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Arabidopsis PCH2 Mediates Meiotic Chromosome Remodeling and Maturation of Crossovers.

Lambing C, Osman K, Nuntasoontorn K, West A, Higgins JD, Copenhaver GP, Yang J, Armstrong SJ, Mechtler K, Roitinger E, Franklin FC - PLoS Genet. (2015)

Bottom Line: We show that the axis associated protein ASY1 is depleted during zygotene concomitant with synaptonemal complex (SC) formation.This leads to a reduction in COs and a failure to form COs between some homologous chromosome pairs leading to univalent chromosomes at metaphase I.Together these data indicate that the axis remodelling defect in Atpch2 disrupts normal patterned formation of COs.

View Article: PubMed Central - PubMed

Affiliation: School of Biosciences, University of Birmingham, Edgbaston, Birmingham, United Kingdom.

ABSTRACT
Meiotic chromosomes are organized into linear looped chromatin arrays by a protein axis localized along the loop-bases. Programmed remodelling of the axis occurs during prophase I of meiosis. Structured illumination microscopy (SIM) has revealed dynamic changes in the chromosome axis in Arabidopsis thaliana and Brassica oleracea. We show that the axis associated protein ASY1 is depleted during zygotene concomitant with synaptonemal complex (SC) formation. Study of an Atpch2 mutant demonstrates this requires the conserved AAA+ ATPase, PCH2, which localizes to the sites of axis remodelling. Loss of PCH2 leads to a failure to deplete ASY1 from the axes and compromizes SC polymerisation. Immunolocalization of recombination proteins in Atpch2 indicates that recombination initiation and CO designation during early prophase I occur normally. Evidence suggests that CO interference is initially functional in the mutant but there is a defect in CO maturation following designation. This leads to a reduction in COs and a failure to form COs between some homologous chromosome pairs leading to univalent chromosomes at metaphase I. Genetic analysis reveals that CO distribution is also affected in some chromosome regions. Together these data indicate that the axis remodelling defect in Atpch2 disrupts normal patterned formation of COs.

No MeSH data available.


Related in: MedlinePlus

Recombination frequency and chiasma distribution in Atpch2-1.(A) Genetic map distance of four distinct intervals on chromosome 5 and two intervals on chromosome 2 in wild type Arabidopsis and Atpch2-1 mutant. Black stars represent a statistical difference in the genetic map distance between wild type and mutant. P value is indicated on the graph when the genetic map distance of an interval is not statistically different between wild type and mutant. Error bars represent the standard error of the mean. (B) Three pairs of adjacent intervals l2fg, I5ab and I5cd were used to estimate genetic CO interference for wild type and Atpch2-1 mutant. CO interference ratio for each pair of intervals is indicated in the table and P value is shown in parentheses. (C) Observed (solid line) and Poisson-predicted (dotted line) distributions of chiasma numbers per cell for wild type (black circle) and Atpch2-1 mutant (white triangle).
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pgen.1005372.g005: Recombination frequency and chiasma distribution in Atpch2-1.(A) Genetic map distance of four distinct intervals on chromosome 5 and two intervals on chromosome 2 in wild type Arabidopsis and Atpch2-1 mutant. Black stars represent a statistical difference in the genetic map distance between wild type and mutant. P value is indicated on the graph when the genetic map distance of an interval is not statistically different between wild type and mutant. Error bars represent the standard error of the mean. (B) Three pairs of adjacent intervals l2fg, I5ab and I5cd were used to estimate genetic CO interference for wild type and Atpch2-1 mutant. CO interference ratio for each pair of intervals is indicated in the table and P value is shown in parentheses. (C) Observed (solid line) and Poisson-predicted (dotted line) distributions of chiasma numbers per cell for wild type (black circle) and Atpch2-1 mutant (white triangle).

Mentions: The cytological analysis (see earlier) suggested a defect in CO formation in Atpch2 mutants. To further examine the recombination phenotype of Atpch2-1 we used the fluorescent-tagged-line (FTL) system [49,50] which relies on the segregation of three genetically linked transgenic markers, each encoding a distinct pollen-specific fluorescent protein expressed post-meiotically. The FTLs are in a qrt1-2 mutant background which prevents the separation of the gametes and facilitates the visualisation of the meiotic recombination events that have occurred between the transgenic markers in the tetrad pollen [51,52]. Three pairs of adjacent genetic intervals, one on each arm of chromosome 5 and another on chromosome 2 were examined (S14 Fig). This revealed that the genetic map distance determined using the Perkins mapping equation [53] in the adjacent intervals I5c and I5d was not significantly affected by the Atpch2-1 mutation (I5c wild type 6.1 cM v Atpch2-1 6.8 cM; P = 0.17; I5d wild type 5.5 cM v Atpch2-1 6.0 cM; P = 0.28) (Fig 5A). However, interval I5a showed a significant decrease in recombination frequency in the presence of Atpch2-1 (15.1 cM) compared to wild type (27.7 cM; P < 0.001), whereas the map distance in interval I5b exhibited a significant increase from 17.3 cM in wild type to 22.3 cM in the mutant (P < 0.001) (Fig 5A). A significant increase in map distance was observed in intervals l2f and l2g in the presence of the Atpch2-1 mutation (l2f wild type 6.1 cM / Atpch2-1 8.0 cM P < 0.001; l2g wild type 5.1 cM / Atpch2-1 7.1 cM P < 0.001) (Fig 5A).


