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Home , Centromere

What Is the CIentromere?

John Erickson

RESEARCH IS CURRENTLYUNDERWAY to clarify the structure and function of the or . Information on this body varies from textbook to textbook, leaving both instructors and Downloaded from http://online.ucpress.edu/abt/article-pdf/41/1/40/36685/4446451.pdf by guest on 27 September 2021 students confused. Thus, a review and reconsideration of how we define and illustrate the centromere, or kinetochore, is appropriate.

The Situation The centromere, or kinetochore, is that point on a where the spindle fibers attach (fig. 1). This attachment allows the chromosome to be pulled toward the poles during of and through a mechanism not yet known. Many textbook FIGURE 1. Diagrammatic representation of kinetochore authors and biologists prefer the term, "kinetochore," structure (A) Two kinetochore filaments of one sister kinetochore. (B) some to avoid confusion with the centriole and others Chromosomal attached to both kinetochore filaments. (C) Continuous microtubules (pole-to-pole) extending because kinetochore aptly connotes a site involving through chromosome arms. (D) Axial elements consisting of a pair of motion. Original articles and reviews tend to use 50 to 80 A fibrils. (E) Leteral fibrils,50 to 80 A, which extend out from kinetochore; biology and texts use centromere. the axial elements. Illustration from Brinkley and Stubblefield (1970) Each anaphase chromosome has a centromere. Rep- used with permission of the authors. lication during interphase includes the centromere along with the rest of the chromosome (Swanson, Merz, and centromere itself. Photographs we see, even of Young 1967). Thus, a chromosome at and excellent preparations, of metaphase - metaphase consists of two , each with its own such as the broadbean Vicia faba and the familiar, centromere. The level of resolution of the light opened-out ("colchicine metaphase") human microscope, however, does not resolve the duplex chromosome illustrations-show a pair of arms nature at the region of the , where the extending each way from the apposed centromeres that chromatids are tightly apposed, being bound together by appear as a single point. proximal on each side of the At the beginning of anaphase, the centromeres separate from each other. The proximal heterochromatin has released its bond, or perhaps that John Erickson is associate professor of biology, I bond has been broken by the pull of the spindle fibers on Western Washington University, Bellingham, the two opposing centromeres. In meiosis, the situation Washington 98225. He received his M.A. degree in 1950 from Indiana University (Bloomington), and is similar. Again, each chromosome replicates with its his Ph.D. degree in 1964 from the University of centromere at interphase before the two meiotic Oregon. In addition, Erickson has received divisions. Of course, replication does not occur in the from the Danforth Foundation fellowships (1962- between meiotic 63) and the National Institutes of Health (1963-64), . ,. interphase (interkinesis) and is a member of the Genetics Society of divisions. Chromosomes pair at zygotene in the first America, the American Genetic Association, and prophase. At diplotene, all four strands including the AAAS. Erickson's principalresearch work centers on meiotic drive in Drosophila involving chromosome breakage and he has published centromere region are visible in good preparations. The several articles on the topic and related information. He also is the co- proximal heterochromatin is visible as dark bands of author of an article on "Genetics of the Male Calico Cat," an admittedly material bindingsister strands together on each side. An "lighter"topic, that appeared in Cat Fancy Magazine. Erickson has just started work on an introductory genetics textbook. His excellent micrograph by James Kezer (fig. 2a) appears as avocations include swimming and sailing. the frontpiece in Swanson, Merz, and Young (1967), in

40 THE AMERICANBIOLOGY TEACHER,JANUARY 1979 concert. Finally, at second anaphase, the sister centromeres separate from each other. A single centromere and its chromosome move toward each pole, as in mitosis. The chapter by Kezer (Stahl 1969) contains photographs and further details.

