The Role of the Sucrose-Responsive IR60b Neuron for Drosophila melanogaster: A Hypothesis

The Role of the Sucrose-Responsive IR60b Neuron for Drosophila melanogaster: A Hypothesis Abstract In a recent paper, Joseph and colleagues (Joseph et al. 2017) have characterized an IR60b receptor-expressing neuron in Drosophila. They showed that it responds to sucrose and serves to limit sucrose consumption, and proposed that it may thereby act to prevent overfeeding. Here, we propose an alternative hypothesis for the functional role of sucrose feeding control, and for how this limitation of sucrose uptake is accomplished. Adult fruit flies feed by excreting saliva onto the food, and imbibing the predigested liquefied food, or by filling the crop, where the food is predigested. Enzymes in the saliva hydrolyze starch and disaccharides into absorbable monosaccharides. Premature ingestion into the midgut would not give the enzymes in the saliva enough time to predigest the food. Thus, IR60b neurons might serve as a sensor to monitor the digestive state of external food or crop content: when disaccharides (sucrose) concentration is high, ingestion to the gut is inhibited, keeping a low concentration of starch and disaccharides in the midgut. insects, nutrition, obesity, sugar sensing, taste receptor Taste is an essential sense for most animals, as it is needed for detecting palatable food, keeping nutrient balance, and rejecting spoiled food. In Drosophila, the gustatory receptors GR64a-f and GR5a are expressed in neurons in taste sensilla on the labial palp and legs and mediate the “sweet” perception of multiple sugars and promote feeding in hungry flies (Dahanukar et al. 2007; Jiao et al. 2007; Fujii et al. 2015), whereas GR43a-expressing neurons in the brain sense hemolymph fructose and regulate feeding in a satiation-dependent manner (Miyamoto et al. 2012). In a recent paper, Joseph and colleagues (Joseph et al. 2017) have characterized an additional sugar-responsive neuron which expresses the receptor IR60b (Koh et al. 2014). These neurons are located in the labral sense organ in the pharynx, where they have direct contact with ingested food. IR60b neurons are selective to sucrose, which is a ubiquitous sugar in fruit and is a disaccharide composed of glucose and fructose. Surprisingly, IR60b neurons have the opposite effect on feeding as the previously known sugar-responsive GR64a-f- and GR5a-expressing neurons: activating IR60b neurons reduces feeding, whereas silencing them increases feeding (Joseph et al. 2017). Therefore, the authors propose that IR60b neurons could be part of a circuit that prevents fruit flies from food overconsumption to maintain homeostasis and balance nutrients. Interestingly, IR60b is under strong stabilizing selection, indicating that protection from overfeeding would exert a strong evolutionary pressure. In this commentary, we propose an alternative function for this receptor. Rather than preventing overfeeding, we propose that IR60b neurons delay the ingestion of undigested sucrose into the gut, thereby providing enough time for its predigestion externally or inside the crop. Insects have evolved a great variety of mouth parts: piercing, cutting, sucking, etc. Fruit flies, similar to their closely related house flies, have sponging mouthparts (Smith 1985). The labellum is sponge-like at the end, with many food channels. The digestive tract in Drosophila is similar to that of other dipterans (Lemaitre and Miguel-Aliaga 2013). Blow flies (Calliphora) feed by releasing saliva or crop content onto their food to liquefy and predigest it (Hansen Bay 1978). The saliva contains digestive enzymes, including amylase to hydrolyze starch into disaccharides (Boer and Hickey 1986) and sucrase (Hansen Bay 1978) to hydrolyze the disaccharide sucrose into the monosaccharides glucose and fructose. On a starch-rich diet, mutant flies with no amylase activity can only survive when kept with wildtype flies, relying