Literature DB >> 23012415

Hydra meiosis reveals unexpected conservation of structural synaptonemal complex proteins across metazoans.

Johanna Fraune1, Manfred Alsheimer, Jean-Nicolas Volff, Karoline Busch, Sebastian Fraune, Thomas C G Bosch, Ricardo Benavente.   

Abstract

The synaptonemal complex (SC) is a key structure of meiosis, mediating the stable pairing (synapsis) of homologous chromosomes during prophase I. Its remarkable tripartite structure is evolutionarily well conserved and can be found in almost all sexually reproducing organisms. However, comparison of the different SC protein components in the common meiosis model organisms Saccharomyces cerevisiae, Arabidopsis thaliana, Caenorhabditis elegans, Drosophila melanogaster, and Mus musculus revealed no sequence homology. This discrepancy challenged the hypothesis that the SC arose only once in evolution. To pursue this matter we focused on the evolution of SYCP1 and SYCP3, the two major structural SC proteins of mammals. Remarkably, our comparative bioinformatic and expression studies revealed that SYCP1 and SYCP3 are also components of the SC in the basal metazoan Hydra. In contrast to previous assumptions, we therefore conclude that SYCP1 and SYCP3 form monophyletic groups of orthologous proteins across metazoans.

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Year:  2012        PMID: 23012415      PMCID: PMC3478637          DOI: 10.1073/pnas.1206875109

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  44 in total

1.  c(3)G encodes a Drosophila synaptonemal complex protein.

Authors:  S L Page; R S Hawley
Journal:  Genes Dev       Date:  2001-12-01       Impact factor: 11.361

2.  Characterization of a novel meiosis-specific protein within the central element of the synaptonemal complex.

Authors:  Geert Hamer; Katarina Gell; Anna Kouznetsova; Ivana Novak; Ricardo Benavente; Christer Höög
Journal:  J Cell Sci       Date:  2006-09-12       Impact factor: 5.285

3.  Synaptonemal complex protein SYCP3 of the rat: evolutionarily conserved domains and the assembly of higher order structures.

Authors:  A Baier; M Alsheimer; J-N Volff; R Benavente
Journal:  Sex Dev       Date:  2007       Impact factor: 1.824

Review 4.  The Hydra polyp: nothing but an active stem cell community.

Authors:  Thomas C G Bosch; Friederike Anton-Erxleben; Georg Hemmrich; Konstantin Khalturin
Journal:  Dev Growth Differ       Date:  2009-11-05       Impact factor: 2.053

5.  Embryogenesis in hydra.

Authors:  V J Martin; C L Littlefield; W E Archer; H R Bode
Journal:  Biol Bull       Date:  1997-06       Impact factor: 1.818

6.  CnNK-2, an NK-2 homeobox gene, has a role in patterning the basal end of the axis in hydra.

Authors:  A Grens; L Gee; D A Fisher; H R Bode
Journal:  Dev Biol       Date:  1996-12-15       Impact factor: 3.582

7.  The neighbor-joining method: a new method for reconstructing phylogenetic trees.

Authors:  N Saitou; M Nei
Journal:  Mol Biol Evol       Date:  1987-07       Impact factor: 16.240

8.  The dynamic genome of Hydra.

Authors:  Jarrod A Chapman; Ewen F Kirkness; Oleg Simakov; Steven E Hampson; Therese Mitros; Thomas Weinmaier; Thomas Rattei; Prakash G Balasubramanian; Jon Borman; Dana Busam; Kathryn Disbennett; Cynthia Pfannkoch; Nadezhda Sumin; Granger G Sutton; Lakshmi Devi Viswanathan; Brian Walenz; David M Goodstein; Uffe Hellsten; Takeshi Kawashima; Simon E Prochnik; Nicholas H Putnam; Shengquiang Shu; Bruce Blumberg; Catherine E Dana; Lydia Gee; Dennis F Kibler; Lee Law; Dirk Lindgens; Daniel E Martinez; Jisong Peng; Philip A Wigge; Bianca Bertulat; Corina Guder; Yukio Nakamura; Suat Ozbek; Hiroshi Watanabe; Konstantin Khalturin; Georg Hemmrich; André Franke; René Augustin; Sebastian Fraune; Eisuke Hayakawa; Shiho Hayakawa; Mamiko Hirose; Jung Shan Hwang; Kazuho Ikeo; Chiemi Nishimiya-Fujisawa; Atshushi Ogura; Toshio Takahashi; Patrick R H Steinmetz; Xiaoming Zhang; Roland Aufschnaiter; Marie-Kristin Eder; Anne-Kathrin Gorny; Willi Salvenmoser; Alysha M Heimberg; Benjamin M Wheeler; Kevin J Peterson; Angelika Böttger; Patrick Tischler; Alexander Wolf; Takashi Gojobori; Karin A Remington; Robert L Strausberg; J Craig Venter; Ulrich Technau; Bert Hobmayer; Thomas C G Bosch; Thomas W Holstein; Toshitaka Fujisawa; Hans R Bode; Charles N David; Daniel S Rokhsar; Robert E Steele
Journal:  Nature       Date:  2010-03-14       Impact factor: 49.962

