Abstract
This paper reports mitotic chromosome numbers of 19 taxa of Allium L. sect. Melanocrommyum Webb et Berthel. from Turkey. Karyotypes of 18 species of Allium sect. Melanocrommyum were diploid with 2n = 16, only A. cyrilli Ten. was tetraploid with 2n = 32. This study includes first reports for 11 Allium species (A. elmaliense İ. G. Deniz et Sümbül, A. lycaonicum Siehe ex Hayek, A. asclepiadeum Bornm., A. nemrutdaghense Kit Tan & Sorger, A. colchicifolium Boiss., A. shatakiense Rech. fil., A. woronowii Miscz., A. nabelekii Kamelin et Seisums, A. stenopetalum Boiss. et Kotschy, A. noëanum Reuter ex Regel, A. tubergenii Freyn). The chromosome count of A. orientale, collected from Turkey, is also reported for the first time in this study. Four accessions (A. nemrutdaghense, A. colchicifolium, A. chrysantherum, and A. cardiostemon) have B-chromosomes. Seven parameters for analyzing karyotype asymmetry were assessed and karyotypic ideograms of 19 taxa of Allium (sect. Melanocrommyum) are given. Microphotographs of somatic metaphases are also provided. All karyotypes are symmetrical, consisting of metacentric and submetacentric chromosome pairs. Only A. nabelekii and A. tubergenii have subtelocentric chromosomes. Karyotype analysis according to Stebbins categories placed chromosomes of studied taxa in symmetric class of 2A, indicating a symmetric karyotype. Only A. noëanum was classified in group 2B. Analysis of karyotype formulae showed that, in general, species of sect. Melanocrommyum form a homogeneous group.
Introduction
Allium is the largest genus of Amaryllidaceae: Allieae, comprising more than 780 species belonging to 15 subgenera (Friesen et al. Citation2006). Recent additions raise the species number to more than 850 species (Keusgen et al. Citation2011). The chromosome numbers of about 550 Allium taxa are known, according to the Index to Plant Chromosome Numbers (IPCN).
Most of these taxa are diploid. Tetraploids and hexaploids seem to be clustered in some groups, e.g. sect. Rhizirideum and sect. Codonoprasum. A basic chromosome number of x = 8 dominates in most subgenera, whereas nearly all taxa of subgenus Amerallium are characterized by x = 7 chromosomes (Fritsch and Astanova Citation1998).
Melanocrommyum is the second largest subgenus, comprising about 169 accepted species and subspecies grouped into 20 sections and 22 subsections (Fritsch et al. Citation2010; Fritsch Citation2012). Chromosome numbers have been reported for approximately 90 of them; karyotypes or ideograms for less than 50. Most taxa are diploid with 2n = 16. The recent classification Sect. Melanocrommyum consists of 43 species (Fritsch Citation2012).
Subgenus Melanocrommyum is represented in Turkey by three sections: Sect. Acanthoprason (two taxa), Sect. Melanocrommyum (28 taxa) and Sect. Kaloprasum (one taxon); in total 31 taxa (Kollmann Citation1984; Davis et al. Citation1988; Özhatay and Tzanoudakis Citation2000; Deniz and Sümbül Citation2004; Eker and Koyuncu Citation2011; Behçet et al. Citation2012; Behçet and Rüstemoğlu Citation2012; Genç et al. Citation2012; Özhatay and Genç Citation2013).
During the revision of the sect. Melanocrommyum in Turkey, numerous field trips have been made and specimens have been collected all around Turkey by the first author, since 2007. For taxonomical studies many herbarium specimens have been examined from the following herbaria: Herbarium of Faculty of Pharmacy of Ankara University (AEF), Ankara University Faculty of Science Herbarium (ANK), British Museum Herbarium (BM), The Herbarium of the Royal Botanic Garden Edinburgh (E), Gazi University Faculty of Science Herbarium (GAZI), Herbarium of Faculty of Science of Hacettepe University (HUB), Herbarium of Faculty of Pharmacy of Istanbul University (ISTE), Herbarium of Faculty of Science of Istanbul University (ISTF), Herbarium of Faculty of Forestry of Istanbul University (ISTO), The Herbarium of the Royal Botanic Garden Kew (K), Yuzuncu Yil University, Faculty of Arts and Sciences, Department of Biology herbarium (VANF).
