AOBPreview published online on November 25, 2008
Annals of Botany, doi:10.1093/aob/mcn230
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Chromosome diversity and evolution in Liliaceae
1 Dipartimento di Biologia, Unità di Botanica Generale e Sistematica, Università di Pisa, via Luca Ghini 5, 56126 Pisa, Italy
2 Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AB, UK
* For correspondence: E-mail lperuzzi{at}biologia.unipi.it
Received: 15 May 2008 Returned for revision: 4 August 2008 Accepted: 20 October 2008
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSSUPPLEMENTARY DATAACKNOWLEDGEMENTSLITERATURE CITED |
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Background and Aims: There is an extensive literature on the diversity of karyotypes found in genera within Liliaceae, but there has been no attempt to analyse these data within a robust phylogenetic framework. In part this has been due to a lack of consensus on which genera comprise Liliaceae and the relationships between them. Recently, however, this changed with the proposal for a relatively broad circumscription of Liliaceae comprising 15 genera and an improved understanding of the evolutionary relationships between them. Thus there is now the opportunity to examine patterns and trends in chromosome evolution across the family as a whole.
Methods: Based on an extensive literature survey, karyo-morphometric features for 217 species belonging to all genera in Liliaceae sensu the APG (Angiosperm Phylogeny Group) were obtained. Included in the data set were basic chromosome number, ploidy, chromosome total haploid length (THL) and 13 different measures of karyotype asymmetry. In addition, genome size estimates for all species studied were inferred from THLs using a power regression model constructed from the data set. Trends in karyotype evolution were analysed by superimposing the karyological data onto a phylogenetic framework for Liliaceae.
Key Results and Conclusions: Combining the large amount of data enabled mean karyotypes to be produced, highlighting marked differences in karyotype structure between the 15 genera. Further differences were noted when various parameters for analysing karyotype asymmetry were assessed. By examining the effects of increasing genome size on karyotype asymmetry, it was shown that in many but not all (e.g. Fritillaria and all of Tulipeae) species, the additional DNA was added preferentially to the long arms of the shorter chromosomes rather than being distributed across the whole karyotype. This unequal pattern of DNA addition is novel, contrasting with the equal and proportional patterns of DNA increase previously reported. Overall, the large-scale analyses of karyotype features within a well-supported phylogenetic framework enabled the most likely patterns of chromosome evolution in Liliaceae to be reconstructed, highlighting diverse modes of karyotype evolution, even within this comparatively small monocot family.
Key words: C-value, chromosomes, genome size, karyotype asymmetry, karyotype evolution, Liliaceae, Liliales, polyploidy
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSSUPPLEMENTARY DATAACKNOWLEDGEMENTSLITERATURE CITED |
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Comparative karyotype analysis of related species has traditionally been used to describe patterns and directions of chromosomal evolution within a group and to infer the evolutionary role that such karyotype changes may have played (e.g. Stebbins, 1971; Stace, 1978; Gonzalez-Aguilera and Fernandez-Peralta, 1984; Watanabe et al., 1995; De Melo Nationiel et al., 1997; Vanzela et al., 1997; Das et al., 1999; Shan et al., 2003). Whereas earlier studies were, to some extent, flawed by the lack of a rigorous phylogenetic framework in which to analyse the data, more recently this problem has been addressed and there are now an increasing number of papers which have analysed karyological data using a well-supported phylogenetic tree. These include the works of Cox et al. (1998) on slipper orchids (Orchidaceae), Watanabe et al. (1999) on Brachyscome (Asteraceae), Venora and collaborators (Venora et al., 2000; Frediani et al., 2005; Caputo et al., 2006; Ruffini Castiglione et al., 2007) on Vicia (Fabaceae), Leitch and colleagues on Nicotiana (Solanaceae) (Lim et al., 2000, 2004, 2006, 2007), Lysak and collaborators on Brassicaceae (Lysak et al., 2005, 2006, 2007; Lysak and Lexer, 2006; Lysak and Mandakova, 2007) and Pires et al. (2006) on Asparagales.
The karyotype is the phenotypic aspect of the chromosome complement as seen at mitotic metaphase. A description of the karyotype typically includes the chromosome number [the product of two variables, basic number (x) and ploidy, resulting in chromosome number (2n)], the absolute and/or relative length of chromosomes (reflecting genome size), the position of primary and secondary constrictions (Levan et al., 1964), the distribution of material with different staining properties (Stebbins, 1971; Stace, 2000; Levin, 2002; Lysak and Lexer, 2006) and the degree of symmetry. A symmetrical karyotype is characterized by mainly metacentric and sub-metacentric chromosomes of approximately equal size. Changes to an asymmetric karyotype can arise by shifts in centromere position towards the telomere (intrachromosomal) and/or by the addition or deletion of chromatin from some but not all chromosomes, leading to differences in size between the largest and smallest chromosomes (interchromosomal). These processes are not usually correlated, though there are some reports that they are in some groups (Stebbins, 1971).
