Heredity 59 (1987) 119—128 The Genetical Society of Great Britain Received 13 October 1986

Nuclear DNA variation in the genus L. (Liliaceae)

R. M. Labani and Departmentof Botany, The University, Sheffield 1. T. Elkington Sb 2TN, U.K. 4C nuclear DNA contents were determined for 42 A ilium species, selected from all major taxonomic sections in the genus. Estimates of nuclear volumes were also made. A range of 4C DNA values from 41•19 pg to 14278 pg was found, largely unrelated to basic chromosome number, polyploidy or taxonomic group, but correlated with flowering time. The results are discussed in relation to distribution of DNA values in the genus, proportions of chromosome C-banding, breeding systems and climatic adaptation.

INTRODUCTION difficult to comment adequately on any possible quantitative relationships between species, with The genus Allium has been studied cytologically taxonomic groupings or indeed on other aspects over many years, commencing with the studies of of the genus' biology. We have therefore, as part Levan(1931, 1932, 1933, 1935, 1936). The c. 400 of a larger study on variation of the genus Allium, perennial species encompass considerable determined nuclear DNA values for 42 species- morphologicalvariation and have been divided chosen to include representatives of all the major into a number of subgenera and sections (see morphological groups in the genus. Vvedenskii, 1935; Steam, 1978, 1980; Wendelbo, 1969, 1971) distributed, mainly in temperate regions of , North Africa, Asia and North MATERIALS AND METHODS America, and with outlying species in Ceylon and South Africa (Steam, 1978). The genus includes Materials series of basic chromosome numbers from x =7 Roots were obtained from seedlings or bulbs to x =10and a number of polyploids. Previous obtained from a variety of sources (table 1). Iden- determinations of nuclear DNA in Allium species tifications of the majority of accessions were have been made by several authors (see table 3). checked by reference to appropriate keys and In common with a range of other Angiosperm reference material in the British Museum (Natural genera (see Bennett and Smith, 1976; Bennett, History). Seeds of A. cepa var. Ailsa Craig were Smith and Heslop-Harrison, 1982) these results grown on filter paper at the same time and used indicate that there is substantial interspecific vari- as a standard. ation in DNA amounts within Allium, but they only cover a total of 32 taxa in the genus. On the basis of the results of Jones and Rees (1968) for Methods 25 taxa Narayan (1983) has suggested that, in Roottips were collected from the samples and A. common with several other genera viz Clarkia, cepa at the same time, fixed directly in 3: 1 alcohol Nicotiana and Lathyrus, the nuclear DNA amounts acetic acid and stored overnight. Fixed root tips of Allium species are dicontinuously distributed, were washed in distilled water and hydrolysed in speciesforming groups in this respect, between iN HC1 at 60°C for 10 minutes; they were then which there are regular increases in DNA amounts. stained in leuco-basic fuchsin for 2 hours at room The small sample of species in Alliumforwhich temperature, washed in running tap water and DNA determinations are so far available make it placed in distilled water. Squash preparations were 120 R. M. LABANI AND T. T. ELKINGTON

Table 1Origins of Allium species used with initial flowering time and self compatibility type

Initial month of Compatibility Subgenera and Sections Taxon flowering type* Source

