The Ionotropic Receptors IR21a and IR25a mediate cool sensing in<i>Drosophila</i>

Ni, Lina; Klein, Mason; Svec, Kathryn V.; Budelli, Gonzalo; Chang, Elaine; Benton, Richard; Samuel, Aravinthan D. T.; Garrity, Paul

doi:10.1101/032540

Cited by 35 publications

(63 citation statements)

References 27 publications

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“…We then tested the humidity preferences of the fruit fly stocks described above. Wild type flies preferred high (saturated NaCl, 70%) over low (saturated LiCl, 20%) humidity but this preference was significantly impaired in IR25a and IR93a mutants, as previously reported 33,35,36,38 . However, we did not detect humidity preference defect with IR93a mutant.…”

Section: Resultssupporting

confidence: 86%

“…Based on the phylogenetic tree of T. mercedesae IR and iGluR genes, together with those of D. melanogaster and Ixodes scapularis 37 , we found only two (out of eight) IRs ( Tm15229 and Tm15231 ) were conserved, having the D. melanogaster orthologs, IR93a and IR25a , respectively. DmIR93a and DmIR25a have been shown to play roles in temperature and humidity preferences 33,35,36 . To test whether the sensory functions of IR93a and IR25a are deeply conserved between fruit flies and mites, we first obtained the full length cDNAs of Tm15229 and Tm15231 by determining both the 5’ and 3’ end sequences using RACE methods.…”

Section: Resultsmentioning

confidence: 99%

“…IRs have specifically evolved in protostomes 30 and are best characterized in the fruit fly, Drosophila melanogaster . Most IRs are expressed in sensory neurons and function as chemoreceptors to detect various odorants and tastants 31,32 Recent studies have also demonstrated that IR21a, IR40a, IR68a, IR93a, and IR25a are critical for thermo- and hygrosensation, suggesting that IRs have diverse physiological roles as well as gating mechanisms 33–36 . IR25a has the same protein domains as iGluRs, is expressed broadly in various sensory neurons, and is deeply conserved in protostomes.…”

Section: Introductionmentioning

confidence: 99%

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Honey bee parasitic mite contains the sensory organ expressing ionotropic receptors with conserved functions

Lei

Liu

Kadowaki

2018

Preprint

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17Honey bee parasitic mites (Tropilaelaps mercedesae and Varroa destructor) detect 18 temperature, humidity, and odor but the underlying sensory mechanisms are poorly 19 understood. To uncover how T. mercedesae responds to environmental stimuli inside a 20 hive, we identified the sensilla-rich sensory organ on the foreleg tarsus. The organ 21 contained four types of sensilla, which may respond to different stimuli based on their 22 morphology. We found the forelegs were enriched with mRNAs encoding sensory 23 proteins such as ionotropic receptors (IRs) and gustatory receptors (GRs), as well as 24 proteins involved in ciliary transport. We also found that T. mercedesae and Drosophila 25 melanogaster IR25a and IR93a are functionally equivalent. These results demonstrate 26 that the structures and physiological functions of ancient IRs have been conserved 27 during arthropod evolution. Our study provides insight into the sensory mechanisms of 28 honey bee parasitic mites, as well as potential targets for methods to control the most 29 serious honey bee pest. 31The number of managed honey bee colonies has declined across North America and 33 Europe in recent years 1 . Pollination by honey bees is critical for maintaining 34 ecosystems and producing many agricultural crops 2,3 . Prevention of honey bee losses 35 has, therefore, become a major issue in apiculture and agriculture. Although there are 36 many potential causes for the observed declines, ectoparasitic mites are considered to be 37 major threats to the health of honey bees and their colonies 1,4 . Varroa destructor is 38 present globally (except Australia) and causes both abnormal brood development and 39 brood death in honey bee colonies 5 . The mites feed on hemolymph and also spread 40 honey bee viruses, particularly deformed wing virus (DWV) 6,7 . In many Asian 41 countries, another honey bee ectoparasitic mite, Tropilaelaps mercedesae, is also 42 prevalent in Apis mellifera colonies 8,9 . These two emerging parasites of A. mellifera 43 share many characteristics 10 . For example, they have similar reproductive strategies 11 44 and both are vectors for DWV [12][13][14][15] . As a result, T. mercedesae or V. destructor 45 infestations have similar negative impacts on A. mellifera colonies [16][17][18] . Although T. 46 mercedesae is currently restricted to Asia, it has the potential to spread and establish 47 worldwide due to the global trade in honey bees. 48V. destructor prefers temperatures of 32 ± 2.9 ℃, reproduces best at 49 32.5-33.4 ℃, and has been shown to discriminate temperature differences of 1 ℃ 19-21 . 50Furthermore, its reproduction also depends on humidity of 55-70 % 22 . These results 51 demonstrate thermo-and hygrosensation of V. destructor play important roles to adapt 52 to the honey bee hive environment; nevertheless, chemoreception must be most 53 important in the various interactions between mites and their honey bee hosts. For 54 example, V. destructor prefers to parasitize nurse bees rather than foragers during its 55 phoreti...

