Recombinant yellow protein of the takeout family and albino-related takeout protein specifically bind to lutein in the desert locust

Recombinant yellow protein of the takeout family and albino-related takeout protein specifically bind to lutein in the desert locust

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Biochemical and Biophysical Research Communications xxx (xxxx) xxx

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Recombinant yellow protein of the takeout family and albino-related takeout protein specifically bind to lutein in the desert locust Ryohei Sugahara a, **, Wataru Tsuchiya b, Toshimasa Yamazaki b, Seiji Tanaka c, Takahiro Shiotsuki d, * a

Faculty of Agriculture and Life Science, Hirosaki University, Bunkyo-cho 3, Hirosaki, Aomori, 036-8561, Japan National Agriculture and Food Research Organization, Advanced Analysis Center, Kannondai 2-1-2, Tsukuba, Ibaraki, 305-8602, Japan Locust Research Laboratory, National Institute of Agro-biological Sciences, Ohwashi, Tsukuba, Ibaraki, 305-8634, Japan d Faculty of Life and Environmental Science, Shimane University, Nishikawatsu-cho 1060, Matsue, Shimane, 690-8504, Japan b c

a r t i c l e i n f o

a b s t r a c t

Article history: Received 6 November 2019 Accepted 18 November 2019 Available online xxx

Yellow protein of the takeout family (YPT) and albino-related takeout protein (ALTO) are involved in body-color polyphenism in Schistocerca gregaria. YPT has been proposed to bind to b-carotene, whereas the physiological role of ALTO is unclear. Structurally, takeout proteins contain a long continuous tunnel to bind specific ligands. However, the specific ligands of YPT and ALTO have not been fully elucidated. Here, we isolated the full coding cDNAs of these proteins and successfully produced recombinant YPT and ALTO using an Escherichia coli expression system. Absorption spectral analyses of YPT with and without carotenoids revealed that this protein bound to lutein. In contrast, obvious binding of YPT to bcarotene and astaxanthin was not detected. Similar results were obtained for ALTO. The presence of juvenile hormone only weakly affected the protein/carotenoid interactions. These results suggested that YPT and ALTO specifically bound to lutein in a juvenile hormone-independent manner. © 2019 Elsevier Inc. All rights reserved.

Keywords: Desert locust Carotenoids Phenotypic plasticity Takeout family Juvenile hormone Recombinant protein

1. Introduction Animal coloration is important for survival and reproductive success via mechanisms of concealment, thermoregulation, warning of toxicity, mimicry, sexual selection, and linkage to beneficial characteristics [1,2]. In particular, body coloration in grasshoppers is involved in predator avoidance, thermoregulation, microhabitat selection, and mating preferences [3e7]. The desert locust Schistocerca gregaria and the migratory locust Locusta migratoria exhibit body color polyphenism in response to biotic and abiotic environmental stimuli [8e11]. Individuals occurring at low and high population densities are often called solitarious and gregarious locusts, respectively [11]. At later instars, solitarious nymphs develop various cryptic body colors, whereas gregarious nymphs assume yellow color with black patterns in S. gregaria and a dirty orange with black patterns in L. migratoria [8,12]. The black patterns of gregarious nymphs are controlled by the neuropeptide [His7]-

* Corresponding author. ** Corresponding author. E-mail addresses: [email protected] (R. Sugahara), [email protected] shimane-u.ac.jp (T. Shiotsuki).

corazonin (Crz) [13]. Green solitarious S. gregaria and L. migratoria nymphs injected with synthetic Crz develop black patterns characteristic of gregarious forms [13e16]. RNA interference (RNAi)mediated knockdown of the Crz precursor gene CRZ in gregarious nymphs reduces the intensity of their black patterning in both locust species [17,18]. S. gregaria and L. migratoria nymphs that have defects in the Crz pathway fail to develop gregarious body coloration, resulting in albinos [19]. We have previously reported that yellow protein of the takeout family (YPT), also known as yellow protein (YP), is responsible for yellowing in S. gregaria nymphs during the last two instars [20]. The expression of YPT is affected by rearing temperature, injection of juvenile hormone (JH) and Crz, and substrate color of the growing environment during these instars [20]. In contrast, rearing temperature and JH injection do not stimulate YPT expression during early instar nymphs, where yellowing is not observed [21]. YPT was originally identified in S. gregaria male adults as the cause of crowdinducing yellowing at sexual maturity [22]. Adult yellowing is particularly noticeable in male locusts; however, yellowing is also observed in female adults both in the laboratory and the field [23,24]. Levels of this protein and its transcripts at sexual maturity are much higher in males than in females [22,25]. Additionally,