Subgenus Rhizirideum Section Rhizirideum A. cernuurn Roth. June Royal Horticultural Society (RHS) Gardens, Wisley, UK A.angulosumL. August C Botanical Garden, Vacratot, Hungary A. harsczewskii Lipsky August RHS Gardens, Wisley UK A. Jarreri Steam May c RHS Gardens, Wisley, UK. (ex Iran) A. rnairei H. Lev. August C Amsterdam, Free University Botanical Garden, Holland A. ochroleucum W. et Kit. August Copenhagen Botanical Garden, Denmark A. obliquurn L. July c Botanical Garden, Goteborg, A. saxatile Bieb. July c Botanical Garden, Goteborg, Sweden Section Schoenoprasum A. schoenoprasumL. July c University of Louis Pasteur, Strasbourg, France A.lineare L. June C Botanical Garden, Karl Marx University, E. Germany Section Cepa A. cepa L. cv. Ailsa Craig June c Suttons Seeds Ltd A. altaicurn Pall. July Botanical Garden, Sheffield University, UK A. fistulosum L. July C RHS Garden, Wisley, UK A. galanthurn Kar. and Kir. August C Botanical Garden, Sheffield University, UK A. pskernense B. Fedtsch. July R. Dadd A. roylei Steam July R.Dadd Section Anguinum A. victorialis L. July Botanical Garden, Sheffield University, UK Subgenus Allium Section Molium A. geyeri Wats. June Royal Botanic Garden, Kew, UK A. moly L. June Van Tubergen, Holland A. oreophilum C. A. Meyer June C Van Tubergen, Holland A. scorzonerifolium Desf. exJune R. Dadd DC. A. trifoliatum Cyr May R. Dadd A. wallichii Kunth. May R. Dadd Section Briseis A. triquetrum L. May C Van Tubergen, Holland Section Ophioscorodon A. ursinum L. April Grindleford, Derbyshire, UK Section Scorodon A. parciflorum Viv. July Botanical Garden, Sheffield University, UK Section Codonoprasum A. flavurn L. July c Botanical Garden, Copenhagen, Denmark A. carinaturn sub.sp. July C Botanical Garden, Copenhagen, puichellurn Bonnier and Denmark Layens A. car,naturn L. subsp. July c Botanical Garden, Copenhagen, carina turn Denmark A. oleraceum L. July Botanical Garden, Copenhagen, Denmark Section Allium A. heldreichii Boiss. May Royal Botanic Garden, Kew, UK A. sphaerocephalon L. August Botanical Garden, Copenhagen, Denmark A. ampeloprasurnL. August Royal Botanic Garden, Kew, UK A.porrurn L. cv. June Suttons Seeds Ltd Musselburgh Subgenus Melanocrommyum Section Melanocrommyum A. atropurpureurn Waldst. and June c Van Tubergen, Holland Kit. A. aflatunense B. Fedtsch. May Van Tubergen, Holland A. cristophii Trautv. June c Van Tubergen, Holland A. giganteurn Rgl. July Van Tubergen, Holland DNA VARIATION IN ALLIUM 121

TableI continued

Initial month of Compatibility Subgenera and Sections Taxon flowering type* Source

A. mac!eanii Baker June — Van Tubergen, Holland A. stipitatum Rgl. June i Van Tubergen, Holland A. karataviense RgI. July i Van Tubergen, Holland A. rosenbachianum Rgl. June i Van Tubergen, Holland A. schubertii Zuec. June c Van Tubergen, Holland

