AOBPreview originally published online on May 19, 2005
Annals of Botany 2005 96(2):229-244; doi:10.1093/aob/mci170
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First Nuclear DNA Amounts in more than 300 Angiosperms
1 Institute of Molecular Plant Sciences, Leiden University, Leiden, The Netherlands and 2 Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AB, UK
* For correspondence. E-mail m.bennett{at}kew.org
Received: 3 February 2005 Returned for revision: 30 March 2005 Accepted: 10 April 2005 Published electronically: 19 May 2005
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONAPPENDIXLITERATURE CITED |
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• Background and Aims Genome size (DNA C-value) data are key biodiversity characters of fundamental significance used in a wide variety of biological fields. Since 1976, Bennett and colleagues have made scattered published and unpublished genome size data more widely accessible by assembling them into user-friendly compilations. Initially these were published as hard copy lists, but since 1997 they have also been made available electronically (see the Plant DNA C-values database www.kew.org/cval/homepage.html). Nevertheless, at the Second Plant Genome Size Meeting in 2003, Bennett noted that as many as 1000 DNA C-value estimates were still unpublished and hence unavailable. Scientists were strongly encouraged to communicate such unpublished data. The present work combines the databasing experience of the Kew-based authors with the unpublished C-values produced by Zonneveld to make a large body of valuable genome size data available to the scientific community.
• Methods C-values for angiosperm species, selected primarily for their horticultural interest, were estimated by flow cytometry using the fluorochrome propidium iodide. The data were compiled into a table whose form is similar to previously published lists of DNA amounts by Bennett and colleagues.
• Key Results and Conclusions The present work contains C-values for 411 taxa including first values for 308 species not listed previously by Bennett and colleagues. Based on a recent estimate of the global published output of angiosperm DNA C-value data (i.e. 200 first C-value estimates per annum) the present work equals 1·5 years of average global published output; and constitutes over 12 % of the latest 5-year global target set by the Second Plant Genome Size Workshop (see www.kew.org/cval/workshopreport.html). Hopefully, the present example will encourage others to unveil further valuable data which otherwise may lie forever unpublished and unavailable for comparative analyses.
Key words: Genome size, C-value, plant DNA C-values database, Genome Size Initiative (GSI), Plant Genome Size workshop and Discussion Meeting, angiosperm, monocots
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONAPPENDIXLITERATURE CITED |
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The DNA amount in the unreplicated gametic nuclear chromosome complement (1C-value) is highly characteristic for taxa and varies over 1000-fold between plant species. Species' DNA amounts [C-value and genome size (1Cx)] are key diversity characters of fundamental significance with many important uses (Bennett and Leitch, 2005a
). However, it is often difficult to know if a genome size measurement exists for a taxon, or where to find it, as such values are widely scattered in the literature or unpublished. Consequently, since 1976, lists of DNA amounts in angiosperm species, compiled for reference purposes, have been published (e.g. Bennett and Smith, 1976), and the data have been pooled and released in electronic form since 1997 (e.g. the Angiosperm DNA C-values database). To extend the coverage to include other plant groups, databases for gymnosperms, pteridophytes and bryophytes were added in 2001 to create the Plant DNA C-values database (release 1·0) with C-values for 3864 land plants. In December 2004 the Plant DNA C-values database was further updated (release 3·0) and included, as a novel feature, C-values for 253 algal species. Release 3·0 has DNA amounts for almost 5000 species from over 500 original sources, including first values for 628 angiosperms not previously included (http://www.kew.org/genomesize/homepage). These lists and databases have been widely used for comparative studies (e.g. Knight et al., 2005; Leitch et al., 2005; Price et al., 2005) and are the main source of information on plant genome sizes cited in the literature. Published lists of angiosperm DNA amounts have been cited over 1500 times, whilst the electronic database has received over 60 000 hits since 2001.
Bennett et al. (2000) and Bennett and Leitch (2005a) noted that C-values for probably a surprisingly large number of plant species had been estimated but, for various reasons, not published and hence were unavailable. Indeed, this was suspected to apply to hundreds of species overall whose genome sizes together constitute an untapped pool of information of considerable potential value. Scientists have therefore been encouraged to communicate them for inclusion in the Plant DNA C-values database, thus making them accessible for comparative studies. The present work is proof of this hypothesis and provides a model example of collaboration to transfer a large body of previously invisible plant genome size data firmly into the public domain.
