Instability of Alien Chromosome Introgressions in Wheat Associated with Improper Positioning in the Nucleus

Alien introgressions introduce beneficial alleles into existing crops and hence, are widely used in plant breeding. Generally, introgressed alien chromosomes show reduced meiotic pairing relative to the host genome, and may be eliminated over generations. Reduced pairing appears to result from a fai...

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Main Authors: Kateřina Perničková, Veronika Koláčková, Adam J. Lukaszewski, Chaolan Fan, Jan Vrána, Martin Duchoslav, Glyn Jenkins, Dylan Phillips, Olga Šamajová, Michaela Sedlářová, Jozef Šamaj, Jaroslav Doležel, David Kopecký
Format: Article
Language:English
Published: MDPI AG 2019-03-01
Series:International Journal of Molecular Sciences
Subjects:
rye
Online Access:https://www.mdpi.com/1422-0067/20/6/1448
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spelling doaj-63a9b12422d54495a460837625f0f7392020-11-24T20:53:58ZengMDPI AGInternational Journal of Molecular Sciences1422-00672019-03-01206144810.3390/ijms20061448ijms20061448Instability of Alien Chromosome Introgressions in Wheat Associated with Improper Positioning in the NucleusKateřina Perničková0Veronika Koláčková1Adam J. Lukaszewski2Chaolan Fan3Jan Vrána4Martin Duchoslav5Glyn Jenkins6Dylan Phillips7Olga Šamajová8Michaela Sedlářová9Jozef Šamaj10Jaroslav Doležel11David Kopecký12Institute of Experimental Botany, Centre of the Region Haná for Biotechnological and Agricultural Research, Šlechtitelů 31, 78371 Olomouc, Czech RepublicInstitute of Experimental Botany, Centre of the Region Haná for Biotechnological and Agricultural Research, Šlechtitelů 31, 78371 Olomouc, Czech RepublicDepartment of Botany and Plant Sciences, University of California, Riverside, CA 92521, USADepartment of Botany and Plant Sciences, University of California, Riverside, CA 92521, USAInstitute of Experimental Botany, Centre of the Region Haná for Biotechnological and Agricultural Research, Šlechtitelů 31, 78371 Olomouc, Czech RepublicDepartment of Botany, Faculty of Science, Palacký University Olomouc, Šlechtitelů 27, 783 71 Olomouc, Czech RepublicInstitute of Biological, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth, Ceredigion, Wales SY23 3DA, UKInstitute of Biological, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth, Ceredigion, Wales SY23 3DA, UKDepartment of Cell Biology, Centre of the Region Haná for Biotechnological and Agricultural Research, Faculty of Science, Palacký University Olomouc, Šlechtitelů 27, 783 71 Olomouc, Czech RepublicDepartment of Botany, Faculty of Science, Palacký University Olomouc, Šlechtitelů 27, 783 71 Olomouc, Czech RepublicDepartment of Cell Biology, Centre of the Region Haná for Biotechnological and Agricultural Research, Faculty of Science, Palacký University Olomouc, Šlechtitelů 27, 783 71 Olomouc, Czech RepublicInstitute of Experimental Botany, Centre of the Region Haná for Biotechnological and Agricultural Research, Šlechtitelů 31, 78371 Olomouc, Czech RepublicInstitute of Experimental Botany, Centre of the Region Haná for Biotechnological and Agricultural Research, Šlechtitelů 31, 78371 Olomouc, Czech RepublicAlien introgressions introduce beneficial alleles into existing crops and hence, are widely used in plant breeding. Generally, introgressed alien chromosomes show reduced meiotic pairing relative to the host genome, and may be eliminated over generations. Reduced pairing appears to result from a failure of some telomeres of alien chromosomes to incorporate into the leptotene bouquet at the onset of meiosis, thereby preventing chiasmate pairing. In this study, we analysed somatic nuclei of rye introgressions in wheat using 3D-FISH and found that while introgressed rye chromosomes or chromosome arms occupied discrete positions in the Rabl’s orientation similar to chromosomes of the wheat host, their telomeres frequently occupied positions away from the nuclear periphery. The frequencies of such abnormal telomere positioning were