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Reproductive Biology |
The Kyoto University Museum, Yoshida-hon-machi, Sakyo, Kyoto, 606-8501, Japan
Received for publication September 11, 2003. Accepted for publication January 8, 2004.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: breakdown of distyly • chromosome numbers • Damnacanthus • heterostyly • pollen dimorphism • polyploidy • Rubiaceae
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Liao, 1976
; Lo, 1979
; Yamazaki, 1987
, 1993
; Ruan, 1999
). Every species of Damnacanthus is a small evergreen shrub, often occurring in natural laurel forests. A conspicuous characteristic of the genus is heterophylly associated with sympodial growth (Robbrecht et al., 1991
).
Naiki and Nagamasu (2003)
reported distyly for Damnacanthus for the first time. Distyly is a genetic dimorphism in which plant populations are comprised of flowers with a long style and short stamens (pin flowers) and flowers with a short style and long stamens (thrum flowers). Distyly has evolved independently on approximately 20 angiosperm families and is known as an outcrossing breeding system (Ganders, 1979
; Barrett, 1992
). Rubiaceae have the largest number of distylous genera within the angiosperm families (Anderson, 1973
; Ganders, 1979
). Some taxa of Damnacanthus are monomorphic, always possessing flowers with a long style and short stamens, similar to the pin flowers in the distylous taxa (Naiki and Nagamasu, 2003
).
Damnacanthus exhibits pollen dimorphism not only for size, but also surface structure of the pollen (Naiki and Nagamasu, 2003
). In the distylous taxa of Damnacanthus, pollen grains from thrum flowers are significantly larger than those from pin flowers. The muri of the pollen grains of Damnacanthus are smooth in pin flowers, whereas the pollen grains of thrum flowers have minute granules on the top and/or on the sides of the muri. In the taxa with monomorphic flowers, in which the style is longer than the stamens like the pin flowers of the distylous taxa, the size of the pollen grains is similar to or a little larger than the thrum pollen grains of the distylous taxa, and the muri always possess minute granules like the thrum flowers of the distylous taxa (Naiki and Nagamasu, 2003
). Therefore, the difference in pollen structure between distylous and monomorphic Damnacanthus is useful in determining whether a flower in a herbarium specimen of Damnacanthus was collected from a distylous or a monomorphic population.
Polyploidy is thought to be a significant process affecting the evolution of vascular plants (Stebbins, 1971
). Successful polyploidization leads to new lineages and the establishment of new species (Lewis, 1980b
). Variation in chromosome number is also one of the most important and useful characteristics for systematic studies. Kiehn (1995)
showed that in Rubiaceae, polyploidy frequently occurred and that karyological characteristics such as ploidy levels, chromosome structures, karyotypes, and DNA content are useful for understanding relationships among taxa in the family.
Previously for Damnacanthus, there has been only one report of chromosome number—for pollen mother cells of D. indicus var. indicus, the chromosome number n is 11 (Robbrecht et al., 1991
). Here, we report new chromosome counts in Damnacanthus, showing that polyploidy also has occurred in the genus. We found that the ploidy level and the occurrence of distyly have a clear correlation in Damnacanthus. We discuss possible evolutionary explanations of this correlation in Damnacanthus.
In Damnacanthus indicus, the most widely and abundantly distributed species in the genus, leaf variation is quite large. The taxonomy of the varieties within D. indicus has been based only on the combination of leaf size and spine length (Makino, 1904
; Koidzumi, 1933
; Yamazaki, 1987
, 1993
). The second aim of this study is to investigate whether a correlation exists between such morphological variations and chromosome number in D. indicus.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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and Ruan (1999)
with the exception of D. giganteus. Damnacanthus giganteus is treated as D. macrophyllus f. giganteus in Yamazaki (1987)
, but Naiki and Nagamasu (2003)
palynologically supported Nakai's treatment (1922)
in which the taxa are treated as an independent species.
Distyly occurrence
Naiki and Nagamasu (2003)
already reported that Damnacanthus biflorus, D. indicus var. microphyllus, D. indicus var. parvispinus, and D. okinawensis are distylous and that D. giganteus and D. macrophyllus have monomorphic flowers, which always have a long style and short stamens, similar to the pin flowers of the distylous taxa (Naiki and Nagamasu, 2003
).
Because there are both distylous and monomorphic populations in Damnacanthus indicus var. major (Naiki and Nagamasu, 2003
), we further investigated the occurrence of distyly in 90 populations of D. indicus (Appendix 1). In other species in Japan, a few additional populations were investigated for distyly (Appendix 1).
