What Is the CIentromere? John Erickson RESEARCH IS CURRENTLYUNDERWAY to clarify the structure and function of the centromere or kinetochore. 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 chromosome where the spindle fibers attach (fig. 1). This attachment allows the chromosome to be pulled toward the poles during anaphase of mitosis and meiosis through a mechanism not yet known. Many textbook FIGURE 1. Diagrammatic representation of metaphase 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 microtubules 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 genetics 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 prophase and excellent preparations, of metaphase chromosomes- metaphase consists of two chromatids, 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 centromeres, where the extending each way from the apposed centromeres that chromatids are tightly apposed, being bound together by appear as a single point. proximal heterochromatin 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 bivalent 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 kinetochores, one for illustration. Courtesy of James Kezer. each sister chromatid, 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 microtubule 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