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Haruka Endo
Graduate School of Bio-Applications and Systems Engineering, Tokyo University of Agriculture and Technology, Koganei, Tokyo, Japan

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Research article
Published: 16 September 2020 in PLOS Biology
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Many herbivorous insects are mono- or oligophagous, having evolved to select a limited range of host plants. They specifically identify host-plant leaves using their keen sense of taste. Plant secondary metabolites and sugars are thought to be key chemical cues that enable insects to identify host plants and evaluate their quality as food. However, the neuronal and behavioral mechanisms of host-plant recognition are poorly understood. Here, we report a two-factor host acceptance system in larvae of the silkworm Bombyx mori, a specialist on several mulberry species. The first step is controlled by a chemosensory organ, the maxillary palp (MP). During palpation at the leaf edge, the MP detects trace amounts of leaf-surface compounds, which enables host-plant recognition without biting. Chemosensory neurons in the MP are tuned with ultrahigh sensitivity (thresholds of attomolar to femtomolar) to chlorogenic acid (CGA), quercetin glycosides, and β-sitosterol (βsito). Only if these 3 compounds are detected does the larva make a test bite, which is evaluated in the second step. Low-sensitivity neurons in another chemosensory organ, the maxillary galea (MG), mainly detect sucrose in the leaf sap exuded by test biting, allowing larvae to accept the leaf and proceed to persistent biting (feeding). The two-factor host acceptance system reported here may commonly underlie stereotyped feeding behavior in many phytophagous insects and determine their feeding habits.

ACS Style

Kana Tsuneto; Haruka Endo; Fumika Shii; Ken Sasaki; Shinji Nagata; Ryoichi Sato. Diet choice: The two-factor host acceptance system of silkworm larvae. PLOS Biology 2020, 18, e3000828 .

AMA Style

Kana Tsuneto, Haruka Endo, Fumika Shii, Ken Sasaki, Shinji Nagata, Ryoichi Sato. Diet choice: The two-factor host acceptance system of silkworm larvae. PLOS Biology. 2020; 18 (9):e3000828.

Chicago/Turabian Style

Kana Tsuneto; Haruka Endo; Fumika Shii; Ken Sasaki; Shinji Nagata; Ryoichi Sato. 2020. "Diet choice: The two-factor host acceptance system of silkworm larvae." PLOS Biology 18, no. 9: e3000828.

Preprint
Published: 31 July 2019
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Oligophagous insect herbivores specifically identify host-plant leaves using their keen sense of taste1. Plant secondary metabolites and sugars are key chemical cues for insects to identify host plants and evaluate their nutritional value, respectively2. However, it is poorly understood how the insect chemosensory system integrates the information from various gustatory inputs. Here we report that a two-step chemosensory system is responsible for host acceptance by larvae of the silkworm Bombyx mori, a specialist for several mulberry species. The first step controlled by a gustatory organ, the maxillary palp (MP), is host-plant recognition during palpation at the leaf edge. Surprisingly, MP detects chlorogenic acid, quercetin glycosides, and β-sitosterol, which stimulate feeding by the silkworm3–6, with ultra-sensitivity (thresholds of aM to fM). Detecting a mixture of these compounds triggers test biting. The second step is evaluation of the sugar content in the leaf sap exuded by test biting. Low-sensitivity chemosensory neurons in another gustatory organ, the maxillary galea (MG), mainly detect sucrose in the leaf sap exuded by test biting, allowing larvae to accept the leaf and proceed to persistent biting. Our present work shows the behavioral and neuronal basis of host acceptance in the silkworm, mainly driven by six phytochemicals. It also reveals that the ultra-sensitive gustation via MP strictly limits initiation of feeding in the silkworm unless it detects a certain combination of host compounds, suggesting an essential role of MP in host-plant selection. The two-step chemosensory system reported herein may commonly underlie stereotyped feeding behavior in phytophagous insects and determine their feeding habits.

ACS Style

Kana Tsuneto; Haruka Endo; Fumika Shii; Ken Sasaki; Shinji Nagata; Ryoichi Sato. The two-step chemosensory system underlying the oligophagy of silkworm larvae. 2019, 1 .

AMA Style

Kana Tsuneto, Haruka Endo, Fumika Shii, Ken Sasaki, Shinji Nagata, Ryoichi Sato. The two-step chemosensory system underlying the oligophagy of silkworm larvae. . 2019; ():1.

Chicago/Turabian Style

Kana Tsuneto; Haruka Endo; Fumika Shii; Ken Sasaki; Shinji Nagata; Ryoichi Sato. 2019. "The two-step chemosensory system underlying the oligophagy of silkworm larvae." , no. : 1.