We examined the occurrence of distyly in the taxa from China and Taiwan: D. angustifolius, D. henryi, D. labordei, D. officinarum, and D. tsaii, using herbarium specimens in HAST, IBSC, KUN, PE, and TAI.
Pollen morphology
Naiki and Nagamasu (2003)
investigated the pollen morphology of Damnacanthus in Japan. In this study, we observed pollen grains of six species of Damnacanthus in Taiwan and China using herbarium specimens, D. angustifolius, D. henryi, D. labordei, D. officinarum, and D. tsaii (Appendix 2; see Supplemental Data accompanying the online version of this article). To observe pollen morphology, the grains were prepared by the acetolysis method (Erdtman, 1960
) after potassium hydroxide digestion. The acetolyzed pollen grains were critical point dried, coated with gold by a fine coater (Model JFC-1200, JEOL, Tokyo, Japan) and observed with a scanning electron microscope (SEM) (Model JSM-5800LV, JEOL).
Chromosome counts
Except for one sample of seed material from China, all investigated plant individuals from China; Japan, South Korea; and Taiwan (Appendix 1) were transplanted to the laboratories of the Kunming Institute of Botany (Chinese Academy of Sciences), the Kyoto University Museum, and the National Taiwan University, respectively. The shoots with roots from larger individuals were cut off and planted, and the remaining shoots were collected as the voucher specimens, whereas whole juveniles were planted without cutting off. Materials from Japan, South Korea, and Taiwan were collected from the same populations as those observed in the distyly occurrence study. About one month later, newly elongated roots were used as follows.
Methods for the observation of somatic chromosomes were modified from those of Oginuma and Nakata (1988)
and Takano (2001)
. Root tips were cut and incubated in 0.002 mol/L 8-hydroxyquinoline at 18°C for 6 h before fixation in Farmer's fixative (3 : 1 ethanol : glacial acetic acid) at 4°C for at least 24 h. The root tips were macerated in 1 mol/L hydrochloric acid at 60°C for 3 min and then suspended in 45% acetic acid for 1 min. After hydrolysis, root tip meristems were isolated and stained with 2% aceto-orcein for 10–30 min, then squashed. Voucher specimens for chromosome counts were deposited in the herbarium at Kyoto University (kyo).
Leaf length and width of Damnacanthus indicus
The leaf length and width of D. indicus from Japan, South Korea (Cheju Island), and Taiwan were measured using calipers. Materials were collected from the same localities as those for chromosome observations (Appendix 1). The average length and width of foliage leaves from 10 individuals per population was used for comparison.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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reported only populations with monomorphic flowers. In all the taxa above, almost no flowers were found with the same length between the style and stamens in both the distylous and monomorphic populations. The anther/stigma distance of the monomorphic flowers is similar to or larger than that of the pin flowers of the distylous taxa. Thus, most monomorphic flowers did not seem to be autogamous. Distyly was found for four species of Damnacanthus in Taiwan and China; these species were D. angustifolius, D. henryi, D. labordei, and D. officinarum. Although all flowers of D. tsaii had long styles, we did not confirm whether D. tsaii is distylous or monomorphic because few flowers were available in the herbarium specimens.
Pollen surface
Pollen grains of Damnacanthus angustifolius, D. henryi, D. labordei, and D. tsaii were spheroid and 4-(5)-orthocolporate or loxocolporate, whereas those of D. officinarum were spheroid and 3-orthocolporate.
In SEM of D. angustifolius (Figs. 1, 2), D. henryi, D. labordei, and D. officinarum, the muri of the pollen grains from the thrum flowers had minute granules along the top and/or on the sides, whereas the muri of the pollen grains from the pin flowers were smooth. In D. tsaii, the muri of the pollen grains have minute granules (Fig. 3) even though the flower has a long style and short stamens.
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), diploid and tetraploid numbers were discovered. In all the species, there was a clear relationship between the occurrence of distyly and ploidy level (Appendix 1). Distylous species, such as D. angustifolius, D. biflorus, D. henryi, D. labordei, and D. okinawensis, were diploid (2n = 22), and monomorphic species, such as D. giganteus and D. macrophyllus, were tetraploid (2n = 44) (Figs. 4, 5, 10 and 11). In D. indicus, the distylous populations were diploid (2n = 22) and the monomorphic populations were tetraploid (2n = 44) (Figs. 6–9; see next section). Damnacanthus tsaii, for which we did not confirm the occurrence of distyly, was also tetraploid (2n = 44). One or two satellite(s) were observed in most chromosomes (Figs. 4, 5, 7–11).