* c, selfcompatible; i, incompatible (Data from Al-Sheikh Hussain, 1977; Badr, 1977; El-Gadi, 1976; EI-Maghbub, 1982; Labani, 1984). made in a drop of distilled water and made per- Allium species for which determinations were mnent by freezing in liquid carbon dioxide and made. Each DNA value represents a single sample mounting in Euparal. Measurements of DNA were of the species; a comparison with other published made within two days using a Vickers M86 scan- values (mostly also listed in Bennett and Smith fling microdensitometer at Amax(approximately 1976; Bennett, Smith and Heslop-Harrison, 1982) 570 nm). Nuclei in early or mid-prophase (4C) is given in table 3. Some of the results show some were selected for scanning. Two readings of similarity to previously published values but gen- absorption were made on each nucleus and the erally lie outside their 95 per cent confidence limits background. (table 3). Only in A. porrum is a previously pub- From these figures the nuclear DNA amounts lished figure (1170pg; Murin 1976) near to the for each sample was calculated using the formula: 95 per cent confidence limit. The other previously published figure for this species (48.2 pg; Ran- 4C nuclear DNA =xC jekar, Pallota and Lafontaine (1978)), is very dis- where A = crepant. The high correlation between the nuclear 4Cnuclear DNA value of A. cepa var. DNA content and nuclear volume (fig. 3) deter- Ailsa Craig i.e., 7600 pg from the determinations of Van't Hof (1965) and Bennet and Smith (1976). mined in the present investigation supports B =mean strongly the value recorded here. It is therefore absorption figure measured for the A. difficult to explain the difference unless Ranjekar cepa sample. C =meanof the absorption figures et aL (1978) were wrong in their DNA determina- measured for the sample nucleus minus those of tion or species identification. In A. schoenoprasum the background readings. DNA values reported are means and standard our value is almost double that recorded by Jones errors of 10 nuclei per root tip for each of three and Rees (1968) for the diploid A. sibiricum which root tips taken from a different seedling or bulb. Steam (1978) includes within A. schoenoprasum. The errors inherent in microdensitometry are dis- In addition to the species listed in table 3 a 4C cussed in detail by Bennett and Smith (1976) and DNA value of 1516 pg is given for A. globosum D. J. Goldstein (1981). Bieb. by Jones and Rees (1968); this value, the Photographs were taken of interphase nuclei highest to be recorded in the genus, should be compared with the value of 4459 pg for A. saxatile from each Allium species, using a Zeiss Ultraphot determined here, since Steam (1978) has shown microscope with phase contrast optics. Prints were made at a final magnification of x3500. Nuclear A. globosum to be included within A. saxatile. volumes were determined using a Graphics tablet Jones (personal communication) has stated that independent identifications of grown by and Apple 11 micro-computer together with a pro- Jones and Rees (1968) were not made, so this and gram for computing volumes from readings of some other values given by them may not be nuclear circumference; this assumed nuclei to be attributable to listed species. spherical, following Sparrow and Nauman (1974). Distributionof nuclear DNA values RESULTS AND DISCUSSION Narayan(1983) has proposed that in Allium, as in Nuclear DNA values several other genera, the distribution of DNA The results (table 2) show that there is considerable amounts between species is discontinuous with variation in 4C nuclear DNA contents in the 42 species group 2C DNA means at intervals of Table 2 Chromosomenumber, polyploid level, 4C nuclear DNA value±S.E., (n =30) 4C DNA amounts pergenome and chromosome, mean chromosomelength±S.E. and mean nuclear volume for all species studied

Mean 4C DNA 4C DNA chromosome Nuclear Chromosome Polyploid value (pg) genome 4C DNA! length volume Subgenera and Sections Taxon number level (pg) chromosome (m3)