In this article, the details of chromosome morphology, karyotype formulae and symmetry index of 19 species of Allium (sect. Melanocrommyum) from Turkey have been investigated, 11 of them described for the first time.
The purpose of the paper is to fill gaps of knowledge in the genus Allium sect. Melanocrommyum.
Material and methods
Plant material: voucher specimens were kept in the herbarium of the Faculty of Pharmacy of Istanbul University (ISTE).
Karyological observations were made on mitotic metaphase cells of root-tips obtained from planted bulbs which were collected in natural habitats from Turkey. Root tips were pretreated in α-monobromonaphthalene at 4°C overnight, washed with distilled water and fixed in Carnoy’s solution (3:1 absolute ethanol: glacial acetic acid) for a minimum of 1 h. The root tips were hydrolyzed for 10–12 minutes in 1N HCl at 60°C, stained using the standard Feulgen technique and squashes were prepared. Permanent slides were made by the liquid CO2 method.
Chromosome measurements were based on five to 25 metaphase plates. Slides were examined under an Olympus BH2 photomicroscope and photographs were taken with the same microscope. The ideograms were drawn from mitotic metaphase.
For the numerical characterization of the karyotypes the following parameters were calculated: (1) shortest (SC) and longest (LC) chromosome length; (2) ratio of longest to shortest chromosome (LC/SC); (3) mean and median of long arm length (p); (4) mean and median of short (q) and total chromosome length (CL); and (5) mean and median of centromeric index (CI = 100 × length of short arm/total chromosome length).
Seven different methods were used to assess the degree of karyotype asymmetry (Table ). A review of each method and a summary of how each asymmetry index was calculated are given in Paszko (Citation2006). Statistical evaluation was carried out using the Mathematica 8.4 software package.
Table 1. Measures of karyotype asymmetry used in the present work.
The nomenclature used for the description of chromosome morphology is that proposed by Levan et al. (Citation1964).
Results
In this paper 19 taxa were examined, of which nine are endemic to Turkey (Kollmann Citation1984; Davis et al. Citation1988; Özhatay and Tzanoudakis Citation2000; Deniz and Sümbül Citation2004). Chromosome numbers of eight of these 19 taxa were reported in previous papers (Table ).
Table 2. Somatic chromosome numbers (2n), voucher number and previous chromosome counts of Allium taxa investigated.
Karyotype formulae and characteristics of the studied species are summarized in Table . Somatic chromosomes of these taxa are illustrated in Figure . Ideograms are shown in Figure .
Table 3. Karyotype formula according to Levan et al. (Citation1964) and the characteristics of the studied Allium taxa.
Figure 1 Microphotograph of somatic metaphases. (a) A. nigrum; (b) A. cyrilli; (c) A. elmaliense; (d) A. lycaonicum; (e) A. orientale; (f) A. asclepiadeum; (g) A. nemrutdaghense; (h) A. colchicifolium; (i) A. kharputense; (j) A. eginense; (k) A. shatakiense; (l) A. woronowii; (m) A. nabelekii; (n) A. cardiostemon 1; (o) A. cardiostemon 2; (p) A. chrysantherum; (q) A. stenopetalum; (r) A. karamanoglui; (s) A. noëanum; (t) A. tubergenii. Scale bars: 10 μm.
Figure 2 Ideograms of taxa. (a) A. nigrum; (b) A. cyrilli; (c) A. elmaliense; (d) A. lycaonicum; (e) A. orientale; (f) A. asclepiadeum; (g) A. nemrutdaghense; (h) A. colchicifolium; (i) A. kharputense; (j) A. eginense; (k) A. shatakiense; (l) A. woronowii; (m) A. nabelekii; (n) A. cardiostemon a; (o) A. cardiostemon b; (p) A. chrysantherum; (q) A. stenopetalum; (r) A. karamanoglui; (s) A. noëanum; (t) A. tubergenii.
Our results confirmed the previous reports that the basic chromosome number of Allium sect. Melanocrommyum is x = 8.
The diploid chromosome number was found to be 2n = 16 in all taxa in this study (Table , ). Only A. cyrilli is tetraploid (Figure b). A. colchicifolium, A. cardiostemon and A. chryantherum have one B-chromosome and A. nemrutdaghense has two B-chromosomes. All species investigated showed symmetric karyotypes consisting of 5–7 metacentric and 1–3 submetacentric chromosome pairs, except for A. nabelekii and A. tubergenii, which showed one subtelocentric chromosome pair. The B-chromosome pairs of A. nemrutdaghense and A. colchicifolium are submetacentric, and those of A. cardiostemon and A. chrysantherum are subtelocentric (Table ).