9.  Organization of the synaptonemal complex during meiosis in Caenorhabditis elegans.

Authors:  Kristina Schild-Prüfert; Takamune T Saito; Sarit Smolikov; Yanjie Gu; Marina Hincapie; David E Hill; Marc Vidal; Kent McDonald; Monica P Colaiácovo
Journal:  Genetics       Date:  2011-08-11       Impact factor: 4.562

Review 10.  Genetics of mammalian meiosis: regulation, dynamics and impact on fertility.

Authors:  Mary Ann Handel; John C Schimenti
Journal:  Nat Rev Genet       Date:  2010-01-06       Impact factor: 53.242

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  23 in total

1.  Dissociation of the X chromosome from the synaptonemal complex in the XY body of the rodent Galea musteloides.

Authors:  Roberta B Sciurano; I Mónica Rahn; Juan C Cavicchia; Alberto J Solari
Journal:  Chromosome Res       Date:  2013-09-17       Impact factor: 5.239

2.  Phylogenies of central element proteins reveal the dynamic evolutionary history of the mammalian synaptonemal complex: ancient and recent components.

Authors:  Johanna Fraune; Céline Brochier-Armanet; Manfred Alsheimer; Ricardo Benavente
Journal:  Genetics       Date:  2013-09-11       Impact factor: 4.562

Review 3.  Amphimixis and the individual in evolving populations: does Weismann's Doctrine apply to all, most or a few organisms?

Authors:  Karl J Niklas; Ulrich Kutschera
Journal:  Naturwissenschaften       Date:  2014-03-16

Review 4.  Evolutionary history of the mammalian synaptonemal complex.

Authors:  Johanna Fraune; Céline Brochier-Armanet; Manfred Alsheimer; Jean-Nicolas Volff; Katharina Schücker; Ricardo Benavente
Journal:  Chromosoma       Date:  2016-03-12       Impact factor: 4.316

5.  Synaptonemal complex extension from clustered telomeres mediates full-length chromosome pairing in Schmidtea mediterranea.

Authors:  Youbin Xiang; Danny E Miller; Eric J Ross; Alejandro Sánchez Alvarado; R Scott Hawley
Journal:  Proc Natl Acad Sci U S A       Date:  2014-11-17       Impact factor: 11.205

6.  Stem cell differentiation trajectories in Hydra resolved at single-cell resolution.

Authors:  Stefan Siebert; Jeffrey A Farrell; Jack F Cazet; Yashodara Abeykoon; Abby S Primack; Christine E Schnitzler; Celina E Juliano
Journal:  Science       Date:  2019-07-26       Impact factor: 47.728

7.  Meiotic behavior, transmission and active genes of B chromosomes in the cichlid Astatotilapia latifasciata: new clues about nature, evolution and maintenance of accessory elements.

Authors:  Adauto Lima Cardoso; Natália Bortholazzi Venturelli; Irene da Cruz; Fábio Malta de Sá Patroni; Diogo de Moraes; Rogério Antonio de Oliveira; Ricardo Benavente; Cesar Martins
Journal:  Mol Genet Genomics       Date:  2022-06-15       Impact factor: 3.291

8.  Plasticity in the Meiotic Epigenetic Landscape of Sex Chromosomes in Caenorhabditis Species.

Authors:  Braden J Larson; Mike V Van; Taylor Nakayama; JoAnne Engebrecht
Journal:  Genetics       Date:  2016-06-08       Impact factor: 4.562

9.  Sex-specific and developmental expression of Dmrt genes in the starlet sea anemone, Nematostella vectensis.

Authors:  Nikki G Traylor-Knowles; Eric G Kane; Vanna Sombatsaphay; John R Finnerty; Adam M Reitzel
Journal:  Evodevo       Date:  2015-04-25       Impact factor: 2.250

10.  Conservation and variability of synaptonemal complex proteins in phylogenesis of eukaryotes.

Authors:  Tatiana M Grishaeva; Yuri F Bogdanov
Journal:  Int J Evol Biol       Date:  2014-07-23
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