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Please cite this article as: R. Sugahara et al., Recombinant yellow protein of the takeout family and albino-related takeout protein specifically bind to lutein in the desert locust, Biochemical and Biophysical Research Communications, https://doi.org/10.1016/j.bbrc.2019.11.113

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secretion of JH from the corpus allatum is necessary for yellowing to occur in male adults [26]. Goodwin and Srisukh (1949) reported that the yellow colors of S. gregaria and L. migratoria are caused by accumulation of bcarotene in the integument according to absorption spectral analyses conducted by comparisons of purified yellow fraction and crystalline b-carotene. Based on this report, Wybrandt and Andersen (2001) hypothesized that YPT with b-carotene results in the bright yellow color observed in males at sexual maturity, and the visible absorption spectrum from yellow extracts was found to be similar to that of b-carotene. The obtained spectrum contains a cluster of three absorption maxima at 425, 450, and 480 nm [25]. However, Goodwin (1949) did not find b-carotene in exuviae, in which we observed yellow pigment under high rearing temperatures [20]. Therefore, we hypothesized that a compound other than b-carotene may be responsible for yellowing in these locusts. The albino-related takeout gene (ALTO), another takeout family gene, is involved in phase polyphenism in S. gregaria [27]. We previously reported that ALTO expression required the presence of Crz [27]. However, knockdown of ALTO in gregarious nymphs did not affect S. gregaria body coloration. Therefore, the role of ALTO in body color polyphenism is unclear. Takeout family genes were first discovered in Drosophila melanogaster and were conserved only in insects [28]. Structurally, takeout proteins feature a long tunnel, in which specific ligands bind [29,30]. Although YPT and ALTO may bind to certain carotenoids, binding assays between these proteins and carotenoids have not been performed. Accordingly, in the current study, we produced recombinant YPT and ALTO and examined the interactions of these proteins with some carotenoids, including b-carotene, lutein, and astaxanthin, in the presence or absence of JH.

Billerica, MA, USA). Protein expression was induced with 0.2 mM isopropyl b-D-thiogalactopyranoside for 16 h at 16  C. E. coli strains expressing each of these proteins were collected and resuspended in phosphate-buffered saline (PBS; pH 7.4) with complete ethylenediaminetetraacetic acid-free protease inhibitor mixture (Roche Diagnostics, Basel, Switzerland). The cells were lysed by sonication and divided into supernatants (soluble fraction) and cell debris (insoluble fraction) by centrifugation at 18,000 rpm (Avanti J-26S XP, Beckman Coulter Inc., Brea, CA, USA) for 30 min. In our preliminary study, both fractions were subjected to sodium dodecyl sulfate polyacrylamide gel electrophoresis (SDS-PAGE), and protein bands corresponding to GST-YPT and GST-ALTO were exclusively detected in the insoluble fraction. Subsequently, to obtain soluble GST-YPT and GST-ALTO, insoluble fractions were suspended in PBS containing 4 mM 3-([3-cholamidopropyl]-dimethylammonio)-1propanesulfonate (CHAPS) detergent and incubated at 4  C for 1 h. The samples were then centrifuged at 18,000 rpm (Avanti J-26S XP, Beckman Coulter Inc.) for 30 min, and supernatants were dialyzed for 16 h at 4  C against PBS. The resulting extracts were applied to a GSTrap HP column (GE Healthcare). Affinity-purified proteins were purified further on a HiTrap Q HP column (GE Healthcare) and a 0e500 mM NaCl linear elution gradient. The purified soluble proteins were collected and stored at 80  C. 2.4. Chemicals JH III was purchased from Sigma-Aldrich (St. Louis, MO, USA) and dissolved in ethanol at a concentration of 1 mM as a stock solution. b-Carotene, lutein, and astaxanthin were purchased from Fujifilm Wako Pure Chemical Corporation (Osaka, Japan) and were dissolved in ethanol at a concentration of 0.5 mM as stock solutions. 2.5. Carotenoid binding assays

