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3. MSH2 shapes the meiotic crossover landscape in relation to interhomolog polymorphism in Arabidopsis

Author

Blackwell, Alexander R, Dluzewska, Julia, Szymanska‐Lejman, Maja, Desjardins, Stuart, Tock, Andrew J, Kbiri, Nadia, Lambing, Christophe, Lawrence, Emma J, Bieluszewski, Tomasz, Rowan, Beth, Higgins, James D, Ziolkowski, Piotr A, and Henderson, Ian R

Subjects
Biotechnology, Genetics, Arabidopsis, Arabidopsis Proteins, Cell Cycle, Chromatin, Chromosomes, Crossing Over, Genetic, DNA Repair, DNA Replication, Homologous Recombination, Meiosis, MutS Homolog 2 Protein, Mutagenesis, Polymorphism, Genetic, Polymorphism, Single Nucleotide, Arabidopsis, MSH2, crossover, meiosis, polymorphism, Biological Sciences, Information and Computing Sciences, Medical and Health Sciences, Developmental Biology
Abstract

During meiosis, DNA double-strand breaks undergo interhomolog repair to yield crossovers between homologous chromosomes. To investigate how interhomolog sequence polymorphism affects crossovers, we sequenced multiple recombinant populations of the model plant Arabidopsis thaliana. Crossovers were elevated in the diverse pericentromeric regions, showing a local preference for polymorphic regions. We provide evidence that crossover association with elevated diversity is mediated via the Class I crossover formation pathway, although very high levels of diversity suppress crossovers. Interhomolog polymorphism causes mismatches in recombining molecules, which can be detected by MutS homolog (MSH) mismatch repair protein heterodimers. Therefore, we mapped crossovers in a msh2 mutant, defective in mismatch recognition, using multiple hybrid backgrounds. Although total crossover numbers were unchanged in msh2 mutants, recombination was remodelled from the diverse pericentromeres towards the less-polymorphic sub-telomeric regions. Juxtaposition of megabase heterozygous and homozygous regions causes crossover remodelling towards the heterozygous regions in wild type Arabidopsis, but not in msh2 mutants. Immunostaining showed that MSH2 protein accumulates on meiotic chromosomes during prophase I, consistent with MSH2 regulating meiotic recombination. Our results reveal a pro-crossover role for MSH2 in regions of higher sequence diversity in A. thaliana.

Published
2020

6. Kinetochore and ionomic adaptation to whole genome duplication

Author

Bray, Sian M, primary, Hamala, Tuomas, additional, Zhou, Min, additional, Busoms, Silvia, additional, Fischer, Sina, additional, Desjardins, Stuart D, additional, Mandakova, Terezie, additional, Moore, Chris, additional, Mathers, Thomas C, additional, Cowan, Laura, additional, Monnahan, Patrick, additional, Koch, Jordan, additional, Wolf, Eva M, additional, Lysak, Martin A, additional, Kolar, Filip, additional, Higgins, James D, additional, Koch, Marcus A, additional, and Yant, Levi, additional

Published
2023
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13. The coordinated regulation of early meiotic stages is dominated by non‐coding RNAs and stage‐specific transcription in wheat

Author

Jiang, Yunfei, primary, N'Diaye, Amidou, additional, Koh, Chu Shin, additional, Quilichini, Teagen D., additional, Shunmugam, Arun S. K., additional, Kirzinger, Morgan W., additional, Konkin, David, additional, Bekkaoui, Yasmina, additional, Sari, Ehsan, additional, Pasha, Asher, additional, Esteban, Eddi, additional, Provart, Nicholas J., additional, Higgins, James D., additional, Rozwadowski, Kevin, additional, Sharpe, Andrew G., additional, Pozniak, Curtis J., additional, and Kagale, Sateesh, additional

Published
2023
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19. Identification, characterization, and rescue of CRISPR/Cas9 generated wheat SPO11-1 mutants

Author

Hyde, Lucy, Osman, Kim, Winfield, Mark, Sanchez-Moran, Eugenio, Higgins, James D, Henderson, Ian R, Sparks, Caroline, Franklin, F Chris H, Edwards, Keith J, Winfield, Mark [0000-0002-5078-4806], and Apollo - University of Cambridge Repository

Subjects
Plant Breeding, Meiosis, SPO11-1, wheat CRISPR/Cas9, genome editing, CRISPR-Cas Systems, Triticum, Chromosomes, wheat transformation
Abstract

