Evidence for intraflagellar transport in butterfly spermatocyte cilia

In the model organism insect Drosophila melanogaster short cilia assemble on spermatocytes that elaborate into 1.8 mm long flagella during spermatid differentiation. A unique feature of these cilia/flagella is their lack of dependence on intraflagellar transport (IFT) for their assembly. Here we show that in the common butterfly Pieris brassicae the spermatocyte cilia are exceptionally long: about 40 µm compared to less than 1 µm in Drosophila. By transmission electron microscopy we show that P. brassicae spermatocytes display several features not found in melanogaster, including compelling evidence of IFT structures and features of motile cilia. Summary statement This work shows ultrastructural definition of the exceptionally long cilia that persist on butterfly (P. brassicae) spermatocytes, including evidence of intraflagellar transport, during meiotic division.

[1]  M. Inagaki,et al.  Primary ciliary signaling: links with the cell cycle. , 2021, Trends in cell biology.

[2]  E. Lorentzen,et al.  Structural insights into the architecture and assembly of eukaryotic flagella , 2020, Microbial cell.

[3]  M. Riparbelli,et al.  Centrioles and Ciliary Structures during Male Gametogenesis in Hexapoda: Discovery of New Models , 2020, Cells.

[4]  M. Riparbelli,et al.  The “transition zone” of the cilium‐like regions in the Drosophila spermatocytes and the role of the C‐tubule in axoneme assembly , 2018, Experimental cell research.

[5]  H. Maiato,et al.  Differential regulation of transition zone and centriole proteins contributes to ciliary base diversity , 2018, Nature Cell Biology.

[6]  T. Ishikawa.  Axoneme Structure from Motile Cilia. , 2017, Cold Spring Harbor perspectives in biology.

[7]  E. Lorentzen,et al.  The Intraflagellar Transport Machinery. , 2016, Cold Spring Harbor perspectives in biology.

[8]  B. Durand,et al.  Transition zone assembly and its contribution to axoneme formation in Drosophila male germ cells , 2016, The Journal of cell biology.

[9]  B. Durand,et al.  Drosophilamelanogaster as a model for basal body research , 2016, Cilia.

[10]  Junmin Pan,et al.  Mechanism of ciliary disassembly , 2016, Cellular and Molecular Life Sciences.

[11]  M. Leroux,et al.  Shared and Distinct Mechanisms of Compartmentalized and Cytosolic Ciliogenesis , 2015, Current Biology.

[12]  G. Witman,et al.  Dynein and intraflagellar transport. , 2015, Experimental cell research.

[13]  M. Riparbelli,et al.  Procentriole assembly without centriole disengagement − a paradox of male gametogenesis , 2014, Journal of Cell Science.

[14]  E. Valente,et al.  Primary cilia in neurodevelopmental disorders , 2014, Nature Reviews Neurology.

[15]  C. Sung,et al.  The roles of evolutionarily conserved functional modules in cilia-related trafficking , 2013, Nature Cell Biology.

[16]  M. Riparbelli,et al.  The cilium-like region of the Drosophila spermatocyte: an emerging flagellum? , 2013, Journal of Cell Science.

[17]  M. Riparbelli,et al.  Unique properties of Drosophila spermatocyte primary cilia , 2013, Biology Open.

[18]  J. Raff,et al.  Drosophila Cep135/Bld10 maintains proper centriole structure but is dispensable for cartwheel formation , 2012, Journal of Cell Science.

[19]  M. Riparbelli,et al.  Assembly and persistence of primary cilia in dividing Drosophila spermatocytes. , 2012, Developmental cell.

[20]  P. Duarte,et al.  BLD10/CEP135 is a microtubule-associated protein that controls the formation of the flagellum central microtubule pair. , 2012, Developmental cell.

[21]  Lacramioara Fabian,et al.  Drosophila spermiogenesis , 2012, Spermatogenesis.

[22]  J. Reiter,et al.  Scoring a backstage pass: Mechanisms of ciliogenesis and ciliary access , 2012, The Journal of cell biology.

[23]  B. Durand,et al.  Drosophila chibby is required for basal body formation and ciliogenesis but not for Wg signaling , 2012, The Journal of cell biology.

[24]  K. Narita,et al.  Structure and function of vertebrate cilia, towards a new taxonomy. , 2012, Differentiation; research in biological diversity.

[25]  L. Tsiokas,et al.  Cilia and cell cycle re-entry , 2011, Cell cycle.

[26]  A. Jarman,et al.  Dilatory is a Drosophila protein related to AZI1 (CEP131) that is located at the ciliary base and required for cilium formation , 2011, Journal of Cell Science.

