Chromosome Numbers and Karyotypes of Representatives of Caryophyllaceae from Korea

Abstract

Somatic chromosome numbers were determined for 15 taxa belonging to six genera of Caryophyllaceae in South Korea, Pseudostellaria (three species), Stellaria (three species), Dianthus (one species), Gypsophila (one species), Lychnis (two species) and Silene (five species), and were compared with previously reported chromosome numbers for each genus and species. This is the first report of chromosome numbers for two species, Silene koreana (2n=24), and S. seoulensis (2n=24). Furthermore, a karyotype analysis of five Silene species indicated that the basic number were all x=12, with the following karyotypic formulas: S. aprica var. oldhamiana (2n=4x=48=48m), S. jenisseensis (2n=2x=24=20m+4sm), S. koreana (2n=2x=24=16m+8sm), S. seoulensis [2n=2x=24+ I=20m (4sat)+4sm], and S. takesimensis [2n=2x=24=20m+4sm (1sat)]. These were the first karyotype analyses for the examined taxa, except S. aprica var. oldhamiana. S. seoulensis had the most asymmetrical karyotype among these species.

Caryophyllaceae Juss. is the largest family in the order Caryophyllales, consisting of 86 genera and approximately 2,200 species. It has a Holarctic distribution with diversity centered in the Mediterranean and Irano-Turanian regions (Bittrich 1993). The family exhibits substantial diversity in morphology, habitats, and growth forms, including annual or perennial herbs, subshrubs, and rarely shrubs (Bittrich 1993, Fior et al. 2006). In Korea, approximately 64 species including eight endemic species belonging to 17 genera are currently recognized (Chung et al. 2017, Hong and Choi 2018).

Since chromosome counts for members of Caryophyllaceae were first reported by Blackburn (1924), the chromosome numbers for approximately 1,480 taxa belonging to 83 genera have been determined (Chromosome Counts Database, CCDB, version 1.46, http://ccdb.tau.ac.il/home/). The chromosome number for the family varies from 2n=24 (Blackburn 1933) to 2n=ca. 312 (Rice et al. 2015); interestingly, the two extremes have both been reported for Silene ciliata Pourr. Turner (1994) has suggested that the most common basic numbers in the family are x=8 and 9, estimating that about 60% taxa are tetraploid or tetraploid derivatives. Some dioecious taxa in Silene have sex chromosomes (Blackburn 1924, Kruckeberg 1954, 1960, Blackburn and Morton 1957). Despite increasing chromosome counts and karyological investigations for members of Caryophyllaceae (Grabowska-Joachimiak and Joachimiak 2002, Song et al. 2004, Sato et al. 2007, Martin et al. 2008, Gholipour and Sheidai 2010) and studies of chromosomal evolution in the family (Turner 1994), chromosome counts for Korean species are relatively rare (Lee 1969, Kwon et al. 2005, Lee and Kim 2007, 2008).

As part of our investigations of chromosome numbers for Korean vascular plants (Chung et al. 2011, 2013, 2016), we report somatic chromosome numbers for 15 taxa, including one endemic species (S. takesimensis Uyeki & Sakata) belonging to six genera of Caryophyllaceae. Additionally, we performed a karyotype analysis of five species in Silene. The aims of the present study thus are to establish chromosome numbers and karyotypes of Korean Caryophyllaceae, and to contribute towards a better understanding of the diversity of chromosomes and ploidy levels in the family.

Materials and methods

Plant materials

Fifteen taxa belonging to six genera (Dianthus, Gypsophila, Lychnis, Pseudostellaria, Silene, and Stellaria) of Caryophyllaceae were collected in South Korea (Table 1). The plants were transplanted, cultivated in the greenhouse of Andong National University (Andong, Province Gyeongsangbuk-do, South Korea), and utilized for analyses of somatic chromosome numbers. Details of sampled populations, including voucher information, are listed in Table 1.

Table 1. Voucher information and chromosome numbers examined of 15 taxa of Caryophyllaceae.

