Interspecific and Intergeneric Hybridization in Baptisia and Thermopsis

in HortScience

Interspecific and intergeneric crosses were performed between species in the genera Baptisia and Thermopsis with the goal of creating hybrids with the best qualities of both parents. Baptisia australis (L.) R. Br. was used as both the male and female parent in intergeneric crosses. Thermopsis chinensis Benth. ex S. Moore, T. lupinoides (L.) Link, and T. villosa Fernald & B.G. Schub. were used as male and female parents in both interspecific and intergeneric crosses. Pollen was collected from B. alba (L.) Vent., B. bracteata Muhl. ex Elliott, and B. lanceolata (Walt.) Ell. and used to make interspecific and intergeneric crosses. Putative hybrids were obtained from both interspecific and intergeneric crosses. Interspecific crosses produced a higher percentage of pollinations resulting in seed set and the number of seeds per pollination than intergeneric crosses. Morphological differences between parent species and progeny were evident in putative hybrids resulting from intergeneric crosses between T. villosa and B. australis and T. villosa and B. alba. Most putative hybrids bloomed during the second year after germination. Because seedlings could be obtained from both interspecific and intergeneric crosses, hybrids within and between the genera Baptisia and Thermopsis are feasible. The Fabaceae family contains 670–750 genera and 18,000–19,000 species. Baptisia (commonly called false or wild indigo) and Thermopsis (commonly named false lupine) of the Fabaceae belong to the tribe Thermopsidae, which comprises 46 species in six genera. All species in Thermopsis and Baptisia are herbaceous; they are the only two genera in Thermopsidae that do not have woody species. Thermopsis contains 23 species and has a wide-spread distribution with species endemic to Asia and much of temperate North America. Although Thermopsis is considered to have originated in central Asia, T. chinensis Benth. ex S. Moore and T. fabacea (Pallas) Candole are thought to have originated in North America and migrated over the Bering Land Strait to Asia. Three Thermopsis species, T. fraxinifolia Nutt. ex M.A. Curtis, T. mollis (Michx.) M.A. Curtis ex A. Gray, and T. villosa Fernald & B.G. Schub., are native to the southeastern United States. Baptisia contains 15–17 species that are endemic to the southeastern and midwestern United States.

Abstract

Interspecific and intergeneric crosses were performed between species in the genera Baptisia and Thermopsis with the goal of creating hybrids with the best qualities of both parents. Baptisia australis (L.) R. Br. was used as both the male and female parent in intergeneric crosses. Thermopsis chinensis Benth. ex S. Moore, T. lupinoides (L.) Link, and T. villosa Fernald & B.G. Schub. were used as male and female parents in both interspecific and intergeneric crosses. Pollen was collected from B. alba (L.) Vent., B. bracteata Muhl. ex Elliott, and B. lanceolata (Walt.) Ell. and used to make interspecific and intergeneric crosses. Putative hybrids were obtained from both interspecific and intergeneric crosses. Interspecific crosses produced a higher percentage of pollinations resulting in seed set and the number of seeds per pollination than intergeneric crosses. Morphological differences between parent species and progeny were evident in putative hybrids resulting from intergeneric crosses between T. villosa and B. australis and T. villosa and B. alba. Most putative hybrids bloomed during the second year after germination. Because seedlings could be obtained from both interspecific and intergeneric crosses, hybrids within and between the genera Baptisia and Thermopsis are feasible. The Fabaceae family contains 670–750 genera and 18,000–19,000 species. Baptisia (commonly called false or wild indigo) and Thermopsis (commonly named false lupine) of the Fabaceae belong to the tribe Thermopsidae, which comprises 46 species in six genera. All species in Thermopsis and Baptisia are herbaceous; they are the only two genera in Thermopsidae that do not have woody species. Thermopsis contains 23 species and has a wide-spread distribution with species endemic to Asia and much of temperate North America. Although Thermopsis is considered to have originated in central Asia, T. chinensis Benth. ex S. Moore and T. fabacea (Pallas) Candole are thought to have originated in North America and migrated over the Bering Land Strait to Asia. Three Thermopsis species, T. fraxinifolia Nutt. ex M.A. Curtis, T. mollis (Michx.) M.A. Curtis ex A. Gray, and T. villosa Fernald & B.G. Schub., are native to the southeastern United States. Baptisia contains 15–17 species that are endemic to the southeastern and midwestern United States.

