analysis
A total of 80 polymorphic bands were identified using three primer pairs that discriminated 20 genotypes: four genotypes from seven populations of U. australis f. tenuicaulis, eight from 10 populations of U. australis f. australis, and eight from nine populations of U. macrorhiza (Table 4). Each population had only one genotype that was occasionally observed in different population(s) (Table 4). The two fertile taxa, U. australis f. tenuicaulis and U. macrorhiza, had 21 and 20 species-specific bands, respectively (Table 4). Both sets of these specific bands were additively observed in sterile U. australis f. australis: 81–100% of U. australis f. tenuicaulis specific bands and 85–95% of U. macrorhiza specific bands (Table 4). The intermediacy of U. australis f. australis was confirmed by PCOA, in which the three taxa were completely discriminated along the first axis (Fig. 2).
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Levels of sterility in Utricularia australis f. australis
Utricularia australis f. australis is almost completely sterile (Tables 2 and 3), consistent with the conclusions of Taylor (1989)
. This result is also supported by the observation of Yamamoto and Kadono (1990)
; the abnormal formation of embryo sac and high percentage of abortive pollen in U. australis f. australis (treated as U. vulgaris var. japonica in their study). While Araki (2000)
reported the fertility of some strains of U. australis f. australis in Japan, the finding could be explained as the misidentification of fertile U. macrorhiza. Indeed, we have confirmed that several populations of U. macrorhiza identified in the present study (M1, M2, M3, M4, M5 in Table 1) were treated as U. australis f. australis by Araki (2000)
. Thus, we conclude that almost complete sterility in U. australis f. australis is unambiguous, at least for those growing in Japan.
Asymmetric crossability between two fertile taxa
The two fertile taxa or "species," Utricularia australis f. tenuicaulis and U. macrorhiza, demonstrate asymmetric crossability (Table 3). When U. australis f. tenuicaulis is used as the maternal parent, the number of seeds produced is equal to that produced by the taxon's intraspecific crosses. However, significantly fewer seeds are produced by the opposite combination (female U. macrorhiza x male U. australis f. tenuicaulis).
The asymmetric crossability observed in this study can be explained by two mechanisms. First, a self-compatible species can be successfully crossed with pollen from a self-incompatible species, whereas the opposite configuration cannot succeed. This is the SC x SI rule (Harrison and Darby, 1955
; Lewis and Crowe, 1958
; De Nettancourt, 1984
; reviewed in Arnold, 1997
) in which S alleles play an essential role for reproductive barriers. Self-compatibility in U. australis f. tenuicaulis is double (32.8%) that in U. macrorhiza (15.9%), demonstrating a pattern consistent with the SC x SI rule.
The second possible explanation for asymmetric crossability is incongruity: a lack of co-adaptation between species that includes their physiological, biochemical, and structural characteristics (Hogenboom, 1975
, 1984
). The disparity in style and pollen tube length could represent a structural incongruity that would result in unilateral success of interspecific hybridization when small-flowered species are used as seed parents (Williams and Rouse, 1988
; Gore et al., 1990
). The body of U. australis f. tenuicaulis is apparently smaller than that of U. macrorhiza (Y. Kameyama, personal observation). Moreover, the pistil length in U. australis f. tenuicaulis (Miki, 1935
) is nearly one-half that in U. macrorhiza (Taylor, 1989
). These structural differences are consistent with the hypothesis of incongruity.
Additional research, however, is required to reveal whether the differences of self-incompatibility (SC x SI rule) and/or structural incongruity in style and pollen tube length are essential for the asymmetric crossability between U. australis f. tenuicaulis and U. macrorhiza.
Hybrid origins and F1 dominance in Utricularia australis f. australis
The hybrid origin of sterile U. australis f. australis from two fertile taxa, U. australis f. tenuicaulis and U. macrorhiza, is clearly demonstrated by several criteria: the additive patterns of AFLP bands, intermediacy in the PCOA scattergram, and the absence of a specific cpDNA haplotype in U. australis f. australis (Table 4, Fig. 2). In addition, most of the cpDNA haplotypes observed in U. australis f. australis are derived from U. australis f. tenuicaulis (9 of 10 populations, or 7 of 8 AFLP genotypes) (Table 4), consistent with the asymmetric crossability between parental species, assuming that cpDNA in these taxa are inherited maternally as they are in the majority of angiosperms (Corriveau and Coleman, 1988
; Harris and Ingram, 1991
).