Variations in Treatment Taking the interpretation summarized above as a starting point, one can imagine how other interpretations might be derived. First, we shall consider statements from textbooks. Few, if any, of the sources surveyed specify when replication of the centromere occurs. My remarks on this aspect are based on descriptions most sources give of the chromosome with its two chromatids that appears Downloaded from http://online.ucpress.edu/abt/article-pdf/41/1/40/36685/4446451.pdf by guest on 27 September 2021 in prophase. A typical statement is, "the chromosome consists of two chromatids joined at a single point, the centromere." A few authors circumvent the problem in an interesting way. In the first edition of Burns (1969), we find, "In well-prepared stained material, each of the chromonemata (chromatids) of a given chromosome may be seen to share a common, small, relatively clear, FIGURE 2a. Photograph of a late diplotene in a spermatocyte spherical zone, the centromere. . . (or of the Costa Rican plethodontid salamander, Oedipina poelzi. Aceto- orcein squash preparation. The centromeres and associated kinetochore)." The third edition of Burns (1976) adds heterochomatin are the conspicuous objects in the lower section of the that the centromere "includes two , one for illustration. Courtesy of James Kezer. each sister , to which the microtubules of the spindle. . .are attached." Hexter and Yost (1976) make a similarstatement. Goodenough and Levine (1974) state on page 154 that ". . .the site of insertion in the centromere region is often called the cen c kinetochore." Students are left to conclude, with the aid of an excellent electron micrograph on a facing page,

br that the chromosome has two kinetochores. The idea that a chromosome has one centromere, composed of ch = chiasma two kinetochores, is also found in Brown (1972). He 'siHI an(l ss HZ = sister strands of the two refers to the work of Brinkley and Stubblefield (1970) homologues using the expression "kinetochores of the cen = centromere. There are foturof these. one for each strand. centromere." Brinkley and Stubblefield (1970) use only br = bridging material holding the the term "kinetochore" in their discussion, centromeres of sister strands however. Nicklas (1971) in reviewing the Brinkley- together. Stubblefield work, again refers to the "two sister kinetochores of the chromosome." "Centromere" does FIGURE 2b. Diagram by James Kezer (Stahl 1969). Labels and not appear. Table 1 indicates the treatment various identifications from the source are as follows: ch = chiasma; ssH, and ssH2 = sister strands of the two homologues; cen = centromere. There authors give the characteristics of the centromere. are four of these one for each strand; br = bridging material holding In mitosis where the separation of centromeres is not centromeres of sister strands together. visible until the beginning of anaphase, one finds the Haynes (1978), in Hexter and Yost (1976), in Stahl statement "the centromere duplicates (or replicates) at (1969),and in Swansonand Webster (1977). Figure2b is metaphase." Parallel problems occur for Kezer's diagram of this process (Stahl meiosis. Some presentations assert that each dyad at 1969). Homologous pairs of strands repel each other metaphase and anaphase I has only one centromere and particularlyat the centromere region at this stage. At that the centromere finally divides at the end of first metaphase, sister centromeres, are still repelled metaphase II. fromthe homologouspairs of chromosomes(except for The confusion associated with when the centromere regionsdistal to a crossover);and at firstanaphase, they divides extends to problems for students to solve at the separateto oppositepoles; dyads move towardthe poles end of textbook chapters. Typically, problems appear in by spindlefibers attached to sistercentromeres, acting in this general form: If an organism has N=12 pairs of

CENTROMERE 41 TABLE1. Survey of Recent Textbooks and RelatedSources

"Pro"indicates in accord with the views set forthin this paper. "Int"means the book, in this matter,is intermediatebetween ex- tremes,or non-committal,or ambivalenton the point,as nearlyas can be judges. "Con"means that the sourceis, on thispoint, con- trary to the viewpoint described here. "---" means nothing found on the item.

Statements and Descriptions Diagrams Chromosome Mitosis Meiosis Mitosis Meiosis Biology texts BSCS Green, 4th ed., 1978 Con Con Con Con Con Curtis,2nd ed., 1975 Pro and Con Con Con Con Con Herreid,1977 Con Con Con Pro and Con Con Keeton, 2nd ed., 1972 Con Con Con Con Con Kimball, 4th ed., 1978 Con --- Con Con Con Kirkand Starr,2nd ed., 1975 Pro and Con Pro Con Con Con Otto and Towle, 1977 Con Con Con Con Con Scheer, 1977 Int Int Int --- Con

Tortoraand Becker, 1978 Con Con Con Con Con Downloaded from http://online.ucpress.edu/abt/article-pdf/41/1/40/36685/4446451.pdf by guest on 27 September 2021 Villee, 7th ed., 1977 Con Con Con Int Int Wilson,et al, 1977 Con Int Int Int Int