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Section: Resultssupporting

confidence: 86%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Honey bee parasitic mite contains the sensory organ expressing ionotropic receptors with conserved functions

Lei

Liu

Kadowaki

2018

Preprint

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“…The participation of ionotropic family receptors in nonchemosensory behaviour is an intriguing aspect of the IR sensation mechanism. Among the non-chemosensory functions of IRs, the involvement of IR25a as a warmth sensor as well as a cool sensor is an interesting phenomenon (Chen et al, 2015;Ni et al, 2016).…”

Section: Conclusion and Future Prospectsmentioning

confidence: 99%

The multidimensional ionotropic receptors of Drosophila melanogaster

Rimal

Lee

2017

Insect Molecular Biology

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Ionotropic receptors (IRs), which form ion channels, can be categorized into conserved 'antennal IRs', which define the first olfactory receptor family of insects, and species-specific 'divergent IRs', which are expressed in gustatory receptor neurones. These receptors are located primarily in cell bodies and dendrites, and are highly enriched in the tips of the dendritic terminals that convey sensory information to higher brain centres. Antennal IRs play important roles in odour and thermosensation, whereas divergent IRs are involved in other important biological processes such as taste sensation. Some IRs are known to play specific biological roles in the perception of various molecules; however, many of their functions have not yet been defined. Although progress has been made in this field, many functions and mechanisms of these receptors remain unknown. In this review, we provide a comprehensive summary of the current state of knowledge in this field.

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“…1-2). Expression of Gal4 drivers for only four other antennal IRs was detected in the dorsal organ: IR21a and IR93a, which act (with IR25a) in cool temperature-sensing 21,40 , IR68a, which functions (with IR25a and IR93a) in moist air sensing 22,24 and IR92a, which mediates olfactory sensitivity to ammonia 14,41 . These observations suggest that the larval dorsal organ, like the adult antenna, has olfactory, thermosensory and hygrosensory roles.…”

Section: Diverse Sensory Neuron Expression and Central Projections Ofmentioning

confidence: 99%

An expression atlas of chemosensory ionotropic glutamate receptors identifies a molecular basis of carbonation detection

Sánchez-Alcañiz

Silbering

Croset

et al. 2018

Preprint

Self Cite

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Taste perception is thought to involve the encoding of appetitive and aversive chemical cues in food through a limited number of sensory pathways. Through expression analysis of the complete repertoire of Drosophila Ionotropic Receptors (IRs), a sensory subfamily of ionotropic glutamate receptors, we reveal that the majority of IRs is expressed in diverse peripheral neuron populations across gustatory organs in both larvae and adults, implying numerous roles in taste-evoked behaviours. We characterise Ir56d, which labels two anatomically-distinct classes of neurons in the proboscis: one represents a subset of sugar-and fatty acid-sensing neurons, while the other responds to carbonated solutions and fatty acids. Mutational analysis shows that IR56d, together with the broadly-expressed co-receptors IR25a and IR76b, is essential for physiological activation by carbonation and fatty acids, but not sucrose. We further demonstrate that carbonation is behaviourally attractive to flies (in an IR56d-dependent manner), but in a distinct way to other appetitive stimuli. Our work provides a valuable toolkit for investigating the taste functions of IRs, defines a molecular basis of carbonation sensing, and illustrates how the gustatory system uses combinatorial expression of sensory receptors in distinct neuron types to coordinate behaviour.Classic models of gustatory perception in mammals highlight the existence of a small number of taste classes signalling nutritive content (e.g., sugars and amino acids) or toxicity (e.g., bitter) that determine -through activation of hard-wired neural circuits -behavioural acceptance or rejection of food 1, 2 . Different classes of tastants are recognised by discrete sensory channels that express distinct, and relatively small, receptor families. For example, detection of all sugars depends upon a single heterodimeric GPCR complex (T1R2/T1R3), while "bitter" cells -which detect an enormous diversity of noxious compounds -co-express a few dozen GPCRs of the T2R family 1, 2 . Such models have been pervasive in interpreting how gustatory perception occurs in other animals, including insects, where analogous segregated sensory pathways for sweet and bitter compounds have been defined [3][4][5][6] . However, in contrast to mammals, where taste -mediated by lingual taste buds -informs only feeding decisions, insect gustation occurs in multiple sensory appendages, including the proboscis, legs, wings and sexual organs, and controls diverse behaviours, such as foraging, feeding, sexual/social recognition and oviposition [3][4][5][6] . In addition to stereotyped appetitive and aversive feeding responses to sweet and bitter compounds respectively, insects display behavioural reactions to many other types of chemicals, including salt 7 , water 8 , carbonation (i.e., aqueous CO 2 ) 9 , organic and inorganic acids 10,11 , and pheromonal cuticular hydrocarbons 12 . The wide-ranging roles of the insect gustatory system are concordantly reflected in the underlying molecular receptors that mediate...

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The Ionotropic Receptors IR21a and IR25a mediate cool sensing inDrosophila

Cited by 35 publications

References 27 publications

Honey bee parasitic mite contains the sensory organ expressing ionotropic receptors with conserved functions

Honey bee parasitic mite contains the sensory organ expressing ionotropic receptors with conserved functions

The multidimensional ionotropic receptors of Drosophila melanogaster

An expression atlas of chemosensory ionotropic glutamate receptors identifies a molecular basis of carbonation detection

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