Extensive dominance of F1 hybrids in U. australis f. australis populations are also demonstrated by AFLP analysis (Table 4). An F1 generation should always be heterogeneous for each set of parent-specific AFLP bands, and 100% of these would be expressed. If later generation hybrids were produced, the proportion of parent-specific AFLP bands observed in BC1 would be 100% and 50% for one parental species and the other, respectively. Similarly, an F2 generation would express 75% of parent-specific bands for both parental species. In the present study, each genotype of U. australis f. australis had 81–100% of U. australis f. tenuicaulis-specific bands and 85– 95% of U. macrorhiza-specific bands (Table 4). Taking into consideration undetected polymorphisms of parental species, the observed band patterns strongly support the absence of post-F1 hybrids in U. australis f. australis populations, a phenomenon that must be caused by extensive hybrid sterility (Tables 2, 3).
High levels of sterility combined with extensive F1 dominance is often observed in a triploid sterile hybrid. However, estimated number of chromosome is 2n = 40 for U. macrorhiza (Löve, 1954
), and n = 18–20 (Reese, 1951
), n = 18, 19, 20, 22 (Casper and Manitz, 1975
) for U. australis f. australis. While no comparable data is available for U. australis f. tenuicaulis, DNA amount estimated by flow cytometry (FCM) is almost equal to both U. australis f. australis and U. macrorhiza (Y. Kameyama et al., unpublished data). Thus, it is reasonable to consider that U. australis f. australis originated from the hybridization between diploid species, U. australis f. tenuicaulis and U. macrorhiza. Moreover, the apparent variation in chromosome complement observed in U. australis f. australis (Reese, 1951
; Casper and Manitz, 1975
) likely reflects the meiotic irregularity due to hybridization, while we have no direct evidence.
There are two modes for the origin of hybrid lineages: homoploidy (i.e., diploid derivatives) and polyploidy. Polyploidy has played a major role in the evolution of many eukaryotes (Soltis and Soltis, 1993
, 1999
) and 70% of all angiosperms have experienced one or more episodes of polyploidization (Masterson, 1994
). Several examples of diploid level speciation, however, have also been demonstrated for flowering plants, such as Helianthus (Rieseberg, 1991
, 2000
) and Iris (Arnold, 1993
). The most widely accepted model for homoploid hybrid speciation is the recombinational model, where rapid chromosomal evolution, strong natural selection for the most fertile or viable hybrid segregants, and the availability of suitable habitat for the establishment of hybrid neospecies play a critical role (reviewed in Rieseberg and Carney, 1998
). In the present study, diploid hybrid U. australis f. australis could not be established as a "new species" from the viewpoint of sexual reproduction, because of the extensive sterility (Tables 2 and 3) and the absence of post-F1 hybrids (Table 4). These results, however, provide insight about the importance of asexual reproduction in aquatic plants.
Interspecific hybrids are highly variable in fertility and vigor, but in general, F1 hybrids of closely related species tend to exceed their parents in vegetative vigor or robustness (Grant, 1975
; Rieseberg and Carney, 1998
). As reviewed in Les and Philbrick (1993)
, several hydrophyte hybrids demonstrate extreme vegetative vigor, allowing them to compete with or even displace parental species. Utricularia australis f. australis has cosmopolitan distributions, while both of the proposed parental species are restricted to rather small areas as described in the Introduction (Taylor, 1989
; Komiya and Shibata, 1980
). Moreover, U. australis f. australis, analyzed in the present study was never found to coexist with its proposed parental species (Table 4), implying its superiority under certain environmental conditions. However, more thorough research is required to reveal the hybrid vigor of U. australis f. australis in relation to habitat selection and to determine whether U. australis f. australis in other geographic regions has the same origin as it does in Japan.
Separate distributions of the proposed parental species (U. australis f. tenuicaulis and U. macrorhiza) and its hybrid (U. australis f. australis) raise the following question: where and how do hybrids originate? One possible answer is that every population of U. australis f. australis derives from colonizing propagules that originated from outside of Japan. Long-distance dispersal by waterbirds is a well-known characteristic of aquatic organisms (Figuerola and Green, 2002
; Green et al., 2002
), which makes the expansion of hybrids possible, even those with low sexual fertility. Another possible answer is that the present populations of U. australis f. australis are relicts of past hybridization events. Isozyme analyses of the hybrid Potamogeton x suecicus (= P. pectinatus x P. filiformis) reveal that each of two populations of P. x suecicus, which is distributed south of the present distribution limit of one parental species P. filiformis, is a single clone and that they may be relicts of the Weichselian glacial period (Hollingsworth et al., 1996a
).
