J. theor. BioL (1975) 49, 111-123

Evidence for Non-random Localization of the Centromere on Mammalian Chromosomes HIROTAMI T. IM~a

Department of Cytology, National Institute of Genetics, Misima, Japan (Received 5 December 1973) Using the accumulated data for mammalian karyotypes, a quantitative analysis of longitudinal distribution of centromeres on chromosomes was made. The size of short arms is given by per cent weight (Sw) relative to the X-containing haploid set, by which the centrometric position is expressed quantitatively. The frequency distribution of the Sw among 16,817 chromosomes of 723 mammalian species showed a V-shape pattern with a distinct antimode lying at Sw ~ 0.6, suggesting a nonrandom localization of the centromere on mammalian chromosomes.

1. Introduction

The crucial point for analysing the karyotype evolution is how to decode the historical processes of the chromosome rearrangements recorded on metaphase chromosome morphologies during the course of evolution. The location of the centromere is the most useful landmark for detecting those biological events, because shifts of centromerie position on chromosomes are caused by chromosome rearrangements which should have played a significant role during karyotype evolution in animals (White, 1973). Since Levan, Fredga & Sandberg (1964) proposed a standard nomenclature for chromosomes in terms of arm ratio based on the location of the centromere, most cytologists have considered that the centromere can locate randomly at every.point on the chromosome between the mid-point and end. If so, an even frequency distribution of the centromedc position should be obtained. However, a quantitative analysis for centromeric position has seldom been investigated. In the present study the location of the centromere is compared statistically based on the chromosome pictures of various mammalian species which have been accumulated during the last decade. Unexpectedly, non-random distribution of centromeric position on chromosomes has been observed. 111

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2. Materials and Methods The materials used were a total of 16,817 individual chromosomes observed in 723 taxonomically distinct mammalian species and subspecies including sibling species and several species showing chromosome polymorphisms (Table 1). They were obtained from the 190 references summarized in the Appendix.

TABLE 1

Taxonomic list of mammals studied Order

Number of species

Rodentia Carnivora Primates Chiroptera Artiodactyla Insectivora Marsupialia Lagomorpha Perissodactyla Edentata Cetacea Proboscidea Tubulidentata Total

287 98 88 80 73 31 31 13 8 8 3 2 1 723

In practice one male karyotype was used for one species but in some cases a female karyotype was adopted. As almost all kinds of karyotypes now available, ranging in chromosome number between n = 3 and n = 42 (Fig. 1) were employed in the present study, biased fluctuations in chromosome size and morphologies due to sampling errors would be negligible. The position of the centromere of the chromosome is expressed quantitatively by the size of the short arm which is determined with the photo cut-out technique of Wurster, Snapper & Benirschke (1971). Both the short arm and long arm in each homologous pair were cut out from enlarged photographs (approximate magnification x 4,000) and weighed with an analytical micro balance within an accuracy of 0.1 mg. As the thickness of the photographic paper used was very uniform, the variation of their weight was less than 0.5 % of each arm weight. The mean weight of the short arms of a homologous pair of chromosomes expressed as a percentage of the total weight of the X-containing haploid set is designated as Sw, in the same way that of long arms as Lw, and that of the whole chromosome as Cw, where Cw = Sw + / - ~ . The relative weight of the Y chromosome is calculated from its percentage of the total weight. Assuming a uniform thickness of the metaphase chromosomes on a glass slide, the size of arms (Sw and Lw) correlates to the per cent volume of the arms against the total volume of haploid set.

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FIo. 1. Histogram showing the haploid chromosome numbers of 723 mammals. Although the size of arms can be determined more simply by per cent length to the total length of haploid set, it was not adopted in the present study, because determination of short arm length less than 1% tended to result in overestimation and error (see Imai, 1973c). 3. Results and Discussion

The frequency distribution of short arm sizes (Sw) when the individual whole chromosome sizes (Cw) are 1.9, 2.5, 3.4, 4.3, 5.1 and 6-4, respectively, is shown in Fig. 2. The figure obviously exhibits V-shape distribution having the antimode lying at about Sw = 0-6. The antimode can be similarly demonstrated in the cumulative data of all size of chromosomes with C , > 1.2 (Fig. 3), which agrees with the preliminary report by Imai (1973a). T.B.