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Figure 13 shows the leaf lengths of the six D. indicus varieties in Japan, South Korea (Cheju Island), and Taiwan. Most diploids had small leaves and were recognized as D. indicus var. microphyllus. Tetraploids tended to have larger leaves than diploids. However, D. indicus var. indicus and D. indicus var. parvispinus in Tokunoshima, D. indicus var. major in Okinawa-jima, and D. indicus var. formosanus in Taiwan, while being diploids, still had a similar leaf size to the observed tetraploids.
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In specimens from Tokunoshima, two diploid varieties, D. indicus var. indicus and D. indicus var. parvispinus, were found (Fig. 14). In this case, unlike the two cases just described, D. indicus var. parvispinus was found in a drier habitat than D. indicus var. indicus, and in the same habitat, D. biflorus also occurred sympatrically. The flowering period of D. indicus var. parvispinus started about 1 wk earlier than D. indicus var. indicus, though a part of the flowering periods of the varieties overlapped.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). One or two pairs of satellite chromosomes are usually observed in Rubiaceae (Kiehn, 1995
); Damnacanthus also possesses this characteristic. Our observations reveal that the distylous Damnacanthus are diploid and the monomorphic Damnacanthus are tetraploid regardless of taxon. In addition to the strong correlation between ploidy level and occurrence of distyly, monomorphic Damnacanthus always have a long style and short stamens with few exceptions in the observed populations.
Naiki and Nagamasu (2003)
reported that pollen morphology of Damnacanthus was different between distylous and monomorphic taxa. They observed that, in the distylous taxa, the muri of pollen grains were smooth in the pin flower and granulate in the thrum flower, whereas in the monomorphic taxa the muri were granulate even though the flower type was like the pin morph of the distylous taxa. Our additional observations of pollen morphology in Damnacanthus in China and Taiwan also confirm the difference between the distylous and monomorphic taxa. The evidence from our pollen observations and the strong correlation between chromosome number and occurrence of distyly in Damnacanthus suggests that tetraploid D. tsaii is a species with monomorphic flowers and that distylous D. officinarum, though we could not observe the chromosomes, is a diploid species.
Polyploidy frequently occurs in plants (Stebbins, 1971
; Grant, 1981
; Masterson, 1994
) and plays a significant role in the speciation of angiosperms (Jackson, 1976
; DeWet, 1980
; Lewis, 1980a
). In various examples of polyploid evolution, few examples exhibit the correlation between chromosome number and the occurrence of distyly. In Turnera (Turneraceae), the diploid and tetraploid species are distylous, whereas the hexaploid and octaploid species are monomorphic (Barrett and Shore, 1987
; Tamari et al., 2001
). In Primula sect. Aleuritia (Primulaceae), the species of low ploidy level (2x, 4x) show distyly and species of high ploidy level (4x, 6x, 8x, 14x) show homostyly, in which stigma and anther heights are equal, although there are some exceptions (Kelso, 1992
; Richards, 1997
). In Amsinckia (Boraginaceae), a correlation between chromosome number and occurrence of distyly is limited to only a portion of the lineages of the phylogenetic tree (Schoen et al., 1997
).
