Transcriptome analysis and RNA interference of cockroach phototransduction indicate three opsins and suggest a major role for TRPL channels

French, Andrew S.; Meisner, Shannon; Liu, Hongxia; Weckström, Matti; Torkkeli, Päivi H.

doi:10.3389/fphys.2015.00207

Cited by 50 publications

(90 citation statements)

References 38 publications

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“…Opsin losses have occurred in other animals, including the American cockroach ( Periplaneta americana ) 28 , deep sea fish 29 , fossorial snakes 30 , caecilians 31 and both nocturnal and aquatic mammals 32–34 . Such losses are typically associated with low-light or spectrally-attenuated environments.…”

Section: Discussionmentioning

confidence: 99%

Overcoming the loss of blue sensitivity through opsin duplication in the largest animal group, beetles

Sharkey

Fujimoto

Lord

et al. 2017

Sci Rep

160

119

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Opsin proteins are fundamental components of animal vision whose structure largely determines the sensitivity of visual pigments to different wavelengths of light. Surprisingly little is known about opsin evolution in beetles, even though they are the most species rich animal group on Earth and exhibit considerable variation in visual system sensitivities. We reveal the patterns of opsin evolution across 62 beetle species and relatives. Our results show that the major insect opsin class (SW) that typically confers sensitivity to "blue" wavelengths was lost ~300 million years ago, before the origin of modern beetles. We propose that UV and LW opsin gene duplications have restored the potential for trichromacy (three separate channels for colour vision) in beetles up to 12 times and more specifically, duplications within the UV opsin class have likely led to the restoration of "blue" sensitivity up to 10 times. This finding reveals unexpected plasticity within the insect visual system and highlights its remarkable ability to evolve and adapt to the available light and visual cues present in the environment.At the molecular level, the wavelength sensitivity of an animal photoreceptor is determined by the photopigment, comprising an opsin protein bound to a light-absorbing chromophore. Insects commonly possess three opsin proteins (UV, SW and LW) that form photopigments maximally sensitive to ultraviolet (~350 nm), blue (~440 nm) and green (~530 nm) wavelengths, respectively. As insect opsin genes form distinct phylogenetic clades according to their spectral class (UV, SW or LW) the sensitivity ranges of an insect visual system can usually be estimated by the complement of opsin genes present. In some insects photopigment sensitivity has extended outside of this range into the violet (~420 nm) and red (>600 nm) region of the light spectrum through duplications of the SW 1,2 and LW opsins 2,3

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Section: Discussionmentioning

confidence: 99%

Overcoming the loss of blue sensitivity through opsin duplication in the largest animal group, beetles

Sharkey

Fujimoto

Lord

et al. 2017

Sci Rep

160

119

View full text Add to dashboard Cite

show abstract

“…However, because RNAi efficacy is variable among insect species (e.g., RNAi experiments were unsuccessful in some studies using Lepidoptera) (Bellés, 2010;Terenius et al, 2011), consideration of the target insect species is required. Previously, RNAi was demonstrated to work well in two cockroach species, P. americana and B. germanica (Cruz et al, 2006;Pueyo et al, 2008;Gomez-Orte & Bellés, 2009;Revuelta et al, 2009;Irles et al, 2013;French et al, 2015;Lozano et al, 2015;Lemonds et al, 2016). For example, the requirement of the melanin pathway for overall body pigmentation in P. americana nymphs and adults was revealed by RNAi of two enzymecoding genes (Lemonds et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

“…Functional analysis of this unique insect group is expected to greatly contribute to the comparative study of V-ATPases. Additionally, RNAi works well as a powerful reverse genetics tool in two other sanitary pest species, P. americana and B. germanica (Cruz et al, 2006;Pueyo et al, 2008;Gomez-Orte & Bellés, 2009;Revuelta et al, 2009;Irles et al, 2013;French et al, 2015;Lozano et al, 2015;Lemonds et al, 2016). Nevertheless there is no report of RNAi in P. fuliginosa, the most abundant pest cockroach species in Japan (The Japanese Society of Pestology, Personal communication).…”

Section: Introductionmentioning

confidence: 99%

Systemic RNAi of V‐ATPase subunit B causes molting defect and developmental abnormalities in Periplaneta fuliginosa

et al. 2018

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The vacuolar (H )-ATPases (V-ATPases) are ATP-driven proton pumps with multiple functions in many organisms. In this study, we performed structural and functional analysis of vha55 gene that encodes V-ATPase subunit B in the smokybrown cockroach Periplaneta fuliginosa (Blattodea). We observed a high homology score of the deduced amino acid sequences between 10 species in seven orders. RNAi of the vha55 gene in P. fuliginosa caused nymphal/nymphal molting defects with incomplete shedding of old cuticles, growth inhibition, as well as bent and wrinkled cuticles of thoraxes and abdominal segments. Since growth inhibition caused by vha55 RNAi did not interfere in the commencement of cockroach molting, molting timing and body growth might be controlled by independent mechanism. Our study suggested V-ATPases might be a good candidate molecule for evolutionary and developmental studies of insect molting.