Two of the present authors have worked together for the past decade to produce pooled lists of plant DNA C-values for reference purposes in both hard copy (Bennett and Leitch, 1995, 1997, 2005a; Bennett et al., 2000) and electronic versions (http://www.kew.org/genomesize/homepage). Meanwhile the present first author has made genome size estimates for angiosperm taxa in several genera, including Helleborus (Zonneveld, 2001), Hosta (Zonneveld and Van Iren, 2000, 2001), Galanthus (Zonneveld et al., 2003) and Agapanthus (Zonneveld and Duncan, 2003), some of which have subsequently been included in a recent compilation by Bennett and Leitch (2005a). While corresponding with Bennett and Leitch about these data and planned future publications, Zonneveld noted that he had also made C-value estimates for taxa in various genera that seemed most unlikely to be published. It emerged that this sample was substantial and included first estimates for hundreds of miscellaneous species, measured mostly out of curiosity.
Given their potential value, it was decided to combine the taxonomic and databasing experience of the Kew-based authors with information amassed in The Netherlands to produce a further reference list in a form similar to other recent plant C-value reference lists (e.g. Bennett and Leitch, 2005a; Kapraun, 2005). The present work is the product of that collaboration. Analysis of the completed Appendix table shows that it contains C-values for 411 angiosperm taxa, including first values for 308 species not listed in any previous compilation by Bennett and colleagues.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONAPPENDIXLITERATURE CITED |
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Plant materials
The present work examined angiosperm taxa available as seed or plants growing in The Netherlands selected primarily for their horticultural interest. The Netherlands has a long tradition of growing and breeding many angiosperm taxa for horticulture, consequently such plant materials are readily available for research purposes.
Estimation of DNA C-values
DNA 2C-values were estimated using flow cytometry with the fluorochrome propidium iodide (PI) as described by Zonneveld and Van Iren (2001). Briefly, somatic nuclei were isolated from leaves by co-chopping them with one of the internal calibration standards (Table 1) in nuclei isolation buffer. After adding 2 mL PI solution (50 mg PI/l in half-strength isolation buffer) the suspension was filtered. Nuclei fluorescence was measured 30 min after the addition of PI using a Partec CA-II flow cytometer. In most cases, several samples, each with at least 5000 nuclei, were measured. The 2C-value of the sample was calculated as follows: (mean of sample peak ÷ mean of standard peak) x 2C DNA amount (pg) of the standard species (see Table 1). Other peaks corresponding to higher C-values (i.e. 4C, 8C and 16C, etc.) were sometimes observed but their DNA amounts were not calculated.
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Internal calibration standards
Five calibration standards, differing in DNA amount, were used (Table 1). In most cases Agave americana was chosen, as previous work showed it to be a reliable and reproducible standard, giving clean peaks with low CVs (Zonneveld and Van Iren, 2001
). If nuclear DNA content of a test species overlapped with that of A. americana, another calibration standard was used whose C-value fell close to that of the unknown. Species with 2C-values below 2·0 pg could usually not be measured with the Partec CA-II flow cytometer available for use, as the peaks tended to be lost in the debris fluorescence. |
RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONAPPENDIXLITERATURE CITED |
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Comparison of C-value data in the Appendix table with those previously reported
To assess the quality of C-value data in the Appendix two comparisons were made.
(1) C-values for 103 species in the Appendix were compared with ‘prime’ (see note (a) in ‘Notes on compiling the Appendix’) C-values for the same species listed in the Plant DNA C-values database (Bennett and Leitch, 2004). Figure 1A shows that generally the two data sets were in good agreement (R2 = 0·9068). However, there were 18 species where previously published ‘prime’ C-values differed by >30 % from those given in the Appendix. These species are represented by open circles in Fig. 1A. The cause(s) of the discrepancies was not clear but possibilities include taxonomic errors or genuine intraspecific variation. For six of the species the different C-values reported were multiples of previous estimates, suggesting that polyploidy may be responsible. Nevertheless, as no chromosome counts were made for any species in the Appendix (except Hydrangea macrophylla), the role of polyploidy is unconfirmed.