Except for Thermopsis barbata Benth. ex Royle, which produces reddish-purple flowers, all species in Thermopsis have yellow flowers (Chen et al., 1994; Wu and Raven, 1994). Flower color in Baptisia ranges from white to yellow to blue (Larisey, 1940). In both Baptisia and Thermopsis, perfect flowers with superior ovaries are borne on terminal racemes, though some Baptisia species produce flowers that occur individually in leaf axils (Chen et al., 1994; Larisey, 1940). Seed pods of Baptisia are inflated while those of Thermopsis are compressed (Chen et al., 1994). Although polyploidy is wide-spread in the Fabaceae, no polyploids have been found in Baptisia and only two polyploids have been found in Thermopsis, T. gracillis Howell and T. divicarpa A. Nelson (Chen et al., 1994). The chromosome numbers of both Baptisia and Thermopsis are based on x = 9, with 2n = 18 for all species, except for T. gracillis and T. divicarpa, which are 2n = 36 (Chen et al., 1994; Cooper, 1936).

Biochemical evidence suggests that Baptisia evolved from Thermopsis in the southeastern United States (Dement and Mabry, 1975). Two phylogenies of Thermopsidae places T. chinensis and T. villosa in the same clade as several species of Baptisia, including B. australis, based on internal transcribed spacer sequences (Wang et al., 2006; Zhang et al., 2015). Thermopsis interspecific hybrids have not been observed by taxonomists (Dement and Mabry, 1975). However, hybridization readily occurs between species of Baptisia (Alston and Turner, 1963; Baetcke and Alston, 1968; Dement and Mabry, 1975; Larisey, 1940; Leebens-Mack and Milligan, 1998).

In the genus Baptisia, interspecific crosses have been used to create many novel cultivars (Ault, 2003; Avent, 2002; Cullina, 2000), some of which are widely available commercially. Thermopsis has not been used to create hybrids to our knowledge and is also not much known or used in the ornamental plant industry. Many species of Thermopsis, particularly T. villosa, are very tolerant of both drought and heat, making Thermopsis a good substitute for lupines in the southeastern United States (Armitage, 1989). Some species of Thermopsis, such as T. lupinoides, originated in coastal areas and are salt tolerant (Hotes et al., 2001; Probatova and Seledets, 2012). Baptisia has proven difficult to propagate vegetatively through cuttings (Ault, 2003; Cullina, 2000). Thermopsis is easier to root than Baptisia (Hawkins et al., 2013) and will bloom 2 years after germination, whereas Baptisia requires 3 years to bloom from seed (personal communication, Heather Alley, State Botanical Garden of Georgia, 2013).

The overall goal of this project was to investigate the feasibility of hybridization within and between species of Baptisia and Thermopsis. Hybrids could potentially have improved drought tolerance, earlier flowering, and higher rates of rooting compared with the parent species. Ideally, the hybrids would combine desirable ornamental qualities with these improved traits. Hybrids could also serve as bridge parents in future breeding to obtain intergeneric cultivars.

Materials and Methods

B. australis, T. chinensis, and T. villosa plants were obtained from Northcreek Nurseries, Inc., Landenberg, PA, as seed-grown liners. An additional genotype of T. villosa was obtained from the State Botanical Garden of Georgia, Athens, GA. T. lupinoides (L.) Link plants were vegetatively produced from a stock plant obtained from Plant Delights Nursery, Raleigh, NC. Plants were potted into 7.6 L trade containers with Fafard 3B Potting Mix (Sun Grow Horticulture, Agawam, MA) consisting of Canadian sphagnum peat (45%), processed pine bark, perlite, and vermiculite, and placed in an enclosed shade house (50% shade) at the University of Georgia (UGA) Horticulture Farm, Watkinsville, GA. All crosses were carried out in the shade house. To increase the diversity of male Baptisia parents, pollen was collected from B. alba (L.) Vent., B. bracteata Muhl. ex Elliott, and B. lanceolata (Walt.) Ell. in Apr. 2013 and used to make crosses (Table 1). The B. alba plant from which the pollen was collected was in the Trial Gardens at the UGA. The B. lanceolata plants were located in Dodge and Laurens County, GA. The B. bracteata plants were from Hancock County, GA.

Table 1.