Increasing crop yields through plant breeding is time consuming and laborious, with the generation of novel combinations of alleles being limited by chromosomal linkage blocks and linkage-drag. Meiotic recombination is essential to create novel genetic variation via the reshuffling of parental alleles. The exchange of genetic information between homologous chromosomes occurs at crossover (CO) sites but CO frequency is often low and unevenly distributed. This bias creates the problem of linkage-drag in recombination 'cold' regions, where undesirable variation remains linked to useful traits. In plants, programmed meiosis-specific DNA double-strand breaks, catalysed by the SPO11 complex, initiate the recombination pathway, although only ~5% result in the formation of COs. To study the role of SPO11-1 in wheat meiosis, and as a prelude to manipulation, we used CRISPR/Cas9 to generate edits in all three SPO11-1 homoeologues of hexaploid wheat. Characterization of progeny lines shows plants deficient in all six SPO11-1 copies fail to undergo chromosome synapsis, lack COs and are sterile. In contrast, lines carrying a single copy of any one of the three wild-type homoeologues are phenotypically indistinguishable from unedited plants both in terms of vegetative growth and fertility. However, cytogenetic analysis of the edited plants suggests that homoeologues differ in their ability to generate COs and in the dynamics of synapsis. In addition, we show that the transformation of wheat mutants carrying six edited copies of SPO11-1 with the TaSPO11-1B gene, restores synapsis, CO formation, and fertility and hence opens a route to modifying recombination in this agronomically important crop.

Published
2022
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26. Identification, characterization, and rescue of CRISPR/Cas9 generated wheat SPO11‐1 mutants.

Author

Hyde, Lucy, Osman, Kim, Winfield, Mark, Sanchez‐Moran, Eugenio, Higgins, James D., Henderson, Ian R., Sparks, Caroline, Franklin, F. Chris H., and Edwards, Keith J.

Subjects
CRISPRS, DOUBLE-strand DNA breaks, HOMOLOGOUS chromosomes, WHEAT, PLANT breeding
Abstract

Summary: Increasing crop yields through plant breeding is time consuming and laborious, with the generation of novel combinations of alleles being limited by chromosomal linkage blocks and linkage‐drag. Meiotic recombination is essential to create novel genetic variation via the reshuffling of parental alleles. The exchange of genetic information between homologous chromosomes occurs at crossover (CO) sites but CO frequency is often low and unevenly distributed. This bias creates the problem of linkage‐drag in recombination 'cold' regions, where undesirable variation remains linked to useful traits. In plants, programmed meiosis‐specific DNA double‐strand breaks, catalysed by the SPO11 complex, initiate the recombination pathway, although only ~5% result in the formation of COs. To study the role of SPO11‐1 in wheat meiosis, and as a prelude to manipulation, we used CRISPR/Cas9 to generate edits in all three SPO11‐1 homoeologues of hexaploid wheat. Characterization of progeny lines shows plants deficient in all six SPO11‐1 copies fail to undergo chromosome synapsis, lack COs and are sterile. In contrast, lines carrying a single copy of any one of the three wild‐type homoeologues are phenotypically indistinguishable from unedited plants both in terms of vegetative growth and fertility. However, cytogenetic analysis of the edited plants suggests that homoeologues differ in their ability to generate COs and in the dynamics of synapsis. In addition, we show that the transformation of wheat mutants carrying six edited copies of SPO11‐1 with the TaSPO11‐1B gene, restores synapsis, CO formation, and fertility and hence opens a route to modifying recombination in this agronomically important crop. [ABSTRACT FROM AUTHOR]

Published
2023
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29. Interacting Genomic Landscapes of REC8-Cohesin, Chromatin, and Meiotic Recombination in Arabidopsis

Author

Lambing, Christophe, Tock, Andrew J, Topp, Stephanie D, Choi, Kyuha, Kuo, Pallas C, Zhao, Xiaohui, Osman, Kim, Higgins, James D, Franklin, F Chris H, Henderson, Ian R, Lambing, Christophe [0000-0001-5218-4217], Tock, Andrew J [0000-0002-6590-8314], Topp, Stephanie D [0000-0001-9464-332X], Choi, Kyuha [0000-0002-4072-3807], Kuo, Pallas C [0000-0001-5435-2026], Zhao, Xiaohui [0000-0001-9922-2815], Osman, Kim [0000-0002-0282-4148], Higgins, James D [0000-0001-6027-8678], Franklin, F Chris H [0000-0003-3507-722X], Henderson, Ian R [0000-0001-5066-1489], and Apollo - University of Cambridge Repository

Subjects
0106 biological sciences, 0301 basic medicine, Heterochromatin, Chromosomal Proteins, Non-Histone, Arabidopsis, Cell Cycle Proteins, Plant Science, Saccharomyces cerevisiae, Biology, 01 natural sciences, Chromosomes, Plant, Chromosomal crossover, 03 medical and health sciences, Suppression, Genetic, Meiosis, Histone methylation, Schizosaccharomyces, Sister chromatids, Crossing Over, Genetic, Homologous Recombination, Cohesin, Arabidopsis Proteins, fungi, Synapsis, Cell Biology, DNA Methylation, Chromatin, Cell biology, Nucleosomes, 030104 developmental biology, Mutation, DNA Transposable Elements, Genome, Plant, 010606 plant biology & botany
Abstract