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“…A transcriptome study in cockroaches found that trpl was approximately 10 times more abundant than trp (French et al 2015). RNAi of trpl reduced electroretinogram (ERG) response much more than trp after 21 days suggesting that, unlike D. melanogaster, cockroach TRPL rather than TRP has a larger contribution to phototransduction (French et al 2015).…”

Section: Ion Channels Used In Diurnal and Nocturnal Insectsmentioning

confidence: 99%

“…Instead a lepidopteran paralog appears to carry out a similar function of chromophore binding (Macias-Muñoz et al 2017). Moreover, as observed in the cockroach, while genes such as TRP and TRPL are conserved and expressed, one gene copy (TRPL) might have a greater impact on phototransduction than the other (French et al 2015). Consequently, investigating both gene gain/loss and the expression of phototransduction genes in Lepidoptera might uncover differences in their visual processing that helps them function in different light environments.…”

Section: Introductionmentioning

confidence: 99%

Evolution of Phototransduction Genes in Lepidoptera

Macias-Muñoz¹,

Briscoe²

2019

Preprint

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Vision is underpinned by phototransduction, a signaling cascade that converts light energy into an electrical signal. Among insects, phototransduction is best understood in Drosophila melanogaster. A survey of phototransduction genes in four insect genomes found gains and losses between D. melanogaster and other insects; this study did not include lepidopterans. Diurnal butterflies and nocturnal moths occupy different light environments and have distinct eye morphologies, which might impact the expression of their phototransduction genes. Here, we used transcriptomics and phylogenetics to identify phototransduction genes that vary between D. melanogaster and Lepidoptera, and between moths and butterflies. Most phototransduction genes were conserved between D. melanogaster and Lepidoptera, with some exceptions. We found two lepidopteran opsins lacking a D. melanogaster ortholog, and using antibodies found that one, a candidate retinochrome which we name unclassified opsin (UnRh), is expressed in the crystaline cone cells and the pigment cells of the butterfly Heliconius melpomene. We also found differences between Lepidoptera and D. melanogaster phototransduction in diacylglycerol regulation where a lepidopteran paralog, DAG, may be taking on a role in vision. Lastly, butterflies express similar amounts of trp and trpl channel mRNAs, while moths express approximately 50x less trp. Since TRP/TRPL channels allow Ca 2+ and Na + influx this might explain why moths appear to express less Calx and Nckx30C Na + /Ca 2+ channel mRNAs. Our findings suggest that while many single-copy D. melanogaster phototransduction genes are conserved in lepidopterans, phototransduction gene expression differences exist between moths and butterflies that may be linked to their visual light environment. 4 downstream pathway by which opsins function might also contribute to differences in visual systems (Plachetzki et al. 2010). Fewer studies have investigated the downstream phototransduction cascade in non-D. melanogaster insects. Studies of phototransduction in other insects have focused on presence, absence, or relative expression of genes in head transcriptomes. In the troglobiont beetle, Ptomaphagus hirtus, for example, 20 genes were identified from adult head mRNA (Friedrich et al. 2011). Exposure of the oriental armyworm, Mythimna separate, to different light environments resulted in differential expression of phototransduction genes in adult heads (Duan et al. 2017). Similarly, phototransduction genes were also differentially expressed between seasonal forms in heads of the butterfly Bicyclus anynana (Macias-Muñoz et al. 2016). One study quantified opsin and TRP channel gene expression and used RNAi to determine that opsin has the largest effect on phototransduction in the nocturnal cockroach Periplaneta americana (but see below)(French et al. 2015). Yet, it remains largely unknown how variable the phototransduction cascade is between insect species.Lepidoptera, moths and butterflies, provide an interesting group in which to invest...

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Transcriptome analysis and RNA interference of cockroach phototransduction indicate three opsins and suggest a major role for TRPL channels

Cited by 50 publications

References 38 publications

Overcoming the loss of blue sensitivity through opsin duplication in the largest animal group, beetles

Overcoming the loss of blue sensitivity through opsin duplication in the largest animal group, beetles

Systemic RNAi of V‐ATPase subunit B causes molting defect and developmental abnormalities in Periplaneta fuliginosa

Evolution of Phototransduction Genes in Lepidoptera

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