Chromophore-Independent Roles of Opsin Apoproteins in Drosophila Mechanoreceptors

Katana, Radoslaw; Guan, Chonglin; Zanini, Damiano; Larsen, Matthew E.; Giraldo, Diego; Geurten, Bart R. H.; Schmidt, Christoph F.; Britt, Steven G.; Göpfert, Martin C.

doi:10.1016/j.cub.2019.07.036

Cited by 15 publications

(9 citation statements)

References 61 publications

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“…Beyond these aspects of cell-type evolution, our results also help to inform the functional evolution of Opsin proteins. The observation that rhabdomeric opsins appear to serve light-independent structural roles in the fly’s mechanosensory cells of the JO and ChO has led to the suggestion that such light-independent, cell-mechanical roles are the ancestral function of animal r-opsins ( Katana et al, 2019 ; Zanini et al, 2018 ), which contrasts with our hypothesis. We would argue, however, that r-opsins only constitute one of nine opsin families that already existed at the dawn of bilaterian evolution, and light sensitivity is a common feature of its extant members ( Ramirez et al, 2016 ).…”

Section: Discussioncontrasting

confidence: 85%

Characterization of cephalic and non-cephalic sensory cell types provides insight into joint photo- and mechanoreceptor evolution

Revilla-i-Domingo

Rajan

Waldherr

et al. 2021

eLife

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Rhabdomeric opsins (r-opsins) are light-sensors in cephalic eye photoreceptors, but also function in additional sensory organs. This has prompted questions on the evolutionary relationship of these cell types, and if ancient r-opsins were non-photosensory. A molecular profiling approach in the marine bristleworm Platynereis dumerilii revealed shared and distinct features of cephalic and non-cephalic of r-opsin1-expressing cells. Non-cephalic cells possess a full set of phototransduction components, but also a mechanosensory signature. Prompted by the latter, we investigated Platynereis putative mechanotransducer, and found nompc and pkd2.1 co-expressed with r-opsin1 in TRE cells by HCR RNA-FISH. To further assess the role of r-Opsin1 in these cells, we studied its signaling properties and unraveled that r-Opsin1 is a Gαq-coupled blue-light receptor. Profiling of cells from r-opsin1 mutants versus wild-types, and a comparison under different light conditions reveals that in the non-cephalic cells, light - mediated by r-Opsin1 - adjusts the expression level of a calcium transporter relevant for auditory mechanosensation in vertebrates. We establish a deep learning-based quantitative behavioral analysis for animal trunk movements, and identify a light- and r-Opsin-1-dependent fine-tuning of the worm's undulatory movements in headless trunks, which are known to require mechanosensory feedback. Our results provide new data on peripheral cell types of likely light-sensory/mechanosensory nature. These results point towards a concept in which such a multisensory cell type evolved to allow for fine-tuning of mechanosensation by light. This implies that light-independent mechanosensory roles of r-opsins may have evolved secondarily.

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Section: Discussioncontrasting

confidence: 85%

Characterization of cephalic and non-cephalic sensory cell types provides insight into joint photo- and mechanoreceptor evolution

Revilla-i-Domingo

Rajan

Waldherr

et al. 2021

eLife

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“…Nonvisual hypothesis. Although we have no way to test this hypothesis, given the data presented here, previous studies of Drosophila have shown that visual opsins can have light-independent functions, including thermal preference (50), mechanoreception (51,52), and larval locomotion. Therefore, we cannot rule out the possibility that some of the opsin transcripts expressed in the N. oerstedii retina have nonvisual functions.…”

Section: Why Do Stomatopods Have So Many Opsins In Their Retinas?mentioning

confidence: 79%

Exceptional diversity of opsin expression patterns in Neogonodactylus oerstedii (Stomatopoda) retinas

