Meiose

The independent research group Meiosis (ME) primarily funded by the European Research Council (project MEIOBARMIX) is interested in the process of plant meiosis that generates genetic variation through homologous recombination.

Our research is closely-linked to the research theme of the department Breeding Research and we contribute with our research to the IPK research theme FSP3 "Mechanisms of Reproduction".

Barley (Hordeum vulgare) is an important cereal crop grown in a variety of climates globally used as animal fodder, food and for brewing. Traditional plant breeding, that harnesses natural genetic variation arising during meiosis, will have a key role to deliver crop improvements in the near future.

Meiosis assures genetic variation by regulated parental genetic exchange based on homologous recombination. However, particularly in cereal crops including barley meiotic recombination events are limited and skewed towards chromosome ends whereby a large portion of the genetic information keeps untapped in breeding programs.

Embarking on molecular genetics, biochemistry and cytogenetic approaches, the overarching aim of the group is to alter the outcome of meiotic recombination with a focus on barley. To do so, projects in the group aim to:

better understand the mechanisms underlying the control of homologous recombination in barley and Arabidopsis thaliana,
to develop novel tools and strategies to study and alter meiotic recombination outcome in barley and Arabidopsis thaliana,
and to translate acquired knowledge into barley.

2024

Crhak Khaitova L, Mikulkova P, Pecinkova J, Kalidass M, Heckmann S, Lermontova I, Riha K:

Heat stress impairs centromere structure and segregation of meiotic chromosomes in Arabidopsis. eLife 12 (2024) e90253. https://dx.doi.org/10.7554/eLife.90253

2023

Ahmadli U, Kalidass M, Crhak Khaitova L, Fuchs J, Cuacos M, Demidov D, Zuo S, Pecinkova J, Mascher M, Ingouff M, Heckmann S, Houben A, Riha K, Lermontova I:

High temperature increases centromere-mediated genome elimination frequency and enhances haploid induction in Arabidopsis. Plant Commun. 4 (2023) 100507. https://dx.doi.org/10.1016/j.xplc.2022.100507

Ayoub M A:

Exploration of strategies to alter the meiotic recombination landscape in barley (Hordeum vulgare). (PhD Thesis) Halle/S., Martin-Luther-Universität Halle-Wittenberg, Naturwissenschaftliche Fakultät III Agrar- und Ernährungswissenschaften, Geowissenschaften und Informatik (2023) 107 pp.

Feng C, Roitinger E, Hudecz O, Cuacos M, Lorenz J, Schubert V, Wang B, Wang R, Mechtler K, Heckmann S:

TurboID-based proteomic profiling of meiotic chromosome axes in Arabidopsis thaliana. Nat. Plants 9 (2023) 616-630. https://dx.doi.org/10.1038/s41477-023-01371-7

Piskorz E W, Xu L, Ma Y, Jiang H:

Double-haploid induction generates extensive differential DNA methylation in Arabidopsis. J. Exp. Bot. 74 (2023) 835-847. https://dx.doi.org/10.1093/jxb/erac397

Steckenborn Coria S:

Towards the induction of site-directed meiotic recombination. (PhD Thesis) Halle/S., Martin-Luther-Universität Halle-Wittenberg, Naturwissenschaftliche Fakultät III Agrar- und Ernährungswissenschaften, Geowissenschaften und Informatik (2023) 106 pp.

Steckenborn S, Cuacos M, Ayoub M A, Feng C, Schubert V, Hoffie I, Hensel G, Kumlehn J, Heckmann S:

The meiotic topoisomerase VI B subunit (MTOPVIB) is essential for meiotic DNA double-strand break formation in barley (Hordeum vulgare L.). Plant Reprod. 36 (2023) 1-15. https://dx.doi.org/10.1007/s00497-022-00444-5

Tamilselvan-Nattar-Amutha S, Hiekel S, Hartmann F, Lorenz J, Dabhi R V, Dreissig S, Hensel G, Kumlehn J, Heckmann S:

Barley stripe mosaic virus-mediated somatic and heritable gene editing in barley (Hordeum vulgare L.). Front. Plant Sci. 14 (2023) 1201446. https://dx.doi.org/10.3389/fpls.2023.1201446

2022

Ahn Y-J:

Development and application of Crystal Digital PCR-based single pollen nucleus genotyping to measure meiotic recombination rates in barley (Hordeum vulgare) in high-throughput. (PhD Thesis) Halle/S., Martin-Luther-Universität Halle-Wittenberg, Institut für Agrar- und Ernährungswissenschaften der Naturwissenschaftlichen Fakultät III (2022) 118 pp.