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(2) A comparison was made between the C-values for seven species in the Appendix and the C-values for these calibration standards given in Bennett and Smith (1991)
. These two datasets showed very close agreement (Fig. 1B) (R2 = 0·9965). Overall, it was concluded that the Appendix C-value data are of high quality.
Representation of C-value data in Appendix
The present Appendix gives C-values for 411 species, of which 308 (75 %) are for species not included in any previous compilation by Bennett and colleagues (Bennett and Smith, 1976, 1991; Bennett et al., 1982, 2000; Bennett and Leitch, 1995, 1997, 2005a) or listed in the Plant DNA C-values database (release 3·0, December 2004). Bennett and Leitch (2005a) analysed the global output of DNA C-values for angiosperms during the past half century. They concluded that the 1997 Angiosperm Genome Size Workshop had stimulated a large increase from an average of about 100 per annum in the early 1990s to almost 200 per annum for 1998–2002. The total number of first C-values for species in the present work therefore equals 1·5 years of average global published output at the record levels achieved in recent years. By any measure, it is a significant contribution to knowledge of this important character. Indeed the present data sample (all from one source) increases the total sample of angiosperm species with genome size estimates by about 7·4 %. Moreover, it constitutes over 12 % of the global target set by the Second Plant Genome Size Workshop (namely to estimate first DNA C-values for about 2500 angiosperm species within a quinquennium; see http://www.rbgkew.org.uk/cval/workshopreport.html). Clearly, one worker can still make a significant contribution to the global pool of information on genome sizes. Failing to make such information visible could seriously impair the scope of the available database and limit the scope of comparative studies.
Table 2 shows how many of the C-values in the Appendix are first values at the species, generic and family level for the three major angiosperm groups (i.e. basal angiosperms, monocots and eudicots). Although monocots constitute only approx. 20 % of all angiosperm species, most of the new C-values in the Appendix are for monocots (i.e. 64 and 65 % of first C-values are for monocot species and genera, respectively).
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Nevertheless, while the present data make a significant contribution to knowledge of C-values at the species level, there has been no significant improvement in representation at the family level. The 1997 Angiosperm Genome Size Workshop recommended a goal of complete familial representation by 2002, as a first C-value was available for only about 30 % of families. Bennett et al. (2000)
noted that in a sixth supplementary list of C-values for 691 species only 12 were also first estimates for families. Later they concluded that significant progress to improve familial representation of angiosperm families was unlikely without careful targeting and the present data for a large sample of untargeted taxa confirm this expectation. Thus, while the Appendix includes 308 first C-values for species, only one of these is also the first value for a family (i.e. Tamaricaceae).
Also as expected, given the lack of specific targeting, the present sample does not make major contributions to filling gaps for any other groups identified as significantly under-represented in the database (e.g. for taxa from bog, fen, tundra, alpine and desert environments, or for halophytic, insectivorous, parasitic, saprophytic and endophytic species; Bennett and Leitch, 2005a). Nevertheless, the present sample does include first values for a few taxa of such interest including two parasitic species Orobanche hederae and Rhinanthus glabra (both in Orobanchaceae) with 1C values of 2·65 and 3·05 pg, respectively. The table also includes two desert species Opuntia microdasys (1C = 2·24 pg) and Rebutia albiflora (1C = 1·91 pg), both in the Cactaceae, and a number of succulents from the families Asparagaceae (Agave, Ledebouria), Bromeliaceae (Tillandsia), Crassulaceae (Aeonium, Graptopetalum, Sedum), Apocynaceae (Ceropegia, Hoodia, Hoya, Catharanthus, Stapelia), Xanthorrhoeaceae (Aloe) and Asteraceae (Senecio) in which the C-values ranged from 1·11 to 16·85 pg.
The range of C-values in the Appendix compared with existing data
Table 3 compares the minimum, maximum, mean, median, mode and range of DNA amounts for all 411 species listed in the Appendix, with the 4119 species listed in the Plant DNA C-values database (release 3·0, December 2004).