on their external starch digestion (Haj-Ahmad and Hickey 1982). In the midgut, transport proteins move monosaccharides into the hemolymph (Lemaitre and Miguel-Aliaga 2013), where the glucose concentration is kept low by conversion to trehalose (Treherne 1958). Predigestion of starch and disaccharides makes foodborne bacteria more susceptible to bactericidal activity in the midgut (Dare et al. 1972; Espinoza-Fuentes and Terra 1987). Therefore, we propose that it may be important for a fly that, after releasing its saliva onto, say, the surface of a banana or ingesting the content into the crop, it waits sufficiently long for the enzymes to hydrolyze starch and disaccharides into monosaccharides. A high concentration of sucrose, as the main disaccharide in the food, would indicate that the predigestion process has not proceeded sufficiently—therefore ingestion should be delayed. When the enzymes have fulfilled their digestive action, sucrose concentration drops while glucose raises, and the fly should now ingest the food into the midgut. In this scenario, IR60b neurons would mediate the “stop” signal: a receptor with high selectivity for disaccharides and low response to monosaccharides, at the very beginning of the alimentary canal. It is also conceivable that IR60b neurons control the digestive state of crop regurgitates, and control whether food is directed to the crop or to the midgut. The more generalist sugar sensing neurons (neurons that express GR5a and GR64a-f) would mediate a positive driving force. Joseph and colleagues (Joseph et al. 2017) show that IR60b neurons respond to both sucrose (at low concentrations) and glucose (at high concentrations) at concentrations that are consistent with our proposal. Banana is one of the fruits with the highest sugar concentration (Widdowson and McCance 1935). It contains 322 mM glucose (IR60b would not respond) and 193 mM sucrose (IR60b would respond). After complete predigestion the crop content would contain 515 mM glucose, which is below the 900 mM glucose that elicited a response in IR60b (Joseph et al. 2017). More complete dose-response curves would be needed to address this point. Likewise, more research is needed to understand the time-scales of IR60b-mediated feeding inhibition and the role of other sensory modalities in controlling crop filling and emptying (Stoffolano and Haselton 2013). Furthermore, the role of physiological conditions in crop and intestinal tracts needs to be addressed: it is known that the pH value of different gut segments is tightly controlled and adapted to the local enzymes (Lemaitre and Miguel-Aliaga 2013). We note that Drosophila larvae lack a crop and use external digestion: they live in their food and engage in social digestion as they feed collectively (Gregg et al. 1990; Dombrovski et al. 2017) and actively regulate external digestion (Sakaguchi and Suzuki 2013). Larvae express IR60b in their dorsal pharyngeal sensilla (Stewart et al. 2015). Control of digestive steps is an important task for all animals: the alimentary canal is divided into different stages, and food is passed from one stage to the next in a carefully controlled manner. For example, in humans the pylorus controls the passage of food from the stomach into the duodenum, and similarly the ileocecal valve controls the passage from the ileum (last section of the small intestine) into the colon (large intestine). In humans, as in flies, predigestion of starch and disaccharides into monosaccharides is the first step in digestion. It is accomplished in the alkaline mouth by enzymes including amylase, and according to some dietologists swallowing into the acidic stomach should be delayed until a food bolus has been completely insalivated, and mouth pre-digestion has occurred. In humans, the osmotic effects of non-absorbable oligo- and disaccharides and their fermentation through intestinal bacteria causes intestinal harm (Shepherd et al. 2013). The pharyngeal reflex is only activated when the food bolus has a texture that indicates sufficient salivation, but we are not aware of a chemosensory component that would signal when to swallow, and would inhibit precocious swallowing. It is conceivable that a downregulation of pharyngeal reflex control, for genetic or cultural reasons (e.g., “fast food” habits), might contribute to dietary problems, including obesity. Thus, studying IR60b neurons (Joseph et al. 2017) in fruit flies can contribute to understanding how digestive steps are organized in animals. References Boer PH , Hickey DA . 