Relationships between Allium taxa based on asymmetry methods (A 1 and A 2, Rec and Syi indices, the relative variation in chromosome length (CVCL) and the coeeficient of variation for the centromeric index (CVCI) indices, and the dispersion index (DI) and asymmetric index (AI)) are shown in Figure and Table , which shows the degree of asymmetry. The remaining methods, TF% (Huziwara Citation1962), As K% (Arano Citation1963), and the A index (Watanabe et al. Citation1999), try to describe only the variation in centromere position in a chromosome complement and they have a perfect or almost perfect positive or negative correlation with the Syi index in Table .
Figure 3–6 (Color online) Scatter diagrams for Allium taxa. (3) the A1 parameter against the A2 parameter; (4) the Rec index against the Syi index; (5) the CVCL parameter against the CVCI parameter; (6) the AI index against the DI index.
Table 4. Karyotypes of studied Allium taxa using different methods of evaluating karyotype asymmetry.
Table 5. Pearson correlation for asymmetry indices and three karyotype characteristics. Significant correlations (one-tailed probability p < 0.05) are in boldface.
Satellites were detected in most analyzed taxa (Figure , Figure ) and they are always small, spherical or sometimes oval, and connected by rather thick threads to the short chromosome arms of the shortest submetacentric chromosome pairs. This is different from the other taxa satellite connected subtelocentric chromosome pairs of A. tubergenii (Figures , ).
The Stebbins (Citation1971) symmetry types are given in Table . In the Stebbins system the karyotypes of taxa, almost all of class 2A, are considered primitive classes in this system. Only A. noëanum was classified in group 2B.
The karyotype asymmetry was assessed based on seven different methods in Table . These methods contain one qualitative classification and eight different quantitative indices.
Using asymmetry indices A 1 and A 2 we could identify the more asymmetric karyotypes among taxa that had similar Stebbins classes of symmetry. For example, in class 2A the taxa A. nabelekii and A. tubergenii possessed the highest A 1 value (0.39); therefore, they have a more asymmetric karyotype. On the other hand A. woronowii and A. karamanoglui possessed the lowest A 1 value (0.23) and, hence, a more symmetric karyotype. Similarly, in class 2B, A. noëanum possessed an A 2 value of 0.32; it is the highest asymmetric karyotype in this group in Table and Figure .
Taxa classified in group 2A also showed the lowest A 2 values (ranging from 0.08 to 0.18), and the highest%TF (from 37.71 to 43.50) in Table .
In general, based on A 1 and %TF intrachromosomal asymmetry, A. nabelekii had the most asymmetrical and evolutionary karyotype, while A. karamanoglui had the most symmetrical karyotype of all the taxa. According to A 2 interchromosomal asymmetry, A. noëanum had the most asymmetrical karyotype of all the taxa in Table . We observed that the intrachromosomal asymmetry index (A 1) varied from 0.23 to 0.39, and the interchromosomal asymmetry index (A 2) ranged from 0.08 to 0.21.
According to the scatter diagrams plotted with AI–DI, A 1–A 2, Syi–Rec and CVCL –CVCI, A. noëanum is more asymmetric than the others (Figures –6). The karyotype formulae obtained and the parameters analyzed are summarized in Table . A. noëanum and A. elmaliense exhibited the most variation in chromosome length, but A. nabelekii has the highest level of variation of the centromeric index.
The analysis of index formulae and the association between quantitative indices and three karyotype characteristics (LC/SC, CL, and CI) reveals three groups among them in Table . The results of variance analysis revealed significant differences between the taxa based on all karyotype characteristics (p < 0.05). The significance of a Pearson correlation coefficient with 0.38, given in Table , is the closest to the value of p < 0.05.
TF%, Syi, As K%, A1 and A were used to evaluate the variation in centromere position in a chromosome complement. Although TF% has a perfect negative correlation with two indices, As K% and A, it has a perfect positive correlation with the Syi index (Table ). On the other hand, the Syi index has shown a perfect negative correlation with As K% and A. Therefore, these indices demonstrated the relationship among the species and it can be stated that TF%, As K% and A indices have a perfect positive or negative correlation with Syi index in Table . It can also be seen that the Rec index had negative correlation with chromosome length (CL) and centromeric index (CI) (Table ).