[27]  P. Dupuis‐Williams,et al.  Ultrastructure of cilia and flagella – back to the future! , 2011, Biology of the cell.

[28]  W. Marshall,et al.  Ciliogenesis: building the cell's antenna , 2011, Nature Reviews Molecular Cell Biology.

[29]  K. Anderson,et al.  The primary cilium: a signalling centre during vertebrate development , 2010, Nature Reviews Genetics.

[30]  B. Yoder,et al.  The Primary Cilium as a Complex Signaling Center , 2009, Current Biology.

[31]  N. Katsanis,et al.  The Vertebrate Primary Cilium in Development, Homeostasis, and Disease , 2009, Cell.

[32]  J. Reiter,et al.  Building it up and taking it down: The regulation of vertebrate ciliogenesis , 2008, Developmental dynamics : an official publication of the American Association of Anatomists.

[33]  J. Scholey.  Intraflagellar transport motors in cilia: moving along the cell's antenna , 2008, The Journal of cell biology.

[34]  M. Bornens,et al.  Structure and duplication of the centrosome , 2007, Journal of Cell Science.

[35]  Keith Gull,et al.  Centriole/basal body morphogenesis and migration during ciliogenesis in animal cells , 2006, Journal of Cell Science.

[36]  J. Reiter,et al.  The Primary Cilium as the Cell's Antenna: Signaling at a Sensory Organelle , 2006, Science.

[37]  N. Hirokawa,et al.  Nodal Flow and the Generation of Left-Right Asymmetry , 2006, Cell.

[38]  J. Scholey,et al.  Functional coordination of intraflagellar transport motors , 2005, Nature.

[39]  L. Quarmby,et al.  Cilia and the cell cycle? , 2005, The Journal of cell biology.

[40]  Maurice J. Kernan,et al.  Mechanosensory-defective, male-sterile unc mutants identify a novel basal body protein required for ciliogenesis in Drosophila , 2004, Development.

[41]  S. Geimer,et al.  Intraflagellar transport (IFT) cargo , 2004, The Journal of cell biology.

[42]  K. Wolf,et al.  The restructuring of the flagellar base and the flagellar necklace during spermatogenesis of Ephestia kuehniella Z. (Pyralidae, Lepidoptera) , 1989, Cell and Tissue Research.

[43]  Maurice J. Kernan,et al.  Intraflagellar Transport Is Required in Drosophila to Differentiate Sensory Cilia but Not Sperm , 2003, Current Biology.

[44]  E. Raff,et al.  Drosophila KAP Interacts with the Kinesin II Motor Subunit KLP64D to Assemble Chordotonal Sensory Cilia, but Not Sperm Tails , 2003, Current Biology.

[45]  M. Brueckner,et al.  Cilia are at the heart of vertebrate left-right asymmetry. , 2003, Current opinion in genetics & development.

[46]  M. Brueckner,et al.  Two Populations of Node Monocilia Initiate Left-Right Asymmetry in the Mouse , 2003, Cell.

[47]  J. Scholey.  Intraflagellar transport. , 2003, Annual review of cell and developmental biology.

[48]  G. Pazour,et al.  Intraflagellar transport and cilia-dependent diseases. , 2002, Trends in cell biology.

[49]  C. Tabin,et al.  Left–right development: Conserved function for embryonic nodal cilia , 2002, Nature.

[50]  R. Sloboda.  A healthy understanding of intraflagellar transport. , 2002, Cell motility and the cytoskeleton.

[51]  J. Rosenbaum,et al.  Intraflagellar transport , 2002, Nature Reviews Molecular Cell Biology.

[52]  P. Lefebvre,et al.  Assembly and motility of eukaryotic cilia and flagella. Lessons from Chlamydomonas reinhardtii. , 2001, Plant physiology.

[53]  N. Kawamura,et al.  Behavior of centrioles during meiosis in the male silkworm, Bombyx mori (Lepidoptera) , 1998, Development, growth & differentiation.

[54]  P. Beech,et al.  Chlamydomonas Kinesin-II–dependent Intraflagellar Transport (IFT): IFT Particles Contain Proteins Required for Ciliary Assembly in Caenorhabditis elegans Sensory Neurons , 1998, The Journal of cell biology.

[55]  K. Wolf,et al.  Spermatocytes of the caddisfly Potamophylax rotundipennis (Trichoptera, Insecta): a fine structure study with emphasis on synaptonemal complex plates associated with chromatin. , 1997, Tissue & cell.

[56]  J. Lafountain,et al.  Analysis of birefringence and ultrastructure of spindles in primary spermatocytes of Nephrotoma suturalis during anaphase. , 1976, Journal of ultrastructure research.