1986 . The alpha-amylase gene in Drosophila melanogaster: nucleotide sequence, gene structure and expression motifs . Nucleic Acids Res . 14 : 8399 – 8411 . Google Scholar CrossRef Search ADS PubMed Dahanukar A , Lei YT , Kwon JY , Carlson JR . 2007 . Two Gr genes underlie sugar reception in Drosophila . Neuron . 56 : 503 – 516 . Google Scholar CrossRef Search ADS PubMed Dare R , Magee JT , Mathison GE . 1972 . In-vitro studies on the bactericidal properties of natural and synthetic gastric juices . J Med Microbiol . 5 : 395 – 406 . Google Scholar CrossRef Search ADS PubMed Dombrovski M , Poussard L , Moalem K , Kmecova L , Hogan N , Schott E , Vaccari A , Acton S , Condron B . 2017 . Cooperative behavior emerges among Drosophila larvae . Curr Biol . 27 : 2821 – 2826.e2 . Google Scholar CrossRef Search ADS PubMed Espinoza-Fuentes FP , Terra WR . 1987 . Physiological adaptations for digesting bacteria. Water fluxes and distribution of digestive enzymes in Musca domestica larval midgut . Insect Biochem . 17 : 809 – 817 . Google Scholar CrossRef Search ADS Fujii S , Yavuz A , Slone J , Jagge C , Song X , Amrein H . 2015 . Drosophila sugar receptors in sweet taste perception, olfaction, and internal nutrient sensing . Curr Biol . 25 : 621 – 627 . Google Scholar CrossRef Search ADS PubMed Gregg TG , McCrate A , Reveal G , Hall S , Rypstra AL . 1990 . Insectivory and social digestion in Drosophila . Biochem Genet . 28 : 197 – 207 . Google Scholar CrossRef Search ADS PubMed Haj-Ahmad Y , Hickey DA . 1982 . A molecular explanation of frequency-dependent selection in Drosophila . Nature . 299 : 350 – 352 . Google Scholar CrossRef Search ADS PubMed Hansen Bay CM . 1978 . The control of enzyme secretion from fly salivary glands . J Physiol . 274 : 421 – 455 . Google Scholar CrossRef Search ADS PubMed Jiao Y , Moon SJ , Montell C . 2007 . A Drosophila gustatory receptor required for the responses to sucrose, glucose, and maltose identified by mRNA tagging . Proc Natl Acad Sci U S A . 104 : 14110 – 14115 . Google Scholar CrossRef Search ADS PubMed Joseph RM , Sun JS , Tam E , Carlson JR . 2017 . A receptor and neuron that activate a circuit limiting sucrose consumption . Elife . 6 : e24992 . doi: 10.7554/eLife.24992 Google Scholar PubMed Koh TW , He Z , Gorur-Shandilya S , Menuz K , Larter NK , Stewart S , Carlson JR . 2014 . The Drosophila IR20a clade of ionotropic receptors are candidate taste and pheromone receptors . Neuron . 83 : 850 – 865 . Google Scholar CrossRef Search ADS PubMed Lemaitre B , Miguel-Aliaga I . 2013 . The digestive tract of Drosophila melanogaster . Annu Rev Genet . 47 : 377 – 404 . Google Scholar CrossRef Search ADS PubMed Miyamoto T , Slone J , Song X , Amrein H . 2012 . A fructose receptor functions as a nutrient sensor in the Drosophila brain . Cell . 151 : 1113 – 1125 . Google Scholar CrossRef Search ADS PubMed Sakaguchi H , Suzuki MG . 2013 . Drosophila melanogaster larvae control amylase secretion according to the hardness of food . Front Physiol . 4 : 200 . Google Scholar CrossRef Search ADS PubMed Shepherd SJ , Lomer MC , Gibson PR . 2013 . Short-chain carbohydrates and functional gastrointestinal disorders . Am J Gastroenterol . 108 : 707 – 717 . Google Scholar CrossRef Search ADS PubMed Smith J . 1985 . Comprehensive insect physiology, biochemistry and pharmacology. Volume 4, Regulation: digestion, nutrition, excretion . Oxford [Oxfordshire] : Perganom Press . Stewart S , Koh TW , Ghosh AC , Carlson JR . 