The chromosomes of Liliaceae have long attracted attention, given their diversity in size, number and structure (e.g. Sato, 1943; Cave, 1970; Sen, 1975; Tamura, 1995). However, attempts to infer patterns of chromosome evolution by comparative karyotype analysis have been hampered by the lack of a rigorous phylogenetic framework together with a lack of agreement over the genera comprising Liliaceae. Examples of some of these contrasting circumscriptions are outlined in Table 1. There is now a general consensus of the genera comprising subfamily Lilioideae [Amana, Cardiocrinum, Erythronium, Fritillaria, Gagea (including Lloydia), Lilium (including Nomocharis), Notholirion and Tulipa] and the phylogenetic relationships between them (Fay and Chase, 2000; Patterson and Givnish, 2002; Fay et al., 2006). Similarly, genera comprising subfamily Medeoloideae (Clintonia and Medeola) and their relationships are well supported (Fay et al., 2006). However, the placement of Tricyrtis, Calochortus and the clade comprising Prosartes, Scoliopus and Streptopus (Streptopeae) has been more problematic (Patterson and Givnish, 2002; Rønsted et al., 2005; Fay et al., 2006). Nevertheless, by taking a broad circumscription of Liliaceae, as used by Chase et al. (2000), Fay and Chase (2000) and the Angiosperm Phylogeny Group (APG II, 2003), the opportunity to examine the wealth of cytogenetic data available for the 15 genera comprising Liliaceae sensu APG II (2003) within a phylogenetic context now exists. Figure 1 summarizes the current understanding of these phylogenetic relationships.
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Despite phylogenetic issues noted above, some previous karyotype analyses have been informative. For example, Tamura (1995, 1998a, b) highlighted differences in karyotype structure between the small and variable number of chromosomes in genera such as Calochortus, Prosartes, Scoliopus, Streptopus and Tricyrtis, and the larger and more stable chromosome numbers found in subfamily Lilioideae (e.g. Lilium, Fritillaria, Tulipa). Tamura (1995. 1998a, b) also noted clear differences in karyotype structure between genera in subfamily Medeoloideae (x = 7) and Lilioideae (x = 12) and the distinct karyotype shared by all representatives of tribe Lilieae, comprising two longer metacentric chromosome pairs and ten shorter telocentric pairs.
More recently, research in Liliaceae sensu APG II (2003) revealed considerable variability in genome size, broadly paralleling chromosome heterogeneity (Leitch et al., 2007). Large genomes (mean 1C = 35·9 pg) characterized subfamilies Lilioideae and Medeloloideae, whereas smaller genomes (mean 1C = 5·6 pg) characterized the remaining genera (Leitch et al., 2007). In their analysis, genome size data were compiled from the Plant DNA C-values database (Bennett and Leitch, 2005b) and Zonneveld et al. (2005), together with new genome size estimates for 23 species of Liliaceae to give a total data set of 78 species. Despite containing some of the largest genomes so far reported in the angiosperms, a phylogenetic analysis revealed that the ancestral genome size reconstructed for the family was just 1C = 6·67 pg, similar to that reported for Smilax in Smilacaceae (sister to Liliaceae) (1C = 5·0 pg).
Given recent advances in understanding phylogenetic relationships within Liliaceae noted above, this paper aims to summarize quantitatively the large amount of karyotype data available in the literature for all genera of Liliaceae (sensu APG II, 2003) and analyse them within a phylogenetic framework to assess possible modes and directions of karyotype evolution.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSSUPPLEMENTARY DATAACKNOWLEDGEMENTSLITERATURE CITED |
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Source of karyotype data
An extensive literature survey was conducted to collate available karyotype data for Liliaceae and Smilaacceae. The index to plant chromosome numbers (eds, P. Goldblatt and D. E. Johnson, Missouri Botanical Garden, St Louis) was consulted (hard copies up to 1979 and then electronically at http://mobot.mobot.org/W3T/Search/ipcn.html) together with other chromosome atlases (e.g. Darlington and Wylie, 1955; Fedorov, 1969) and internet resources (e.g. Kew Bibliographic Databases, ISI Web of Science, Google Scholar).
In total, karyotype data were collected for 405 accessions of Liliaceae (386) and Smilacaceae (19). Data were available for 217 species, including representatives of all genera comprising these two families. Only literature with published idiograms, and/or karyotype measurements and/or good metaphase plates with magnification or scale bar indicated were considered. When 2n mitotic metaphase plates were measured, the graphic method proposed by Plummer et al. (2003) was used to match homologous chromosomes. This involves plotting the relative length of each chromosome [= (length of individual chromosome/total length of all chromosomes)/100] against its arm ratio, in order to pair chromosomes.
Karyotype analysis
A data matrix of 53 karyotype features was assembled including basic chromosome number (x), ploidy, chromosome number (2n) and chromosome total haploid length (THL). For analysis of karyotype asymmetry, all known methods of assessing this character were used (Table 2). A review of each method and a summary of how each asymmetry index was calculated is given in Paszko (2006). For the present analyses, two coefficients of variation (CVs) were found to be particularly informative measures of asymmetry. The CVCI index evaluates differences in centromere position for each chromosome in the karyotype and provides a measure of intrachromosomal asymmetry. In contrast, the CVCL gives a measure of interchromosomal asymmetry as it reflects how variable the chromosome sizes are in the karyotype. In both cases, the larger the value the greater the asymmetry in the karyotype.