Taxa	Voucher specimen	Locality	2n
P. davidii (Franch.) Pax	G.Y.Chung et al. 130629-160	Mt. Myeonsan, Seokpo-myeon, Bonghwa-gun, GB	32
P. heterophylla (Miq.) Pax	G.Y.Chung et al. 130412-001	Hongjesa temple, Socheon-myeon, Bonghwa-gun, GB	32
P. palibiniana (Takeda) Ohwi	G.Y.Chung et al. 120602-067	Mt. Myeonsan, Seokpo-myeon Bonghwa-gun, GB	32
Stellaria alsine var. undulata (Thunb.) Ohwi	G.Y.Chung et al. 130502-001	Songcheon-dong, Andong-si, GB	44
S. aquatica (L.) Scop.	G.Y.Chung et al. 130530-001	Songcheon-dong, Andong-si, GB	28
S. media (L.) Vill.	G.Y.Chung et al. 120923-109	Mt. Myeonsan, Seokpo-myeon Bonghwa-gun, GB	42
Dianthus chinensis L.	G.Y.Chung et al. 130715-001	Mt. Agisan, Imdong-myeon, Andong-si, GB	30
Gypsophila oldhamiana Miq.	G.Y.Chung et al. 130915-049	Mt. Sangwonsan, Dalseong-gun, DG	34
Lychnis cognata Maxim.	G.Y.Chung et al. 130705-001	Mt. Irwolsan, Irwol-myeon, Yeongyang-gun, GB	24
L. fulgens Fisch. ex Spreng.	G.Y.Chung et al. s.n.	Mt. Geumjeongsan, Dong-myeon, Yangsan-si, GN	24
Silene aprica var. oldhamiana (Miq.) C.Y.Wu	G.Y.Chung et al. 130613-001	Gimnyeong beach, Gujwa-eup, JJ	48
S. jenisseensis Willd.	G.Y.Chung et al. 130808-001	Mt. Seoraksan, Buk-myeon, Inje-gun, GW	24
S. koreana Kom.	G.Y.Chung et al. 130628-001	Dosan-myeon, Andong-si, GB	24FR
S. seoulensis Nakai	G.Y.Chung et al. 130705-002	Mt. Irwolsan, Irwol-myeon, Yeongyang-gun, GB	24FR
*S. takesimensis Uyeki & Sakata	G.Y.Chung et al. 090624-016	Do-dong, Ulleung-gun, GB	24

Abbreviations: GB: Province Gyeongsangbuk-do, GN: Prov. Gyeongsangnam-do, GW: Prov. Gangwon-do, DG: Prov. Daegu, JJ: Prov. Jeju-do. *Endemic to Korea; ^FR: the first report for the taxon.

Chromosome observation and karyotype analysis

Actively growing root tips were pretreated with distilled water at 4°C for 24 h and fixed in Farmer’s fluid (absolute ethanol : glacial acetic acid=3 : 1). The fixed roots were stored at 4°C for 24 h before maceration using 1 M HCl at 60°C for 5 to 10 min. Samples were then double-stained with Feulgen reagent and 2% aceto-carmine. Stained materials were squashed and used to prepare slides. The slides were observed by microscopy (Olympus AX-70, Tokyo, Japan), and microphotographs were obtained by a digital camera (Olympus DP2-BSW). For karyotype analyses, the chromosome sizes were measured by KaryoType (Altınordu et al. 2016) and karyotypic characters were assessed based on following asymmetry parameters (Table 2): a degree of karyotype asymmetry (Watanabe et al. 1999), asymmetry index (Paszko 2006), and Stebbins’s karyotype asymmetry classification (Stebbins 1971).

Table 2. Karyotypic characters of five Korean Silene taxa.