2. Materials and methods 2.1. Cloning of full-length YPT and ALTO cDNA The nucleotide sequences of S. gregaria YPT and ALTO were analyzed for a Niger strain [31]. The 50 region of the YPT cDNA was determined by 50 rapid amplification of cDNA ends (RACE) analyses. The cDNA library was prepared from the pronota of gregarious nymphs at day 5 of the third instar, which were shortly before ecdysis to the fourth instar and is known to show high YPT expression [20]. The primers used for RACE analysis and full-length YPT cloning are listed in Table S1. The full-length open reading frames (ORFs) of YPT and ALTO were inserted into the pENTR11 vector (Invitrogen, Carlsbad, CA, USA) [27]. Nucleotide sequences of YPT and ALTO were deposited in DDBJ (accession numbers: YPT, LC495730; ALTO, LC369735). 2.2. Construction of glutathione S-transferase (GST)-YPT and GSTALTO expression vectors Putative signal peptides were found in the first 22 and 17 amino acid residues of YPT and ALTO, respectively. Primers were designed to exclude the signal peptide sequences of YPT and ALTO (Table S1). The PCR products encoding mature YPT (amino acid residues 23e273) and ALTO (amino acid residues 18e271) were inserted into the pGEX-2T vector (GE Healthcare UK Ltd., Buckinghamshire, England) containing an N-terminal GST tag. 2.3. Production of GST-YPT and GST-ALTO in Escherichia coli The expression constructs for GST-YPT and GST-ALTO were introduced into E. coli strain BL21 (DE3) cells (EMD Millipore Corp.,

Carotenoid metabolism produces diverse carotenoid compositions in the petals of plants, resulting in color variations [32]. Thus, yellowing in S. gregaria may be caused by multiple carotenoids. Previous reports have proposed that crowd-induced yellowing at sexual maturity may be derived from b-carotene [22,33] and that the yellow pigment lutein and the red pigment astaxanthin contribute to diverse coloration in organisms [32,34]. Accordingly, these three pigments were analyzed. The binding between recombinant takeout proteins and carotenoids was evaluated by measuring changes in the peak positions and heights in the absorption spectra after mixing these components. The absorption spectrum for YPT alone was measured to obtain standard data. The ultraviolet and visible absorption spectra were measured on a SpectraMax M (Molecular Devices, Sunnyvale, CA, USA) between 250 and 600 nm at 25  C in 20 mM Tris-HCl (pH 8.5), 100 mM NaCl, and 8 mM CHAPS. The proteins, carotenoids, and JH were added at a concentration of 5 mM to corresponding samples. Each sample was incubated for 6 h at 25  C before measuring the absorption spectra. 3. Results 3.1. Isolation of YPT and ALTO genes and the proteins encoded by these genes We previously reported the full-length ORF of ALTO mRNA [27]. To determine the full-length sequence of YPT, a 50 RACE was performed. After identification of the translation initiation codon of the gene, the full-length ORF of YPT was inserted into a cloning vector and sequenced. The full coding sequences of YPT and ALTO yielded proteins of 273 and 271 amino acid residues with calculated

Please cite this article as: R. Sugahara et al., Recombinant yellow protein of the takeout family and albino-related takeout protein specifically bind to lutein in the desert locust, Biochemical and Biophysical Research Communications, https://doi.org/10.1016/j.bbrc.2019.11.113

