Abstract
For normal transition through meiosis, chromosomes rely on pairing with their homologues. Chromosomes which fail to pair, univalents, behave irregularly and may undergo various types of breakage across their centromeres. Here, we analyzed the meiotic behavior of misdivision products themselves: isochromosomes and telocentrics in wheat. Both types of chromosomes behaved in the same fashion as standard 2-armed chromosomes. The 2 most frequent scenarios were separation of sister chromatids in anaphase I or monopolar/bipolar attachment of the univalent to the spindle apparatus with unseparated chromatids. Misdivision was rare, and its frequency appeared directly related to the size of the centromere. The previously deduced relationship between misdivision frequency and chromosome size was likely erroneous and can be explained by a general relationship between chromosome length and the size of its centromere. Pairing of identical arms in isochromosomes did not protect them from misdivision. It is not chiasmate pairing that protects from misdivision but mechanistic issues that arise through that pairing.
Journal Section:
Editor's choice
References
1.
Birchler JA, Han F: Maize centromeres: structure, function and epigenetics. Annu Rev Genet 43:287-303 (2009).
[PubMed]
2.
Birchler JA, Han F: Meiotic behavior of small chromosomes in maize. Front Plant Sci 4:505 (2013).
[PubMed]
3.
Cheng Z, Dong F, Langdon T, Ouyang S, Buell CR, et al: Functional rice centromeres are marked by a satellite repeat and a centromere-specific retrotransposon. Plant Cell 14:1691-1704 (2002).
[PubMed]
4.
Coogan TP, Rosenblum IY: DNA double-strand damage and repair following γ-irradiation in isolated spermatogenic cells. Mutat Res 194:183-191 (1988).
[PubMed]
5.
Darlington CD: Misdivision and the genetics of the centromere. J Genet 37:341-364 (1939).
6.
Dawe RK: Meiotic chromosome organization and segregation in plants. Annu Rev Plant Physiol Plant Mol Biol 49:371-395 (1998).
[PubMed]
7.
Francki MG: Identification of Bilby, a diverged centromeric Ty1-copia retrotransposon family from cereal rye (Secale cereale L.). Genome 44:266-274 (2001).
[PubMed]
8.
Friebe B, Zhang P, Linc G, Gill BS: Robertsonian translocations in wheat arise by centric misdivision of univalents at anaphase I and rejoining of broken centromeres during interkinesis of meiosis II. Cytogenet Genome Res 109:293-297 (2005).
[PubMed]
9.
Guo X, Su H, Shi Q, Fu S, Wang J, et al: De novo centromere formation and centromeric sequence expansion in wheat and its wide hybrids. PLoS Genet 12:e1005997 (2016).
[PubMed]
10.
Han F, Lamb JC, McCaw ME, Gao Z, Zhang B, et al: Meiotic studies on combinations of chromosomes with different sized centromeres in maize. Front Plant Sci 9:785 (2018).
[PubMed]
11.
Henikoff S, Ahmad K, Malik HS: The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293:1098-1102 (2001).
[PubMed]
12.
International Wheat Genome Sequencing Consortium (IWGSC): Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361:eaar7191 (2018).
[PubMed]
13.
Kaszas E, Birchler JA: Misdivision analysis of centromere structure in maize. EMBO J 15:5246-5255 (1996).
[PubMed]
14.
Koo DH, Sehgal SK, Friebe B, Gill BS: Structure and stability of telocentric chromosomes in wheat. PLoS One 10:e0137747 (2015).
[PubMed]
15.
Liu C, Qi L, Liu W, Zhao W, Wilson J, et al: Development of a set of compensating Triticum aestivum-Dasypyrum villosum Robertsonian translocation lines. Genome 54:836-844 (2011).
[PubMed]
16.
Lukaszewski AJ: Reconstruction in wheat of complete chromosomes 1B and 1R from the 1RS.1BL translocation of “Kavkaz” origin. Genome 36:821-824 (1993).
[PubMed]
17.
Lukaszewski AJ: Chromatid and chromosome type breakage-fusion-bridge cycles in wheat (Triticum aestivum L.). Genetics 140:1069-1085 (1995).
[PubMed]
18.
Lukaszewski AJ: Further manipulation by centric misdivision of the 1RS.1BL translocation in wheat. Euphytica 94:257-261 (1997a).
19.
Lukaszewski AJ: Construction of midget chromosomes in wheat. Genome 40:566-569 (1997b).
[PubMed]
20.
Lukaszewski AJ: Behavior of centromeres in univalents and centric misdivision in wheat. Cytogenet Genome Res 129:97-109 (2010).
[PubMed]
21.
Lukaszewski AJ: Misdivision of centromeres, in Jiang J, Birchler JA (eds): Plant Centromere Biology, pp 111-128 (John Wiley and Sons, Inc., Ames 2013).
22.
Lukaszewski AJ: A set of new 1RS translocations from wheat cv. Amigo in a uniform genetic background. Euphytica 213:214 (2017).
23.
Lukaszewski AJ, Kopecky D, Linc G: Inversions of chromosome arms 4AL and 2BS in wheat invert the patterns of chiasma distribution. Chromosoma 121:201-208 (2012).
[PubMed]
24.
Massoudi-Nejad A, Nasuda S, McIntosh RA, Endo TR: Transfer of rye chromosome segments to wheat by gametocidal system. Chromosome Res 10:349-357 (2002).
[PubMed]
25.
Paliulis LV, Nicklas RB: Kinetochore rearrangement in meiosis II requires attachment to the spindle. Chromosoma 113:440-446 (2005).
[PubMed]
26.
Phelps-Durr TL, Birchler JA: An asymptotic determination of minimum centromere size for the maize B chromosome. Cytogenet Genome Res 106:309-313 (2004).
[PubMed]
27.
Sears ER: The behavior of isochromosomes and telocentrics in wheat. Chromosoma 4:535-550 (1952).
[PubMed]
28.
Sears ER, Sears LMS: The telocentric chromosomes of wheat, in Ramanujam S (ed): Proc 5th Int Wheat Genet Symp, pp 389-407 (The Indian Society of Genetics and Plant Breeding, Indian Agricultural Research Institute, New Delhi 1978).
29.
Sears LMR: Misdivision of five different 3B monosomes in Chinese Spring wheat. Wheat Inf Service 37:9-13 (1973).
30.
Sebesta EE, Wood EA: Transfer of greenbug resistance from rye to wheat with X-rays, in: Agronomy Abstracts ASA, pp 61-62, Madison (1978).
31.
Wang J, Liu Y, Su H, Guo X, Han F: Centromere structure and function analysis in wheat-rye translocation lines. Plant J 91:199-207 (2017).
[PubMed]
32.
Wyman C, Kanaar R: DNA double-strand break repair: all's well that ends well. Annu Rev Genet 40:363-383 (2006).
[PubMed]
33.
Yu HG, Dawe RK: Functional redundancy in the maize meiotic kinetochore. J Cell Biol 151:131-142 (2000).
[PubMed]
34.
Zhang P, Friebe B, Lukaszewski AJ, Gill BS: The centromere structure in Robertsonian wheat-rye translocation chromosomes indicates that centric breakage-fusion can occur at different positions within the primary constriction. Chromosoma 110:335-344 (2001).
[PubMed]
© 2019 S. Karger AG, Basel
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
2019
You do not currently have access to this content.
