DNA repair and crossing over favor similar chromosome regions as discovered in radiation hybrid of Triticum

Ajay Kumar; Filippo M. Bassi; Etienne Paux; Omar Al-Azzam; Monika M. de Jimenez; Anne M. Denton; Yong Q. Gu; Eric Huttner; Andrzej Kilian; Sachin Kumar; Aakash Goyal; Muhammad J. Iqbal; Vijay K. Tiwari; Munevver Dogramaci; Harindra S. Balyan; Harcharan S. Dhaliwal; Pushpendra K. Gupta; Gursharn S. Randhawa; Catherine Feuillet; Wojciech P. Pawlowski; Shahryar F. Kianian

doi:10.1186/1471-2164-13-339

DNA repair and crossing over favor similar chromosome regions as discovered in radiation hybrid of Triticum

Ajay Kumar, Filippo M. Bassi, Etienne Paux, Omar Al-Azzam, Monika M. de Jimenez, Anne M. Denton, Yong Q. Gu, Eric Huttner, Andrzej Kilian, Sachin Kumar, Aakash Goyal, Muhammad J. Iqbal, Vijay K. Tiwari, Munevver Dogramaci, Harindra S. Balyan, Harcharan S. Dhaliwal, Pushpendra K. Gupta, Gursharn S. Randhawa, Catherine Feuillet, Wojciech P. PawlowskiShahryar F. Kianian

Plant Pathology

Research output: Contribution to journal › Article › peer-review

20 Scopus citations

Abstract

Background: The uneven distribution of recombination across the length of chromosomes results in inaccurate estimates of genetic to physical distances. In wheat (Triticum aestivum L.) chromosome 3B, it has been estimated that 90% of the cross over events occur in distal sub-telomeric regions representing 40% of the chromosome. Radiation hybrid (RH) mapping which does not rely on recombination is a strategy to map genomes and has been widely employed in animal species and more recently in some plants. RH maps have been proposed to provide i) higher and ii) more uniform resolution than genetic maps, and iii) to be independent of the distribution patterns observed for meiotic recombination. An in vivo RH panel was generated for mapping chromosome 3B of wheat in an attempt to provide a complete scaffold for this ~1 Gb segment of the genome and compare the resolution to previous genetic maps.Results: A high density RH map with 541 marker loci anchored to chromosome 3B spanning a total distance of 1871.9 cR was generated. Detailed comparisons with a genetic map of similar quality confirmed that i) the overall resolution of the RH map was 10.5 fold higher and ii) six fold more uniform. A significant interaction (r = 0.879 at p = 0.01) was observed between the DNA repair mechanism and the distribution of crossing-over events. This observation could be explained by accepting the possibility that the DNA repair mechanism in somatic cells is affected by the chromatin state in a way similar to the effect that chromatin state has on recombination frequencies in gametic cells.Conclusions: The RH data presented here support for the first time in vivo the hypothesis of non-casual interaction between recombination hot-spots and DNA repair. Further, two major hypotheses are presented on how chromatin compactness could affect the DNA repair mechanism. Since the initial RH application 37 years ago, we were able to show for the first time that the iii) third hypothesis of RH mapping might not be entirely correct.

Original language	English (US)
Article number	339
Journal	BMC Genomics
Volume	13
Issue number	1
DOIs	https://doi.org/10.1186/1471-2164-13-339
State	Published - Jul 24 2012

Bibliographical note

Funding Information:
The authors wish to thank Justin Hegstad and Allen Peckrul for assistance in the development of RH panel and capable technical support throughout the research; Dr. Matthew Hayden (VABC, Melbourne, AUS) for precious contributions in designing the DEASY control marker; Dr. Nellye Cubizolles (INRA, Clermont Ferrand, FR) for technical support in the use of cfp markers; Dr. Cyrille Saintenac (INRA, Clermont Ferrand, FR) and his collaborators for making publicly available their excellent work. This work was supported by funding from the National Science Foundation, Plant Genome Research Program (NSF-PGRP) grant No. IOS-0822100 to SFK. Additional support from the NSF-PGRP Developing Country Collaboration aided the assistance of student interns A.Kumar, S.K., A.G., and V.T.; F.M.B was partially supported by Program Master and Back Regione Autonoma della Sardegna and Monsanto Beachell-Borlaug International Scholarship.