Flowers of all observed monomorphic (= tetraploid) populations of Damnacanthus were like the pin flowers of the distylous taxa with few exceptions, whereas the pollen size and sculpture were like the thrum flowers of the distylous taxa. In Damnacanthus, it is likely that the breakdown of distylous to monomorphic flowers was caused by recombination and polyploidization. By analogy with the supergene model of Primula (e.g., Dowrick, 1956
; Richards, 1997
), it might be expected that pollen incompatibility of the distylous (= diploid) Damnacanthus is closely linked to pollen size/morphology, and as a result of recombination within a coadapted linkage group, self-fertile monomorphic flowers could sometimes occur, and they possess thrum-type pollen characters and pin- type anther position as well as female characters. According to the Primula model, only when a diploid pin-type self-fertile monomorph (gPa/gpa; G/g controls female characters, P/p controls pollen size, and A/a controls anther position) forms an allopolyploid with a diploid thrum (GPA/gpa) is it likely that a stable disomic tetraploid distylous condition can establish. Thus, tetraploids are likely to establish successfully from the diploid recombinational monomorphs that will themselves probably disappear as a result of inbreeding depression that is not suffered by the tetraploid descendants. However, in Damnacanthus, monomorphic flowers might have resulted from the genetic control failure of the distylous system caused by polyploidy, like segregation failures resulting from polysomic inheritance for pin/thrum factors in polyploid. Esser (1953)
reported that artificially tetraploid plants of Lythrum (Lythraceae) and Fagopyrum (Polygonaceae) produced from distylous species showed breakdown of heterostylous to monomorphic flowers. He states that this may either be the result of spontaneous mutation after colchicine treatment or, as the result of chromosome doubling, a new combination of the subgenes within the gene controlling several distylous characters. Shore and Barrett (1986)
produced hexaploids using colchicine, by doubling triploid seedlings from crosses between diploid and tetraploid populations of Turnera ulmifolia var. intermedia. Because tetraploid populations and the synthesized hexaploids of T. ulmifolia showed distyly and self-incompatibility, they concluded that the breakdown of distylous to monomorphic flowers in T. ulmifolia was not a necessary outcome of polyploidy.
In the monomorphic T. ulmifolia, there are various combinations of stigma and anther heights between the populations. The populations with larger stigma–anther height separation have a higher outcrossing rate (Barrett and Shore, 1987
). Barrett and Shore (1987)
hypothesized that selection pressures favoring outcrossing resulted in the reestablishment of nondistylous herkogamy in some monomorphic populations. Based on the observations of Tremayne and Richards (1993)
in Primula section Muscarioides, Richards (1997)
also supported the hypothesis. In P. bellidifolia (which also has distylous populations) and P. watsonii, monomorphic populations have various degrees of herkogamy. Large separations in stigma–anther heights in monomorphic flowers of the tetraploid Damnacanthus also suggest outcrossing. Selection pressures for outcrossing might have resulted in the monomorphic flowers of Damnacanthus. However, the monomorphic varieties of Turnera ulmifolia, which are polyploid, are self-compatible (Barrett and Shore, 1987
), and monomorphic flowers in distylous genera usually favor selfing (Barrett, 1992
; Richards, 1997
). Most heterostylous taxa in angiosperms are self-incompatible (Ganders, 1979
), and in general, the same is true of Rubiaceae (Bawa and Beach, 1983
). However, there are a few self-compatible distylous species in Rubiaceae (Bawa and Beach, 1983
; Riveros et al., 1995
). Crossing and population genetic experiments in both the diploid-distylous and the tetraploid-monomorphic Damnacanthus are required to investigate whether they have self-incompatibility and high outcrossing rate in wild.
Chromosome number, leaf size, and distribution in Damnacanthus indicus
Polyploidization sometimes increases plant size, with tetraploids being larger than diploids (Lewis, 1980b
). In Damnacanthus indicus, tetraploid populations tend to have larger leaves and plant size than diploid populations. However, the leaf size of the diploid populations of D. indicus in Tokunoshima and Okinawa-jima and the middle part of Taiwan cannot be distinguished from any the tetraploid populations, although no tetraploid population can be found in these areas.
Another well-known effect of polyploidization is the different distribution patterns between diploids and polyploids (Lewis, 1980b
; Richards, 1997
). Polyploids are distributed in wider areas and places with more severe climates, such as colder or drier areas. Populations of tetraploid D. indicus exist in more northern areas than diploid D. indicus. Figure 12 shows the populations of Damnacauthus found at its northernmost limits. The distribution of plants in laurel forests in Japan is limited by the low temperature during winter and secondly, by precipitation and sea wind (Hattori and Nakanishi, 1985
). Yamazaki (1959)
found that D. indicus exists in the area in which the annual average temperature is l4°C and more. This agrees with the tetraploid populations of D. indicus. The diploid populations of D. indicus cannot be explained only by considering the annual average temperature, though it is important to note that the limitation line of the annual average temperature is thought to be between 15° and 16°C in western Japan.
Several historical factors should be also considered in plant distribution (Cain, 1944
; Good, 1964
). Most plants in laurel forests in Japan are thought to have been dispersed to limited areas, such as refugia during the last glacial age; later, the plants may have gradually expanded their distribution (Hattori, 1987
). Within these plants, some species are not thought to have fully reached their potential range, because enough time may not have passed for full distribution and expansion of the species (Hattori, 1987
). In D. indicus, the tetraploid populations are likely to have already reached their maximum distribution, whereas the diploid populations still seem to be expanding their area of distribution into eastern regions in Japan.