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FzG. 2. Frequency distribution of S , when C,, = 1.2 (broken line) and when C,, = 1.9, 2.5, 3.4, 4.3, 5.1 and 6"4 (solid lines with numerical orders). Sw, size of short arms in weight. Cw, size of whole chromosomes in weight. The ordinate at Cw]2is twice the actual observation, for the class interval at that point is half of the others.

Though the V-shape pattern was not found in the chromosomes with C,, ~< 1.2 (Fig. 2), those chromosomes are very few (about 3y/~). The V-shape distribution here demonstrated seems to be a basic pattern of mammalian chromosomes. The data of frequency distribution of Sw were schematically summarized in Fig. 4. The distribution curve has two modes at Sw = 0 and Cw/2, and a single antimode at S,, = 0.6, which is fixed in every size of chromosomes. If the DNA strands are uniformly folded in the metaphase chromosomes as suggested by the recent electron microscopic studies (Comings & Okada, 1970; Stubblefield & Wray, 1971), the Sw values may roughly correspond to the DNA content. A linear relationship between the DNA content of metaphase chromosomes and their size has also been demonstrated by Radley (1966). Furthermore, Bachmann (1972) revealed that deviation in the genome size of mammals fails within + 30 Yo, which make it possible to compare the Sv of different mammalian species as absolute values within

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the limited error (_+30yo). Assuming that the mammalian haploid genome contains about 3 x 109 nucleotide pairs (see White, 1973), the short arms with S,, = 0.6 roughly correspond to 1 "8 x i07 nucleotide pairs (c. 6 x I03 tt in D N A strand length). The bimodal distribution of short arm sizes (Sw) with the antimode at Sw = 0.6, which means in other words that the position of the centromere is non-random in mammalian chromosomes, may suggest at least two possibilities. One is that the short arms with S,, ~< 0.6 and Sw > 0.6 are structurally different. The recent data on constitutive heterochromatin by the C-banding method suggest that minute short arms of acrocentrics are totally heterochromatic and short arms of large sized metacentrics are euchromatic (Hsu & Arrighi, 1971; Yunis & Yasmineh, 197I). To test this assumption, the sizes of euchromatic and heterochromatic short arms were calculated from the chromosomes of eight mammals, Ovis arnmon, guinea pig, mouse, calf, human, Mierotus agrestis, Maeaca mulatta and Cerco-

116

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z |

0

,,,,

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mammalian chromosomes. &, values indicate the distance from the terminal of short arms to the centromere.

pithecus aetiops, using the karyotypes in the Chromosome Atlasses by Hsu & Benirschke (1967, 1968, 1969) and the data of C-bands by Hsu & Ardghi (1971), Yunis & Yasmineh (1971), Pera (1972), and Stock & Hsu (1973). As shown in Fig. 5, the frequency distribution of heterochromatic short arms is monomodal having the distinct mode at Sw = 0, where heterochromatic short arms with Sw ~< 0"6 are 89"8 %. On the other hand, the euchromatic short arms are all Sw I> 0.6. Although we need further accumulation of data especially on euchromatic short arms, the present result seems to support the assumption mentioned above. The heterochromatic short arms with S~, > 0.6 may be best interpreted by the assumption of Bradshaw & Hsu (1972) that heterochromatic arms may "grow" by addition of heterochromatin which is probably compatible with the satellite D N A (repetitious DNA) suggested by Pardue & Gall (1970) and Yunis & Yasmineh (1971). The other possible interpretation of the V-shape pattern of Fig. 4 is that chromosome rearrangements in the short arms with Sw - 0.6 are apt to occur more easily than the other size of short arms. It is well documented by many cytologists that during the course of mammalian karyotype evolution chromosome morphologies have often changed from "acrocentric

NON-RANDOM LOCALIZATION OF CENTROMERBS

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0.6 0.8 1.0 1.2 1.4 Per cent weight of short crms (Sw)