Taxa	2n	Ploidy level	Karyotype formula	Chromosome size variation (µm)	TCL (µm)	HCL (µm)	A	AI	ST
S. aprica var. oldhamiana	48	4x	48m	2.39–4.13	159.64	39.91	0.13	291.70	1A
S. jenisseensis	24	2x	20m+4sm	2.70–4.89	94.80	47.40	0.18	134.73	2A
S. koreana	24	2x	16m+8sm	2.86–5.97	92.04	46.02	0.19	178.99	2A
S. seoulensis	24	2x	20m4sat+4sm	1.58–4.95	90.51	46.05	0.20	192.62	2B
S. takesimensis	24	2x	20m+4sm2sat	2.91–5.87	97.29	48.65	0.19	150.09	2A

TCL: Total chromosome length, HCL: total chromosome length of the haploid complement, A: degree of karyotype asymmetry (Watanabe et al. 1999), AI: asymmetry index (Paszko 2006), ST: Stebbins’ karyotype asymmetry classification (Stebbins 1971).

Results and discussion

Chromosome numbers for 15 taxa belonging to six genera of Caryophyllaceae

Pseudostellaria is a genus with 16 (Bittrich 1993) to 21 species (Zhang et al. 2017), comprising mostly perennial herbs in Asia, Europe, and North America; it is characterized by root tubers and dimorphic chasmogamous and cleistogamous flowers (Bittrich 1993, Sadeghian et al. 2015). The genus has 2n=12, 14, 32, 64, and 96 chromosomes, and 2n=32 is the most frequently reported count (Lee 1969, Löve and Löve 1988, Choi and Pak 1999, Choi et al. 2001, Hong and Choi 2018).

In Korea, eight species including two hybrids have been cataloged, among which four species are known to be endemic (Chung et al. 2017, Hong and Choi 2018). We found that three species in Pseudostellaria (P. davidii, P. heterophylla, and P. palibiniana) consistently had 2n=32 chromosomes (Figs. 1–3) and agreed with those of previous reports from Russia, China, and Korea (Choi and Pak 1999, Choi et al. 2001, Probatova et al. 2015).

Figs. 1–15. Microphotographs of metaphase plates of Caryophyllaceae. 1. P. davidii (2n=32), 2. P. heterophylla (2n=32), 3. P. palibiniana (2n=32), 4. Stellaria alsine var. undulata (2n=44), 5. S. aquatica (2n=28), 6. S. media (2n=42), 7. D. chinensis (2n=30), 8. G. oldhamiana (2n=34), 9. Lychnis cognata (2n=24), 10. L. fulgens (2n=24), 11. Silene aprica var. oldhamiana (2n=48), 12. S. jenisseensis (2n=24), 13. S. koreana (2n=24), 14. S. seoulensis (2n=24), 15. S. takesimensis (2n=24). Arrow indicates B chromosome.

Stellaria includes about 150–200 species of annual or perennial herbs. Some species are cosmopolitan and others occur mainly in Eurasia to East Asia (Bittrich 1993), and eight species grow in the Korean peninsula (Hong and Choi 2018). Stellaria is one of the most chromosomally diverse genera in the family, varying from 2n=20 to 2n=188 (Bittrich 1993, Rice et al. 2015). Basic numbers for the genus have been reported as x=10, 11, 12, 13, 14, and 15, with x=13 predominating (Morton 1984, 2005, Turner 1994, Keshavarzi and Bozchaloyi 2014).