Sympatric distribution of two varieties of Damnacanthus indicus
We found that in the varieties of Damnacanthus indicus, there are three types of sympatric distribution: diploid and tetraploid, two diploid, and two tetraploid. Sympatrically distributed diploids and tetraploids can be sometimes distinguished from each other (Borrill and Lindner, 1971
). In the case of sympatric diploid D. indicus var. microphyllus and tetraploid D. indicus var. major, the diploid and tetraploid can be easily distinguished by leaf and plant sizes and do not seem to cross each other because no triploid nor plant of intermediate leaf size were found.
Of two sympatric diploid varieties of D. indicus from Tokunoshima, D. indicus var. parvispinus can be identified by the almost glabrous pedicel and calyx lobes, which differ from the other varieties that have hairy pedicels and calyx lobes. It resembles D. biflorus, although its other characteristics differ considerably. The habitat of D. indicus var. parvispinus also differs from D. indicus var. indicus. Damnacanthus indicus var. parvispinus could be recognized as a species level, although crossability between D. indicus var. indicus and D. indicus var. parvispinus should be investigated.
The treatment of the two sympatric tetraploid D. indicus var. indicus and D. indicus var. major is more difficult. Because no feature other than the combination of leaf and spine lengths distinguishes the two, we need to do additional crossing experiments to determine whether they are genetically isolated.
The taxonomy of the varieties of D. indicus based on leaf size (Yamazaki, 1987
, 1993
) should be revised or treated as one species without using the variety rank, except for D. indicus var. parvispinus.
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FOOTNOTES |
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2 Present address: Osaka Museum of Natural History, 1-23 Nagai Park, Higashi-sumiyoshi, Osaka, 546-0034. E-mail: Akiyo.Naiki{at}ma7.seikyou.ne.jp
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LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Barrett S. C. H. 1992 Heterostylous genetic polymorphism: model systems for evolutionary analysis. In S. C. H. Barrett [ed.], Evolution and function of heterostyly. Monographs on theoretical and applied genetics, vol. 15, 1–29. Springer, Berlin, Germany
Barrett S. C. H. J. S. Shore 1987 Variation and evolution of breeding systems in the Turnera ulmifolia L. complex (Turneraceae). Evolution 41: 340-354[CrossRef][ISI]
Bawa K. S. J. H. Beach 1983 Self-incompatibility systems in the Rubiaceae of a tropical lowland wet forest. American Journal of Botany 70: 1281-1288[CrossRef][ISI]
Borrill M. R. Lindner 1971 Diploid-tetraploid sympatry in Dactylis (Gramineae). New Phytologist 70: 1111-1124[CrossRef][ISI]
Cain S. A. 1944 Foundations of plant geography. Harper, New York, New York, USA
DeWet J. M. J. 1980 Origins of polyploids. In W. H. Lewis [ed.], Polyploidy—biological relevance, 3–15. Plenum, New York, New York, USA
Dowrick V. P. J. 1956 Heterostyly and homostyly in Primula obconica. Heredity 10: 219-236
Erdtman G. 1960 The acetolysis method—a revised description. Svensk Botanisk Tidskrift 54: 561-564
Esser K. 1953 Genomverdopplung und Pollenschlauchwachstum bei Heterostylen. Zeitschrift für Induktive Abstammungs- und Vererbungslehre 85: 28-50
Ganders F. R. 1979 The biology of heterostyly. New Zealand Journal of Botany 17: 607-635[ISI]
Good R. 1964 Geography of the flowering plants, 2nd ed. Longman, London, UK
Grant V. 1981 Plant speciation, 2nd ed. Columbia University Press, New York, New York, USA
Hattori T. 1987 The distribution and environment of plants occurring in lucidophyllus forests. Vegetation Science 4: 9-14 (in Japanese)
Hattori T. S. Nakanishi 1985 On the distributional limits of the lucidophyllous forest in the Japanese Archipelago. Botanical Magazine, Tokyo 98: 317-333[CrossRef][ISI]