Subgenus Rhizirideum Section Rhizirideum A. cernuum 14 2x 9124±091 4562 652 1322±053 142684 A. angulosum 16 2x 6454±053 3227 403 751 109212 A. barsczewski 16 2x 7178±157 3589 449 N/A 146322 A. farreri 16 2x 12071±147 6036 754 1115±091 168780 A. mairei 16 2x 6947±094 3474 434 780±028 101180 A. ochroleucum 16 2x 7282 3641 455 691±017 119630 A. obliquum 16 2x 4119±028 2060 257 600±015 75942 A. saxatile 16 2x 4459±065 2230 279 673±033 77136 Section Schoenoprasum A. schoenoprasum 32 4x 6066±055 1516 190 538±012 107984 .4. lineare 48 6x 10274±093 1712 214 480±013 172224 Section Cepa A. a!taicunl 16 2x 5421 2710 339 N/A 121162 A. fistulosurn 16 2x 5620±060 2810 351 873±038 74099 A. galanthurn 16 2x 6953±073 3476 435 898±056 125618 A. pskemense 16 2x 7481±052 3741 468 N/A 123667 A. roylei 16 2x 7003±068 3502 438 N/A 117898 Section Anguinum A. victorialis 16 2x 8642±141 4321 540 1295±031 137928 Subgenus Allium Section Molium A. geyeri 14 2x 10814±064 5407 772 N/A 152290 A. moly 14 2x 10198±085 5099 728 1228±043 178144 A. oreophilum 14 2x 7236±065 3618 517 1026±014 141990 A. scorzonerfo1ium 14 2x 8726±113 43.63 623 12.00±037 123386 A. tr4foliatum 21 3x 7385±148 2462 352 855±043 121922 A. wallichit 28 4x 11913±096 2978 426 N/A 192102 Section Briseis A. triquetrum 18 2x 8915±094 4458 495 866±055 134668 Section Ophioscorodon A. ursinum 14 2x 14278± 101 7139 1020 2465±063 222628 Section Scorodon A. parciflorum 16 2x 9159±078 4580 572 1201±041 149608 Section Codonoprasum A.flavum 16 2x 8490±218 4245 531 703±016 130920 A. carinatum subsp. pulchellum 16 2x 7060±100 3530 441 840±030 111216 A. carinatum subsp carinatum 24 3 x 10056±155 3352 419 930±020 152070 A. oleraceum 40 5x 10556±112 21i1 264 792±017 148774 Section Allium A. heldreichii 16 2x 8867±126 4434 554 930±023 147940 A. .sphaerocephalon 16 2x 4965±086 2483 310 846±023 114858 A. ampeloprasum 32 4x 11964±116 2991 374 893±025 164162 A. porrum 32 4x 12115± 196 3029 379 1023±035 164324 Subgenus Melanocrommyum Section Melanocrommyum A. atropurpureum 16 2x 11366±133 5683 710 1256±039 169308 A. aflatunense 16 2x 12459±101 6229 779 1107±027 178444 A. cristophii 16 2x 9641±090 4820 603 1264±035 139198 A. giganteum 16 2x 8239±124 4120 5•15 1131±032 135832 A. macleanii 16 2x 11738±068 5869 734 1048±032 166594 A. stipitatum 16 2x 10912±194 5456 682 1062±028 149080 A. karataviense 18 2x 9618±107 4809 5•34 982±044 156749 A. rosenbachianum 16 2x 11584±132 5792 724 1065±027 164196 A. schubertii 16 2x 11165±096 5583 698 1671±046 154220

* Data from Al-Sheikh Hussain, 1977; Badr, 1977; El-Gadi, 1976; EI-Maghbub, 1982; Labani, 1984 and S. White (personal communication) 124 R. M. LABANI AND T. T. ELKINGTON

Table3 Comparison between A/humnuclearDNA values determined and their 95%confidencelimits and other published values

Chromosome4CDNA valueConfidence Taxon number (2n)determined (pg)limits Published 4C DNA values (pg)

A. eernuum 14 9124 8945—9303 664 (Jones and Rees, 1968) A. angulosum 36, 32 6454 (2n =16)6350—6558 824 (2n= 32;Jones and Rees, 1968) A. .cchoenoprasum 16, 32 6066 (2n =32)5957-6174 304 (2n= 16;A.sibiricum; Jonesand Rees, 1968) 312 (2n16;Ranjekar eta!.,1978) 338 (2n =16;Jones and Rees, 1968) A. fistulosum 16 5620 5502—5738 501 (Van't 1-lof, 1965) 526 (Jones and Rees, 1968) A. galanthum 16 6953 68 10.-7096 488 (Jones and Rees, 1968) A. mo!y 14 10198 10031—10364 904 (Ranjekar ci a!., 1978) A. oreophi!um 14 7236 7110—7363 892 (A. ostrowskianum; Ranjekar ci a!.,1978) A. triquet rum 18 8915 8731—9099 726 (Jones and Rees, 1968) A. carinatum suhsp. carinatum 16, 24 10056 (2n =24)9753—10360 448 (2n —16;Bösen and Nag!, 1978) 653 (2n =24;Nag! and Fusenig, 1979) A. porrurn 32 12115 11731—12499 482 (Ranjekar eta!.,1978) 1170(Murin, 1976) A. karataviense 96!8 9408-9829 908 (Jones and Rees, 1968)