We investigated three taxa, S. alsine var. undulata, S. aquatica, and S. media, and detected 2n=44, 28, and 42 chromosomes (Figs. 4–6), respectively. S. aquatica is sometimes included in Myosoton, which is a monotypic genus with 2n=28 chromosomes (Bittrich 1993, Sato et al. 2007). We found that this species is diploid with a basic number of x=14, confirming the previous count from Japan (Tani 1981). S. media is a polymorphic annual (or biennial) herb and cosmopolitan with multiple chromosome numbers of 2n=18, 20, 22, 26, 28, 36, 40, 42, and 44 (Keshavarzi and Bozchaloyi 2014, Rice et al. 2015, Probatova et al. 2018). Our chromosome count of 2n=42 (Fig. 6) was following previous reports for various populations, without any clear relation to geographical distribution (Gadella and Kliphuis 1971, Morton 2005). According to Morton (2005), S. media has several cytotypes (2n=40–42), which sometimes occur in sympatry in North America. Variation in basic numbers and the occurrence of aneuploidy are unclear for the species; it is difficult to determine the chromosome number owing to the small chromosome sizes. S. alsine is widely distributed in temperate regions of Europe to Asia and is divided into three varieties. Diploids with 2n=24 have been reported for S. alsine from Europe and North America (Blackburn and Morton 1957, Gadella and Kliphuis 1972, Löve and Kjellqvist 1974, Morton 2005). Among the varieties, only S. alsine var. undulata is distributed in Korea, and our chromosome number, 2n=44 (Fig. 4), differs from a previous report (2n=46) from Japan (Tani 1981).

Dianthus has a basic number of x=15 and three reported ploidy levels (di-, tetra-, and hexaploid) (Ishii 1930, Carolin 1957, Turner 1994, Weiss et al. 2002). Among the six species recognized in Korea, D. chinensis was included in this study. We detected 2n=30 (Fig. 7) chromosomes with a basic number of x=15, confirming previous results for the species in Korea (Lee and Kim 2008) and Japan (Ishii 1930, Nakano and Mii 1993).

We investigated the chromosomes of G. oldhamiana, one of two Korean native Gypsophila species. Our chromosome number for the species was 2n=34 (Fig. 8) with a basic number of x=17, in agreement with a previous report from China (Song et al. 2004). However, Lee and Kim (2007) reported that G. oldhamiana collected from Korea has 2n=36 chromosomes. According to Pringle (2005), the basic number x=17 is common in the genus Gypsophila, but x=12 and 18 are also found in Eurasian species, and aneuploidy is occasionally observed in the genus. To clarify chromosomal relationships at the specific level, further studies of either different ploidy levels or real aneuploidy are required.

The genus Lychnis is sometimes treated as a member of Silene (Melzheimer 1980). The basic numbers for the genus are x=7 and 12 (Turner 1994). Among the four species recognized in Korea (Hong and Choi 2018), two species (L. cognata and L. fulgens) were included in this study. We found that both were diploid with 2n=24 (Figs. 9, Fig. 10). L. cognata is a perennial herb distributed mainly in China, Far East of Russia, and Korea (Lu et al. 2001, Hong and Choi 2018), and two cytotypes have been reported in Russia: 2n=14 (Ornduff 1967) and 2n=24 (Fedorov 1974). L. fulgens has a similar distribution to that of L. cognata, occurring in China, Japan, Korea, and Russia. Our chromosome number (2n=24) for L. fulgens agrees with an earlier report from the Far East of Russia (Probatova et al. 2009).

The genus Silene contains about 700 species throughout the world and exhibits great diversity in habitat, morphology, and reproductive system (Greuter 1995). Most species are hermaphrodites, although a few species are dioecious, gynodioecious, and rarely trioecious (Desfeux et al. 1996). Silene chromosomes have been studied extensively owing to the sex chromosomes composed of distinguishable XY or XX chromosomes in some dioecious species, such as S. latifolia, S. dioica, S. marizii, S. heuffelii, and S. diclinis (Blackburn 1923, 1924, Lewis 1942, Charlesworth 2002, Lengerova et al. 2003, Mrackova et al. 2008, Marais et al. 2011). Furthermore, owing to the reasonably large chromosomes, several chromosome counts have been reported (Kruckeberg 1954, 1960, Bari 1973, Melzheimer 1978, Morton 2005, Sheidai et al. 2008, Gholipour and Sheidai 2010, Luo et al. 2011). Previously, four basic numbers for the genus have been reported, i.e., x=9, 10, 12, and 23, with frequent basic numbers of x=10 and 12 overall, x=9 in S. conica and S. lacera (2n=2x=18), and x=23 in S. firma (2n=2x=46) (Van Loon and Snelders 1979, Van Loon 1982, Rice et al. 2015).