Randall R S, Jourdain C, Nowicka A, Kaduchová K, Kubová M, Ayoub M A, Schubert V, Tatout C, Colas I, Kalyanikrishna, Desset S, Mermet S, Boulaflous-Stevens A, Kubalová I, Mandáková T, Heckmann S, Lysak M A, Panatta M, Santoro R, Schubert D, Pecinka A, Routh D, Baroux C:

Image analysis workflows to reveal the spatial organization of cell nuclei and chromosomes. Nucleus 13 (2022) 277-299. https://dx.doi.org/10.1080/19491034.2022.2144013

Schreiber M, Gao Y, Koch N, Fuchs J, Heckmann S, Himmelbach A, Börner A, Özkan H, Maurer A, Stein N, Mascher M, Dreissig S:

Recombination landscape divergence between populations is marked by larger low-recombining regions in domesticated rye. Mol. Biol. Evol. 39 (2022) msac131. https://dx.doi.org/10.1093/molbev/msac131

2021

Ahn Y-J, Fuchs J, Houben A, Heckmann S:

High throughput measuring of meiotic recombination rates in barley pollen nuclei using Crystal Digital PCR TM. Plant J. 107 (2021) 649-661. https://dx.doi.org/10.1111/tpj.15305

Cuacos M, Heckmann S:

Arabidopsis thaliana. Brassicaceae (Calender Page). In: Houben A (Ed.): Chromosome Biology 2021. 4th Edition. Gatersleben, Germany: IPK (2021) 1.

Cuacos M, Lambing C, Pachon-Penalba M, Osman K, Armstrong S J, Henderson I R, Sanchez-Moran E, Franklin F C H, Heckmann S:

Meiotic chromosome axis remodelling is critical for meiotic recombination in Brassica rapa. J. Exp. Bot. 72 (2021) 3012-3027. https://dx.doi.org/10.1093/jxb/erab035

2020

Ahn Y-J, Cuacos M, Ayoub M A, Kappermann J, Houben A, Heckmann S:

In planta delivery of chemical compounds into barley meiocytes – EdU as compound example. In: Pradillo M, Heckmann S (Eds.): Plant Meiosis: methods and protocols. (Series: Methods in molecular biology, Vol. 2061) New York, NY: Humana Press (2020) 978-1-4939-9817-3, 381-402. https://dx.doi.org/10.1007/978-1-4939-9818-0_27

Ayoub M A, Heckmann S:

Hordeum vulgare. Poaceae (Calender Page). In: Houben A (Ed.): Plant Cytogenetics 2020. 3th Edition. Gatersleben, Germany: IPK (2020) 1.

Chen E C H, Mathieu S, Hoffrichter A, Ropars J, Dreissig S, Fuchs J, Brachmann A, Corradi N:

More filtering on SNP calling does not remove evidence of inter-nucleus recombination in dikaryotic arbuscular mycorrhizal fungi. Front. Plant Sci. 11 (2020) 912. https://dx.doi.org/10.3389/fpls.2020.00912

Desjardins S D, Ogle D E, Ayoub M A, Heckmann S, Henderson I R, Edwards K J, Higgins J D:

MutS homologue 4 and MutS homologue 5 maintain the obligate crossover in wheat despite stepwise gene loss following polyploidization. Plant Physiol. 183 (2020) 1545-1558. https://dx.doi.org/10.1104/pp.20.00534

Dreissig S, Fuchs J, Himmelbach A, Mascher M, Houben A:

Quantification of recombination rate and segregation distortion by genotyping and sequencing of single pollen nuclei. In: Pradillo M, Heckmann S (Eds.): Plant Meiosis: methods and protocols. (Series: Methods in molecular biology, Vol. 2061) New York, NY: Humana Press (2020) 978-1-4939-9817-3, 281-300. https://dx.doi.org/10.1007/978-1-4939-9818-0_20

Dubey R:

Targeted meiotic DNA Double strand break induction using the CRISPR/Cas9 system analyzed via single pollen genotyping. (Master Thesis) Zaragoza, Catalonia, Spain, Spain University of Lleida, Instituto Agronómico Mediterráneo de Zaragoza (IAMZ-CIHEAM) (2020) 70 pp.

Garavello M, Cuenca J, Dreissig S, Fuchs J, Navarro L, Houben A, Aleza P:

Analysis of crossover events and allele segregation distortion in interspecific citrus hybrids by single pollen genotyping. Front. Plant Sci. 11 (2020) 615. https://dx.doi.org/10.3389/fpls.2020.00615

Khosravi S, Dreissig S, Schindele P, Wolter F, Rutten T, Puchta H, Houben A:

Live Cell CRISPR imaging in plant cells with a telomere-specific guide RNA. In: Heinlein M (Ed.): RNA Tagging: methods and protocols. (Series: Methods in molecular biology, Vol. 2166) New York, NY: Humana Press (2020) 1940-6029 (Electronic)1064-3745 (Linking), 343-356. https://dx.doi.org/10.1007/978-1-0716-0712-1_20