Detailed data for Fabaceae crosses. The number of pollinations for each cross, the percentage of pollinations resulting in seed, the number of seed obtained from all pollinations, the percentage of germination of the seed, and the number of seedlings per pollination.

Table 1.

Interspecific and intergeneric crosses were made from March to May 2013. A total of 2544 crosses were made; of the crosses, 1550 were interspecific and 994 were intergeneric. Details of all crosses are shown in Table 1.

Flowers of the female parents were emasculated immediately before pollination. Pollen was collected from the male parent onto a small paintbrush and used to pollinate the female parent. Reciprocal crosses were made where possible. Because some species bloomed at different times or had brief periods of overlapped blooming, reciprocal crosses could not always be performed. Seed pods were collected once ripe from May to Aug. 2013. Seeds were extracted from the pods and counted. Seeds were scarified in 0.1 m sulfuric acid for 20 min, rinsed, and soaked for several hours in water to imbibe before being sown in a potting media containing bark, peatmoss, and perlite. Germination data were taken at 4 weeks after sowing. A maximum of 25 seedlings of each interspecific and intergeneric cross were potted up into 2.8-L trade containers with a pine bark-based medium containing added micronutrients and moved into an enclosed shade house at the UGA Horticulture Farm. In Oct. 2013, the seedlings were transplanted to the field at the UGA Horticulture Farm for overwintering and further evaluation. The seeds from the crosses between the genotype of T. villosa obtained from the State Botanical Garden and B. australis were sown and germinated later than that of the other crosses. The seedlings resulting from those crosses were overwintered in a shade house as they were too young to be overwintered in the field.

During 2014 and 2015, morphological traits of the putative hybrids were assessed. The shapes of leaflets and stipules were evaluated and compared with the characteristics of the parent species.

In 2015, 25 of the F1 plants were selected to continue in the breeding program. Cuttings were taken of the 25 plants in May, rooted, planted in 2.8-L trade containers with a pine bark-based media, and placed upon the nursery pad at the UGA Horticulture Farm for evaluation of growth and form in containers.

Results

Success rate of individual crosses varied widely (Table 1). All interspecific combinations of parents set seed and had seed germination (Table 2). Rates of seed set among seed parents in interspecific crosses ranged from 20.8% to 40.0% (Table 2). Seed germination percentages among interspecific crosses grouped by seed parent ranged from 53.3% to 93.5% (Table 2). Rates of seed set among pollen parents in interspecific crosses ranged from 15.9% to 44.0% (Table 2). The percentage of seed germination among interspecific crosses grouped by pollen parents ranged from 33.3% to 89.5% (Table 2).

Table 2.

Interspecific crosses by seed parent and by pollen parent. For seed parent—the number of pollen parent species crossed with seed parent species and total number of pollinations made per seed parent species. For pollen parent—the number of seed parent species crossed with pollen parent species and the total number of pollinations made per pollen parent species. For both seed and pollen parents—the percentage of pollinations resulting in seed set, the total number of seeds resulting from all pollinations, and the percentage of germination of the seed.

Table 2.

Most but not all intergeneric combinations of parents had seed set and germination (Tables 1 and 3). When used as a seed parent, T. lupinoides set no seed when crossed with either B. alba or B. australis. The cross of B. australis as a seed parent to T. chinensis as a pollen parent also yielded no seed (Table 1). However, all other intergeneric cross combinations resulted in seed set and germination.

Table 3.

Intergeneric crosses by seed parent and by pollen parent. For seed parent—the number of pollen parent species crossed with seed parent species and the total number of pollinations made per seed parent species. For pollen parent—the number of seed parent species crossed with pollen parent species and the total number of pollinations made per pollen parent species. For both seed and pollen parents—the percentage of pollinations resulting in seed set, the total number of seeds resulting from all pollinations, and the percentage germination of the seed.

Table 3.

Among seed parents in intergeneric crosses that set seed, the rate of seed set ranged from 9.0% to 12.0% (Table 3). The seed germination percentage among seed parents in intergeneric crosses that set seed ranged from 40.0% to 86.4% (Table 3). Among pollen parents in intergeneric crosses that set seed, the rate of seed set ranged from 9.7% to 20.0% (Table 3). The percentage of seed germination among pollen parents in intergeneric crosses that set seed ranged from 71.1% to 87.5% (Table 3).