Review
Published: 19 February 2019 in Toxins
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When ABC transporter family C2 (ABCC2) and ABC transporter family B1 (ABCB1) were heterologously expressed in non-susceptible cultured cells, the cells swelled in response to Cry1A and Cry3 toxins, respectively. Consistent with the notion that 3D-Cry toxins form cation-permeable pores, Bombyx mori ABCC2 (BmABCC2) facilitated cation-permeable pore formation by Cry1A when expressed in Xenopus oocytes. Furthermore, BmABCC2 had a high binding affinity (KD) to Cry1Aa of 3.1 × 10−10 M. These findings suggest that ABC transporters, including ABCC2 and ABCB1, are functional receptors for 3D-Cry toxins. In addition, the Cry2 toxins most distant from Cry1A toxins on the phylogenetic tree used ABC transporter A2 as a receptor. These data suggest that 3D-Cry toxins use ABC transporters as receptors. In terms of inducing cell swelling, ABCC2 has greater activity than cadherin-like receptor. The pore opening of ABC transporters was hypothesized to be linked to their receptor function, but this was repudiated by experiments using mutants deficient in export activity. The synergistic relationship between ABCC2 and cadherin-like receptor explains their ability to cause resistance in one species of insect.

ACS Style

Ryoichi Sato; Satomi Adegawa; Xiaoyi Li; Shiho Tanaka; Haruka Endo. Function and Role of ATP-Binding Cassette Transporters as Receptors for 3D-Cry Toxins. Toxins 2019, 11, 124 .

AMA Style

Ryoichi Sato, Satomi Adegawa, Xiaoyi Li, Shiho Tanaka, Haruka Endo. Function and Role of ATP-Binding Cassette Transporters as Receptors for 3D-Cry Toxins. Toxins. 2019; 11 (2):124.

Chicago/Turabian Style

Ryoichi Sato; Satomi Adegawa; Xiaoyi Li; Shiho Tanaka; Haruka Endo. 2019. "Function and Role of ATP-Binding Cassette Transporters as Receptors for 3D-Cry Toxins." Toxins 11, no. 2: 124.

Journal article
Published: 02 August 2018 in Insect Biochemistry and Molecular Biology
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Cry proteins from Bacillus thuringiensis (Bt) have been used to control insect pests either as formulated sprays or as in Bt-crops. However, field-evolved resistance to Bt proteins is threatening the long-term use of Bt products. The SeABCC2 locus has been genetically linked to resistance to a Bt bioinsecticide (Xentari™) in Spodoptera exigua (a mutation producing a truncated form of the transporter lacking an ATP binding domain was found in the resistant insects). Here, we investigated the role of SeABCC2 in the mode of action of Cry1Aa, Cry1Ab, Cry1Ac, Cry1Ca, and two Cry1A-1Ca hybrids by expressing the receptor in Sf21 and HEK293T cell lines. Cell toxicity assays showed that Sf21 cells expressing SeABCC2 become susceptible to Cry1A proteins. HEK293T cells expressing the transporter were found susceptible to Cry1A proteins but not to Cry1Ca. The results with the Cry1A-1Ca hybrids suggest that domain II from Cry1Ab/c is crucial for the toxicity to Sf21 cells, whereas domain III from Cry1Aa/b is crucial for the toxicity to HEK293T cells. Binding assays showed that the Cry1Ac binding is of high affinity and specific to cells expressing the SeABCC2 transporter. Heterologous competition experiments support a model in which domain II of Cry1Ab/c has a common binding site in the SeABCC2 protein, whereas domain III of Cry1Aa/b binds to a different binding site in the SeABCC2 protein.

ACS Style

María Martínez-Solís; Daniel Pinos; Haruka Endo; Leivi Portugal; Ryoichi Sato; Juan Ferré; Salvador Herrero; Patricia Hernández-Martínez. Role of Bacillus thuringiensis Cry1A toxins domains in the binding to the ABCC2 receptor from Spodoptera exigua. Insect Biochemistry and Molecular Biology 2018, 101, 47 -56.

AMA Style

María Martínez-Solís, Daniel Pinos, Haruka Endo, Leivi Portugal, Ryoichi Sato, Juan Ferré, Salvador Herrero, Patricia Hernández-Martínez. Role of Bacillus thuringiensis Cry1A toxins domains in the binding to the ABCC2 receptor from Spodoptera exigua. Insect Biochemistry and Molecular Biology. 2018; 101 ():47-56.