Khosravi S, Ishii T, Dreissig S, Houben A:

Application and prospects of CRISPR/Cas9-based methods to trace defined genomic sequences in living and fixed plant cells. Chromosome Res. 28 (2020) 7-17. https://dx.doi.org/10.1007/s10577-019-09622-0

Le Goff S, Keçeli B N, Jeřábková H, Heckmann S, Rutten T, Cotterell S, Schubert V, Roitinger E, Mechtler K, Franklin F C H, Tatout C, Houben A, Geelen D, Probst A V, Lermontova I:

The H3 histone chaperone NASPSIM3 escorts CenH3 in Arabidopsis. Plant J. 101 (2020) 71-86. https://dx.doi.org/10.1111/tpj.14518

Pradillo M, Heckmann S (Eds.):

Plant Meiosis: methods and protocols. (Series: Methods in molecular biology, Vol. 2061) New York, NY: Humana Press (2020) 978-1-4939-9817-3, 410 pp. https://dx.doi.org/10.1007/978-1-4939-9818-0

Schmidt C, Fransz P, Rönspies M, Dreissig S, Fuchs J, Heckmann S, Houben A, Puchta H:

Changing local recombination patterns in plants by CRISPR/Cas mediated chromosome engineering. Nat. Commun. 11 (2020) 4418. https://dx.doi.org/10.1038/s41467-020-18277-z

Schubert V, Neumann P, Marques A, Heckmann S, Macas J, Pedrosa-Harand A, Schubert I, Jang T-S, Houben A:

Super-resolution microscopy reveals diversity of plant centromere architecture. Int. J. Mol. Sci. 21 (2020) 3488. https://dx.doi.org/10.3390/ijms21103488

Valuchova S, Mikulkova P, Pecinkova J, Klimova J, Krumnikl M, Bainar P, Heckmann S, Tomancak P, Riha K:

Imaging plant germline differentiation within Arabidopsis flowers by light sheet microscopy. eLife 9 (2020) e52546. https://dx.doi.org/10.7554/eLife.52546

2019

Demidov D, Heckmann S, Weiss O, Rutten T, Tomaštíková E D, Kuhlmann M, Scholl P, Municio C M, Lermontova I, Houben A:

Deregulated phosphorylation of CENH3 at Ser65 affects the development of floral meristems in Arabidopsis thaliana. Front. Plant Sci. 10 (2019) 928. https://dx.doi.org/10.3389/Fpls.2019.00928

Dreissig S, Mascher M, Heckmann S:

Variation in recombination rate is shaped by domestication and environmental conditions in barley. Mol. Biol. Evol. 36 (2019) 2029–2039. https://dx.doi.org/10.1093/molbev/msz141

Ishii T, Schubert V, Khosravi S, Dreissig S, Metje-Sprink J, Sprink T, Fuchs J, Meister A, Houben A:

RNA-guided endonuclease – in situ labelling (RGEN-ISL): a fast CRISPR/Cas9-based method to label genomic sequences in various species. New Phytol. 222 (2019) 1652-1661. https://dx.doi.org/10.1111/nph.15720

2018

Chambon A, West A, Vezon D, Horlow C, De Muyt A, Chelysheva L, Ronceret A, Darbyshire A R, Osman K, Heckmann S, Franklin F C H, Grelon M:

Identification of ASYNAPTIC4, a component of the meiotic chromosome axis. Plant Physiol. 178 (2018) 233–246. https://dx.doi.org/10.1104/pp.17.01725

Chen E C, Mathieu S, Hoffrichter A, Sedzielewska-Toro K, Peart M, Pelin A, Ndikumana S, Ropars J, Dreissig S, Fuchs J, Brachmann A, Corradi N:

Single nucleus sequencing reveals evidence of inter-nucleus recombination in arbuscular mycorrhizal fungi. eLife 7 (2018) e39813. https://dx.doi.org/10.7554/eLife.39813

Lambing C, Heckmann S:

Tackling plant meiosis: from model research to crop improvement. Front. Plant Sci. 9 (2018) 829. https://dx.doi.org/10.3389/fpls.2018.00829

Osman K, Yang J, Roitinger E, Lambing C, Heckmann S, Howell E, Cuacos M, Imre R, Dürnberger G, Mechtler K, Armstrong S, Franklin F C H:

Affinity proteomics reveals extensive phosphorylation of the Brassica chromosome axis protein ASY1 and a network of associated proteins at prophase I of meiosis. Plant J. 93 (2018) 17-33. https://dx.doi.org/10.1111/tpj.13752

2017

Kappermann J:

Beeinflussung der Anzahl und Verteilung meiotischer Rekombinationsereignisse in der Gerste (Hordeum vulgare) mittels Manipulation epigenetischer Faktoren anhand von Chemikalien. (Bachelor Thesis) Köthen, Hochschule Anhalt (2017)

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