Seedlings began to break winter dormancy in Mar. 2014. During the spring of 2014, 46 of the initial 237 seedlings bloomed (Table 4). Survival during the first year was high, with all but 21 seedlings surviving (Table 4). In 2015, 171 of the surviving seedlings bloomed (Table 4). During 2015, 29 additional seedlings died (Table 4).

Table 4.

Mortality and bloom rates for 2014 and 2015. Initial seedlings from each cross, seedling mortality in 2014 and 2015, seedlings remaining by second year after planting, percent seedling mortality by second year after planting, seedlings blooming in 2014 and 2015, and percent of seedlings blooming by second year after planting.

Table 4.

Morphological differences in leaflet shape varied widely among crosses (Table 5). The leaflet shape of the putative hybrids of the T. lupinoides x T. villosa (NC) cross was ovate, as is typical of T. villosa, instead of the elliptic shape characteristic of T. lupinoides (Table 5). Putative hybrids of the T. chinensis x T. villosa (NC) also had ovate leaflets instead of the obovate leaflets typical of T. chinensis (Table 5).

Table 5.

Leaflet morphology of parent species and putative hybrids.

Table 5.

Morphological differences in stipule shape also varied widely among crosses (Table 6). For example, of the 23 surviving putative hybrids of the T. villosa (NC) x B. australis cross in May 2014, 21 plants had stipules that were lanceolate in shape instead of being ovate and clasping as is characteristic of the seed parent (Table 6). However, all putative hybrids of the B. australis x T. villosa (NC) cross had stipules resembling those of the seed parent. In addition, putative hybrids of this cross looked just like the female parent in growth habit and flowering morphology. All 23 of the putative hybrids from the T. villosa (NC) x B. alba cross had lanceolate stipules, as did the 13 putative hybrids from the T. villosa (NC) x B. lanceolata cross and the 24 surviving putative hybrids of the T. villosa (NC) x T. lupinoides cross (Table 6). By contrast, all the putative hybrids between the T. villosa (BG) obtained from the State Botanical Garden of Georgia and B. australis looked exactly like T. villosa (BG) (data not shown).

Table 6.

Stipule morphology of parent species and putative hybrids.

Table 6.

Remarkably, putative hybrids of the T. lupinoides x T. villosa (NC) cross all had lanceolate or linear to lanceolate stipules, which did not resemble those of either parent. However, the stipules of the putative hybrids from the T. chinensis x T. villosa (NC) cross were all similar to those of the female parent.

Growth habit of some putative hybrids where T. villosa (NC) was the female parent also showed differences from that of the seed parent. Growth habit of the 21–23 surviving putative T. villosa (NC) x B. australis hybrids looked more compact than T. villosa in the first year in the field and had a branching structure similar to B. australis instead of being largely single-stemmed as is typical of T. villosa (Fig. 1A–C). All putative hybrids from the T. villosa (NC) x B. alba cross, the T. villosa (NC) x B. lanceolata cross, and the T. villosa (NC) x T. lupinoides cross also had a multistem branching habit. Height data taken in the third year in the field of putative hybrids with T. villosa female parentage that had undergone selection showed a marked decrease in height from the average height of T. villosa (Table 7).

Fig. 1.
Fig. 1.

(A) Seedling of T. villosa x B. australis cross with examples of parent species. Note multibranching habit of hybrid, unlike female parent. Inflorescence morphology of hybrid is also different from female parent, with flowers more widely spaced along inflorescence. (B) T. villosa (NC) was obtained from Northcreek Nurseries. (C) B. australis.

Citation: HortScience horts 52, 9; 10.21273/HORTSCI12039-17

Table 7.

Height in cm of putative interspecific and intergeneric F1 hybrids having T. villosa female parents compared with mean height of female parent species. Putative hybrids were selected from the original F1 population. Mean height of female parent species was 92.0 cm in the field.

Table 7.

Cuttings taken of the selected F1 plants rooted at the rate of 84.0% to 100.0%, with the exception of the putative hybrids of the T. chinensis x B. alba cross which rooted at 36.7% (Table 8). Cuttings rooted within 4 weeks. Most of the plants produced by cuttings and potted into containers in 2015 bloomed in Spring 2016 (data not shown).

Table 8.

Rooting data for putative hybrids.

Table 8.