In spite of the F1 dominance and hybrid sterility in U. australis f. australis, AFLP genotypes are highly polymorphic among its populations (Table 4, Fig. 2). This result implies that hybridization occurred between several different AFLP genotypes of parental species, U. australis f. tenuicaulis and U. macrorhiza, because both later generation hybridization and sexual reproduction are unlikely in U. australis f. australis. In addition, the parental species have the monomorphic AFLP genotype within each population (Table 4). Thus, we conclude that the polymorphic AFLP genotypes observed in U. australis f. australis originated from the recurrent hybridization between several parental populations.
The type of breeding system is one of the most important factors influencing the patterns of genetic variation within and among populations. The low levels of intrapopulation differentiation observed in the three Utricularia (Table 4) are most likely due to widespread clonal multiplication, as has been reported for some aquatic plants (Hofstra et al., 1995
; Hollingsworth et al., 1996b
). In the case of Myriophyllum and Potamogeton species, there is limited variation between populations and even less variation within populations (Hofstra et al., 1995
). The patterns of distribution of isozyme phenotypes and genotypes over populations suggest that both Myriophyllum and Potamogeton populations are often started by a single colonizing propagule, or several propagules of identical genotype, which then spread predominantly through vegetative propagation (Hofstra et al., 1995
). A similar scenario is appropriate for Utricularia populations, while the origin of U. australis f. australis depended on the hybridization between two fertile taxa, U. australis f. tenuicaulis and U. macrorhiza.
The spatial and historical origins of U. australis f. australis remain unclear. However, it is clear from our studies that it is/ was produced by recurrent hybridization between U. australis f. tenuicaulis and U. macrorhiza and that sterile F1 hybrids may perpetuate by asexual reproduction with presumed hybrid vigor.
Taxonomic implications
To our knowledge, this is the first report of unambiguous hybridization in the genus Utricularia; such hybridization has been proposed in the past, but either has been rejected or not demonstrated, as pointed out by Taylor (1989)
. Although taxonomical classification is not the main focus of the present study, some taxonomical implications can be offered for U. australis.
Two morphologically similar taxa, sterile U. japonica (Makino, 1914
) and fertile U. tenuicaulis (Miki, 1935
) have been recognized in Japan. Komiya and Shibata (1980)
regarded U. japonica as a straightforward synonym of U. australis and the latter as a forma of this taxon, U. australis f. tenuicaulis. While several different opinions exist (Tamura, 1953
; Tamura, 1981
; Kadono, 1994
), the classification of Komiya and Shibata (1980)
is accepted in Taylor's monograph (1989)
.
The present study clearly demonstrates that sterile U. australis f. australis originated from hybridization between U. australis f. tenuicaulis and U. macrorhiza. Thus, we suggest U. australis f. australis and U. australis f. tenuicaulis should be treated as different taxonomic groups. However, because U. australis comprises a large number of synonyms across the world, we cannot assign relevant scientific names to U. australis f. australis and U. australis f. tenuicaulis without further studies. AFLP analysis could play a major role for revision of these taxa.
Conclusions
Utricularia australis f. australis clearly originated from the asymmetric hybridization between U. australis f. tenuicaulis (mostly as female) and U. macrorhiza (mostly as male). This asymmetric crossability is likely due to the differences of self-compatibility (SC x SI rule) and/or structural incongruity in style and pollen tube length. The hybrid U. australis f. australis has extensive sterility, with no existence of post-F1 generation detected by AFLP analysis. Recurrent hybridizations between parental species and the subsequent perpetuation by asexual reproduction are demonstrated by unique, but monomorphic, AFLP genotypes observed in each U. australis f. australis population. Coexistence of the hybrids and parental species has not been observed, implying the superiority of sterile U. australis f. australis at least under certain environmental conditions. Whether populations of U. australis f. australis are maintained by colonizing propagules or as relicts of past hybridization events remains unclear.
FOOTNOTES
1 We acknowledge the considerable advice of Dr. Satoru Araki, Research Center for Coastal Lagoon Environments, Shimane University. Technical advice was also given by Dr. Yuji Isagi, Faculty of Integrated Arts and Sciences, Hiroshima University; Dr. Yoshihisa Suyama, Graduate School of Agricultural Science, Tohoku University; and Dr. Hiroyuki Shibaike, Department of Biological Safety, National Institute for Agro-Environmental Sciences. Experimental crosses were conducted with the cooperation of Dr. Toshio Iwakuma, Graduate School of Environmental Earth Science, Hokkaido University. This study was supported by a grant-in-aid from the Ministry of Education, Culture, Sports, Science and Technology for the 21st Century Center of Excellence Program, and from the Japan Society for the Promotion of Science (JSPS) for Scientific Research (15370006, 16370007) and Research Fellowships for Young Scientists. 
4 Corresponding author (ohara{at}ees.hokudai.ac.jp
) fax: +81-11-706-4525
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