425 pg. Sincehis data were restricted to 25 taxa DNA contents in relation to basic chromosome studied by Jones and Rees (1968) it was thought number, polyploid levels and genomes worthwhile to plot the distributions of the 75 DNA values available for the genus (see table 2; Bennett Thespecies sampled vary in ploidy level from 2 and Smith 1976; Ranjekar et a!. 1978; Bennett, to 6x and have basic chromosome members of Smith and Heslop-Harrison, 1982). Figure 1 plots n =7,8 and 9 (table 2). The 4C nuclear content the distribution as DNA 4C values and shows that per nucleus ranges from 4119 pg in A. obliquum although some discontinuities exist, there are no (2n =16)to 14278 pg in A. ursinum (2n =14) regular groups with means separated at 85 pg and showing that there are significant differences in alternating discontinuities. Comparison of the nuclear DNA content, amounting to a 4 fold vari- values of Jones and Rees (1968) with subsequent ation, which are unrelated to ploidy level. Also determinations (fig. 1) shows that the apparent there is no correlation between variation in basic discontinuities recognised by Narayan (1983) are number and DNA content; an analysis of variance the result of inadequate sampling in this large of mean 4C DNA amounts of the species studied, genus. It is possible that some of the discontinuous grouped by base number (x =7,8 species; x =8, DNA distributions suggested for other genera 32 species; x =9,2 species) shows that there is no (Rees and Narayan, 1981; Narayan, 1982, 1983) significant variation (Table 4). These findings may also result from a similar sampling error, confirm those of Jones and Rees (1968). particularly in Lathyrus where determinations of 4C nuclear DNA values per genome have been only 24 North temperate species are available from calculated (table 2) and show a wide variation a world total of 130 species (Willis, 1966). between species. In the closely related A. carinatum

Species samples 4

i rI n in niiiiin nil 1d] n m u nnIhu ii n 30 40 50 60 70 80 90 100 110 120 130 140 150 4C DNA/nucleus(pg.)

Figure 1 Histogram showing distribution of all Al//urnnuclearDNA values determined, published figures recalculated as 4C values where necessary; those of Jones and Rees (1968), as used by Narayan (1983) are shaded. DNA VARIATION IN ALLIUM 125

subsp. carinaturn (4C DNA/genome 33.52 pg)and (table 2). These results show that there is a sig- subsp. puichellum (4C DNA/genome 3530 pg) the nificant variation in nuclear volume between the similar DNA amounts/genome suggest that A. A/hum species studied, with a range of 7410 p.m3 carinatum subsp. carina turn is an autopolyploid for A. fistulosum (2n =16)to 22263 p.m3 for A. based on A. carinatum subsp. puichellurn; this has ursinurn (2n =14);there is a close association (cor- previously been proposed on cytological grounds relation coefficient 0814; p

Meanchromosome length (m) 25 -f

20-

15- + + +4. * ++ + * +4- 10 + ++ + 1- + +*+ + + -4- 5 4.

0 2 4 8 10 4C DNA/chromosome (pg.) Figure 2 Relation of mean 4C DNA values per chromosome for all Allium species studied and the mean chromosome lengths, obtained from mitotic metaphase root tip cells, pretreated with 005% colchicine for 4 hours and stained with leuco-basic fuchsin. 126 R. M. LABANI AND T. T ELKINGTON

Nuclear volume (im) DNA content and taxonomic groups 2200 Toinvestigate possible correlations between taxonomic groups and DNA nuclear content in 2000 Allium an analysis of variance (Table 5) was car- ried out on DNA amounts using subgenera to 1800 f partition the between section variance according + to the taxonomic classification of Steam (1978) 1600 * *4* given in table 2. The variance ratio is not significant H- showing that there is no correlation between DNA 1400 4+ + nuclear content and subgenera for this sample of + species. 1200 4- ++ -4- Table 5 Analysis of variance of mean sectional 4C DNA 1000 amounts partitioned by subgenera, according to the taxonomic classifications of Steam (1978) (see table 2) 800 ++ + AND VA source df S.S. MS. F