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The range of C-values in the present sample (1C = 0·6–95·5 pg) falls within that reported for the Plant DNA C-values database (1C = 0·1–127·4 pg), although it is somewhat enriched in species with larger genomes, leading to higher mean and modal values compared with the larger sample in the database (Table 3); thus the minimum C-value in the Appendix is the same as the modal value for species in the database. This probably reflects the greater proportion of monocots in the present sample with large genomes. Indeed the 43 species (approx. 10 %) with the largest genomes in the Appendix are all monocots from the orders Asparagales, Commelinales or Liliales; these groups have previously been shown to contain species with the largest recorded angiosperm genomes (Leitch et al., 1998
; Soltis et al., 2003). (NB The presence of only eight species with 2C-values <2·0 pg is, in large part, due to technical difficulties encountered in estimating C-values in species with smaller genomes, as noted in Materials and methods.) Analysis at the family level showed that in half of the 66 families already represented in the Plant DNA C-values database, the new data did not increase the range of C-values previously reported for a family. In only eight families was the minimum C-value decreased as a result of new data, whereas in 25 families the maximum C-value increased, sometimes greatly. For example, in Garryaceae and Escalloniaceae, which both previously had a C-value for just one species, the addition of an estimate for one new species increased the range of C-values for each family over 8- and 15-fold, respectively.
Future plans
Participants at the 2003 Plant Genome Size Workshop formalized their international collaboration as the Genome Size Initiative (GSI; Bennett and Leitch, 2005b), whose aims are to improve the availability, quality and understanding of genome size data, and to provide a focus for monitoring progress and facilitating discussions in a holistic genomic context. Further, in a keynote address opening the 2003 Plant Genome Size Discussion Meeting, Bennett reiterated the potential value of unpublished genome size data, and the need to make it visible as follows: ‘There are probably over 1000 prime C-value estimates for plant species, equal to 4 years of known global output, unlocated in publications or unpublished. Such genome size data are almost valueless if potential users cannot easily access and assess them. It is impossible to over-emphasise the importance of publishing C-value data or linking them to the database by informing the co-ordinators of its existence, so that others can assess its quality and use it’. The present work supports this sentiment and the aims of GSI. Hopefully, it will encourage others to emulate this example and unveil further useful data which otherwise may lie forever unpublished.
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APPENDIX |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONAPPENDIXLITERATURE CITED |
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Notes on compiling the Appendix
C-value data were compiled into the Appendix table whose form is similar to that of previous lists of DNA amounts by Bennett and colleagues (i.e. Bennett and Smith, 1976
, 1991; Bennett et al., 1982; Bennett and Leitch, 1995, 1997; Bennett et al., 2000). Additional information on compiling the Appendix is given below. (a) Assignment of entry numbers and ‘prime’ entries. The numbering of the Appendix table generally follows that for previous lists of DNA amounts (see above). Taxa are arranged alphabetically by genus and species with a new number usually being assigned for each new species.
For 42 species in the Appendix more than one estimate was made for the same species (e.g. for different cultivars, varieties, etc.). In most cases, the C-values were very similar and the different accessions were assigned the same entry number but were distinguished by letters, sorted here by increasing DNA amounts. For example, C-values are reported for two cultivars of Crocus chrysanthus, a species not included previously in any of the lists mentioned above. The smaller of the two values, for ‘Dorothy’, is listed as entry number 113a, while the larger, for ‘Blue Pearl’, is 113b. Where several estimates are available for the same species, the ‘a’ value is automatically chosen in any arithmetical or statistical calculations. In this context, a single estimate for a species and ‘a’ values are referred to as ‘prime entries’.
For 18 species the C-values between accessions differed by >10 %. Taxonomic heterogeneity, polyploidy and/or intraspecific variation are the most likely explanations (especially where a range of chromosome numbers has previously been reported for the species), yet until chromosome counts are made, the cause(s) of the differences remains unknown and the different accessions of a species were usually assigned the same entry number. In six Senecio species (S. herreianus, S. kleiniiformis, S. mweroensis, S. nyikensis, S. pendulus and S. radicans), however, the different C-values so strongly suggested the presence of polyploidy that they were given separate entry numbers in accordance with previous practice (e.g. Bennett and Leitch, 2005a).
For 103 species, where one or more C-value had previously been listed by Bennett and colleagues, the estimate in the Appendix was given a number and the next available letter in the alphabet. For example, three previous C-values have been reported for Allium ampeloprasum, thus the entry for this species in the Appendix was assigned the letter ‘d’.
(b) Taxonomic authorities. Taxonomic authorities of the species studied were taken from the International Plant Names Index (IPNI) (http://www.ipni.org/index.html). A superscript ‘b’ following a species name indicates that the taxonomic authority was unknown or unclear (i.e. more than one entry in IPNI).