Discussion

Crossing between species in Baptisia and Thermopsis appears feasible as putative hybrids of several of the intergeneric crosses made in this study had morphological differences as compared with the female parent or had a combination of traits of both parents. Further evaluation is needed to determine whether the intergeneric crosses where B. australis is the female parent produced true hybrids, because the F1 progenies of the B. australis x T. villosa cross all resembled the female parent. Other factors can help indicate hybridity. Ninety percent of the progenies of the B. australis x T. villosa crosses bloomed during the second year from seed, even though B. australis normally blooms during the third year from seed. Earlier blooming might indicate hybridity of these plants, as changes in flowering time are sometimes seen in hybrid plants. In a project to create ornamental Allium hybrids from fall-blooming and summer-blooming species, hybrids of Allium chinense x A. schubertii and of A. thunbergii x A. caeruleum bloomed at a time intermediate to both parents (Nomura et al., 2002). Moreover, the ornamental Allium hybrids created from these crosses bloomed by 2 years after pollination, more quickly than other ornamental Alliums (Nomura et al., 2002). Furthermore, rooting data may support hybridity in the T. chinensis x B. alba progenies, as T. chinensis roots well but putative hybrids with B. alba had a decreased rooting percentage. Intergeneric hybrids of chrysanthemum [Chrysanthemum grandiflorum (Ramat.) Kitamura] and mugwort (Artemesia vulgaris L.) had a rooting ability that was less than that of the easily-rooted mugwort parent but greater than that of the chrysanthemum parent (Deng et al., 2012).

Pre- or post-zygotic barriers between parents in interspecific and intergeneric crosses will often preclude fertilization of the ovule after pollination, resulting in low seed set. Because the percentage of crosses with seed was higher in interspecific crosses than in intergeneric crosses, barriers to fertilization seem to be much lower in the interspecific crosses. Although such a result is typical in many species, it is not always the case. Intergeneric crosses in brooms (genera Genista and Cystisus, family Fabaceae) showed greater fertility than interspecific crosses (Bellenot-Kapusta et al., 2006). However, the number of seedlings recovered from intergeneric crosses could be increased using embryo rescue or ovule culture. Ovule culture was necessary to produce an intergeneric hybrid from a cross between Dendranthema nakingense and Tanacetum vulgare because of the post-zygotic barriers to fertilization (Tang et al., 2011).

Pollen collection and storage may be tools to increase the variety of crosses that may be made, as well as the number of pollinations for each type of cross. Stored pollen was used successfully to create interspecific hybrids of Acacia auriculiformis and A. mangium (Kato et al., 2012). Pollen storage was also used to create interspecific hybrids between summer- and autumn-flowering ornamental Allium species (Nomura et.al., 2002). The blooming period for T. lupinoides and T. chinensis did not overlap substantially with the blooming period for B. australis, whereas that of T. villosa did. Storage of pollen from all three species could allow more intergeneric crosses to be made between B. australis and the Asian species of Thermopsis.

Other Baptisia and Thermopsis species should be added to the breeding program to increase genetic diversity. B. alba would be a good addition, because using the species as a male parent in intergeneric crosses with T. villosa and T. chinensis yielded progeny. Additional genotypes of B. australis could be added to increase the genetic diversity. Because B. cinera (Raf.) Fernald & B.G. Schub. and B. sphaerocarpa Nutt. were found to be in the same phylogenetic clade as T. chinensis and T. villosa (Wang et al., 2006; Zhang et al., 2015), these species would also be good additions to the breeding program. Additional Thermopsis species to consider adding to the program, based on phylogenetic studies, would be T. montana Nutt. and T. rhombifolia (Nutt. ex Pursh) Nutt. ex Richardson (Wang et al., 2006; Zhang et al., 2015).

Literature Cited

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    • Search Google Scholar
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Contributor Notes

We thank Vickie Waters for technical assistance and help with data collection.This article is part of a thesis submitted by Susan M. Hawkins as part of the fulfillment of a Master’s Degree.

Corresponding author. E-mail: ruter@uga.edu.

  • View in gallery

    (A) Seedling of T. villosa x B. australis cross with examples of parent species. Note multibranching habit of hybrid, unlike female parent. Inflorescence morphology of hybrid is also different from female parent, with flowers more widely spaced along inflorescence. (B) T. villosa (NC) was obtained from Northcreek Nurseries. (C) B. australis.

