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Modulating crossover positioning by introducing large structural changes in chromosomes.

Ederveen A, Lai Y, van Driel MA, Gerats T, Peters JL - BMC Genomics (2015)

Bottom Line: Interestingly, two independent cases of induced structural changes in the same chromosomal interval were found on both chromosomes 1 and 2.In contrast, deletions in chromosome arms carrying the nucleolar organizing region did not change recombination frequencies in the remainder of those chromosomes.When taken together, these observations show that changes in the physical structure of the chromosome can have large effects on the positioning of COs within that chromosome.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Plant Physiology, Radboud University Nijmegen, Institute for Water and Wetland Research (IWWR), Heyendaalseweg 135, 6525 AJ, Nijmegen, The Netherlands. a.ederveen@science.ru.nl.

ABSTRACT

Background: Crossing over assures the correct segregation of the homologous chromosomes to both poles of the dividing meiocyte. This exchange of DNA creates new allelic combinations thus increasing the genetic variation present in offspring. Crossovers are not uniformly distributed along chromosomes; rather there are preferred locations where they may take place. The positioning of crossovers is known to be influenced by both exogenous and endogenous factors as well as structural features inherent to the chromosome itself. We have introduced large structural changes into Arabidopsis chromosomes and report their effects on crossover positioning.

Results: The introduction of large deletions and putative inversions silenced recombination over the length of the structural change. In the majority of cases analyzed, the total recombination frequency over the chromosomes was unchanged. The loss of crossovers at the sites of structural change was compensated for by increases in recombination frequencies elsewhere on the chromosomes, mostly in single intervals of one to three megabases in size. Interestingly, two independent cases of induced structural changes in the same chromosomal interval were found on both chromosomes 1 and 2. In both cases, compensatory increases in recombination frequencies were of similar strength and took place in the same chromosome region. In contrast, deletions in chromosome arms carrying the nucleolar organizing region did not change recombination frequencies in the remainder of those chromosomes.

Conclusions: When taken together, these observations show that changes in the physical structure of the chromosome can have large effects on the positioning of COs within that chromosome. Moreover, different reactions to induced structural changes are observed between and within chromosomes. However, the similarity in reaction observed when looking at chromosomes carrying similar changes suggests a direct causal relation between induced change and observed reaction.

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Recombination frequencies and allele frequencies of Arabidopsis chromosomes (I, II and IV) carrying large chromosomal deletions or putative inversions. Sections a, c and e show RF over the length of the respective deletion (Δ) or putative inversion (↔) chromosomes (M2→). In the M2 chromosome bars blue sections indicate heterozygous presence of SNPs while red sections show regions of LOH indicating the presence of deletions. Sections b, d and f show col-0 allele frequency over this same length of chromosome. Sections g, h and I show average recombination frequency over the whole chromosomes, their North and South arms. The legends specify the positions of identified deletions and/or inferred putative inversions carried on the respective chromosomes. Black graphs and bars represent data from 3 independent control individuals. Other colors refer to data collected from individual aberrant chromosomes. To be noted in these figures are: zero RF at positions of deletions or putative inversions; upregulations of RF up to 300% of WT in affected chromosomes; Col-0 allele frequency at 0,5 at sites of deletions; variable averages of RF in North and South arms of chromosomes while Whole chromosome RF is mostly comparable to control levels; variable positioning of upregulation in respect to aberration and absence of effects in chromosome 2 and 4 North arm deletions.
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Fig2: Recombination frequencies and allele frequencies of Arabidopsis chromosomes (I, II and IV) carrying large chromosomal deletions or putative inversions. Sections a, c and e show RF over the length of the respective deletion (Δ) or putative inversion (↔) chromosomes (M2→). In the M2 chromosome bars blue sections indicate heterozygous presence of SNPs while red sections show regions of LOH indicating the presence of deletions. Sections b, d and f show col-0 allele frequency over this same length of chromosome. Sections g, h and I show average recombination frequency over the whole chromosomes, their North and South arms. The legends specify the positions of identified deletions and/or inferred putative inversions carried on the respective chromosomes. Black graphs and bars represent data from 3 independent control individuals. Other colors refer to data collected from individual aberrant chromosomes. To be noted in these figures are: zero RF at positions of deletions or putative inversions; upregulations of RF up to 300% of WT in affected chromosomes; Col-0 allele frequency at 0,5 at sites of deletions; variable averages of RF in North and South arms of chromosomes while Whole chromosome RF is mostly comparable to control levels; variable positioning of upregulation in respect to aberration and absence of effects in chromosome 2 and 4 North arm deletions.