Chicago/Turabian Style

María Martínez-Solís; Daniel Pinos; Haruka Endo; Leivi Portugal; Ryoichi Sato; Juan Ferré; Salvador Herrero; Patricia Hernández-Martínez. 2018. "Role of Bacillus thuringiensis Cry1A toxins domains in the binding to the ABCC2 receptor from Spodoptera exigua." Insect Biochemistry and Molecular Biology 101, no. : 47-56.

Journal article
Published: 19 June 2018 in Peptides
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Enteroendocrine cells in the insect midgut are thought to secrete peptide hormones in response to the nutritional state. However, the role of dietary compounds in inducing peptide hormone secretion from enteroendocrine cells in insects remains unknown. In the present study, we demonstrated that several dietary compounds from mulberry leaves, including glucose, amino acids, and the secondary metabolite chlorogenic acid, induced significant secretion of tachykinin-related peptides from isolated silkworm midguts at the luminal concentrations measured in fed larvae. This study provides evidence that the insect midgut senses a non-nutritious secondary metabolite in addition to nutrient metabolites to monitor luminal food status and secretes a feeding regulatory hormone, suggesting that a unique dietary sensory system modulates insect feeding via enteroendocrine control.

ACS Style

Takayuki Yamagishi; Haruka Endo; Keisuke Fukumura; Shinji Nagata; Tohru Hayakawa; Satomi Adegawa; Mayu Kasubuchi; Ryoichi Sato. Glucose, some amino acids and a plant secondary metabolite, chlorogenic acid induce the secretion of a regulatory hormone, tachykinin-related peptide, from the silkworm midgut. Peptides 2018, 106, 21 -27.

AMA Style

Takayuki Yamagishi, Haruka Endo, Keisuke Fukumura, Shinji Nagata, Tohru Hayakawa, Satomi Adegawa, Mayu Kasubuchi, Ryoichi Sato. Glucose, some amino acids and a plant secondary metabolite, chlorogenic acid induce the secretion of a regulatory hormone, tachykinin-related peptide, from the silkworm midgut. Peptides. 2018; 106 ():21-27.

Chicago/Turabian Style

Takayuki Yamagishi; Haruka Endo; Keisuke Fukumura; Shinji Nagata; Tohru Hayakawa; Satomi Adegawa; Mayu Kasubuchi; Ryoichi Sato. 2018. "Glucose, some amino acids and a plant secondary metabolite, chlorogenic acid induce the secretion of a regulatory hormone, tachykinin-related peptide, from the silkworm midgut." Peptides 106, no. : 21-27.

Short communication
Published: 07 April 2018 in Biochemical and Biophysical Research Communications
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The taste sensing system is crucial for food recognition in insects and other animals. It is commonly believed that insect gustatory receptors (Grs) expressed in gustatory organs are indispensable for host plant selection. Many behavioral studies have shown that mono- or oligo-phagous lepidopteran insects use the balance between feeding attractants and feeding deterrents in host plants and that these are sensed by taste organs for host plant recognition. However, the molecular mechanism underlying taste recognition, especially of feeding deterrents, remains to be elucidated. To better understand this mechanism, we studied orphan Grs, including Bombyx mori Gr (BmGr) 16, BmGr18, and BmGr53, from the mono-phagous insect, Bombyx mori. Using Calcium imaging in mammalian cells, we first confirmed in lepidoptera insects that three of the putative bitter Grs widely responded to structurally different feeding deterrents. Although the phylogenetic distance of these Grs was considerable, they responded to partially overlapping deterrents of plant secondary metabolites. These findings suggest that not only these three Grs but also most of the Grs that have been assigned to putative bitter Grs are feeding-deterrent receptors that play a role in host plant recognition.

ACS Style

Mayu Kasubuchi; Fumika Shii; Kana Tsuneto; Takayuki Yamagishi; Satomi Adegawa; Haruka Endo; Ryoichi Sato. Insect taste receptors relevant to host identification by recognition of secondary metabolite patterns of non-host plants. Biochemical and Biophysical Research Communications 2018, 499, 901 -906.

AMA Style

Mayu Kasubuchi, Fumika Shii, Kana Tsuneto, Takayuki Yamagishi, Satomi Adegawa, Haruka Endo, Ryoichi Sato. Insect taste receptors relevant to host identification by recognition of secondary metabolite patterns of non-host plants. Biochemical and Biophysical Research Communications. 2018; 499 (4):901-906.

Chicago/Turabian Style

Mayu Kasubuchi; Fumika Shii; Kana Tsuneto; Takayuki Yamagishi; Satomi Adegawa; Haruka Endo; Ryoichi Sato. 2018. "Insect taste receptors relevant to host identification by recognition of secondary metabolite patterns of non-host plants." Biochemical and Biophysical Research Communications 499, no. 4: 901-906.