Out of 16 taxa including three endemic species recognized on the Korean peninsula, four taxa (S. aprica var. oldhamiana, S. jenisseensis, S. koreana, and S. seoulensis) and one endemic species (S. takesimensis) were included in this study. We found that the taxa were all diploids with 2n=24 (Figs. 12–15), except S. aprica var. oldhamiana, which was tetraploid with 2n=48 (Fig. 11). The basic number for these taxa was constant at x=12. S. aprica var. oldhamiana has three cytotypes, 2n=24, 48, and 72 (Erst et al. 2018). Our chromosome count (2n=48) for the variety agreed with data obtained by Lee and Kim (2007). Moreover, previous studies (Kwon et al. 2005, Lee and Kim 2008) have shown that both S. jenisseensis and S. takesimensis have 2n=24 chromosomes, in agreement with our counts. We revealed the chromosome numbers of two species, S. koreana and S. seoulensis, for the first time.

Karyotype analyses of five Silene taxa

The mean total chromosome length for the five Silene taxa in this study ranged from 90.51 µm in S. seoulensis to 159.64 µm in S. aprica var. oldhamiana, and the mean haploid chromosome length ranged from 39.91 µm in S. aprica var. oldhamiana to 48.65 µm in S. takesimensis (Table 2). We observed the smallest chromosome in S. seoulensis (2.78 µm) and the largest in S. koreana (5.97 µm) (Table 2). The previously reported haploid chromosome lengths for Silene were 26.33–47.26 µm (Sheidai et al. 2008) and 45.32 µm (Martin et al. 2008), similar to our results. The karyotype of the examined taxa was present in detail (Table 2). Accordingly, the chromosome complements for all taxa were composed mainly of median and submedian chromosomes of Levan et al. (1964), with an arm ratio from 1.00 to 3.00 (Table S1). All chromosomes of S. aprica var. oldhamiana were composed of 48 medians (Fig. 16), three taxa (S. jenisseensis, S. seoulensis, and S. takesimensis) were composed of 20 medians and four submedian (Figs. 17, 19, 20), and S. koreana was composed of 16 medians and eight submedian (Fig. 18). Satellites were found in S. seoulensis and S. takesimensis (Figs. 19, 20). The karyotypic formula for S. aprica var. oldhamiana has been reported as 36m+12sm by Lee and Kim (2007), while all chromosomes investigated in this study were composed of 48 medians. In angiosperms, asymmetrical karyotypes are generally derived from symmetrical karyotypes (Stebbins 1971, Stace 1989). It is widely accepted that there is an evolutionary trend toward increasing chromosome sizes and karyotype diversity (Stebbins 1971, Liu et al. 2006). The karyotypes of five Silene taxa from Korea were categorized as 1A, 2A, and 2B based on Stebbins’ karyotype classification (Stebbins 1971). According to the parameters ST, A, and AI, S. seoulensis had the most asymmetrical karyotype (Table 2). These were the first karyotype analyses for the examined taxa, except S. aprica var. oldhamiana.

Figs. 16–20. Karyotype of chromosomes in Silene. 16. S. aprica var. oldhamiana (2n=4x=48=48m), 17. S. jenisseensis (2n=2x=24=20m+4sm), 18. S. koreana (2n=2x=24=16m+8sm), 19. S. seoulensis [2n=2x=24+I=20m (4sat)+4sm], 20. S. takesimensis [2n=2x=24=20m+4sm (2sat)]. Arrow indicates satellite and b is B chromosome.

In Silene, B chromosomes have been reported in several species, such as S. claviformis, S. marschallii, S. propinqua, and S. maritima (Cobon et al. 1983, Sheidai et al. 2008). In this study, we observed one short B chromosome in a plant of S. seoulensis Nakai (Fig. 19).

Acknowledgments

This study was supported by the Andong National University under Grant.

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