Mentions: BC1 generations (90 individuals) of the selected 16 M2Δs and those of three control individuals were genotyped for 66 SNP markers spread over the genome at ~15-20 cM intervals. In all 20 deletion chromosomes examined except one, Col-0 allele frequency in the BC generation was at 0.5% at the deletion site (Figure 2 b, d, f and Additional file 2: b, d, f). Col-0 allele frequencies gradually drop back to 0.25 as more recombination events take place with distance to the deletion. This shows that of chromosomes that have incurred substantial deletions, only those parts that have recombined with the non-deletion chromosome can be transmitted to the next generation whereas those chromosomes that are missing substantial amounts of DNA are not found in the backcross. However, one exception to this rule was observed in M2Δ-9 where a region of LOH (nsnp = 14) measuring 0.3 Mb was present adjacent to the centromere (11.4-11.7 Mb) of chromosome 5 (Additional file 2: V-A e, f). While we do not have data on the BC1 genotype composition at this location, the Col-0 allele frequency of chromosome 5 in the backcross of this individual was ~0.25 at all measured locations. This observation suggests that the absence of this 0.3 Mb stretch of DNA did not inhibit transmission of this chromosome to the next generation. We propose that the vicinity to the centromere of this relatively small deletion may have masked it from selection mechanisms.Figure 2


Modulating crossover positioning by introducing large structural changes in chromosomes.

Ederveen A, Lai Y, van Driel MA, Gerats T, Peters JL - BMC Genomics (2015)

Recombination frequencies and allele frequencies of Arabidopsis chromosomes (I, II and IV) carrying large chromosomal deletions or putative inversions. Sections a, c and e show RF over the length of the respective deletion (Δ) or putative inversion (↔) chromosomes (M2→). In the M2 chromosome bars blue sections indicate heterozygous presence of SNPs while red sections show regions of LOH indicating the presence of deletions. Sections b, d and f show col-0 allele frequency over this same length of chromosome. Sections g, h and I show average recombination frequency over the whole chromosomes, their North and South arms. The legends specify the positions of identified deletions and/or inferred putative inversions carried on the respective chromosomes. Black graphs and bars represent data from 3 independent control individuals. Other colors refer to data collected from individual aberrant chromosomes. To be noted in these figures are: zero RF at positions of deletions or putative inversions; upregulations of RF up to 300% of WT in affected chromosomes; Col-0 allele frequency at 0,5 at sites of deletions; variable averages of RF in North and South arms of chromosomes while Whole chromosome RF is mostly comparable to control levels; variable positioning of upregulation in respect to aberration and absence of effects in chromosome 2 and 4 North arm deletions.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
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getmorefigures.php?uid=PMC4359564&req=5