20 40 60 80 100 120 laO i0 Subgenus 2 12945 6472 3649 (P>005) 4C DNA/nucleus (pg.) Residual 8 14191 1774

Figure 3 Relation of mean 4C DNA values per nucleus and mean nuclear volumes of interphase cells determined from 30 nuclei DNA content and breeding system Although there are no direct data on the breeding range of flowering plants including Lolium systems of the species studied, some data are avail- (Thomas, 1981), Secale (Bennett, Gustafson and able on self compatibility and incompatibility in Smith, 1977), Gibasis karwinskyana (Kenton, some species studied (table 1). Comparison of 1983) and Zea mays (Rayburn, Price, Smith and DNA values for these species shows that self- Gold, 1985). In Allium, however, there is no corre- compatible species have lower DNA amounts, (4C lation between increase in DNA nuclear content mean of 18 species, 8027 pg) than self-incompat- and proportion of C-banded material in the kary- ible species (4C mean of 10 species 9736 pg); but otype. Indeed A. ursinum with the largest DNA these differences are not significant (t-value 2003; content (7139pg 4C DNA/genome) has one of df=26; P>005). There is no evidence therefore the lowest proportions of C-banded chromosome of an association between nuclear DNA content material in the genus (04 per cent) (Labani, 1984), and breeding system in Allium species. Differences while Allium species with the highest proportions, in nuclear DNA content related to breeding system in section Codonoprasum (Vosa, 1976; Al-Sheikh- have been described in several other genera, some Hussain, 1977), have 10-30 per cent of C-banded have outbreeding species with higher DNA con- material, hut only moderate DNA amounts (21 '11— tents i.e., Lathyrus (Rees and Hazarika, 1969; Rees 4245 4C DNA/genome). If therefore there is any and Jones, 1972) and Microseris (Price and Bach- relationship between nuclear DNA and repetitive mann, 1975; Price, 1976) where the differences are DNA it would appear to be unrelated to the pro- also correlated with the perennial and annual portion of C-banded heterochromatin. habits of the out- and in-breeding species respec- tively; by contrast in Lolium outbreeding species have lower nuclear DNA contents than inbreeding species (Rees et a!, 1966; Rees and Jones, 1967, Table4 Analysisof variance of species 4C DNA amounts 1972). partitioned by basic chromosome number

ANOVA DNAcontent and adaptation source df S.S. M.S. F Recentexplanations of variation in DNA content Basic number 2 11486 5743 095 (P>005) 46022 between species have often focussed on selective Residual 39 234849 mechanisms. Thus Bennett (1972) and Smith and DNA VARIATION IN ALLIUM 127

Bennett (1975) have suggested minimum gener- available on the flowering time of the Allium ation time and life cycle type as being selective species studied. The month of initial flowering factors. More recently Grime and Mowforth (1982) (table 1) plotted against DNA content is given in and Grime (1983) have suggested that the nuclear fig. 4. The correlation coefficient is highly sig- DNA content of vascular plants has been subject nificant (p

+ * e.u -4 BENNETT, M. D. 1972. Nuclear DNA content and minimum August generation time in herbaceous plants. Proc. Roy. Soc. Lond. B., 181, 109—135. BENNETT, M. 0., GUSTAFSON, J. P. AND SMITH, J. B. 1977. July ++ 4-4+*+4+++++-# Variations in nuclear DNA in the genus Secale. Chromosoma (Berl.), 61, 149-176. BENNETT, M. D. AND SMITH, .i. n. 1976. Nuclear DNA amounts in angiosperms. Phil. Trans. Roy. Soc. Lond. B., 277, 201- June +4- +**-+1.•*+** 226. BENNETT, M. D., SMITH, J, B. AND HESLOP-HARRISON, J. S. 1982. Nuclear DNA amounts in angiosperms. Proc. Roy. Soc. Lond. B., 216, 179-199. May BOSEN, H. AND NAGL, w. 1978. Short duration of the mitotic and endomitotic cell cycle in the heterochromatin-rich monocot Allium carinatum. Cell. Rio!. mt. Rep., 2, 565—571. DEUMLING, B. AND GREILHUBER,J.1982. Characterization April + of heterochromatin in different species of the Scilla sibirica group (Liliaceae) by in situ hybridization of satellite DNAs 20 40 60 80 100 120 140 160 and fluorochrome banding. Chromosoma (Berl.), 84, 535- 555. 4CDNA/nucleus (pg.) EL-GAOl,A. 1976. Studies on species relationships in Allium Figure 4 Relation of initial montb of flowering of Allium subgenus Rhizirideum (Koch) Wendelbo. Ph.D. Thesis, species, determined from established plants growing in University of Sheffield. open ground at Sheffield University Experimental Garden, EL-MAGHBUB, K. 1982. Cytology and species relationships in and mean 4C DNA values; correlation coefficient =—061 Allium subgenus Rhizirideum (Koch) Wendelbo. Ph.D. (p