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molecular masses of 28 and 30 kDa, respectively. 3.2. Production of recombinant YPT and ALTO To investigate whether YPT and ALTO physically bound to certain carotenoids, recombinant YPT and ALTO with an N-terminal GST tag were produced using an E. coli expression system. These proteins generated in E. coli were solubilized by adding the detergent CHAPS and purified by glutathione-affinity (GSTrap) chromatography after buffer change with 1  PBS by dialysis. The eluted samples were fractionated by ion exchange chromatography, and fractions containing each recombinant protein were pooled. The samples were verified by SDS-PAGE (Fig. 1). From this process, we obtained sufficient amounts of GST-YPT and GST-ALTO proteins for binding assays with carotenoids. 3.3. Recombinant YPT specifically bound to lutein To evaluate the interactions between YPT and some carotenoids, recombinant GST-YPT was mixed with b-carotene, lutein, or astaxanthin, and changes in the ultraviolet and visible absorption spectra were examined. Because previous studies have reported that JH has important roles in expressing yellow body color in S. gregaria [20,26], the effects of JH on the YPT/carotenoid interaction were also examined. The spectrum for YPT had an ultraviolet absorption maximum at 275 nm, whereas absorption of YPT in the 325e490 region was slightly increased after b-carotene addition (Fig. 2A). The presence of JH only weakly affected the increased absorption. Introduction of lutein markedly affected the spectrum for YPT (Fig. 2B). A cluster of four maxima at 380, 425, 450, and 475 nm in the visible region appeared. In addition, the ultraviolet absorption maximum at 275 nm was slightly enhanced. The presence of JH only weakly affected the spectrum changes caused by lutein. Absorption of YPT in the 325e600 region was slightly increased after astaxanthin addition (Fig. 2C); however, the addition of JH only weakly influenced this response.

Fig. 2. Binding of recombinant GST-YPT with three carotenoids. The ultraviolet and visible absorption spectra were measured for the indicated samples. Three carotenoids, i.e., b-carotene (A), lutein (B), and astaxanthin (C), were subjected to analyses with YPT. b-C, b-carotene; Lut, lutein; Ast, astaxanthin. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

3.4. Recombinant ALTO specifically bound to lutein

Fig. 1. Purification of GST-YPT and GST-ALTO produced by the E. coli expression system. GST-tagged proteins were purified through affinity chromatography and ion exchange chromatography. Samples were resolved by SDS-PAGE on 15% gels and visualized by Coomassie Brilliant Blue (CBB) staining. M, protein markers.

Similar assays were performed for recombinant GST-ALTO. The spectrum for the protein had an ultraviolet absorption maximum at 275 nm. Absorption measurements for the mixture of ALTO and bcarotene were slightly higher than that for the protein alone at many wavelengths (Fig. 3A). A cluster of four maxima at 380, 425, 450, and 475 nm in the visible region appeared after lutein addition, similar to the YPT/lutein spectrum (Fig. 3B). A slight enhancement of the ultraviolet absorption maximum at 275 nm was also detected. In the presence of astaxanthin, absorption slightly increased at many wavelengths (Fig. 3C). The presence of JH only weakly influenced the absorption of each of the three carotenoids.

Please cite this article as: R. Sugahara et al., Recombinant yellow protein of the takeout family and albino-related takeout protein specifically bind to lutein in the desert locust, Biochemical and Biophysical Research Communications, https://doi.org/10.1016/j.bbrc.2019.11.113

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Fig. 3. Binding of recombinant GST-ALTO with three carotenoids. The ultraviolet and visible absorption spectra were measured for the indicated samples. Three carotenoids, i.e., b-carotene (A), lutein (B), and astaxanthin (C), were subjected to analyses with ALTO. b-C, b-carotene; Lut, lutein; Ast, astaxanthin. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

