Genetics of Graviperception in Animals

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

doi:10.1016/s0065-2660(05)55004-1

Cited by 27 publications

(28 citation statements)

References 133 publications

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“…In Drosophila, negative gravitaxis requires a Johnston's organ, a mechanosensory structure located in the antenna that also detects near-field sound (Sun et al, 2009;Kamikouchi et al, 2009). Although the existence of graviperception mechanisms in C. elegans has been reported (Beckingham et al, 2005), there is no information about where and how gravity is perceived in nematodes. Lee et al (Lee et al, 2012) found that nictation is regulated by IL2 neurons in C. elegans.…”

Section: Discussionmentioning

confidence: 99%

Negative gravitactic behavior ofCaenorhabditis japonicadauer larvae

Okumura

Tanaka

Yoshiga

2013

Journal of Experimental Biology

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SUMMARYGravity on Earth is a constant stimulus and many organisms are able to perceive and respond to it. However, there is no clear evidence that nematodes respond to gravity. In this study, we demonstrated negative gravitaxis in a nematode using dauer larvae (DL) of Caenorhabditis japonica, which form an association with their carrier insect Parastrachia japonensis. Caenorhabditis japonica DL demonstrating nictation, a typical host-finding behavior, had a negative gravitactic behavior, whereas non-nictating C. japonica and C. elegans DL did not. The negative gravitactic index of nictating DL collected from younger nematode cultures was higher than that from older cultures. After a 24h incubation in M9 buffer, nictating DL did not alter their negative gravitactic behavior, but a longer incubation resulted in less pronounced negative gravitaxis. These results are indicative of negative gravitaxis in nictating C. japonica DL, which is maintained once initiated, seems to be affected by the age of DL and does not appear to be a simple passive mechanism.Supplementary material available online at

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Section: Discussionmentioning

confidence: 99%

Negative gravitactic behavior ofCaenorhabditis japonicadauer larvae

Okumura

Tanaka

Yoshiga

2013

Journal of Experimental Biology

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“…Although several recent studies suggest that the JO is used in gravitational sensing in Drosophila (Armstrong et al, 2006;Baker et al, 2007;Kamikouchi et al, 2009;Sun et al, 2009), insects are known to have other mechanosensory systems capable of measuring gravity and posture (Beckingham et al, 2005). Thus, we cannot assume that immobilizing the antennal joint removes all cues about the flies' orientation in the gravitational field.…”

Section: Sensory Modalities Involved In Cone Assessmentmentioning

confidence: 93%

Object preference by walking fruit flies, Drosophila melanogaster, is mediated by vision and graviperception

Robie

Straw

Dickinson

2010

Journal of Experimental Biology

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SUMMARYWalking fruit flies, Drosophila melanogaster, use visual information to orient towards salient objects in their environment, presumably as a search strategy for finding food, shelter or other resources. Less is known, however, about the role of vision or other sensory modalities such as mechanoreception in the evaluation of objects once they have been reached. To study the role of vision and mechanoreception in exploration behavior, we developed a large arena in which we could track individual fruit flies as they walked through either simple or more topologically complex landscapes. When exploring a simple, flat environment lacking three-dimensional objects, flies used visual cues from the distant background to stabilize their walking trajectories. When exploring an arena containing an array of cones, differing in geometry, flies actively oriented towards, climbed onto, and explored the objects, spending most of their time on the tallest, steepest object. A fly's behavioral response to the geometry of an object depended upon the intrinsic properties of each object and not a relative assessment to other nearby objects. Furthermore, the preference was not due to a greater attraction towards tall, steep objects, but rather a change in locomotor behavior once a fly reached and explored the surface. Specifically, flies are much more likely to stop walking for long periods when they are perched on tall, steep objects. Both the vision system and the antennal chordotonal organs (Johnston's organs) provide sufficient information about the geometry of an object to elicit the observed change in locomotor behavior. Only when both these sensory systems were impaired did flies not show the behavioral preference for the tall, steep objects. Supplementary material available online at

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“…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).…”

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.

149

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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Genetics of Graviperception in Animals

Cited by 27 publications

References 133 publications

Negative gravitactic behavior ofCaenorhabditis japonicadauer larvae

Negative gravitactic behavior ofCaenorhabditis japonicadauer larvae

Object preference by walking fruit flies, Drosophila melanogaster, is mediated by vision and graviperception

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

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