For each genus, a mean haploid idiogram was built as follows. Using karyoytype data for each species, chromosome pairs were arranged into decreasing lengths, then the absolute lengths of the long and short arms of each chromosome pair were taken. The data were then pooled to produce a mean length of each chromosome pair for a genus (e.g. the data for the longest chromomosome pair of all Lilium species were pooled to give the mean value for Lilium chromosome pair I). It is noted that since the study was based almost exclusively on measurements of Feulgen-stained chromosomes, there was no possibility of identifying and analysing homoeologous chromosomes between taxa. Instead the ‘mean karyotype’ of each genus refers only to the shape of the haploid karyotype.
Genome size estimates inferred from the THL
According to Levin (2002, and literature cited therein), the correlation between THL and 1C values typically exceeds r = 0·85 within species and between species in related genera, and THL has thus been considered a good proxy for genome size. In the present study, THLs were measured for all species analysed. To transform THL into an inferred 1Cx (= monoploid genome size, which represents the DNA amount in the basic haploid chromosome complement and is calculated by dividing the 2C DNA amount by the ploidy level; Greilhuber et al., 2005) estimate for each species, first a predictive regression model was built by plotting the mean THL for each genus (Table 3, based on data in Supplementary Data 1, available online) against the mean 1Cx genome size for each genus using data taken from the Plant DNA C-values database (Bennett and Leitch, 2005b), Leitch et al. (2007) and Zonneveld et al. (2005) (Table 3, Fig. 2A). Using these data, 11 common linear regression models were tested. All were significant at the 0·01 level. The highest r2 value (0·92) was obtained with a Cubic curve equation, but this was rejected because it altered the extreme values too much. Among the remaining models, a linear curve (r2 = 0·86) was excluded as it gave negative 1Cx estimates for small THL values. From six other equally well fitting curves (r2 = 0·85–0·86), the power regression model was selected as it gave the most reasonable outputs for both small and large THL values (Fig. 2A).
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Correlations
For continuous quantitative data, Pearson's correlation coefficient was used, whereas for mixed scalar and ordinal data Spearman's rho coefficient was calculated. Correlations were considered as weak (up to 0·3), average (up to 0·5), good (up to 0·80) and high (>0·80). Only correlations significant at the 1 % level or higher are discussed.
Phylogenetic framework and inferred basic chromosome numbers
The phylogenetic framework for Liliaceae used in this study (Fig. 1) was derived mainly from the work of Patterson and Givnish (2002) and Fay et al. (2006), together with additional data from the phylogenetic analysis of Tan et al. (2005, restoration of Amana), Rønsted et al. (2005, sinking of Nomocharis), Peterson et al. (2004, 2008), Peruzzi et al. (2008a, b) and M. Zarrei et al. (unpubl. res.) concerning the sinking of Lloydia in Gagea. Smilacaceae is the sister family to Liliaceae (Patterson and Givnish, 2002; Fay et al., 2006). All nodes for which bootstrap support and branch length did not fit the requirements for the 0·95 binomial confidence interval (Zander, 2004) were collapsed. The resulting phylogenetic tree is almost identical to the one used by Leitch et al. (2007) in their genome size study (except for the relationships between Amana, Erythronium and Tulipa).
The ancestral basic chromosome number for Liliaceae was inferred to be x = 8 based on the frequency of 2n = 32 counts in Smilax (Smilacaceae) and cytological data suggesting the genus to be palaeopolyploid (Vijayavalli and Mathew, 1987). This is also considered to be the ancestral basic number for Streptopus, Scoliopus and Prosartes given the frequency of species in these genera based on x = 8. An ancestral basic chromosome number of x = 9 was adopted for the highly variable Calochortus (x ranging from 6 to 10) based on the parsimony analysis of Patterson and Givnish (2004), and x = 13 for the chromosomally stable genus Tricyrtis as suggested by Nakamura (1968). An ancestral basic number of the Medeoloideae + Lilioideae clade is more equivocal, although basic numbers of x = 7 for Medeloideae and x = 12 for Lilioideae are well supported by previous karyotype studies together with the suggestion that their karyotypes may be related by Robertsonian rearrangements (e.g. Tamura, 1998b).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSSUPPLEMENTARY DATAACKNOWLEDGEMENTSLITERATURE CITED |
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Inferring genome size from THLs
In general there was a broad agreement between the mean inferred 1Cx value for each genus and values from genome size studies, although there were some discrepancies in Lilium and Fritillaria. Nevertheless this approach was considered robust enough to infer 1Cx values from THL measurements for all accessions studied, and these are given in Supplementary Data 1, available online.