Keywords

Chromatin
Deletion mutant
Gamma radiation
Non homologous end joining
Physical mapping
Radiation hybrid
Wheat chromosome 3B

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Kumar, A., Bassi, F. M., Paux, E., Al-Azzam, O., de Jimenez, M. M., Denton, A. M., Gu, Y. Q., Huttner, E., Kilian, A., Kumar, S., Goyal, A., Iqbal, M. J., Tiwari, V. K., Dogramaci, M., Balyan, H. S., Dhaliwal, H. S., Gupta, P. K., Randhawa, G. S., Feuillet, C., ... Kianian, S. F. (2012). DNA repair and crossing over favor similar chromosome regions as discovered in radiation hybrid of Triticum. BMC Genomics, 13(1), Article 339. https://doi.org/10.1186/1471-2164-13-339

Kumar, A, Bassi, FM, Paux, E, Al-Azzam, O, de Jimenez, MM, Denton, AM, Gu, YQ, Huttner, E, Kilian, A, Kumar, S, Goyal, A, Iqbal, MJ, Tiwari, VK, Dogramaci, M, Balyan, HS, Dhaliwal, HS, Gupta, PK, Randhawa, GS, Feuillet, C, Pawlowski, WP & Kianian, SF 2012, 'DNA repair and crossing over favor similar chromosome regions as discovered in radiation hybrid of Triticum', BMC Genomics, vol. 13, no. 1, 339. https://doi.org/10.1186/1471-2164-13-339

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abstract = "Background: The uneven distribution of recombination across the length of chromosomes results in inaccurate estimates of genetic to physical distances. In wheat (Triticum aestivum L.) chromosome 3B, it has been estimated that 90% of the cross over events occur in distal sub-telomeric regions representing 40% of the chromosome. Radiation hybrid (RH) mapping which does not rely on recombination is a strategy to map genomes and has been widely employed in animal species and more recently in some plants. RH maps have been proposed to provide i) higher and ii) more uniform resolution than genetic maps, and iii) to be independent of the distribution patterns observed for meiotic recombination. An in vivo RH panel was generated for mapping chromosome 3B of wheat in an attempt to provide a complete scaffold for this ~1 Gb segment of the genome and compare the resolution to previous genetic maps.Results: A high density RH map with 541 marker loci anchored to chromosome 3B spanning a total distance of 1871.9 cR was generated. Detailed comparisons with a genetic map of similar quality confirmed that i) the overall resolution of the RH map was 10.5 fold higher and ii) six fold more uniform. A significant interaction (r = 0.879 at p = 0.01) was observed between the DNA repair mechanism and the distribution of crossing-over events. This observation could be explained by accepting the possibility that the DNA repair mechanism in somatic cells is affected by the chromatin state in a way similar to the effect that chromatin state has on recombination frequencies in gametic cells.Conclusions: The RH data presented here support for the first time in vivo the hypothesis of non-casual interaction between recombination hot-spots and DNA repair. Further, two major hypotheses are presented on how chromatin compactness could affect the DNA repair mechanism. Since the initial RH application 37 years ago, we were able to show for the first time that the iii) third hypothesis of RH mapping might not be entirely correct.",

keywords = "Chromatin, Deletion mutant, Gamma radiation, Non homologous end joining, Physical mapping, Radiation hybrid, Wheat chromosome 3B",

author = "Ajay Kumar and Bassi, {Filippo M.} and Etienne Paux and Omar Al-Azzam and {de Jimenez}, {Monika M.} and Denton, {Anne M.} and Gu, {Yong Q.} and Eric Huttner and Andrzej Kilian and Sachin Kumar and Aakash Goyal and Iqbal, {Muhammad J.} and Tiwari, {Vijay K.} and Munevver Dogramaci and Balyan, {Harindra S.} and Dhaliwal, {Harcharan S.} and Gupta, {Pushpendra K.} and Randhawa, {Gursharn S.} and Catherine Feuillet and Pawlowski, {Wojciech P.} and Kianian, {Shahryar F.}",

note = "Funding Information: The authors wish to thank Justin Hegstad and Allen Peckrul for assistance in the development of RH panel and capable technical support throughout the research; Dr. Matthew Hayden (VABC, Melbourne, AUS) for precious contributions in designing the DEASY control marker; Dr. Nellye Cubizolles (INRA, Clermont Ferrand, FR) for technical support in the use of cfp markers; Dr. Cyrille Saintenac (INRA, Clermont Ferrand, FR) and his collaborators for making publicly available their excellent work. This work was supported by funding from the National Science Foundation, Plant Genome Research Program (NSF-PGRP) grant No. IOS-0822100 to SFK. Additional support from the NSF-PGRP Developing Country Collaboration aided the assistance of student interns A.Kumar, S.K., A.G., and V.T.; F.M.B was partially supported by Program Master and Back Regione Autonoma della Sardegna and Monsanto Beachell-Borlaug International Scholarship.",

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T1 - DNA repair and crossing over favor similar chromosome regions as discovered in radiation hybrid of Triticum

AU - Kumar, Ajay

AU - Bassi, Filippo M.

AU - Paux, Etienne

AU - Al-Azzam, Omar

AU - de Jimenez, Monika M.

AU - Denton, Anne M.

AU - Gu, Yong Q.

AU - Huttner, Eric

AU - Kilian, Andrzej

AU - Kumar, Sachin

AU - Goyal, Aakash

AU - Iqbal, Muhammad J.

AU - Tiwari, Vijay K.

AU - Dogramaci, Munevver

AU - Balyan, Harindra S.