and astaxanthin was not detected. Importantly, the spectra for mixtures of lutein and each protein displayed a cluster of three absorption maxima at 425, 450, and 475 nm, similar to a previously reported spectrum for yellow extracts of S. gregaria [22]. This result implied that YPT-dependent yellowing may be accomplished by lutein rather than b-carotene. The spectral analysis in the current study revealed that the absorption results for YPT and ALTO slightly increased after adding bcarotene at several wavelengths. Similarly, addition of astaxanthin to YPT and ALTO slightly increased absorption at many wavelengths. These results may be related to the presence of free carotenoids. The effects of free carotenoids on absorption may explain the increased absorption measurements at 275 and 380 nm after lutein introduction for each protein. Thus, in this study, no evidence was obtained to support that b-carotene or astaxanthin bound to YPT and ALTO. JH binding protein, another takeout family protein, has been shown to interact with JH [40]. This compound is required for yellowing in male adults [26], suggesting that JH regulates YPT at the transcriptional and/or protein level. Our previous study revealed that JH injection increased YPT expression in late instar desert locust nymphs [20]. It is also possible that the YPT protein may physically bind to JH, resulting in conformational changes and increasing its affinity for the carotenoid. However, our current findings showed that recombinant YPT was unlikely to bind to JH, suggesting that JH did not physically affect the function of YPT protein in body color change. Many takeout family genes (23 in D. melanogaster) have also been found in insects [41]. Several products of these genes are involved in circadian behaviors, feeding, male courtship behaviors, and phase polyphenism [42e45]. However, the functions and ligands of most takeout proteins remain unclear. To the best of our knowledge, YPT is the first takeout gene reported to be involved in body color. In this study, we found that ALTO may also be involved in insect body color. Thus, these results suggest the possible roles of takeout family genes in the control of body color in other insects. Although recombinant YPT and ALTO specifically bound to lutein, the physiological statuses of these proteins in live animals should be determined. Information regarding the amounts of carotenoids in locusts is important for determining the ligands of YPT and ALTO in vivo. Contents of b-carotene and astaxanthin in locusts were estimated according to the absorption spectra for locust extracts, as reported previously [33,38]. However, this method is not useful for the determination of objective materials. Further studies are necessary to quantify the amounts of lutein, b-carotene, and astaxanthin using liquid chromatography/mass spectrometry. Declaration of competing interest The authors declare that they have no competing interests.

4. Discussion Acknowledgments Carotenoids are involved in expressing body coloration in many organisms [35,36]. In S. gregaria, the YPT protein is responsible for developing yellow body color [20e22,25], whereas b-carotene has been suggested to be responsible for yellowing [22,33,37,38]. ALTO is exclusively expressed in the integument and is regulated by Crz signaling in S. gregaria [27]. Moreover, locust black color is expressed in the integument mediated by Crz signaling [39], and ALTO may be involved in locust body coloration. In the current study, we successfully generated recombinant YPT and ALTO. The absorption spectra for these proteins notably changed after adding lutein, but showed only slight differences after the addition of bcarotene or astaxanthin. This result indicated that both proteins specifically bound to lutein, whereas obvious binding to b-carotene

We wish to thank Ms. Utako Takano and Mr. Shoichi Enoki for maintaining the locust colonies. In addition, we wish to express our gratitude to Ms. Takayo Nakakura for the assistance with the experimental work. We further thank Messrs. Hirokazu Tomiyama and Kameo Tsukada of the NARO Field Management Section for providing the feed grass for locusts. This work was partially funded by a Grant-in-Aid for JSPS Fellows (no. 15J08228) to RS, JSPS Kakenhi, Japan. Appendix A. Supplementary data Supplementary data to this article can be found online at

Please cite this article as: R. Sugahara et al., Recombinant yellow protein of the takeout family and albino-related takeout protein specifically bind to lutein in the desert locust, Biochemical and Biophysical Research Communications, https://doi.org/10.1016/j.bbrc.2019.11.113