Variabilities in inferred 1Cx values for each genus are illustrated by the boxplots shown in Fig. 3 which are superimposed onto the consensus phylogenetic framework of Liliaceae (from Fig. 1). This figure highlights the contrast between the large and wide range of genome sizes in subfamily Lilioideae, especially in tribe Lilieae, compared with the smaller and narrow range of genome sizes encountered in the remaining genera. The only exceptions to this were found in Gagea and Scoliopus. The mean genome size for Gagea (inferred mean 1Cx = 6·86 pg) was less than half the next smallest genome size in the tribe (for Amana with an inferred mean 1Cx of 14·69 pg). Scoliopus stood out because the genome size for this genus (inferred 1Cx = 17·80 pg) was more than three times larger than that for Prosartes (inferred mean 1Cx = 5·08 pg) and Streptopus (inferred mean 1Cx = 3·43 pg) in the same clade.
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Constructing mean haploid idiograms for each genus
Mean haploid idiograms for all genera superimposed onto the consensus phylogenetic framework of Liliaceae are shown in Fig. 1 using data taken from Table 4. The different sizes of the karyotypes largely reflect the patterns already noted from the boxplots in Fig. 3, with the relatively small chromosomes of Gagea compared with other genera in subfamily Lilioideae and the larger chromosomes in Scoliopus compared with Calochortus, Prosartes, Streptopus and Tricyrtis standing out as exceptions.
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Karyotype asymmetry
Results for the 13 different measures of karyotype asymmetry are given in Supplementary Data 1, available online. Pearson's correlation coefficients between each of the different measures varied from weak to strong, negative to positive and insignificant to significant (Supplementary Data 2, available online).
Two of these measures, CVCL and CVCI, which represent the degree of heterogeneity within a chromosome complement in terms of chromosome length (interchromosomal variation) and centromere position (intrachromosomal variation), respectively, were analysed in greater detail. Boxplots showing the range of values obtained for these two parameters for each genus are given in Fig. 4, arranged phylogenetically. Figure 5 summarizes differences between genera in these two measures of karyotype asymmetry by plotting the CVCI and CVCL values for each species.
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Karyotype asymmetry and genome size
In general, there was a good positive correlation between 1Cx and CVCI across Liliaceae (r = 0·65, Fig. 6A; Supplementary Data 2, available online), indicating that increases in genome size were generally accompanied by increasing karyotype asymmetry through increasing variability in centromere position. This correlation was also found for various subgroups within Liliaceae including Tricyrtis (r = 0·56), Lilioideae (r = 0·59), Lilieae (r = 0·23) and Lilium (r = 0·32). However, the correlation was negative for Fritillaria (within Lilieae, r = –0·33) and for all Tulipeae (r = –0·37).
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The relationship between 1Cx and CVCL in Liliaceae was generally negative (r = –0·49, Fig. 6B). This correlation was also found for many sub-groups analysed alone, including Tricyrtis (r = –0·36), Lilioideae (r = –0·46) and Tulipeae (r = –0·46). The least negative Pearson's coefficient values were found in Lilium (r = –0·22) and Lilieae (r = –0·17).
Trends in karyotype asymmetry and genome size were also analysed for individual chromosomes. This was done by plotting, for each chromosome in the karyotype, its R (arm ratio) value against the inferred 1Cx for the accession (data not shown). [The R value is a measure of chromosomal asymmetry calculated by dividing the length of the long arm by the length of the short arm for each chromosome; see Levan et al. (1964). A metacentric chromosome has an R value of 1 whereas higher R values are associated with increasingly acrocentric chromosomes.] This approach revealed that the larger, often metacentric (i.e. chromosome pairs I and II) and smaller sub-metacentric to telocentric chromosomes (chromosome pairs IV and higher) undergo different patterns of karyotype evolution. While there was a strong positive correlation with smaller chromosomes from IV to XII (r = 0·92–0·98), indicating that the additional DNA is associated with increasing intrachromosomal asymmetry, chromosome pairs I–III had a low negative correlation with genome size (r values ranging from –0·14 to –0·18), implying that as genome size increases these chromosomes become more symmetric. This pattern was observed for all genera except Fritillaria and genera in Tulipeae.
When Smilacaceae were analysed alone, there were no relevant differences in the relationships between 1Cx and R values for the larger and shorter chromosomes. In all cases, the correlations were positive and high (r = 0·70–0·98) or not significant (depending on the chromosome).
