Gravitaxis in <i>Drosophila melanogaster</i>: a forward genetic screen

Armstrong, J. Douglas; Texada, Michael J.; Munjaal, Ravi P.; Baker, Dean A.; Beckingham, Kathy

doi:10.1111/j.1601-183x.2005.00154.x

Cited by 76 publications

(127 citation statements)

References 45 publications

(76 reference statements)

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“…Further studies indicated that these changed responses arise from altered chordotonal neuron function, but provided no information as to whether yuri is uniquely expressed in these neurons (Armstrong et al, 2006). Studies here reveal that yuri is expressed ubiquitously, indicating that yuri is not dedicated to gravitaxic responses but rather that the yuri c263 mutation disrupts yuri expression in a manner that specifically affects this function.…”

Section: Roles Of the Yuri Isoformsmentioning

confidence: 86%

“…The P insertion yuri c263 (Armstrong et al, 2006) and SUPor-P insertion KG03019 (Roseman et al, 1995) were mobilized with the Δ2-3 transposase at 99B (Robertson et al, 1988). Standard genetic schemes generated stocks of viable excisions.…”

Section: Imprecise Excisionsmentioning

confidence: 99%

“…The first mutation at the locus, yuri c263 , was identified in a screen for mutants affecting gravitaxis. Altered gravitaxis was shown to result from perturbed expression of yuri in subsets of chordotonal neurons (Armstrong et al, 2006). The molecular functions of the locus identified here suggest that yuri mediates specialized actin-and microtubule-related activities in Drosophila tissues.…”

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confidence: 95%

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yuri gagarinis required for actin, tubulin and basal body functions inDrosophilaspermatogenesis

Texada

Simonette

Johnson

et al. 2008

Journal of Cell Science

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A unique feature of the genus Drosophila is the formation of unusually long sperm tails. Sperm lengths of millimeters are common within this group, with the 1.8 mm sperm of D. melanogaster being fairly typical. This marked expansion in sperm length reflects an unusual aspect of spermatogenesis in these organisms: in contrast to other species in which an intraflagellar transport system is used for growth of the sperm flagellum (Scholey, 2006), Drosophila sperm axonemes are assembled in syncytial cysts by a mechanism that does not require, and is not limited by, this system (Han et al., 2003;Sarpal et al., 2003). This unusual sperm axoneme development and the resulting expansion of sperm tail length have led to distinctive features of spermatogenesis not found in other species. In D. bifurca, a special 'sperm roller' has evolved to package its 6-centimeter-long gametes (Joly et al., 2003). In D. melanogaster, a highly evolved individualization process that generates 64 individual sperm from an elongate cyst containing 64 syncytial spermatids has been identified and studied (Noguchi and Miller, 2003;Tokuyasu et al., 1972a). The distinctive molecular mechanisms needed for this process include a motile filamentous actin system (the investment, or actin, cones) that traverses the entire length of the sperm tails, removing excess cytoplasm and investing each sperm in its own plasma membrane. A specialized microtubulerich structure (the dense complex) is also associated with the sperm nuclei and functions to position the basal body and also possibly to strengthen the nuclei as they undergo extreme condensation (A. D. Tates, Cytodifferentiation during spermatogenesis in Drosophila melanogaster, PhD thesis, Rijksuniversiteit Leiden, The Netherlands, 1971) (Tokuyasu, 1974).We have identified a locus, yuri gagarin (yuri), that we show here has multiple roles in the generation of elongate individualized sperm. The gene is only highly conserved in the genus Drosophila, suggesting specialized roles in these organisms. Interestingly, yuri was initially identified through its function in another specialized organ system of insects and arthropods: the chordotonal organs. These are complex mechanosensory structures with roles in proprioception and graviperception. The first mutation at the locus, yuri c263 , was identified in a screen for mutants affecting gravitaxis. Altered gravitaxis was shown to result from perturbed expression of yuri in subsets of chordotonal neurons (Armstrong et al., 2006). The molecular functions of the locus identified here suggest that yuri mediates specialized actin-and microtubule-related activities in Drosophila tissues. ResultsThe yuri locus in D. melanogaster and other Drosophilids In addition to the cDNA (GH14032) encoding a ~30 kDa protein that we used previously (Armstrong et al., 2006), we identified 11 further yuri ESTs/cDNAs from adult testis, ovary, S2 cells and embryos through FlyBase. Sequencing of these new cDNAs established that three major transcript classes are generated from yuri (Fig...

