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PD Dr. Michael Kroiher

Research

Evolution of developmental mechanisms

My interest is to understand the evolution of molecular decision-making processes during the early development of animal organisms. With regard to this question, we are conducting comparative studies on nematodes, also known as threadworms.

Representatives of nematodes are found worldwide in all terrestrial and marine habitats. Estimates of the age of the taxon vary between 500 and 1000 million years, and the range in species number extends from tens of thousands to many millions. The molecular phylogenetic tree divides the taxon with 12 clades into the basal Enoplea and the derived Chromadorea. Genome sequences in the hundreds from all the different clades of the taxon are now freely available.

With the derived C. elegans, the nematodes provide one of the best-studied models for development. C. elegans is characterised by cell constancy, a constant cell lineage and an unchanging cell pattern. In this, the mechanisms of early development have been largely elucidated cell biologically and molecularly. In particular, it has become clear that both the spatial and temporal positioning of maternal components and cell-cell interactions between individual, neighbouring cells are essential for early development.

We were able to show that in other nematodes the molecular mechanisms of early development can differ significantly compared to C. elegans. It is striking that basal species show regulative development and that there is obviously an evolutionary trend towards mosaic forms of embryogenesis as known from C. elegans.

Nematodes from different clades with two characteristic features are studied

(I) Species that reproduce parthenogenetically

C. elegans is a hermaphrodite, i.e. it self-fertilises. This is crucial because the sperm exerts a polarising influence on the egg. The entry site of the sperm determines the posterior pole of the embryo. In contrast, there are numerous species that reproduce parthenogenetically, i.e. without the involvement of sperm. Here it is extremely interesting to see how the establishment of the primary axis is molecularly controlled without the polarising influence of sperm.

(II) Species that have a different cell pattern than C. elegans

C. elegans has an invariant cell pattern. Here, a series of inductions within narrow time windows and specific spatial patterns via the WNT and NOTCH signalling pathways are necessary to control cell differentiation towards the worm. Numerous nematodes exhibit a cell pattern in early development that differs from C. elegans. The aim is to elucidate to what extent the inductions that take place here are comparable to those of C. elegans.

Analysis of gene expression

The temporal and spatial localisation of gene expression is a prerequisite for comparing developmental mechanisms. We have established the novel multiplex hybridisation chain reaction (HCR) in situ technique for expression analysis during early development in various nematodes.

Analysis of gene function

The functional analysis of gene products is indispensable for understanding the evolution of developmental mechanisms. The CRISPR/Cas9 method is currently used for such studies. The technique is well advanced in the model nematode C. elegans. In two other nematodes, we have recently found out the conditions for "knock-out" mutations. "Knock-in” mutations work at least for short sequences with CRISPR/Cas9.

Publications

Heger P., Kroiher M., Ndifon N., & Schierenberg E. (2010). Conservation of MAP kinase activity and MSP genes in parthenogenetic nematodes. BMC Dev Biol: 10, 51.

Schiffer P.H., Kroiher M., Kraus C., Koutsovoulos G.D., Kumar S., Camps J.I., Nsah N.A., Stappert D., Morris K., Heger P., Altmüller J., Frommolt P., Nürnberg P., Thomas W.K., Blaxter M.L. & Schierenberg E. (2013). The genome of Romanomermis culicivorax: revealing fundamental changes in the core developmental genetic toolkit in Nematoda. BMC Genomics: 14, 923. doi: 10.1186/1471-2164-14-923.

Schiffer P.H., Nsah N.A., Grotehusmann H., Kroiher M., Loer C. & Schierenberg E. (2014). Developmental variations among Panagrolaimid nematodes indicate developmental system drift within a small taxonomic unit. Dev Genes Evol: 224, 183. doi: 10.1007/s00427-014-0471-2.

Hiraki H., Kagoshima H., Kraus C., Schiffer P.H., Ueta Y., Vogt T., Kroiher M., Schierenberg E. & Kohara Y. (2017). Genome analysis of the nematode Diploscapter coronatus: Insights into peculiarities of parthenogenetic reproduction. BMC Genomics: 18, 478. doi: 10.1186/s12864-017-3860-x.

Kraus C., Kagoshima H., Hiraki H., Schiffer P.H., Vogt T., Kroiher M., Kohara Y. & Schierenberg E. (2017). Oogenesis, early embryogenesis and reproductive mode in the parthenogenetic nematode Diploscapter coronatus: Gene expression and genomic background. Evodevo: 8, 16. doi: 10.1186/s13227-017-0081-y.

Schiffer PH., Polsky AL., Cole AG., Camps JIR., Kroiher M., Silver DH., Grishkevich V., Anavy L., Koutsovoulos G., Hashimshony T. &Yanai I. (2018). The gene regulatory program of Acrobeloides nanus reveals conservation of phylum-specific expression. Proc Natl Acad Sci U S A: 115, 4459. doi: 10.1073/pnas.1720817115.

Schiffer PH., Danchin EGJ., Burnell AM., Creevey CJ., Wong S., Dix I., O'Mahony G., Culleton BA., Rancurel C., Stier G., Martínez-Salazar EA., Marconi A., Trivedi U., Kroiher M., Thorne MAS., Schierenberg E., Wiehe T. & Blaxter M. (2019). Signatures of the Evolution of Parthenogenesis and Cryptobiosis in the Genomes of Panagrolaimid Nematodes. iScience: 21, 587. doi: 10.1016/j.isci.2019.10.039.

Hellekes V., Claus D., Seiler J., Illner F., Schiffer PH. & Kroiher M. (2023). CRISPR/Cas9 mediated gene editing in non-model nematode Panagrolaimus sp. PS1159. Front Genome Ed: 3. doi: 10.3389/fgeed.2023.1078359.

Teaching

B.Sc. (Bachelor of Science Biology)

  • Pflichtmodul: Biologie IIA: Evolution, Entwicklung und Systematik der Tiere

  • Wahlpflichtmodul: Grundlagen der Entwicklungsbiologie

  • Wahlpflichtmodul: Modellsysteme und Methoden in der Zellbiologie

M.Sc. (Master of Science Biologie)

  • Seminar modul: Molecular Genetics

    • lecture

    • tutorial

    • seminar

  • Subject modul: Methods in Cell and Developmental Biology

BA (Bachelor of Arts; Lehramt HRGs)

  • Seminar: Mensch und Umwelt

BA (Bachelor of Arts; Lehramt Gym/Ge und BK)

  • Pflichtmodul Biologie IIA: Evolution, Entwicklung und Systematik der Tiere

M.Ed. (Master of Education) Gymn Ges BK

  • Seminar: Aktuelle und gesellschaftsrelevante Aspekte der Biologie

  • Wahlpflichtmodul: Entwicklung und Evolution

  • Wahlpflichtmodul: Anatomie der Wirbeltiere