Polyploidy
Overall the percentage of polyploids in Liliaceae was low (16 % for the whole data set). Many genera were exclusively diploid (Cardiocrinum, Erythronium, Medeola, Notholirion, Prosartes, Scoliopus and Tricyrtis) and only three genera had 50 % or more polyploids (Amana, Clintonia and Gagea) (Fig. 7). Plotting the relationship between the occurrence of polyploids and mean inferred 1Cx genome size for each genus revealed that most polyploids (94 %) occurred in species with 1Cx genome sizes <25 pg (Fig. 7); above this DNA amount, the number of polyploid species was small (Fig. 8). In all genera, the species with the highest inferred 1Cx values were always diploid (Fig. 8).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSSUPPLEMENTARY DATAACKNOWLEDGEMENTSLITERATURE CITED |
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The reliability of inferring genome size from THLs
Whereas previous studies have highlighted the potential for using chromosome data as a proxy for genome size (e.g. Narayan and Rees, 1976; Raina and Rees, 1983; Ceccarelli et al., 1995), it has also been shown that chromosomes of a species can vary considerably in size without any change in DNA amount depending on the method of chromosome preparation as well as the phosphate concentration of the growth medium or type of root analysed (Bennett and Rees, 1967, 1969; Bennett, 1970). Given this, it was necessary to check if the karyotype data available for Liliaceae could be used to infer genome sizes. Using the approaches outlined, a new predictive regression model for inferring genome size from the THL of chromosome complements was produced specifically for Liliaceae and the closely allied Smilacaceae. In general there was broad agreement between ‘real’ genome size values obtained using ‘best practice’ genome size estimation techniques (flow cytometry and Feulgen microdensitometry) and those inferred from THL measurements (Fig. 2B). The largest differences occurred in Lilium. One explanation is that Lilium is a large genus (approx. 100 species) and, while there are karyological data for 58 species, genome size data are only available for ten species. It is possible that the smaller mean 1Cx values from genome size data are due to the small number of species analysed. From the data given in Supplementary Data 1 (available online), Lilium species with the largest THLs have not had their genome sizes measured using best practice techniques. Whilst it is recognized that accurate genome size estimates will never be obtained from THLs, given the wealth of karyotype information available compared with the amount of genome size information, it was felt that the current approach was appropriate for providing some insights into patterns of genome evolution across Liliaceae.
Patterns of genome size evolution across Liliaceae
Superimposing inferred genome size data onto a phylogenetic tree of Liliaceae revealed similar patterns to those predicted from chromosome data by Tamura (1995, 1998a, b) and observed by Leitch et al. (2007), most notably the striking differences between the genome size profiles of (a) genera in subfamily Lilioideae and Medeoloideae and (b) the remaining genera (Calochortus, Tricyrtis, Prosartes, Scoliopus and Streptopus) (Figs 1 and 3). However, the considerably larger data set available in the present work (217 species compared with 78 species in Leitch et al., 2007) highlighted two exceptions to this general pattern: (1) the relatively large genomes in Scoliopus (inferred 1Cx = 17·2 pg) compared with Prosartes (mean inferred 1Cx = 5·1 pg), Streptopus (inferred mean 1Cx = 3·4 pg), Calochortus (inferred mean 1Cx = 5·4 pg) and Tricyrtis (inferred mean 1Cx = 7·9 pg); and (2) the small Gagea genomes (inferred mean 1Cx = 6·9 pg) compared with the remaining genera in subfamily Lilioideae (inferred mean 1Cx range 14·7–56·3 pg).
Overall, although statistical analysis of genome size evolution across the family has revealed it to be punctuated with a significantly large shift and subsequent radiation in genome size at the base of Lilioideae (Leitch et al., 2007), more localized genome size changes in the branches leading to Gagea and Scoliopus have also taken place. For Scoliopus the larger genomes most probably represent the result of localized genome size increases, whereas for Gagea genome downsizing would appear to be the more parsimonious explanation. However, the possibility that its small genome size represents the ancestral state with all other genera in the clade having experienced an increase cannot be ruled out, particularly in light of recent data suggesting that the predominant direction of genome size evolution in angiosperms is upwards (Hawkins et al., 2009). The nature of the evolutionary forces driving these changes remains unknown, although analysis suggests that genome size evolution in Liliaceae is passive rather than adaptive (Leitch et al., 2007).
In general, there is a positive correlation between genome size and the percentage of repetitive DNA for both tandem and dispersed repeats (Levin, 2002; Gregory, 2005). As for the effects that repetitive non-coding DNA has on the organism, there are broadly two different viewpoints. One of them interprets non-coding DNA as ‘junk’ DNA, whereas the other interprets repetitive DNA as adaptive in various aspects of plant structure and function, i.e. a larger genome is correlated with larger cell volumes and longer cell cycles (reviewed in Gregory, 2001; Bennett and Leitch, 2005a; Leitch and Bennett, 2007). The latter view seems to be the best supported, at least for Liliaceae, since genome size is related to morphological, ecological and/or adaptive changes (see Patterson and Givnish, 2002, for fuller discussion), although, as noted above, the analysis by Leitch et al. (2007) suggested that large genomes evolved passively.
Karyotype structure in Liliaceae
Figure 1, which gives a mean haploid karyotype for each genus, and data in Supplementary Data 1 (online) highlight the considerable diversity in karyotype structure in Liliaceae, already noted in previous studies (e.g. Tamura, 1995, 1998a, b). There is considerable variation in chromosome number (x = 6–13), ploidy (2x–6x; and up to 11x in Gagea; Peruzzi, 2008, and references cited therein), chromosome size (1·00–37·73 µm) and karyotype asymmetry. By superimposing these data onto the phylogenetic framework, patterns and trends in karyotype evolution can be seen.