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Section: Roles Of the Yuri Isoformsmentioning

confidence: 86%

Section: Imprecise Excisionsmentioning

confidence: 99%

mentioning

confidence: 95%

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yuri gagarinis required for actin, tubulin and basal body functions inDrosophilaspermatogenesis

Texada

Simonette

Johnson

et al. 2008

Journal of Cell Science

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“…Since then, several genes influencing this behavior have been identified (11)(12)(13). However, those genes are expressed in both central and peripheral nervous systems, and the nature of their role in the sensory organ that detects gravity remains unknown.…”

Section: T He Primary Mechanosensory Organ That Detects Gravity Inmentioning

confidence: 99%

TRPA channels distinguish gravity sensing from hearing in Johnston's organ

Sun¹,

Liu²,

Ben‐Shahar³

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

147

169

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Although many animal species sense gravity for spatial orientation, the molecular bases remain uncertain. Therefore, we studied Drosophila melanogaster, which possess an inherent upward movement against gravity-negative geotaxis. Negative geotaxis requires Johnston's organ, a mechanosensory structure located in the antenna that also detects near-field sound. Because channels of the transient receptor potential (TRP) superfamily can contribute to mechanosensory signaling, we asked whether they are important for negative geotaxis. We identified distinct expression patterns for 5 TRP genes; the TRPV genes nanchung and inactive were present in most Johnston's organ neurons, the TRPN gene nompC and the TRPA gene painless were localized to 2 subpopulations of neurons, and the TRPA gene pyrexia was expressed in cap cells that may interact with the neurons. Likewise, mutating specific TRP genes produced distinct phenotypes, disrupting negative geotaxis (painless and pyrexia), hearing (nompC), or both (nanchung and inactive). Our genetic, physiological and behavioral data indicate that the sensory component of negative geotaxis involves multiple TRP genes. The results also distinguish between different mechanosensory modalities and set the stage for understanding how TRP channels contribute to mechanosensation. Drosophila ͉ transient receptor potential ͉ geotaxis T he primary mechanosensory organ that detects gravity in Drosophila appears to be Johnston's organ (1). This organ is located in the second antennal segment. It consists of over 200 scolopidia arrayed in a bowl shape (2), with each scolopidium containing mechanosensory chordotonal neurons and their support cells (3-5) (Fig. 1A). Johnston's organ is well known as a detector of near-field sound (3-6). Air particle displacement vibrates the third antennal segment, deforming the cuticle at the joint between segments 2 and 3 where the sensory units of Johnston's organ attach. It was proposed that the third segment may also be deflected by gravity (7), and the geometry of Johnston's organ suggests it could respond to gravity irrespective of head orientation (2). Indeed, recent work indicates that Johnston's organ can also respond to gravity, as well as to wind (1,8). Thus, Johnston's organ may detect multiple different mechanosensory stimuli, and investigations of specific molecular mechanisms underlying these sensory functions may benefit our understanding of other polymodal sensory structures such as the inner ear and dorsal root ganglion in mammals.Almost 50 years ago, Hirsch and colleagues demonstrated that negative geotaxis is genetically encoded in Drosophila (9, 10). Since then, several genes influencing this behavior have been identified (11-13). However, those genes are expressed in both central and peripheral nervous systems, and the nature of their role in the sensory organ that detects gravity remains unknown. The goal of this work was to identify genes involved in sensory aspects of negative geotaxis and in so doing to obtain genetic data to discriminate...

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“…8D) and GFP::Sop (data not shown), or translation factors GFP::eIF-4E and GFP::eRF1 (data not shown) showed no loss of fluorescence in neighboring cells. Similarly, FLIP experiments with the RNA-binding protein Ypsilon schachtel (Yps), a component of the oskar RNP (Armstrong et al, 2006;Wilhelm et al, 2000), revealed no evidence for its movement between cells (Fig. 8E).…”

Section: Intercellular Movement Of Proteins Through Follicle Cell Rinmentioning

confidence: 99%

Intercellular protein movement in syncytialDrosophilafollicle cells

Airoldi

McLean

Shimada

et al. 2011

Journal of Cell Science

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SummaryRing canals connecting Drosophila germline, follicle and imaginal disc cells provide direct contact of cytoplasm between cells. To date, little is known about the formation, structure, or function of the somatic ring canals present in follicle and imaginal disc cells. Here, we show by confocal and electron microscopy that Pavarotti kinesin-like protein and Visgun are stable components of somatic ring canals. Using live-cell confocal microscopy, we show that somatic ring canals form from the stabilization of mitotic cleavage furrows. In contrast to germline cells, syncytial follicle cells do not divide synchronously, are not maximally branched and their ring canals do not increase in size during egg chamber development. We show for the first time that somatic ring canals permit exchange of cytoplasmic proteins between follicle cells. These results provide insight into the composition and function of ring canals in somatic cells, implying a broader functional significance for syncytial organization of cells outside the germline.

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Gravitaxis in Drosophila melanogaster: a forward genetic screen

Cited by 76 publications

References 45 publications

yuri gagarinis required for actin, tubulin and basal body functions inDrosophilaspermatogenesis

yuri gagarinis required for actin, tubulin and basal body functions inDrosophilaspermatogenesis

TRPA channels distinguish gravity sensing from hearing in Johnston's organ

Intercellular protein movement in syncytialDrosophilafollicle cells

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