FLAVEI.L, R. is. 1982.Sequence amplification, deletion and PRICE, H. J. AND BACHMANN, K. 1975.DNA content and rearrangement: major sources of variation during species evolution in the Microseridinae. Ann. J. Bot., 62, 262—267. divergence. In Dover, G. A. and Flavell, R. B. (eds.) RANJEKAR,P. K., I'AL,I.OTA, 0. AND LAFONTAINE, J. G. 1978. Genome Evolution Academic Press, London pp. 301—323. Analysis of genomes. V. Comparative study of GOLDSTEIN,D. .,. 1981.Errors in microdensitometry. His- molecular properties of DNAs of seven Allium species. tochem. J.,13, 251-267. Biochem,Genet,, 16, 957-970. GRIME,.t. p. 1983.Prediction of weed and crop response to RAYILURN,A. I..., PRICE, H. J., SMITH, J. I). AND GOLD, J. R. climate based upon measurements of nuclear DNA con- 1985.C-band heterochromatin and DNA content in Zea tent. Aspects of Applied Biology 4. Influence of environ- mays. Amer. I Dot., 72, 1610-1617. mental factors on herbicide performance and crop and RisES,H., CAMERON, F. M., HAZARIKA, M. H. ANI) JONES, G. weed biology, 87-98. ii. 1966.Nuclear variation between diploid Angiosperms. GRIME,J. P. AND MOWFORTH, M. A. 1982.Variation in genome Nature, Land., 211, 828-830. size—an ecological interpretation. Nature, Lond,, 299, 151— REE.S,H. AND HAZARIKA, H. H. 1969.Chromosome evolution 153. in Lathyrus. Chromosomes Today, 2, 158-165. Oliver and JOHN,B. AND M]KLOS, a.L,G.1979. Functional aspects of Boyd, Edinburgh. satellite DNA and heterochromatin. Ann. Rev. (ytol., 58, RUES,H. AND JONES, R. N. 1967.Chromosome evolution in 1-114. Lolium. Heredity, 22, 1—18. JONES, R. N. AND REES, H. 1968.Nuclear DNA variation in RELS,FL. AND JONES, R N. 1972.The origin of the wide species Allium. Heredity, 23, 591-605. variation in nuclear DNA content. mt. Rev. Cytol., 32, KENTON,A. 1983.Qualitative and quantitative chromosome 53-92. change in the evolution of Gihasis,InBrandham, P. E. RUES,H. ANt) NARAVAN, R. K. J. 1981.Chromosomal DNA in and Bennett, M. I). (eds.) Kew ChromosomeConference II higher plants. Phil. Trans. R. Soc. Lond. B, 292, 569-578. George Allen and Unwin, pp. 273-282. SMITH,J. B. AND BENNETI, M. 0. 1975.DNA variation in the LABANI,e..1984. Biosystematics and taxonomic relationships genus Ranunculus. Heredity, 35, 231-239. in the genus Allium L. Ph. 13. Thesis, University of Sheflield. SPARROW,A H. AND MIKSCHE, J. P. 1961.Correlation of I,EVAN,A. 1931.Cytological studies in Allium. I. A preliminary nuclear volume and DNA content with higher plant toler- note. Hereditas, 15, 347—356. ance to chronic radiation. Science, 134, 282-283. LEVAN,A. 1932.Cytological studies in Allium. II. Chromosome SPARROW,A. II. AND NAUMAN, A. F. 1974.Evolutionary morphological contribution. Hereditas, 16, 257—294. changes