Karyotype asymmetry.
Significant differences in karyotype asymmetry are apparent within Liliaceae based on the various measures of karyotype asymmetry analysed. Most of the correlations found among different karyotype asymmetry measures (Supplementary Data 2, available online) agreed with data reported by Paszko (2006) for Calamagrostis (Poaceae), and overall the present study supports her conclusions concerning the general validity of the different measures of karyotype asymmetry tested. However, from the present data, the asymmetry index (AI) which Paszko proposed as a new measure of asymmetry, aiming to capture the degree of asymmetry in a single value, is strongly and positively correlated with CVCI (r = 0·85, a measure of asymmetry based on variation in centromere position between chromosomes in the karyotype) but not significantly correlated with CVCL (r = 0·08, a measure of asymmetry based on variation in chromosome lengths between chromosomes in the karyotype). For this reason, it was felt that the AI value proposed by Paszko does not adequately reflect all aspects of karyotype asymmetry in Liliaceae. Instead it seems more meaningful to retain these two separate parameters which reflect two different aspects of karyotype asymmetry, variation in chromosome length (CVCL) and centromere position (CVCI).
Boxplots summarizing the values of these two parameters for each genus (Fig. 4) highlight the wide range and large values of CVCI in Calochortus and tribe Lilieae compared with other genera. This indicates that their karyotypes are considerably more asymmetric in terms of variation in the position of the centromeres than those of other genera of Liliaceae. In contrast, there was less variation in the range of values obtained for CVCL between and within different genera.
Plotting CVCL and CVCI values for each genus highlights further differences in karyotype asymmetry between different genera (Fig. 5). For example, the asymmetric karyotypes that characterize species in Lilieae are due more to variation in the position of the centromere (large CVCI values) than to differences between the chromosome sizes in the karyotype (i.e. lower values of CVCL; Fig. 5A). Karyotypes in Tulipeae are generally less asymmetric than in Lilieae as most have a narrower range of values for both CVCL and CVCI (Figs 4 and 5B), as also found in Medeoloideae (Figs 4 and 5C). An exception to this pattern is the relatively high CVCL values in Gagea within Tulipeae. For the remaining genera in Liliaceae, increasing karyotype asymmetry arises through increasing variation in chromosome lengths (wide range of CVCL values) rather than shifts in centromere position (narrow range of CVCI; Fig. 5C), a pattern also observed in Smilax in Smilacaceae. There were no species with large CVCL and CVCI values, indicating that there are no karyotypes that are asymmetric in terms of both large differences in chromosome length and centromere position in Liliaceae. The only comparable study using CVCL and CVCI to describe karyotype asymmetry was that of Paszko (2006). However, this study was restricted to just eight species of Calamagrostis (Poaceae) and the data were not viewed within a phylogenetic framework. To what extent the patterns observed here are specific to Liliaceae or represent more general patterns of karyotype asymmetry evolution is currently unknown.
Karyotype asymmetry and genome size.
Overall, an analysis of the relationship between 1Cx and CVCI showed these two parameters were positively correlated (Fig. 6A), indicating that genome size increases are generally accompanied by increasing intrachromosomal asymmetry through increased variability in centromere position within the karyotype (r = 0·65). Such a pattern suggests that the additional DNA is not being added uniformly across the karyotype. This correlation was also found for various subgroups within Liliaceae including Tricyrtis (r = 0·56), Lilioideae (r = 0·59), Lilieae (r = 0·23) and Lilium (r = 0·32). However, for Fritillaria (in Lilieae) and the whole of Tulipeae, the correlation was negative (r = –0·33 for Fritillaria and –0·37 for Tulipeae), suggesting that the distribution of the additional DNA followed a different pattern from that noted for the rest of the family.
The relationship between 1Cx and CVCL was generally negative (Fig. 6B), indicating that an increase in genome size is accompanied by decreasing size differences between chromosomes of the karyotype (i.e. a more symmetrical karyotype). This correlation was also found for some sub-groups analysed alone: Tricyrtis, Lilioideae and Tulipeae.
The analysis of changes in individual chromosome asymmetry with genome size provided some insights into how the additional DNA is distributed across the karyotype. Whereas the large metacentric chromosomes (e.g. chromosome pairs I and II) became more symmetrical with increasing genome size, the smaller sub-metacentric and telocentric chromosomes (i.e. chromosome pairs IV and above) became more asymmetrical. Such a pattern implies that the additional DNA is added mainly to the long arms of the smaller chromosomes rather than being distributed evenly between all chromosome arms of the karyotype complement. As far as we are aware, this type of chromosome evolution pattern has not been noted before.