The A 1 value as well as the scatter diagram based on CVCL and CVCI displayed a relationship among the species with respect to karyotype asymmetry (Figure , Table ). Karyotype asymmetry depends on both the relative variation in chromosome length (CVCL ) and the relative variation in centromeric index (CVCI ). The other asymmetry index, the AI index, can be defined as the product of these components. It gives a measure of the heterogeneity of chromosome length and centromeric position in a given karyotype. The AI index value is proportional to karyotype asymmetry. In this case, if we look at Table and Figure , it is seen that the most symmetrical karyotype is the A. stenopetalum, while A. noëanum exhibited the most asymmetrical karyotype. On the other hand the DI index (Figure , Table ) gave a broad measurement but could not indicate the asymmetry of a particular karyotype.
Table 6. Chromosome statistics for Allium taxa.
Discussion
Our results are similar to previous counts. However, different counts are given for A. nigrum (2n = 16, 32), A. cyrilli (2n = 16, 32, 40) and A. orientale (2n = 16, 24, 32) by Sopova (Citation1972), Karavokyrou and Tzanoudakis (Citation1991) and Tzanoudakis (Citation1999) (Table ). These three taxa may be polyploid species. However large numbers of plates are investigated in this study, but our results never changed. These three taxa sometimes intermix and may be misidentified by the authors. This probability should be considered.
In this study karyotypes of 11 Allium species were reported for the first time. A. orientale was also reported for first time collected from Turkey. During the PhD study the authors we observed that A. lycaonicum and A. stenopetalum were misidentified (Genç 2010), which are used as examined material by Koyuncu and Özhatay (Citation1983) and Özhatay (Citation1993). Therefore chromosome counts of these species were ignored.
According to our morphological results A. cardiostemon is close to A. chrysantherum, and A. colchicifolium is close to A. nemrutdaghense. These species which are close together had generally B-chromosomes.
Analysis of karyotype formulae showed that, in general, species of sect. Melanocrommyum form a homogeneous group.
The mean values of the chromosome long arm varied from 4.43 μm in A. woronowii to 10.44 μm in A. nabelekii. Averages of the chromosome short arm varied from 3.36 μm in A. woronowii to 6.58 μm in A. nigrum. The mean values of chromosome total length varied from 8.94 μm in A. woronowii to 18.78 μm in A. elmaliense (Table ).
The chromosomes were mostly metacentric (m) or sub-metacentric (sm) in all taxa except for A. nabelekii and A. tubergenii, which had one pair sub-telocentric (st) chromosomes (Table ). These results generally overlap with Fritsch and Astanova’s (Citation1998) results. The Stebbins (Citation1971) symmetry type and the asymmetry indices of Romero-Zarco (1986) are given in Table and the latter are represented graphically in Figures . Regarding the Stebbins’ system, the karyotype of taxa mostly seizes 2A class which is considered majorly primitive class in this system.
Based on interchromosomal symmetry, A. karamanoglui had the most asymmetrical and the most evolved karyotype, while A. nabelekii had the most symmetrical karyotype. However, intrachromosomal symmetry information showed that A. nabelekii had the most asymmetrical karyotype.
In order to describe karyotype asymmetry between species of the Allium (sect. Melanocrommyum), CVCL and CVCI parameter values were plotted (Figure ). In contrast to the study of Peruzzi et al. (Citation2009), it is seen that the values of these two parameters are close to each other. Therefore, there was small variation in the range of values for CVCL and CVCI between karyotypes of Allium. In this case, we can say that karyotypes in Allium have a smaller and a narrower range of values for both CVCL (8.30–20.84) and CVCI (8.88–21.96) (Table ). If we compare these parameters with the parameters of Peruzzi et al. (2009, figure , p. 468), the studied Allium taxa are separated from the studied genera of the Peruzzi et al. (Citation2009) as a nearly homogenous group.
Acknowledgments
This work was supported partly by the Research Fund of Istanbul University, Istanbul, Turkey (project number 798). The authors would like to thank Assoc. Prof. Dr. Ali Kandemir, Assistant Prof. Dr. İ. Gökhan Deniz, Assistant Prof. Dr. Candan Aykurt and Assistant Prof. Dr. İsmail Türkoğlu for their field-trip guidance. We are also grateful to Prof. Dr. Mehmet Koyuncu for sharing knowledge and the specimens.
Related Research Data
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