2015 . Candidate ionotropic taste receptors in the Drosophila larva . Proc Natl Acad Sci U S A . 112 : 4195 – 4201 . Google Scholar CrossRef Search ADS PubMed Stoffolano JG Jr , Haselton AT . 2013 . The adult Dipteran crop: a unique and overlooked organ . Annu Rev Entomol . 58 : 205 – 225 . Google Scholar CrossRef Search ADS PubMed Treherne JE . 1958 . The absorption and metabolism of some sugars in the locust, Schistocerca gregaria (Forsk.) . J Exp Biol . 35 : 611 – 625 . Widdowson EM , McCance RA . 1935 . The available carbohydrate of fruits: Determination of glucose, fructose, sucrose and starch . Biochem J . 29 : 151 – 156 . Google Scholar CrossRef Search ADS PubMed © The Author(s) 2018. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Chemical Senses Oxford University Press

The Role of the Sucrose-Responsive IR60b Neuron for Drosophila melanogaster: A Hypothesis

Chemical Senses , Volume Advance Article (5) – Mar 13, 2018

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Abstract

Abstract In a recent paper, Joseph and colleagues (Joseph et al. 2017) have characterized an IR60b receptor-expressing neuron in Drosophila. They showed that it responds to sucrose and serves to limit sucrose consumption, and proposed that it may thereby act to prevent overfeeding. Here, we propose an alternative hypothesis for the functional role of sucrose feeding control, and for how this limitation of sucrose uptake is accomplished. Adult fruit flies feed by excreting saliva onto the food, and imbibing the predigested liquefied food, or by filling the crop, where the food is predigested. Enzymes in the saliva hydrolyze starch and disaccharides into absorbable monosaccharides. Premature ingestion into the midgut would not give the enzymes in the saliva enough time to predigest the food. Thus, IR60b neurons might serve as a sensor to monitor the digestive state of external food or crop content: when disaccharides (sucrose) concentration is high, ingestion to the gut is inhibited, keeping a low concentration of starch and disaccharides in the midgut. insects, nutrition, obesity, sugar sensing, taste receptor Taste is an essential sense for most animals, as it is needed for detecting palatable food, keeping nutrient balance, and rejecting spoiled food. In Drosophila, the gustatory receptors GR64a-f and GR5a are expressed in neurons in taste sensilla on the labial palp and legs and mediate the “sweet” perception of multiple sugars and promote feeding in hungry flies (Dahanukar et al. 2007; Jiao et al. 2007; Fujii et al. 2015), whereas GR43a-expressing neurons in the brain sense hemolymph fructose and regulate feeding in a satiation-dependent manner (Miyamoto et al. 2012). In a recent paper, Joseph and colleagues (Joseph et al. 2017) have characterized an additional sugar-responsive neuron which expresses the receptor IR60b (Koh et al. 2014). These neurons are located in the labral sense organ in the pharynx, where they have direct contact with ingested food. IR60b neurons are selective to sucrose, which is a ubiquitous sugar in fruit and is a disaccharide composed of glucose and fructose. Surprisingly, IR60b neurons have the opposite effect on feeding as the previously known sugar-responsive GR64a-f- and GR5a-expressing neurons: activating IR60b neurons reduces feeding, whereas silencing them increases feeding (Joseph et al. 2017). Therefore, the authors propose that IR60b neurons could be part of a circuit that prevents fruit flies from food overconsumption to maintain homeostasis and balance nutrients. Interestingly, IR60b is under strong stabilizing selection, indicating that protection from overfeeding would exert a strong evolutionary pressure. In this commentary, we propose an alternative function for this receptor. Rather than preventing overfeeding, we propose that IR60b neurons delay the ingestion of undigested sucrose into the gut, thereby