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FIG. 5. Frequency distribution o f the size o f totally heterochromatic short arms (solid

line) and euchromatie short arms (broken line). or telocentric" (chromosomes with Sw ~< 0.6 in the present term; see Imai, 1973b) to "metacentric, submetacentric or subtelocentric" (S~, > 0.6) or vice versa by chromosome rearrangements such as pericentric inversion and whole arm transpositions (so-called Robertsonian rearrangement) (Amrud, 1968; Bianchi, Reig, Molina & Dulout, 1971; Fredga & Bergstr0m, 1970; Gustavsson & Sundt, 1969; Hsu & Arrighi, 1968; McFee, Banner & Rary, 1966; Patton, 1970; Thaeler, 1968; Wahrman, Goitein & Nevo, 1969; Wurster & Benirschke, I968). The reason for the limited size of short arms (limited length of D N A strand in other words) having higher frequency in the chromosome rearrangements is unknown. The two possibilities mentioned above would be co-operative. When the size of short arms grew up to = 0"6 by addition of heterochromatin, the chromosomal change may occur by pericentric inversion or a whole arm transposition such as centric fusion. The author is indebted to Dr K. Moriwaki, National Institute of Genetics, Misima, for making this study possible and for his kind advice in the preparation of the manuscript. REFERENCES AMRUD,J. (1968). Hereditas 62, 293. BACttMANN,K. (1972). Chromosoma 37, 85. BtANCm,N. O., REIG,O. A., MOLINA,O. J. & DULotrr, F. N. (1971). Evolution 25, 724. BRADSI-IAW,W. N. & Hsu, T. C. (1972). Cytogenetica 11, 436.

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COMBOS, D. E. & OKADA,1". A. (1970). Cytogenetics 9, 436. FReDOA, K. & BERGSTROM,U. (1970). Hereditas 66, 145. GUSTAVSSON,I. & S ~ T , C. O. (1969). Chromosoma 28, 245. I-Isu, T. C. & ARIUGHI,F. E. (1968). Cytogenetics 7, 417. H_so, T. C. & Asmom, F. E. (1971). Chromosoma 34, 243. I-Isu, T. C. & BB~m~SCI-IK~,K. (1967, 1968, 1969). An Atlas of Mammalian Chromosomes, vols 1, 2 and 3. New York: Springer-Verlag. IMAI,H. T. (1973a). Annual Report, National Institute of Genetics, Japan, No. 23, 46. IMAI, H. T. (1973b). Annual Report, National Institute of Genetics, Japan, No. 23, 50. IMAI, H. T. (1973c). Annual Report, National Institute of Genetics, Japan, No. 23, 53. LEVAN,A., FREDGA,K. & SANDBERG,A. A. (1964). Hereditas 52, 201. M c F ~ , A. F., BANNER,M. W. & RARY,J. M. (1966). Cytogenetics 5, 75. PATRON,J. L. (1970). Chromosoma 31, 41. PAmaue, M. L. & GALL,J. G. (1970). Science, N.Y. 168, 1356. ~.r.A, F. (1972). Chromosoma 36, 263. RADI~Y, J. M. (1966). Expl Cell Res. 41, 217. STOCK,A. D. & Hsu, T. C. (1973). Chromosoma 43, 21I. STtmBL~mLD, E. & WRAY,W. (1971). Chromasoma 32, 262. THAV.I~, C. S., JR (1968). Chromosoma 25, 172. Ytmls, J. J. & YASMIN~, W. G. (1971). Science, N. Y. 174, 1200. WAtmMAN,J., GottEn% R. & NEvo, E. (1969). Science, N. Y. 159, 82. WmTS, M. J. D. (1973). Animal Cytology and Evolution, 3rd edn. London: Cambridge University Press. Wtmsmt, D. H. & Bm,m~scx-H~, K. (1968). Chromosoma 25, 152. WURST~R,D. H., SNAI'P~t, J. R. & BENmSCH~, K. (1971). Cytogenetics 10, 153.

APPENDIX C h r o m o s o m e Bibliography

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NON-RANDOM LOCALIZATION OF CENTROMERES

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Evidence for non-random localization of the centromere on mammalian chromosomes.

J. theor. BioL (1975) 49, 111-123 Evidence for Non-random Localization of the Centromere on Mammalian Chromosomes HIROTAMI T. IM~a Department of Cyt...
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