To date, two main patterns for the addition of DNA in a chromosome complement have been described (reviewed by Levin, 2002). For ‘proportional increase’, the amount of DNA added to each chromosome arm is proportional to its length. This pattern does not result in a change in karyotype asymmetry with increasing DNA amount and thus the values for CVCI and CVCL remain unchanged as the genome size changes. This pattern has been observed in several genera including Aloe and Gasteria (Xanthorrhoeaceae) (Brandham and Doherty, 1998) and in some species of Oxalis (Oxalidaceae) (De Azkue and Martinez, 1988). For ‘equal increase’, the same amount of DNA is added to each chromosome arm regardless of its size. This will result in an increase in karyotype symmetry, and hence a decrease in CVCI and CVCL with increasing genome size. Examples of genera showing this pattern include Vigna (Fabaceae) (Parida et al., 1990), Vicia (Fabaceae) (Raina and Rees, 1983), Papaver (Papaveraceae) (Srivastava and Lavania, 1991) and Hypochaeris (Asteraceae) (Cerbah et al., 1998a, b).
In many genera in Liliaceae, however, a third pattern is apparent. Here there is an ‘unequal increase’, i.e. the amount of DNA added varies between longer and shorter chromosome arms unequally, leading to an overall increase in karyotype asymmetry with genome size. This pattern gives rise to the observed increase in CVCI but a slight decrease in CVCL with increasing genome size.
Such a pattern may, in part, be influenced by an upper limit on chromosome size for a particular karyotype, as reported for both monocots and eudicots (Schubert and Oud, 1997; Hudakova et al., 2002). Nevertheless, other factors such as the involvement of Robertsonian translocations will also play a role as exceptions to the unequal increase pattern are found in Fritillaria (with some of the largest chromosomes of Liliaceae) and Tulipeae. In these groups, the increase in genome size is accompanied by a general decrease in asymmetry (decreasing CVCI) and is typical of the equal increase pattern noted above.
Of course there are other types of chromosome change which can contribute to asymmetry variation between species and genera (reviewed by Schubert, 2007) including pericentric inversions and/or differential translocations of DNA between smaller and larger chromosomes (if there is no change in chromosome number) and Robertsonian fissions and fusions (if accompanied by changes in chromosome number); such karyotype changes have also been reported in some species of Liliaceae. Indeed the low, but significant, negative correlation between CVCI and CVCL probably in part reflects the occurrence of Robertsonian translocations which are found in several genera including Cardiocrinum, Fritillaria, Streptopus and Tricyrtis (Darlington, 1973; Zhongyan et al., 1989; Tamura, 1995; Zhang and Gu, 2005).
Ploidy, genome size and karyotype asymmetry
The average negative correlation between the percentage of polyploid species and genome size found in almost all investigated taxa (Fig. 8) agrees with many other published studies for other groups of angiosperms (e.g. D'Ovidio and Marchi, 1990; Levin, 2002) and across angiosperms as a whole (Leitch and Bennett, 2004). The occurrence of polyploidy was also found to be related to genome size (Fig. 7). Thus genera with mean 1Cx values up to 25 pg showed a wide range of polyploidy from 0 to 80 % depending on the genus, whereas the occurrence of polyploidy in genera with mean 1Cx values above 25 pg was low (0·8 % in Lilium and 3 % in Fritillaria) or non-existent (in Notholirion and Cardiocrinum). These results agree broadly with those previously reported by Grif (2000) based on an analysis at family level, namely that the percentage of polyploids in a family decreased with increasing mean genome size for the family. It is noted that out of the 11 monocot families analysed by Grif, Liliaceae had the largest mean genome size (1C = approx. 20 pg) and the lowest percentage of polyploids (20 %).
Trends and patterns of karyotype evolution in Liliaceae
According to the present study (and also Leitch et al., 2007, concerning genome size evolution), ancestral karyotypes in Liliaceae are likely to have had small genomes (1Cx = approx. 6 pg), low CVCI values, relatively high CVCL values (similar to Smilax) and x = 8. From this evolutionary starting point, different trends in karyotype evolution at the generic level are apparent.
Streptopus, Scoliopus and Prosartes. In the small clade comprising Streptopus, Scoliopus and Prosartes (15 species in total), although there was some variation in chromosome number (in Prosartes; 2n = 12, 16 and 18) and ploidy (Streptopus; up to 6x based on x = 8), the karyotypes are largely similar to those in the outgroup Smilacaceae in terms of structure (i.e. range of CVCL and CVCI) and genome size, with the notable exception of the >2-fold increase in genome size in Scoliopus. Given that only one species of Scoliopus (out of two recognized) was analysed, the mode of DNA addition is difficult to determine.
Tricyrtis. In Tricyrtis the karyotype has maintained similar karyotypic features to those in Smilacaceae, Streptopus and Prosartes (small and narrow range of genome sizes and a karyotype that is not strongly asymmetric). The main difference in Tricyrtis was the increase in the basic chromosome number from x = 8 to x = 13 which may have arisen via an ancient palaeopolyploid event followed by loss of DNA. The predominant chromosome number for Tricyrtis is 2n = 26 although counts of 2n = 24 have been reported in T. hirta, possibly linked to Robertsonian translocations (Takahashi, 1991).