in genome and chromosome sizes and in DNA LEVAN,A. 1933.Cytological studies in Allium. III. Allium content in the grasses. Brookhaven Symp. Biol., 25,367-389. carinatum and A. oleraceum.Hereditas, 18,101-114. STEARN.w.1.1978.European species of Alliumandallied LEVAN,A. 1935.Cytological studies in Allium. VI. The chromo- genera of Alliaceae: a synonymic enumeration, Ann. Musei some morphology of diploid species of Allium. Hereditas, Goulandri.s, 4, 83—198. 20, 289-330. STEARN,W. i. 1980.Allium. In Tutin, T. G., Heywood, V. H., LEVAN,A. 1936.Die zytologie von Allium cepa xfislulosum. Burges, N. A., Moore, D. M., Valentine, D. H., Walters, Hereditas,21,195—214. S. M. and Webb, D. A. (eds.) FloraEuropea,Cambridge LF.VAN,A. 1937.Cytological studies in the Allium paniculalum University Press, 5, 49—69. group.1-lereditas, 23, 317-370. THOMAS,II. H. 1981.The Giemsa C-band karyotype of six MURIN,A. 1976.Polyploidy and mitotic cycle. Nucleus, 19, Lolium species. Heredity, 46, 263—267. 192—195. VAN'THOF, j. 1965.Relationships between mitotic cycle dur- NAGL,W. AND El-IRENDORFER, F. 1974.DNA content, hetero- ation, S period duration and average rate of DNA synthesis chromatin, mitotic index and growth in perennial and in the root meristem cells of several plants, ExpI. Cell Res., annual Anthemideae (Asteraceae) Plant Syst. Evol., 123, 39,45-58. 35—54. VAN'THO?, J. AND SPARROW. A. 1. 1963.A relationship NAGL,W. AND 1-USENIG, ii. p. 1979.Types of chromatin between DNA content, nuclear volume and minimum organization in plant nuclei. P1. Syst. Evol. Suppl., 2, 221- mitotic cycle time. Proc. Nat. Aad. Sci., 49, 897-902. 233. VOSA,C.a. 1976. Heterochromatic handing patterns in Allium, NARAYAN,IC K. ,j. 1982.Discontinuous l)NA variation in the II. Ueterochromatic variation in species of the Paniculatum evolution of plant species: the genus Lathyrus. Evolution, group. Chromosoma(Berl.), 57,119—133. 36, 877—891. vvFI)t:NSKLI,A. 1. 1935.Allium. In V. L. Komarov ed, Floraof NARAYAN,R. K. . 1983.Chromosome change in the evolution the USSR. Leningrad, Academy of Sciences, USSR. of Lathyrus species. In Brandham, P. E. and Bennett, M. wENl)f-.Lt3o,i'. 1969.New subgenera, sections and species of i). (eds.) Kew chromosome ConferenceII,George Allen Allium. Bot. Notiser, 122, 35—37. and Unwin, pp. 243-250. WENDELBO,'. 1971.Alliaceae. In Rechinger, K. H. (ed.) Flora I'ARODA,R. S. ANI) RIIS, ii. 1971.Nuclear DNA variation in Iranica, Akademische I)ruck u. Verlagsanstalt, Graz, Aus. Eu-Sorghums. Chromosoma (Berl.), 32, 353-363. tria, 76. PRICE,H. .i. 1976.Evolution of DNA content in higher plants. WILLIS,J. C. 1966.A Dictionary of Flowering Plants, 7th edn. Bot. Rev., 42, 27—52. Rev. H. K. Airy Shaw, Cambridge University Press,