Porter

Awata

Bok

et al. 2020

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

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Stomatopod crustaceans possess some of the most complex animal visual systems, including at least 16 spectrally distinct types of photoreceptive units (e.g., assemblages of photoreceptor cells). Here we fully characterize the set of opsin genes expressed in retinal tissues and determine expression patterns of each in the stomatopod Neogonodactylus oerstedii. Using a combination of transcriptome and RACE sequencing, we identified 33 opsin transcripts expressed in each N. oerstedii eye, which are predicted to form 20 long-wavelength–sensitive, 10 middle-wavelength–sensitive, and three UV-sensitive visual pigments. Observed expression patterns of these 33 transcripts were highly unusual in five respects: 1) All long-wavelength and short/middle-wavelength photoreceptive units expressed multiple opsins, while UV photoreceptor cells expressed single opsins; 2) most of the long-wavelength photoreceptive units expressed at least one middle-wavelength–sensitive opsin transcript; 3) the photoreceptors involved in spatial, motion, and polarization vision expressed more transcripts than those involved in color vision; 4) there is a unique opsin transcript that is expressed in all eight of the photoreceptive units devoted to color vision; and 5) expression patterns in the peripheral hemispheres of the eyes suggest visual specializations not previously recognized in stomatopods. Elucidating the expression patterns of all opsin transcripts expressed in the N. oerstedii retina reveals the potential for previously undocumented functional diversity in the already complex stomatopod eye and is a first step toward understanding the functional significance of the unusual abundance of opsins found in many arthropod species’ visual systems.

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“…LACE has been used to study the effect of opsins on the locomotion in Drosophila larvae (Zanini et al, 2018 ; Katana et al, 2019 ), revealing that these animals require visual opsins for proper locomotion and body contractions. The here published data set illustrates LACE's ability to faithfully track the contractions and locomotion of Drosophila larvae.…”

Section: Methodsmentioning

confidence: 99%

“…In example I, we analyse the peristaltic movement of Drosophila late 3rd instar larvae. The ion channel mutants nan 36a and iav 1 display disturbed chordotonal neuron function (Kim et al, 2003 ; Gong et al, 2004 ; Zhang et al, 2013 ), causing locomotion and contraction defects (Zanini et al, 2018 ; Katana et al, 2019 ). We use these mutants and the wild-type to illustrate the ability of LACE to detect genetic alterations in the body movements of small limbless animals.…”

Section: Introductionmentioning

confidence: 99%

A Markerless Pose Estimator Applicable to Limbless Animals

Garg

André

Giraldo

et al. 2022

Front. Behav. Neurosci.

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The analysis of kinematics, locomotion, and spatial tasks relies on the accurate detection of animal positions and pose. Pose and position can be assessed with video analysis programs, the “trackers.” Most available trackers represent animals as single points in space (no pose information available) or use markers to build a skeletal representation of pose. Markers are either physical objects attached to the body (white balls, stickers, or paint) or they are defined in silico using recognizable body structures (e.g., joints, limbs, color patterns). Physical markers often cannot be used if the animals are small, lack prominent body structures on which the markers can be placed, or live in environments such as aquatic ones that might detach the marker. Here, we introduce a marker-free pose-estimator (LACE Limbless Animal traCkEr) that builds the pose of the animal de novo from its contour. LACE detects the contour of the animal and derives the body mid-line, building a pseudo-skeleton by defining vertices and edges. By applying LACE to analyse the pose of larval Drosophila melanogaster and adult zebrafish, we illustrate that LACE allows to quantify, for example, genetic alterations of peristaltic movements and gender-specific locomotion patterns that are associated with different body shapes. As illustrated by these examples, LACE provides a versatile method for assessing position, pose and movement patterns, even in animals without limbs.

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Chromophore-Independent Roles of Opsin Apoproteins in Drosophila Mechanoreceptors

Abstract: Highlights d Drosophila mechanosensation requires opsins but no retinal chromophore d Mechanosensory opsin function is independent of the retinal attachment site d Mechanosensation involves visual chromophore pathway components d Mechanosensory organs express chromophore pathway genes

Cited by 15 publications

References 61 publications

Characterization of cephalic and non-cephalic sensory cell types provides insight into joint photo- and mechanoreceptor evolution

Characterization of cephalic and non-cephalic sensory cell types provides insight into joint photo- and mechanoreceptor evolution

Exceptional diversity of opsin expression patterns in Neogonodactylus oerstedii (Stomatopoda) retinas

A Markerless Pose Estimator Applicable to Limbless Animals

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