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https://doi.org/10.1016/j.bbrc.2019.11.113. References [1] M.E. Protas, N.H. Patel, Evolution of coloration patterns, Annu. Rev. 24 (2008) 425e446, https://doi.org/10.1146/annurev.cellbio.24.110707.175302. [2] A. Roulin, The evolution, maintenance and adaptive function of genetic colour polymorphism in birds, Biol. Rev. 79 (2004) 815e848. [3] K.D.L. Umbers, M.E. Herberstein, J.S. Madin, Colour in insect thermoregulation: empirical and theoretical tests in the colour-changing grasshopper, Kosciuscola tristis, J. Insect Physiol. 59 (2013) 81e90, https://doi.org/10.1016/ j.jinsphys.2012.10.016. [4] J.M. Dearn, Color pattern polymorphism, in: R.F. Chapman, A. Joern (Eds.), Biology of Grasshoppers, John Wiley Sons, New York, 1990, pp. 517e549. [5] M.A. Chappell, D.W. Whitman, Grasshopper thermoregulation, in: R.F. Chapman, A. Joern (Eds.), Biology of Grasshoppers, John Wiley Sons, New York, 1990, pp. 143e172. [6] A. Forsman, Thermal capacity of different colour morphs in the pygmy grasshopper Tetrix subulata, Ann. Zool. Fenn. 34 (1997) 145e149. €, A. Forsman, Differential habitat selection by pygmy grasshopper [7] J. Ahnesjo color morphs; interactive effects of temperature and predator avoidance, Evol. Ecol. 20 (2006) 235e257, https://doi.org/10.1007/s10682-006-6178-8. [8] M.P. Pener, Locust phase polymorphism and its endocrine relations, Adv. Insect Physiol. 23 (1991) 1e79. [9] M.P. Pener, S.J. Simpson, Locust phase polyphenism: an update, Adv. Insect Physiol. 36 (2009) 1e272. [10] B. Uvarov, Grasshoppers and Locusts: a Handbook of General Acridology. Vol. 1. Anatomy, Physiology, Development, Phase Polymorphism, Introduction to Taxonomy, Cambridge university press, 1966. [11] B. Uvarov, Grasshoppers and Locusts: a handbook of general acridology, in: Behaviour, Ecology, Biogeography, Population Dynamics, vol. 2, Centre for Overseas Pest Research, 1977. [12] S. Tanaka, K. Harano, Y. Nishide, Re-examination of the roles of environmental factors in the control of body-color polyphenism in solitarious nymphs of the desert locust Schistocerca gregaria with special reference to substrate color and humidity, J. Insect Physiol. 58 (2012) 89e101, https://doi.org/10.1016/ j.jinsphys.2011.10.002. [13] A.I. Tawfik, S. Tanaka, A. De Loof, L. Schoofs, G. Baggerman, E. Waelkens, R. Derua, Y. Milner, Y. Yerushalmi, M.P. Pener, Identification of the gregarization-associated dark-pigmentotropin in locusts through an albino mutant, Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 7083e7087. http://www.ncbi. nlm.nih.gov/pubmed/10359842. [14] S. Tanaka, Endocrine mechanisms controlling body-color polymorphism in locusts, Arch. Insect Biochem. Physiol. 47 (2001) 139e149. [15] S. Tanaka, Hormonal control of body-color polymorphism in Locusta migratoria: interaction between [His7]-corazonin and juvenile hormone, J. Insect Physiol. 46 (2000) 1535e1544. http://www.sciencedirect.com/science/article/ pii/S0022191000000810. [16] B. Hoste, S.J. Simpson, S. Tanaka, D.-H. Zhu, A. De Loof, M. Breuer, Effects of [His7]-corazonin on the phase state of isolated-reared (solitarious) desert locusts, Schistocerca gregaria, J. Insect Physiol. 48 (2002) 981e990. http:// www.ncbi.nlm.nih.gov/pubmed/12770045. [17] R. Sugahara, S. Saeki, A. Jouraku, T. Shiotsuki, S. Tanaka, Knockdown of the corazonin gene reveals its critical role in the control of gregarious characteristics in the desert locust, J. Insect Physiol. 79 (2015) 80e87, https:// doi.org/10.1016/j.jinsphys.2015.06.009. [18] R. Sugahara, S. Tanaka, A. Jouraku, T. Shiotsuki, Functional characterization of the corazonin-encoding gene in phase polyphenism of the migratory locust, Locusta migratoria (Orthoptera: acrididae), Appl. Entomol. Zool. 51 (2016) 225e232, https://doi.org/10.1007/s13355-015-0391-2. [19] R. Sugahara, S. Tanaka, A. Jouraku, T. Shiotsuki, Two types of albino mutants in desert and migratory locusts are caused by gene defects in the same signaling pathway, Gene 608 (2017) 41e48, https://doi.org/10.1016/ j.gene.2017.01.022. [20] R. Sugahara, S. Tanaka, Environmental and hormonal control of body color polyphenism in late-instar desert locust nymphs: role of the yellow protein, Insect Biochem. Mol. Biol. 93 (2018) 27e36, https://doi.org/10.1016/ j.ibmb.2017.12.004. [21] R. Sugahara, S. Tanaka, Yellowing and YPT gene expression in the desert locust, Schistocerca gregaria: effects of developmental stages and fasting, Arch. Insect Biochem. Physiol. 101 (2019) e21551, https://doi.org/10.1002/ arch.21551. [22] G.B. Wybrandt, S.O. Andersen, Purification and sequence determination of a yellow protein from sexually mature males of the desert locust, Schistocerca gregaria, Insect Biochem. Mol. Biol. 31 (2001) 1183e1189, https://doi.org/ 10.1016/S0965-1748(01)00064-9. [23] Y. Nishide, S. Tanaka, Yellowing, morphology and behaviour in sexually mature gynandromorphs of the desert locust Schistocerca gregaria, Physiol. Entomol. 37 (2012) 379e383, https://doi.org/10.1111/j.13653032.2012.00854.x.