Arabidopsis PCH2 Mediates Meiotic Chromosome Remodeling and Maturation of Crossovers.

Lambing C, Osman K, Nuntasoontorn K, West A, Higgins JD, Copenhaver GP, Yang J, Armstrong SJ, Mechtler K, Roitinger E, Franklin FC - PLoS Genet. (2015)

Recombination frequency and chiasma distribution in Atpch2-1.(A) Genetic map distance of four distinct intervals on chromosome 5 and two intervals on chromosome 2 in wild type Arabidopsis and Atpch2-1 mutant. Black stars represent a statistical difference in the genetic map distance between wild type and mutant. P value is indicated on the graph when the genetic map distance of an interval is not statistically different between wild type and mutant. Error bars represent the standard error of the mean. (B) Three pairs of adjacent intervals l2fg, I5ab and I5cd were used to estimate genetic CO interference for wild type and Atpch2-1 mutant. CO interference ratio for each pair of intervals is indicated in the table and P value is shown in parentheses. (C) Observed (solid line) and Poisson-predicted (dotted line) distributions of chiasma numbers per cell for wild type (black circle) and Atpch2-1 mutant (white triangle).
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pgen.1005372.g005: Recombination frequency and chiasma distribution in Atpch2-1.(A) Genetic map distance of four distinct intervals on chromosome 5 and two intervals on chromosome 2 in wild type Arabidopsis and Atpch2-1 mutant. Black stars represent a statistical difference in the genetic map distance between wild type and mutant. P value is indicated on the graph when the genetic map distance of an interval is not statistically different between wild type and mutant. Error bars represent the standard error of the mean. (B) Three pairs of adjacent intervals l2fg, I5ab and I5cd were used to estimate genetic CO interference for wild type and Atpch2-1 mutant. CO interference ratio for each pair of intervals is indicated in the table and P value is shown in parentheses. (C) Observed (solid line) and Poisson-predicted (dotted line) distributions of chiasma numbers per cell for wild type (black circle) and Atpch2-1 mutant (white triangle).
Mentions: The cytological analysis (see earlier) suggested a defect in CO formation in Atpch2 mutants. To further examine the recombination phenotype of Atpch2-1 we used the fluorescent-tagged-line (FTL) system [49,50] which relies on the segregation of three genetically linked transgenic markers, each encoding a distinct pollen-specific fluorescent protein expressed post-meiotically. The FTLs are in a qrt1-2 mutant background which prevents the separation of the gametes and facilitates the visualisation of the meiotic recombination events that have occurred between the transgenic markers in the tetrad pollen [51,52]. Three pairs of adjacent genetic intervals, one on each arm of chromosome 5 and another on chromosome 2 were examined (S14 Fig). This revealed that the genetic map distance determined using the Perkins mapping equation [53] in the adjacent intervals I5c and I5d was not significantly affected by the Atpch2-1 mutation (I5c wild type 6.1 cM v Atpch2-1 6.8 cM; P = 0.17; I5d wild type 5.5 cM v Atpch2-1 6.0 cM; P = 0.28) (Fig 5A). However, interval I5a showed a significant decrease in recombination frequency in the presence of Atpch2-1 (15.1 cM) compared to wild type (27.7 cM; P < 0.001), whereas the map distance in interval I5b exhibited a significant increase from 17.3 cM in wild type to 22.3 cM in the mutant (P < 0.001) (Fig 5A). A significant increase in map distance was observed in intervals l2f and l2g in the presence of the Atpch2-1 mutation (l2f wild type 6.1 cM / Atpch2-1 8.0 cM P < 0.001; l2g wild type 5.1 cM / Atpch2-1 7.1 cM P < 0.001) (Fig 5A).

Bottom Line: We show that the axis associated protein ASY1 is depleted during zygotene concomitant with synaptonemal complex (SC) formation.This leads to a reduction in COs and a failure to form COs between some homologous chromosome pairs leading to univalent chromosomes at metaphase I.Together these data indicate that the axis remodelling defect in Atpch2 disrupts normal patterned formation of COs.

View Article: PubMed Central - PubMed

Affiliation: School of Biosciences, University of Birmingham, Edgbaston, Birmingham, United Kingdom.

ABSTRACT
Meiotic chromosomes are organized into linear looped chromatin arrays by a protein axis localized along the loop-bases. Programmed remodelling of the axis occurs during prophase I of meiosis. Structured illumination microscopy (SIM) has revealed dynamic changes in the chromosome axis in Arabidopsis thaliana and Brassica oleracea. We show that the axis associated protein ASY1 is depleted during zygotene concomitant with synaptonemal complex (SC) formation. Study of an Atpch2 mutant demonstrates this requires the conserved AAA+ ATPase, PCH2, which localizes to the sites of axis remodelling. Loss of PCH2 leads to a failure to deplete ASY1 from the axes and compromizes SC polymerisation. Immunolocalization of recombination proteins in Atpch2 indicates that recombination initiation and CO designation during early prophase I occur normally. Evidence suggests that CO interference is initially functional in the mutant but there is a defect in CO maturation following designation. This leads to a reduction in COs and a failure to form COs between some homologous chromosome pairs leading to univalent chromosomes at metaphase I. Genetic analysis reveals that CO distribution is also affected in some chromosome regions. Together these data indicate that the axis remodelling defect in Atpch2 disrupts normal patterned formation of COs.

No MeSH data available.


Related in: MedlinePlus