Meiosis recombines genetic variation and influences eukaryote genome evolution. During meiosis, DNA double-strand breaks (DSBs) enter interhomolog repair to yield crossovers and noncrossovers. DSB repair occurs as replicated sister chromatids are connected to a polymerized axis. Cohesin rings containing the REC8 kleisin subunit bind sister chromatids and anchor chromosomes to the axis. Here, we report the genomic landscape of REC8 using chromatin immunoprecipitation sequencing (ChIP-seq) in Arabidopsis (Arabidopsis thaliana). REC8 associates with regions of high nucleosome occupancy in multiple chromatin states, including histone methylation at H3K4 (expressed genes), H3K27 (silent genes), and H3K9 (silent transposons). REC8 enrichment is associated with suppression of meiotic DSBs and crossovers at the chromosome and fine scales. As REC8 enrichment is greatest in transposon-dense heterochromatin, we repeated ChIP-seq in kyp suvh5 suvh6 H3K9me2 mutants. Surprisingly, REC8 enrichment is maintained in kyp suvh5 suvh6 heterochromatin and no defects in centromeric cohesion were observed. REC8 occupancy within genes anti-correlates with transcription and is reduced in COPIA transposons that reactivate expression in kyp suvh5 suvh6. Abnormal axis structures form in rec8 that recruit DSB-associated protein foci and undergo synapsis, which is followed by chromosome fragmentation. Therefore, REC8 occupancy correlates with multiple chromatin states and is required to organize meiotic chromosome architecture and interhomolog recombination.

Published
2020

35. The Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: Evidence for two classes of recombination in Arabidopsis

Author

Higgins, James D., Arnstrong, Susan J., Franklin, Christopher, F., and Jones, Gareth H.

Subjects
Chromosomes -- Research, Fluorescent antibody technique -- Methods, Immunofluorescence -- Methods, Arabidopsis -- Research, Biological sciences
Abstract

The identification and characterization of the Arabidopsis homologue of MSH4 (AtMSH4) is reported which can only be detected in floral tissues, consistent with a role in reproduction. Immunofluorescence studies indicate that its expression is limited to early meiotic prophase I, preceding the synapsis of homologous chromosomes.

Published
2004

37. MSH 2 shapes the meiotic crossover landscape in relation to interhomolog polymorphism in Arabidopsis

Author

Blackwell, Alexander R, primary, Dluzewska, Julia, additional, Szymanska‐Lejman, Maja, additional, Desjardins, Stuart, additional, Tock, Andrew J, additional, Kbiri, Nadia, additional, Lambing, Christophe, additional, Lawrence, Emma J, additional, Bieluszewski, Tomasz, additional, Rowan, Beth, additional, Higgins, James D, additional, Ziolkowski, Piotr A, additional, and Henderson, Ian R, additional

Published
2020
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46. Analysis of the recombination landscape of hexaploid bread wheat reveals genes controlling recombination and gene conversion frequency

Author

Gardiner, Laura-Jayne, primary, Wingen, Luzie U., additional, Bailey, Paul, additional, Joynson, Ryan, additional, Brabbs, Thomas, additional, Wright, Jonathan, additional, Higgins, James D., additional, Hall, Neil, additional, Griffiths, Simon, additional, Clavijo, Bernardo J., additional, and Hall, Anthony, additional

Published
2019
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48. Kinetochore and ionomic adaptation to whole-genome duplication in Cochleariashows evolutionary convergence in three autopolyploids

Author

Bray, Sian M., Hämälä, Tuomas, Zhou, Min, Busoms, Silvia, Fischer, Sina, Desjardins, Stuart D., Mandáková, Terezie, Moore, Chris, Mathers, Thomas C., Cowan, Laura, Monnahan, Patrick, Koch, Jordan, Wolf, Eva M., Lysak, Martin A., Kolar, Filip, Higgins, James D., Koch, Marcus A., and Yant, Levi

Abstract

Whole-genome duplication (WGD) occurs in all kingdoms and impacts speciation, domestication, and cancer outcome. However, doubled DNA management can be challenging for nascent polyploids. The study of within-species polyploidy (autopolyploidy) permits focus on this DNA management aspect, decoupling it from the confounding effects of hybridization (in allopolyploid hybrids). How is autopolyploidy tolerated, and how do young polyploids stabilize? Here, we introduce a powerful model to address this: the genus Cochlearia, which has experienced many polyploidization events. We assess meiosis and other polyploid-relevant phenotypes, generate a chromosome-scale genome, and sequence 113 individuals from 33 ploidy-contrasting populations. We detect an obvious autopolyploidy-associated selection signal at kinetochore components and ion transporters. Modeling the selected alleles, we detail evidence of the kinetochore complex mediating adaptation to polyploidy. We compare candidates in independent autopolyploids across three genera separated by 40 million years, highlighting a common function at the process and gene levels, indicating evolutionary flexibility in response to polyploidy.

Published
2024
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