5

[24] S. Tanaka, K. Maeno, S.O. Mohamed, S.O. Ely, M.A.B. Ebbe, Upsurges of desert locust populations in Mauritania: body coloration, behavior and morphological characteristics, Appl. Entomol. Zool. 45 (2010) 641e652, https://doi.org/ 10.1303/aez.2010.641. [25] F. Sas, M. Begum, T. Vandersmissen, M. Geens, I. Claeys, S. Van Soest, J. Huybrechts, R. Huybrechts, A. De Loof, Development of a real-time PCR assay for measurement of yellow protein mRNA transcription in the desert locust Schistocerca gregaria: a basis for isolation of a peptidergic regulatory factor, Peptides 28 (2007) 38e43, https://doi.org/10.1016/j.peptides.2006.09.015. [26] M.P. Pener, P. Lazarovici, Effect of exogenous juvenile hormones on mating behaviour and yellow colour in allatectomized adult male desert locusts, Physiol. Entomol. 4 (1979) 251e261, https://doi.org/10.1111/j.13653032.1979.tb00202.x. [27] R. Sugahara, S. Tanaka, A. Jouraku, T. Shiotsuki, Identification of a transcription factor that functions downstream of corazonin in the control of desert locust gregarious body coloration, Insect Biochem. Mol. Biol. 97 (2018) 10e18, https://doi.org/10.1016/j.ibmb.2018.04.004. [28] L. Sarov-Blat, W.V. So, L. Liu, M. Rosbash, The Drosophila takeout gene is a novel molecular link between circadian rhythms and feeding behavior, Cell 101 (2000) 647e656, https://doi.org/10.1016/S0092-8674(00)80876-4. [29] C. Hamiaux, D. Stanley, D.R. Greenwood, E.N. Baker, R.D. Newcomb, Crystal structure of Epiphyas postvittana takeout 1 with bound ubiquinone supports a role as ligand carriers for takeout proteins in insects, J. Biol. Chem. 284 (2009) 3496e3503, https://doi.org/10.1074/jbc.M807467200. [30] R. Suzuki, Z. Fujimoto, T. Shiotsuki, W. Tsuchiya, M. Momma, A. Tase, M. Miyazawa, T. Yamazaki, Structural mechanism of JH delivery in hemolymph by JHBP of silkworm, Bombyx mori, Sci. Rep. 133 (2011) 1e9, https:// doi.org/10.1038/srep00133. [31] S. Tanaka, Y. Nishide, Behavioral phase shift in nymphs of the desert locust, Schistocerca gregaria: special attention to attraction/avoidance behaviors and the role of serotonin, J. Insect Physiol. 59 (2013) 101e112, https://doi.org/ 10.1016/j.jinsphys.2012.10.018. , S. Naqvi, L. Shi, T. Capell, [32] C. Zhu, C. Bai, G. Sanahuja, D. Yuan, G. Farre P. Christou, The regulation of carotenoid pigmentation in flowers, Arch. Biochem. Biophys. 504 (2010) 132e141, https://doi.org/10.1016/ j.abb.2010.07.028. [33] T.W. Goodwin, The biochemistry of locusts. 2. Carotenoid distribution in solitary and gregarious phases of the African migratory locust (Locusta migratoria migratorioides R. & F.) and the desert locust (Schistocerca gregaria Forsk.), Biochem. J. 45 (1949) 472e479. [34] D.P.L. Toews, N.R. Hofmeister, S.A. Taylor, The evolution and genetics of carotenoid processing in animals, Trends Genet. 