Genetics Texts Burns, 3rd ed., 1976 Pro Pro Con Crow, 7th ed., 1976 ------Con Con Farnsworth,1978 Pro Pro Pro Con* Con* Gardner,5th ed., 1975 Con Con Con Int Con Goodenoughand Levine, 1974 Int** Con Con Int Con Herskowitz, 2nd ed., 1977 Pro Int --- Con Con Hexter and Yost, 1976 Pro Con Con Con Con Jenkins, 1975 Con Con Con Con Con King,2nd ed., 1965 Con Int Con Con Con Levine,2nd ed., 1973 Con Con Con Con Con Merrell, 1975 --- Con Int Con Con Rothwell,1976 Con Con Con Con Con Stahl, 2nd ed., 1969 --- Int and Con Pro Con Pro Strickberger,2nd ed., 1976 --- Pro Pro Con Pro and Con Suzukiand Griffiths,1976 Con Con Con Con Con

Human Genetics Texts Hartl, 1977 Int and Con Int Con Con Con Lernerand Libby,1976 Con Con Con Con Con Levitan and Montagu, 2nd ed., 1977 --- Con Int Con Con Moody, 2nd ed., 1975 Con Int Int Con Con Nagle, 1974 Con Con Con Con Con Novitski, 1977 Con Con Con Pro and Con Con Rothwell,1977 Con Con Con Con Con Stern, 3rd ed., 1973 Con Con Con Con Con Stine, 1977 Con Con Con --- Con Sutton, 2nd ed., 1975 Con Con Con Con Con Winchester,2nd ed., 1975 Con Con Con Con Con

Cell Biologyand Cytology Texts Pro Pro ------Brown, 1972 Pro --- Swanson, Merz and Young, 1967 Pro Con Pro --- Swanson and Webster,4th ed., 1977 Int Int Pro --Con

*An explanation for this form of the diagrams is given, page 126. **See body of this paper for explanation. Where two entries appear, e.g., "Pro and Con," both are to be found, usually on separate pages.

42 THE AMERICANBIOLOGY TEACHER, JANUARY 1979 chromosomes, how manytetrads (=bivalents)are found 1969). Figure 3b shows an imaginarytransition stage, at first meiotic prophase? How many strands? How and figure3c shows a roundedcentromere without the many centromeres? The questions go on to encompass proximal heterochromatic blocks. Figure 3c is, of other meiotic stages and mitosis. Instructors who course, typical of the sketch found in many sources espouse the view presented here using a textbook reviewed in this article;interestingly, it does bear one followingthe contraryviewpoint find themselves in the similarity to pubished micrographs such as that of awkward position of differing from the author's Kezer. A spot of light,sometimes ovoid, corresponding publishedanswers. to the open center in figure 3a, is often evident in Confusion also surrounds diagrams of mitosis and photomicrographs. Figure 3d shows how the meiosis. In mitosis, it takes the formof representingthe interpretation of 3c looks at anaphase I. For its centromere of an anaphase chromosome as a small, appearance at other stages, consult any of the texts open circle. The "centromere" of a prophase- reviewed. Figure 3e shows how anaphase I might be metaphasechromosome is representedas a largercircle drawn accordingto the view espoused in this article. with two arms on each side. In meiosis, the diagrams reflectthe same idea, witha largecircle for the common centromerebeing carried through the firstdivision up to SuggestionsAre Needed anaphase II. In one of the textbooks surveyed (Suzuki Downloaded from http://online.ucpress.edu/abt/article-pdf/41/1/40/36685/4446451.pdf by guest on 27 September 2021 My purpose in preparingthis article is to urge the and Griffiths1976), these concepts are illustratedin a flip classificationand the standardizationof the centromere, movie on the edges of pages showing the large circle or kinetochore,in biologyand genetics textbooks. It is pinchingdown to two small circles at anaphase. possiblethat some mightwish to signifythe new usage by switchingto "kinetochore,"following that statement of Chromosome Brinkleyand Stubblefield(1970) and of Nicklas (1971) that each chromatid has a kinetochore, and the

Chromatid metaphase chromosome has two sister kinetochores. Proximal I invitereaders of this journalto share theirviews with Heterochromatin- "The Centromere" me. A futurearticle will appear reporting the responses

Centromeres and suggestions received.