  • AlstonR.E.TurnerB.L.1963Natural hybridization among four species of Baptisia (Leguminosae)Amer. J. Bot.50159173

  • ArmitageA.M.1989Herbaceous perennial plants: A treatise on their identification culture and garden attributes. Varsity Press Athens GA

  • AultJ.2003Breeding and development of new ornamental plants from North American native taxaActa Hort.6243742

  • AventT.2002Revenge of the ‘Redneck Lupines’Horticulture9970

  • BaetckeK.P.AlstonR.E.1968The composition of a hybridizing population of Baptisia sphaerocarpa and Baptisia leucophaeaEvolution22157165

    • Search Google Scholar
    • Export Citation
  • Bellenot-KapustaV.PesteilC.CadicA.2006Diversity study and breeding of brooms (tribe of Genisteae)Acta Hort.7142936

  • ChenC.J.MendenhallM.G.TurnerB.L.1994Taxonomy of Thermopsis (Fabaceae) in North AmericaAnn. Mo. Bot. Gard.81714742

  • CooperD.C.1936Chromosome numbers in the LeguminosaeAmer. J. Bot.23231233

  • CullinaW.2000A guide to growing and propagating native flowers of North America. Houghton Mifflin Co. New York NY

  • DementW.A.MabryT.J.1975Biological implications of flavonoid chemistry in Baptisia and ThermopsisBiochem. Syst. Ecol.39194

  • DengY.ChenS.ChangQ.WangH.ChenF.2012The chrysanthemum × Artemisia vulgaris intergeneric hybrid has better rooting ability and higher resistance to alternaria leaf spot than its chrysanthemum parentSci. Hort.134185190

    • Search Google Scholar
    • Export Citation
  • HawkinsS.M.ChappellM.MartinM.T.Jr2013Defining a protocol for vegetative propagation of Baptisia, Eupatorium and ThermopsisJ. Environ. Hort.31162168

    • Search Google Scholar
    • Export Citation
  • HotesS.PoschlodP.SakaiH.InoueT.2001Vegetation, hydrology, and development of a coastal mire in Hokkaido, Japan, affected by flooding and tephra depositionCan. J. Bot.79341361

    • Search Google Scholar
    • Export Citation
  • KatoK.YamaguchiS.ChigiraO.OgawaY.IsodaK.2012Tube pollination using stored pollen for creating Acacia auriculiformis hybridsJ. Trop. For. Sci.24209216

    • Search Google Scholar
    • Export Citation
  • LariseyM.M.1940A monograph of the genus BaptisiaAnn. Mo. Bot. Gard.27119244

  • Leebens-MackJ.MilliganB.G.1998Pollination biology in hybridizing Baptisia (Fabaceae)Populations. Amer. J. Bot.85500507

  • NomuraY.KazumaT.MakaraK.NagaiT.2002Interspecific hybridization of autumn-flowering Allium species with ornamental Alliums and the characteristics of the hybrid plantsSci. Hort.95223237

    • Search Google Scholar
    • Export Citation
  • PolhillR.M.RavenP.H.StirtonC.H.1981Evolution and systematics of the Leguminosae p. 1–26. In: R.M. Polhill and P.H. Raven(eds.). Advances in legume systematics. Royal Botanic Gardens Kew Richmond UK

  • ProbatovaN.S.SeledetsV.P.2012Ecological ranges and ecological niches of plant species in the monsoon zone of Pacific Russia. 1st ed. Nova Science Publishers Hauppauge NY

  • TangF.WangH.ChenS.ChenF.LiuZ.FangW.2011Intergeneric hybridization between Dendranthema nankingense and Tanacetum vulgareSci. Hort.13216

    • Search Google Scholar
    • Export Citation
  • WangH.C.YangJ.B.ComptonJ.A.SunH.2006A phylogeny of Thermopsideae (Leguminosae: Papilionoideae) inferred from nuclear ribosomal internal transcribed spacer (ITS) sequencesBot. J. Linn. Soc.151365373

    • Search Google Scholar
    • Export Citation
  • WenJ.NieZ.-L.Ickert-BondS.M.2016Intercontinental disjunctions between eastern Asia and western North America in vascular plants highlight the biogeographic importance of the Bering land bridge from late Cretaceous to NeogeneJ. Syst. Evol.54469490

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    • Export Citation
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