providing enough time for its predigestion externally or inside the crop. Insects have evolved a great variety of mouth parts: piercing, cutting, sucking, etc. Fruit flies, similar to their closely related house flies, have sponging mouthparts (Smith 1985). The labellum is sponge-like at the end, with many food channels. The digestive tract in Drosophila is similar to that of other dipterans (Lemaitre and Miguel-Aliaga 2013). Blow flies (Calliphora) feed by releasing saliva or crop content onto their food to liquefy and predigest it (Hansen Bay 1978). The saliva contains digestive enzymes, including amylase to hydrolyze starch into disaccharides (Boer and Hickey 1986) and sucrase (Hansen Bay 1978) to hydrolyze the disaccharide sucrose into the monosaccharides glucose and fructose. On a starch-rich diet, mutant flies with no amylase activity can only survive when kept with wildtype flies, relying on their external starch digestion (Haj-Ahmad and Hickey 1982). In the midgut, transport proteins move monosaccharides into the hemolymph (Lemaitre and Miguel-Aliaga 2013), where the glucose concentration is kept low by conversion to trehalose (Treherne 1958). Predigestion of starch and disaccharides makes foodborne bacteria more susceptible to bactericidal activity in the midgut (Dare et al. 1972; Espinoza-Fuentes and Terra 1987). Therefore, we propose that it may be important for a fly that, after releasing its saliva onto, say, the surface of a banana or ingesting the content into the crop, it waits sufficiently long for the enzymes to hydrolyze starch and disaccharides into monosaccharides. A high concentration of sucrose, as the main disaccharide in the food, would indicate that the predigestion process has not proceeded sufficiently—therefore ingestion should be delayed. When the enzymes have fulfilled their digestive action, sucrose concentration drops while glucose raises, and the fly should now ingest the food into the midgut. In this scenario, IR60b neurons would mediate the “stop” signal: a receptor with high selectivity for disaccharides and low response to monosaccharides, at the very beginning of the alimentary canal. It is also conceivable that IR60b neurons control the digestive state of crop regurgitates, and control whether food is directed to the crop or to the midgut. The more generalist sugar sensing neurons (neurons that express GR5a and GR64a-f) would mediate a positive driving force. Joseph and colleagues (Joseph et al. 2017) show that IR60b neurons respond to both sucrose (at low concentrations) and glucose (at high concentrations) at concentrations that are consistent with our proposal. Banana is one of the fruits with the highest sugar concentration (Widdowson and McCance 1935). It contains 322 mM glucose (IR60b would not respond) and 193 mM sucrose (IR60b would respond). After complete predigestion the crop content would contain 515 mM glucose, which is below the 900 mM glucose that elicited a response in IR60b (Joseph et al. 2017). More complete dose-response curves would be needed to address this point. Likewise, more research is needed to understand the time-scales of IR60b-mediated feeding inhibition and the role of other sensory modalities in controlling crop filling and emptying (Stoffolano and Haselton 2013). Furthermore, the role of physiological conditions in crop and intestinal tracts needs to be addressed: it is known that the pH value of different gut segments is tightly controlled and adapted to the local enzymes (Lemaitre and Miguel-Aliaga 2013). We note that Drosophila larvae lack a crop and use external digestion: they live in their food and engage in social digestion as they feed collectively (Gregg et al. 1990; Dombrovski et al. 2017) and actively regulate external digestion (Sakaguchi and Suzuki 2013). Larvae express IR60b in their dorsal pharyngeal sensilla (Stewart et al. 2015). Control of digestive steps is an important task for all animals: the alimentary canal is divided into