Fig2: Recombination frequencies and allele frequencies of Arabidopsis chromosomes (I, II and IV) carrying large chromosomal deletions or putative inversions. Sections a, c and e show RF over the length of the respective deletion (Δ) or putative inversion (↔) chromosomes (M2→). In the M2 chromosome bars blue sections indicate heterozygous presence of SNPs while red sections show regions of LOH indicating the presence of deletions. Sections b, d and f show col-0 allele frequency over this same length of chromosome. Sections g, h and I show average recombination frequency over the whole chromosomes, their North and South arms. The legends specify the positions of identified deletions and/or inferred putative inversions carried on the respective chromosomes. Black graphs and bars represent data from 3 independent control individuals. Other colors refer to data collected from individual aberrant chromosomes. To be noted in these figures are: zero RF at positions of deletions or putative inversions; upregulations of RF up to 300% of WT in affected chromosomes; Col-0 allele frequency at 0,5 at sites of deletions; variable averages of RF in North and South arms of chromosomes while Whole chromosome RF is mostly comparable to control levels; variable positioning of upregulation in respect to aberration and absence of effects in chromosome 2 and 4 North arm deletions.
Mentions: BC1 generations (90 individuals) of the selected 16 M2Δs and those of three control individuals were genotyped for 66 SNP markers spread over the genome at ~15-20 cM intervals. In all 20 deletion chromosomes examined except one, Col-0 allele frequency in the BC generation was at 0.5% at the deletion site (Figure 2 b, d, f and Additional file 2: b, d, f). Col-0 allele frequencies gradually drop back to 0.25 as more recombination events take place with distance to the deletion. This shows that of chromosomes that have incurred substantial deletions, only those parts that have recombined with the non-deletion chromosome can be transmitted to the next generation whereas those chromosomes that are missing substantial amounts of DNA are not found in the backcross. However, one exception to this rule was observed in M2Δ-9 where a region of LOH (nsnp = 14) measuring 0.3 Mb was present adjacent to the centromere (11.4-11.7 Mb) of chromosome 5 (Additional file 2: V-A e, f). While we do not have data on the BC1 genotype composition at this location, the Col-0 allele frequency of chromosome 5 in the backcross of this individual was ~0.25 at all measured locations. This observation suggests that the absence of this 0.3 Mb stretch of DNA did not inhibit transmission of this chromosome to the next generation. We propose that the vicinity to the centromere of this relatively small deletion may have masked it from selection mechanisms.Figure 2

Bottom Line: Interestingly, two independent cases of induced structural changes in the same chromosomal interval were found on both chromosomes 1 and 2.In contrast, deletions in chromosome arms carrying the nucleolar organizing region did not change recombination frequencies in the remainder of those chromosomes.When taken together, these observations show that changes in the physical structure of the chromosome can have large effects on the positioning of COs within that chromosome.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Plant Physiology, Radboud University Nijmegen, Institute for Water and Wetland Research (IWWR), Heyendaalseweg 135, 6525 AJ, Nijmegen, The Netherlands. a.ederveen@science.ru.nl.

ABSTRACT

Background: Crossing over assures the correct segregation of the homologous chromosomes to both poles of the dividing meiocyte. This exchange of DNA creates new allelic combinations thus increasing the genetic variation present in offspring. Crossovers are not uniformly distributed along chromosomes; rather there are preferred locations where they may take place. The positioning of crossovers is known to be influenced by both exogenous and endogenous factors as well as structural features inherent to the chromosome itself. We have introduced large structural changes into Arabidopsis chromosomes and report their effects on crossover positioning.

Results: The introduction of large deletions and putative inversions silenced recombination over the length of the structural change. In the majority of cases analyzed, the total recombination frequency over the chromosomes was unchanged. The loss of crossovers at the sites of structural change was compensated for by increases in recombination frequencies elsewhere on the chromosomes, mostly in single intervals of one to three megabases in size. Interestingly, two independent cases of induced structural changes in the same chromosomal interval were found on both chromosomes 1 and 2. In both cases, compensatory increases in recombination frequencies were of similar strength and took place in the same chromosome region. In contrast, deletions in chromosome arms carrying the nucleolar organizing region did not change recombination frequencies in the remainder of those chromosomes.

Conclusions: When taken together, these observations show that changes in the physical structure of the chromosome can have large effects on the positioning of COs within that chromosome. Moreover, different reactions to induced structural changes are observed between and within chromosomes. However, the similarity in reaction observed when looking at chromosomes carrying similar changes suggests a direct causal relation between induced change and observed reaction.

Show MeSH
Related in: MedlinePlus