3a 3b 3c References BIOLOGICALSCIENCES CURRICULUMSTUDY. 1978. Biologicalscience: an ecological approach. (BSCS Green A/k Version). Nancy Lehman Haynes, ed. Chicago: Rand Mcnallyand Company. BRINKLEY,B.R. and STUBBLEFIELD,E. 1970. Ultrastruc- ture and interactionof the kinetochore and centriole in meiosis. In Advances in cell biology, Volume 1, David M. vv3d 3e Prescott, L. Goldstein, and E. McConkley, eds. New York: Appleton-Century-Crofts. BROWN, W.V. 1972. Textbook of . St. Louis, FIGURE3. Figure3a is a representativeof the chromosome,with its Missouri:C.V. Mosby Company. two chromatidsdrawn from the diploteneappearance in micrographs, BURNS, G.W. 1969. The science of genetics. New andfor the centromereregion, partly after Swanson, Merz, and Young York: The MacmillanCompany. (1977)figure 2.13. Figure3b is an imaginarytransition stage. Figure3c . 1976. The science of genetics. 3rd ed. New York: is the form shown in many texts in biologyand genetics, presumably The MacmillanCompany. derivedfrom 3a through3b. Note that single, large circle is drawn, CROW, J.F. 1976. Genetics notes. 7th ed. Minneapolis, identifiedas the common centromerefor the two chromatidsof the Minnesota:Burgess PublishingCompany. chromosome, or for a dyad at first meiosis. Figure 3d shows first anaphase, as illustratedin typical texts. Figure 3e shows how first CURTIS, H. 1975. Biology. 2nd ed. New York: Worth anaphasemight be representedaccording to the interpretationshown Publishers,Inc. in 3a. FARNSWORTH,M.W. 1978. Genetics. New York: Harper and Row, Publishers. Figure 3 suggests how a combination of what is GARDNER, E. 1975. Principles of genetics. 5th ed. New known,what is conjectured,and what is seen mightlead York: John Wileyand Sons, Inc. to the illustrationsthat we findin the literature.Figure 3a GOODENOUGH, U. and LEVINE, R.P. 1974. Genetics. shows the interpretationpropounded in this article. The New York: Holt, Rinehart, and Winston. HARTL, D.L. 1977. Our uncertain heritage. Philadelphia: centromere region is representedas slender, following J.B. LippincottCompany. Swanson, Merz, and Young (1967),figure 2.13, and with HERREID, C.F. II. 1977. Biology. New York: Macmillan reference to Kezer's photographs and diagram(Stahl PublishingCompany. (Continued on p. 47)