(c) Family and higher order group. The family, order and higher group given for each species in Appendix columns 3, 4 and 5, respectively, follows the Angiosperm Phylogeny Group (APG) system (APG II, 2003). The following abbreviations were used: BA = basal angiosperm; M = monocot; E = eudicot.
(d) Chromosome number, ploidy and voucher information. The sentiment of the Convention on Biological Diversity (United Nations Environment Programme, 1992), which noted the need to make biodiversity data available despite imperfections, merits support. Thus, while the species listed in the Appendix generally lack a voucher and information on chromosome number and ploidy level, they can make a valuable contribution to knowledge of plant C-values.
Chromosome numbers and/or ploidy information were entered for 90 taxa where previous C-value reports also included this information and the C-values agreed closely with those reported here. For example, a C-value of 2·9 pg for Achillea filipendulina was previously estimated by Dabrowska (1992), who also reported that the accession studied had 2n = 2x = 18. As the 1C-value of 2·88 pg for the same species in the Appendix was very similar to that of Dabrowska (1992), the chromosome number and ploidy data were also entered.
(e) Life cycle types. Information on the type of life cycle for species in the Appendix was either taken from the literature or internet. The following abbreviations were used: A = annual; B = biennial; AP = annual–perennial; P = perennial. A superscript ‘e’ indicates that life cycle information was either unknown or unclear to the present authors.
(f) DNA amounts and conversion factor. 1C and 4C values listed in the Appendix were determined by appropriate calculation of the 2C-value. For 1C-values in megabase pairs (Mbp) the conversion factor of 1 pg = 980 Mb (Cavalier-Smith, 1985; Bennett et al., 2000) was used.
(g) Standard species. The abbreviation used to indicate which of the five calibration standards was used to estimate the 2C-value for each species in the Appendix is given in Table 1.
(h) Chromosome numbers in Hyacinthus. Brandham and West (1993) reported chromosome numbers in 13 Hyacinthus orientalis cultivars and noted that aneuploidy was common. Two of the cultivars studied (‘Pink Pearl’ and ‘Delft Blue’) were the same as those listed in the Appendix. Since the cultivars are clonal the chromosome numbers given in Brandham and West can be assumed to be the same as those studied here. Thus ‘Pink Pearl’ is listed as a diploid with 2n = 16, while ‘Delft Blue’ is an aneuploid tetraploid with 2n = 4x – 2 = 30. Based on similar C-values in cultivars ‘Pink Pearl’ and ‘White Pearl’ (28·4 and 27·3 pg, respectively), the latter is also entered as diploid. Further, as the DNA amounts for cultivars ‘Delft Blue’ and ‘Anna Marie’ are similar (43·4 and 42·4 pg, respectively), the latter is entered as circa tetraploid, although the exact chromosome number is unknown. The higher C-value cultivar ‘L’Innocence' (51·60 pg) suggests it is pentaploid.
(i) Sanseveria tricasciata ploidy chimeras. The leaves of Sanseveria trifasciata ‘Laurentii’ and ‘Forescate’ are ploidy chimeras (Zonneveld and Van Iren, 2000). Most plant leaves are built up from three layers, L1, L2 and L3, which develop from the apical meristem. In the variegated S. trifasciata ‘Laurentii’ the yellow leaf edge corresponds to cells derived from L1 and the green cells in the leaf centre from L3. Between L1 and L3 is a single layer of cells which comprise L2, from which the floral meristem and hence the gametes will arise. Measurements of 2C values from leaf tissue taken from the yellow edge gave a 2C value of 5·2 pg whereas nuclei isolated from the green central tissue (L3) were 2C = 2·6 pg. As it was difficult to be sure of obtaining cells from L2, the 1C value of the gametes is unclear. Thus this value has been omitted from the Appendix, and just the 2C and 4C values from the layer with the lowest DNA amount (i.e. from L3) are entered. In S. trifasciata ‘Forescate’ cells in the green central tissue had a 2C value of 7·8 pg (L3) whereas those at the yellow edge (L1) were 2C=5·2 pg. Again, the 1C value was omitted and just the 2C and 4C values for the layer with the lowest DNA amount (i.e. from L1) were entered.
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