similar to the frequencies of out-of-bouquet telomere positioning at leptotene, and of pairing failure at metaphase I. This study indicates that improper positioning of alien chromosomes that leads to reduced pairing is not a strictly meiotic event but rather a consequence of a more systemic problem. Improper positioning in the nuclei probably impacts the ability of introgressed chromosomes to migrate into the telomere bouquet at the onset of meiosis, preventing synapsis and chiasma establishment, and leading to their gradual elimination over generations.https://www.mdpi.com/1422-0067/20/6/1448chromatin3D-FISHnucleusintrogressionryehybridwheatgenome stability
collection DOAJ
language English
format Article
sources DOAJ
author Kateřina Perničková
Veronika Koláčková
Adam J. Lukaszewski
Chaolan Fan
Jan Vrána
Martin Duchoslav
Glyn Jenkins
Dylan Phillips
Olga Šamajová
Michaela Sedlářová
Jozef Šamaj
Jaroslav Doležel
David Kopecký
spellingShingle Kateřina Perničková
Veronika Koláčková
Adam J. Lukaszewski
Chaolan Fan
Jan Vrána
Martin Duchoslav
Glyn Jenkins
Dylan Phillips
Olga Šamajová
Michaela Sedlářová
Jozef Šamaj
Jaroslav Doležel
David Kopecký
Instability of Alien Chromosome Introgressions in Wheat Associated with Improper Positioning in the Nucleus
International Journal of Molecular Sciences
chromatin
3D-FISH
nucleus
introgression
rye
hybrid
wheat
genome stability
author_facet Kateřina Perničková
Veronika Koláčková
Adam J. Lukaszewski
Chaolan Fan
Jan Vrána
Martin Duchoslav
Glyn Jenkins
Dylan Phillips
Olga Šamajová
Michaela Sedlářová
Jozef Šamaj
Jaroslav Doležel
David Kopecký
author_sort Kateřina Perničková
title Instability of Alien Chromosome Introgressions in Wheat Associated with Improper Positioning in the Nucleus
title_short Instability of Alien Chromosome Introgressions in Wheat Associated with Improper Positioning in the Nucleus
title_full Instability of Alien Chromosome Introgressions in Wheat Associated with Improper Positioning in the Nucleus
title_fullStr Instability of Alien Chromosome Introgressions in Wheat Associated with Improper Positioning in the Nucleus
title_full_unstemmed Instability of Alien Chromosome Introgressions in Wheat Associated with Improper Positioning in the Nucleus
title_sort instability of alien chromosome introgressions in wheat associated with improper positioning in the nucleus
publisher MDPI AG
series International Journal of Molecular Sciences
issn 1422-0067
publishDate 2019-03-01
description Alien introgressions introduce beneficial alleles into existing crops and hence, are widely used in plant breeding. Generally, introgressed alien chromosomes show reduced meiotic pairing relative to the host genome, and may be eliminated over generations. Reduced pairing appears to result from a failure of some telomeres of alien chromosomes to incorporate into the leptotene bouquet at the onset of meiosis, thereby preventing chiasmate pairing. In this study, we analysed somatic nuclei of rye introgressions in wheat using 3D-FISH and found that while introgressed rye chromosomes or chromosome arms occupied discrete positions in the Rabl’s orientation similar to chromosomes of the wheat host, their telomeres frequently occupied positions away from the nuclear periphery. The frequencies of such abnormal telomere positioning were similar to the frequencies of out-of-bouquet telomere positioning at leptotene, and of pairing failure at metaphase I. This study indicates that improper positioning of alien chromosomes that leads to reduced pairing is not a strictly meiotic event but rather a consequence of a more systemic problem. Improper positioning in the nuclei probably impacts the ability of introgressed chromosomes to migrate into the telomere bouquet at the onset of meiosis, preventing synapsis and chiasma establishment, and leading to their gradual elimination over generations.
topic chromatin
3D-FISH
nucleus
introgression
rye
hybrid
wheat
genome stability
url https://www.mdpi.com/1422-0067/20/6/1448
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