CENTROMERE 43 Because Dracunculusinfects persons in remoterural MOODY, P.A. 1975. Genetics of man. 2nd ed. New areas, its economic effects are difficultto assess. In York: W.W. Norton and Company. many regions of Africa and India, the incidence of NAGLE,J.J. 1974. Heredityand human affairs. St. Louis, the Missouri:C.V. Mosby Company. infection is usually highest during planting NICKLAS,R.B. 1971. Mitosis. In Advances in cell biology, season. Those incapacitatedwith sores of Dracunculus Volume 2. David M. Prescott, L. Goldstein, and E. cannot work in the fieldsand their absence reduces the McConkley,eds. New York: Appleton-Century-Crofts. productionof desperatelyneeded food. Over halfof the NOVITSKI,E. 1977. Human Genetics. Englewood Cliffs, inhabitants(53%) of four villagesnear Ibadan,Nigeria, New Jersey: Prentice-Hall,Inc. OTTO, J.H. and TOWLE,A. 1977. ModernBiology. New had guineaworms during March, 1966, and nearly half of York: Holt, Rinehart,and Winston. the working-agepatients (those 15 to 40 years of age) in ROTHWELL, N.V. 1976. Understanding genetics. Balti- this group missed at least two and one-halfmonths of more: The Williamsand WilkinsCompany. work because of the sores and secondary bacterial . 1977. Human genetics. Englewood Cliffs, New infections. Jersey: Prentice-Hall,Inc. The worm is most prevalentin regions where food SCHEER,B.T. 1977. Patternsof life. New York: Harperand Row, Publishers. production is minimal and malnutrition STAHL, F.W. 1969. The mechanics of inheritance. 2nd widespread.Starvation can only be prevented if the ed. EnglewoodCliffs, New Jersey: Prentice-Hall,Inc. maximumproduction of food is maintained.Consider- STERN,C. 1973. Principlesof humangenetics. 3rd ed. San Downloaded from http://online.ucpress.edu/abt/article-pdf/41/1/40/36685/4446451.pdf by guest on 27 September 2021 ing that each infectedindividual is incapacitatedfor four Francisco:W.H. Freemanand Company. weeks or longer, the toll on the productivityof the STRINE,G.J. 1977. Biosocialgenetics. New York:Macmil- lan PublishingCompany, Inc. is Children and population astounding. older STRICKBERGER,M.W. 1976. Genetics. 2nd ed. New inhabitantsmay suffer from starvation as a consequence York: MacmillanPublishing Company, Inc. of the reduced harvest. SUTTON, H.E. 1975. An introduction to human The guineaworm demonstrates that thoughthe world genetics. 2nd ed. New York: Holt, Rinehartand Winston. enteredthe technicalage over 200 years ago, manyof its SUZUKI,D.T. andGRIFFITHS, A.J.F. 1976. An introduction to genetic analysis. San Francisco:W.H. Freeman and inhabitantsstill suffer from Stone Age diseases. Company. SWANSON,C.P., MERZ,T., and YOUNG,W.J. 1967. Cyto- Acknowledgment-The photographsof guinea worms were genetics. EnglewoodCliffs, New Jersey: Prentice-Hall,Inc. provided by Devubrata Seth, Departmentof Parasitology, . and WEBSTER, P.L. 1977. The cell. 4th SarabhaiResearch Centre, Baroda,India. ed. EnglewoodCliffs, New Jersey: Prentice-Hall,Inc. TORTORA,G.J. andBECKER,J.F. 1978. Lifescience. 2nd ed. New York: MacMillanPublishing Company, Inc. References VILLEE, C.A. 1977. Biology. 7th ed. Philadelphia:W.B. SaundersCompany. MULLER,R.L. 1971. Dracunculusand Dracunculiasis.Ad- WILSON,E.O., EISNER,T., BRIGGS,W.R., DICKERSON, vances in Parisitology9:73. R.E.,METZENBERG, R.L., O'BRIEN, R.D., SUSMAN,M., and BOGGS, W.E. 1977. Life: cells, organisms, popula- tions. Sunderland, Massachusetts:Sinauer Associates, Inc. ...from 43 WINCHESTER, A.M. 1975. Human genetics. 2nd ed. Centromere p. Columbus,Ohio: CharlesE. MerrillPublishing Company. HERSKOWITZ, I.H. 1977. Principles of genetics. 2nd ed. New York: MacmillanPublishing Company. HEXTER,W. and YOST, H.T., JR. 1976. The science of genetics. EnglewoodCliffs, New Jersey: Prentice-Hall,Inc. JENKINS, J.B. 1975. Genetics. Boston: Houghton Mifflin Company. KEETON, W.T. 1972. Biological science. 2nd ed. New Evolutionof Evolution York: W.W. Norton and Company,Inc. KIMBALL,J.W. 1978. Biology. 4th ed. Reading,Massachu- Would it be too bold to in setts: Addison-WesleyPublishing Company. imagine, that the great KING, R.C. 1965. Genetics. 2nd ed. New York: Oxford length of time, since the earth began to exist, UniversityPress. perhaps millions of ages before the commence- KIRK,D. and STARR,C. 1975. Biologytoday. 2nded. New ment of the history of mankind,would it be too bold York: CRM-Random House. to imagine that all warm-blooded have LERNER,I.M. and LIBBY,W.J. 1976. Heredity,evolution, and society. 2nd ed. San Francisco: W.H. Freemanand arisen from one living filament which theGreat First Company. Cause embued with animality... and thus possessing LEVINE, L. 1973. Biology of the . St. Louis, the faculty of continuing to improve by its own in- Missouri:C.V. Mosby Company. herent activity, and of delivering down those LEVITAN, M. and MONTAGU, A. 1977. Textbook of improvements by generation to its posterity, world human genetics. 2nd ed. New York: Oxford University Press. without end! MERRELL,D.J. 1975. An introduction to genetics. New Erasmus Darwin York: W.W. Norton and Company. (Grandfatherof Charles Robert Darwin)

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