Calochortus. Karyotypically, Calochortus (comprising approx. 65 species) is more variable than the genera mentioned above, with considerable variation in basic chromosome number (x = 6, 7, 8, 9 and 10), genome size (inferred 1Cx values range 8·5-fold) and asymmetry (especially CVCI, Fig. 5C) compared with the presumed ancestral state in, for example, Streptopus and Smilax. The mechanisms involved in generating this karyotype diversity are currently unknown, although a role for translocations, fusions and fissions has been proposed (Beal, 1939). (For a more detailed discussion of chromosome diversity and evolution in the genus see Patterson and Givnish, 2004.)
Lilioideae + Medeoloideae. The Lilioideae + Medeoloideae clade is the most diverse of Liliaceae. This clade has experienced large increases in genome size (2- to 25-fold), and the two types of karyotype asymmetry (i.e. intra- and interchromosomal, reflected in the values for CVCI and CVCL, respectively) have contrasting influences on karyotype evolution, depending on the taxonomic group concerned.
Subfamily Medeoloideae The most plesiomorphic karyotype in the Lilioideae + Medeoloideae clade is probably found in Medeoloideae which, apart from an increase in genome size (2– to 3-fold) and a reduction in the basic chromosome number from x = 8 to x = 7, has maintained low karyotype asymmetry features with a karyotype consisting of seven large, more or less metacentric chromosome pairs. Of the five species of Clintonia, only one is diploid (C. udenesis, 2n = 2x = 14). The remaining four are tetraploid, making this the genus with the highest percentage of polyploids in Liliaceae. Medeola is monotypic (M. virginiana is the sole species) and has 2n = 14 chromosomes.
Subfamily Lilioideae. In this subfamily the basic chromosome number increased to x = 12. It has been suggested that this arose through multiple reciprocal centric fissions (Tamura, 1995) probably involving the five smaller chromosome pairs of a Medeoleae-like ancestor or, less probably, through polyploidy. The majority of species in this subfamily have retained a base number of x = 12, with just a few exceptions in some Fritillaria (e.g. F. montana and F. ruthenica with 2n = 18) and Gagea species. However, whereas polyploidy is fairly common in Tulipeae (40·7 %, according to the present data set), it is rare in Lilieae (1·54 %).
Tribe Lilieae. In this tribe the karyotype evolved towards a further increase of intrachromosomal asymmetry (up to 3-fold increase in CVCI, Fig. 5A) and genome size (up to 7-fold in some Fritillaria and Lilium species), mostly through unequal addition of DNA to the long arms of the ten smaller telocentric pairs (III–XII; with Fritillaria being an exception). As a consequence of this unequal addition of DNA, this mode of karyotype evolution was accompanied by a small reduction in interchromosomal asymmetry (0·5– to 0·7-fold, Fig. 5A compared with 5C).
Tribe Tulipeae. In contrast to the sister tribe Lilieae, the main mechanism of chromosome evolution in Tulipeae was shown to be an equal change in the amount of DNA for each chromosome arm, regardless of its length, although there was some evidence of preferential addition or subtraction of DNA from the smaller chromosomes. Consequently, the two largest chromosome pairs are telocentric/sub-telocentric rather than typically metacentric (as in Lilieae), and these changes are accompanied by variations in interchromosomal asymmetry (i.e. CVCL, Fig. 5B). Within this framework, two distinct pathways of karyotype evolution are apparent: (1) a massive reduction in genome size (up to 0·3- to 0·5-fold) in Gagea accompanied by an increase in interchromosomal asymmetry (CVCL up to 2- to 3-fold), leaving the intrachromosomal asymmetry (CVCI) almost unchanged; and (2) an increase in genome size in Amana, Erythronium and Tulipa through the addition of equal amounts of DNA to each chromosome regardless of length, leading to a reduction in both their inter- and intrachromosomal asymmetries (i.e. CVCL and CVCI) with respect to Gagea (Fig. 5B).
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CONCLUSIONS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSSUPPLEMENTARY DATAACKNOWLEDGEMENTSLITERATURE CITED |
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In summary, through this combined approach of collating all available information (karyomorphometric data, genome size, phylogeny) for species of Liliaceae it has been possible to reconstruct the most likely patterns of chromosome evolution in this family. Such an approach has highlighted the diverse modes of karyotype evolution to be found even within this comparatively small angiosperm family.
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SUPPLEMENTARY DATA |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSSUPPLEMENTARY DATAACKNOWLEDGEMENTSLITERATURE CITED |
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Supplementary Data are available at Annals of Botany online and consist of (1) karyotype features in the studied literature accessions of Liliaceae and Smilacaceae; and (2) Pearson's correlation coefficients among all published modalities of karyotype asymmetry measurements and genome size.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSSUPPLEMENTARY DATAACKNOWLEDGEMENTSLITERATURE CITED |
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The authors wish to thank Professor F. Garbari, Professor R. Cremonini (University of Pisa) and Professor C. G. Vosa (Oxford University) for discussions about the work, comments and suggestions, and two anonymous reviewers who greatly improved an earlier version of the manuscript. Financial funding (EX60%) from the University of Pisa is gratefully acknowledged.
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSSUPPLEMENTARY DATAACKNOWLEDGEMENTSLITERATURE CITED |
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