Jackson R. C. 1976 Evolution and systematic significance of polyploidy. Annual Review of Ecology and Systematics 7: 209-234
Kanjilal U. N. A. Das P. C. Kanjilal R. N. De 1939 Flora of Assam, vol. 3, 80. The Government of Assam, Assam, India
Kelso S. 1992 The genus Primula as a model for evolution in the Alaskan flora. Arctic and Alpine Research 24: 82-87[CrossRef][ISI]
Kiehn M. 1995 Chromosome survey of the Rubiaceae. Annals of the Missouri Botanical Garden 82: 398-408[CrossRef][ISI]
Koidzumi G. 1933 Damnacanthus Gaertn. f. Acta Phytotaxonomica et Geobotanica 2: 224-226 (in Japanese)
Lewis W. H. 1980a Polyploidy in species populations. In W. H. Lewis [ed.], Polyploidy—biological relevance, 103–144. Plenum, New York, New York, USA
Lewis W. H. 1980b Polyploidy in angiosperms: dicotyledons. In W. H. Lewis [ed.], Polyploidy—biological relevance, 241–268. Plenum, New York, New York, USA
Liao J. C. 1976 Genus Damnacanthus in Taiwan. Bulletin of the Experimental Forest of National Taiwan University 117: 133-136
Lo H. S. 1979 A revision of the genus Damnacanthus Gaertn. f. from China. Acta Phytotaxonomica Sinica 17: 104-109 (in Chinese)
Makino T. 1904 Observations on the flora of Japan. Botanical Magazine, Tokyo 18: 31-35
Masterson J. 1994 Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms. Science 264: 421-424
Naiki A. H. Nagamasu 2003 Distyly and pollen dimorphism in Damnacanthus (Rubiaceae). Journal of Plant Research 116: 105-113[ISI][Medline]
Nakai T. 1922 Trees and shrubs indigenous in Japan proper, vol. 1. Gamopetalae or Metachlamydeae. Seibido, Tokyo, Japan (in Japanese)
Oginuma K. M. Nakata 1988 Cytological studies on phanerogams in Southern Peru, I. Karyotype of Acaena ovalifolia. Bulletin of the National Science Museum. Series B, Botany 14: 53-56
Richards A. J. 1997 Plant breeding systems, 2nd ed. Chapman and Hall, London, UK
Riveros G. M. O. R. Barría A. M. Humaña 1995 Self-compatibility in distylous Hedyotis salzmannii (Rubiaceaeae). Plant Systematics and Evolution 194: 1-8[CrossRef][ISI]
Robbrecht E. C. Puff A. Igersheim 1991 The genera Mitchella and Damnacanthus—evidence for their close alliance; comments on the campylotropy in the Rubiaceae and the circumscription of the Morindeae. Blumea 35: 307-345[ISI]
Ruan Y. Z. 1999 Damnacanthus. In E. C. Chen [ed.], Rubiaceae. II. Rubioideae. Flora Reipublicae Popularis Sinicae, vol. 71, 167–176. Science Press, Peking, China (in Chinese)
Schoen D. J. M. O. Johnston A.-M. L'Heureux J. V. Marsolais 1997 Evolutionary history of the mating system in Amsinckia (Boraginaceae). Evolution 51: 1090-1099[CrossRef][ISI]
Shore J. S. S. C. H. Barrett 1986 Genetic modifications of dimorphic incompatibility in the Turnera ulmifolia L. complex (Turneraceae). Canadian Journal of Genetics and Cytology 28: 796-807[ISI]
Stebbins G. L. 1971 Chromosomal evolution in higher plants. Edward Arnold, London, UK
Takano A. 2001 Cytological analyses of 19 taxa in Globba (Zingiberaceae). Acta Phytotaxonomica et Geobotanica 52: 65-74
Tamari F. A. Athanasiou J. S. Shore 2001 Pollen tube growth and inhibition in distylous and homostylous Turnera and Piriqueta (Turneraceae). Canadian Journal of Botany 79: 578-591[CrossRef][ISI]
Tremayne M. A. J. Richards 1993 Homostyly and herkogamous variation in Primula L. section Muscarioides Balf. f. Evolutionary Trends in Plants 7: 67-72[ISI]
Yamazaki T. 1959 The distribution of plants in Japan. Natural Science and Museums 26: 1-19 (in Japanese)
Yamazaki T. 1987 The genus Damnacanthus in Japan, Korea and Taiwan. Journal of Phytogeography and Taxonomy 35: 69-74 (in Japanese)
Yamazaki T. 1993 Damnacanthus. In K. T. Iwatsuki, K. Yamazaki, D. E. Boufford, and H. Ohba [eds.], Flora of Japan, vol. 3a, 224–225. Koudansha, Tokyo, Japan
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