33 (2017) 171e182, https:// doi.org/10.1016/j.tig.2017.01.002. [35] A.L. Bezzerides, K.J. Mcgraw, R.S. Parker, J. Husseini, Elytra color as a signal of chemical defense in the Asian ladybird beetle Harmonia axyridis, Behav. Ecol. Sociobiol. 61 (2007) 1401e1408, https://doi.org/10.1007/s00265-007-0371-9. [36] B. Yuangsoi, O. Jintasataporn, N. Areechon, P. Tabthipwon, The pigmenting effect of different carotenoids on fancy carp (Cyprinus carpio), Aquacult. Nutr. 17 (2011) e306ee316, https://doi.org/10.1111/j.1365-2095.2010.00764.x. [37] A. De Loof, J. Huybrechts, M. Geens, T. Vandersmissen, B. Boerjan, L. Schoofs, Sexual differentiation in adult insects: male-specific cuticular yellowing in Schistocerca gregaria as a model for reevaluating some current (neuro)endocrine concepts, J. Insect Physiol. 56 (2010) 919e925, https://doi.org/10.1016/ j.jinsphys.2010.02.021. [38] T.W. Goodwin, S. Srisukh, The biochemistry of locusts. 1. The carotenoids of the integument of two locust species (Locusta migratoria migratorioides R. & F. and Schistocerca gregaria Forsk.), Biochem. J. 45 (1949) 263e268. [39] S. Tanaka, The role of [His7]-corazonin in the control of body-color polymorphism in the migratory locust, Locusta migratoria (Orthoptera: acrididae), J. Insect Physiol. 46 (2000) 1169e1176. http://www.sciencedirect.com/ science/article/pii/S0022191099002280#. [40] K. Touhara, K.A. Lerro, B.C. Bonning, B.D. Hammock, G.D. Prestwich, Ligand binding by a recombinant insect juvenile hormone binding protein, Biochemistry 32 (1993) 2068e2075. [41] S. Saurabh, N. Vanaphan, W. Wen, B. Dauwalder, High functional conservation of takeout family members in a courtship model system, PLoS One 13 (2018) e0204615. [42] K. Fujikawa, K. Seno, M. Ozaki, A novel Takeout-like protein expressed in the taste and olfactory organs of the blowfly, Phormia regina, FEBS J. 273 (2006) 4311e4321, https://doi.org/10.1111/j.1742-4658.2006.05422.x. [43] W. Guo, X. Wang, Z. Ma, L. Xue, J. Han, D. Yu, L. Kang, CSP and takeout genes modulate the switch between attraction and repulsion during behavioral phase change in the migratory locust, PLoS Genet. 7 (2011) e1001291, https:// doi.org/10.1371/journal.pgen.1001291. [44] B. Dauwalder, S. Tsujimoto, J. Moss, W. Mattox, The Drosophila takeout gene is regulated by the somatic sex-determination pathway and affects male courtship behavior, Genes Dev. 16 (2002) 2879e2892, https://doi.org/ 10.1101/gad.1010302.rily. [45] L. Sarov-Blat, W.V. So, L. Liu, M. Rosbash, The Drosophila takeout gene is a novel molecular link between circadian rhythms and feeding behavior, Cell 101 (2000) 647e656, https://doi.org/10.1016/S0092-8674(00)80876-4.

Please cite this article as: R. Sugahara et al., Recombinant yellow protein of the takeout family and albino-related takeout protein specifically bind to lutein in the desert locust, Biochemical and Biophysical Research Communications, https://doi.org/10.1016/j.bbrc.2019.11.113