AU - Dhaliwal, Harcharan S.

AU - Gupta, Pushpendra K.

AU - Randhawa, Gursharn S.

AU - Feuillet, Catherine

AU - Pawlowski, Wojciech P.

AU - Kianian, Shahryar F.

N1 - Funding Information: The authors wish to thank Justin Hegstad and Allen Peckrul for assistance in the development of RH panel and capable technical support throughout the research; Dr. Matthew Hayden (VABC, Melbourne, AUS) for precious contributions in designing the DEASY control marker; Dr. Nellye Cubizolles (INRA, Clermont Ferrand, FR) for technical support in the use of cfp markers; Dr. Cyrille Saintenac (INRA, Clermont Ferrand, FR) and his collaborators for making publicly available their excellent work. This work was supported by funding from the National Science Foundation, Plant Genome Research Program (NSF-PGRP) grant No. IOS-0822100 to SFK. Additional support from the NSF-PGRP Developing Country Collaboration aided the assistance of student interns A.Kumar, S.K., A.G., and V.T.; F.M.B was partially supported by Program Master and Back Regione Autonoma della Sardegna and Monsanto Beachell-Borlaug International Scholarship.

PY - 2012/7/24

Y1 - 2012/7/24

N2 - Background: The uneven distribution of recombination across the length of chromosomes results in inaccurate estimates of genetic to physical distances. In wheat (Triticum aestivum L.) chromosome 3B, it has been estimated that 90% of the cross over events occur in distal sub-telomeric regions representing 40% of the chromosome. Radiation hybrid (RH) mapping which does not rely on recombination is a strategy to map genomes and has been widely employed in animal species and more recently in some plants. RH maps have been proposed to provide i) higher and ii) more uniform resolution than genetic maps, and iii) to be independent of the distribution patterns observed for meiotic recombination. An in vivo RH panel was generated for mapping chromosome 3B of wheat in an attempt to provide a complete scaffold for this ~1 Gb segment of the genome and compare the resolution to previous genetic maps.Results: A high density RH map with 541 marker loci anchored to chromosome 3B spanning a total distance of 1871.9 cR was generated. Detailed comparisons with a genetic map of similar quality confirmed that i) the overall resolution of the RH map was 10.5 fold higher and ii) six fold more uniform. A significant interaction (r = 0.879 at p = 0.01) was observed between the DNA repair mechanism and the distribution of crossing-over events. This observation could be explained by accepting the possibility that the DNA repair mechanism in somatic cells is affected by the chromatin state in a way similar to the effect that chromatin state has on recombination frequencies in gametic cells.Conclusions: The RH data presented here support for the first time in vivo the hypothesis of non-casual interaction between recombination hot-spots and DNA repair. Further, two major hypotheses are presented on how chromatin compactness could affect the DNA repair mechanism. Since the initial RH application 37 years ago, we were able to show for the first time that the iii) third hypothesis of RH mapping might not be entirely correct.

AB - Background: The uneven distribution of recombination across the length of chromosomes results in inaccurate estimates of genetic to physical distances. In wheat (Triticum aestivum L.) chromosome 3B, it has been estimated that 90% of the cross over events occur in distal sub-telomeric regions representing 40% of the chromosome. Radiation hybrid (RH) mapping which does not rely on recombination is a strategy to map genomes and has been widely employed in animal species and more recently in some plants. RH maps have been proposed to provide i) higher and ii) more uniform resolution than genetic maps, and iii) to be independent of the distribution patterns observed for meiotic recombination. An in vivo RH panel was generated for mapping chromosome 3B of wheat in an attempt to provide a complete scaffold for this ~1 Gb segment of the genome and compare the resolution to previous genetic maps.Results: A high density RH map with 541 marker loci anchored to chromosome 3B spanning a total distance of 1871.9 cR was generated. Detailed comparisons with a genetic map of similar quality confirmed that i) the overall resolution of the RH map was 10.5 fold higher and ii) six fold more uniform. A significant interaction (r = 0.879 at p = 0.01) was observed between the DNA repair mechanism and the distribution of crossing-over events. This observation could be explained by accepting the possibility that the DNA repair mechanism in somatic cells is affected by the chromatin state in a way similar to the effect that chromatin state has on recombination frequencies in gametic cells.Conclusions: The RH data presented here support for the first time in vivo the hypothesis of non-casual interaction between recombination hot-spots and DNA repair. Further, two major hypotheses are presented on how chromatin compactness could affect the DNA repair mechanism. Since the initial RH application 37 years ago, we were able to show for the first time that the iii) third hypothesis of RH mapping might not be entirely correct.

KW - Chromatin

KW - Deletion mutant

KW - Gamma radiation

KW - Non homologous end joining

KW - Physical mapping

KW - Radiation hybrid

KW - Wheat chromosome 3B

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DNA repair and crossing over favor similar chromosome regions as discovered in radiation hybrid of Triticum

Abstract

Bibliographical note

Keywords

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