different stages, and food is passed from one stage to the next in a carefully controlled manner. For example, in humans the pylorus controls the passage of food from the stomach into the duodenum, and similarly the ileocecal valve controls the passage from the ileum (last section of the small intestine) into the colon (large intestine). In humans, as in flies, predigestion of starch and disaccharides into monosaccharides is the first step in digestion. It is accomplished in the alkaline mouth by enzymes including amylase, and according to some dietologists swallowing into the acidic stomach should be delayed until a food bolus has been completely insalivated, and mouth pre-digestion has occurred. In humans, the osmotic effects of non-absorbable oligo- and disaccharides and their fermentation through intestinal bacteria causes intestinal harm (Shepherd et al. 2013). The pharyngeal reflex is only activated when the food bolus has a texture that indicates sufficient salivation, but we are not aware of a chemosensory component that would signal when to swallow, and would inhibit precocious swallowing. It is conceivable that a downregulation of pharyngeal reflex control, for genetic or cultural reasons (e.g., “fast food” habits), might contribute to dietary problems, including obesity. Thus, studying IR60b neurons (Joseph et al. 2017) in fruit flies can contribute to understanding how digestive steps are organized in animals. References Boer PH , Hickey DA . 1986 . The alpha-amylase gene in Drosophila melanogaster: nucleotide sequence, gene structure and expression motifs . Nucleic Acids Res . 14 : 8399 – 8411 . Google Scholar CrossRef Search ADS PubMed Dahanukar A , Lei YT , Kwon JY , Carlson JR . 2007 . Two Gr genes underlie sugar reception in Drosophila . Neuron . 56 : 503 – 516 . Google Scholar CrossRef Search ADS PubMed Dare R , Magee JT , Mathison GE . 1972 . In-vitro studies on the bactericidal properties of natural and synthetic gastric juices . J Med Microbiol . 5 : 395 – 406 . Google Scholar CrossRef Search ADS PubMed Dombrovski M , Poussard L , Moalem K , Kmecova L , Hogan N , Schott E , Vaccari A , Acton S , Condron B . 2017 . Cooperative behavior emerges among Drosophila larvae . Curr Biol . 27 : 2821 – 2826.e2 . Google Scholar CrossRef Search ADS PubMed Espinoza-Fuentes FP , Terra WR . 1987 . Physiological adaptations for digesting bacteria. Water fluxes and distribution of digestive enzymes in Musca domestica larval midgut . Insect Biochem . 17 : 809 – 817 . Google Scholar CrossRef Search ADS Fujii S , Yavuz A , Slone J , Jagge C , Song X , Amrein H . 2015 . Drosophila sugar receptors in sweet taste perception, olfaction, and internal nutrient sensing . Curr Biol . 25 : 621 – 627 . Google Scholar CrossRef Search ADS PubMed Gregg TG , McCrate A , Reveal G , Hall S , Rypstra AL . 1990 . Insectivory and social digestion in Drosophila . Biochem Genet . 28 : 197 – 207 . Google Scholar CrossRef Search ADS PubMed Haj-Ahmad Y , Hickey DA . 1982 . A molecular explanation of frequency-dependent selection in Drosophila . Nature . 299 : 350 – 352 . Google Scholar CrossRef Search ADS PubMed Hansen Bay CM . 1978 . The control of enzyme secretion from fly salivary glands . J Physiol . 274 : 421 – 455 . Google Scholar CrossRef Search ADS PubMed Jiao Y , Moon SJ , Montell C . 2007 . A Drosophila gustatory receptor required for the responses to sucrose, glucose, and maltose identified by mRNA tagging . Proc Natl Acad Sci U S A . 104 : 14110 – 14115 . Google Scholar CrossRef Search ADS PubMed Joseph RM , Sun JS , Tam E , Carlson JR . 2017 . A receptor and neuron that activate a circuit limiting sucrose consumption . Elife . 6 : e24992 . doi: 10.7554/eLife.24992 Google Scholar PubMed Koh TW , He Z , Gorur-Shandilya S , Menuz K , Larter NK , Stewart S , Carlson JR . 2014 . The Drosophila IR20a clade of ionotropic receptors are candidate taste and pheromone receptors . Neuron . 83 : 850 – 865 . Google Scholar CrossRef Search ADS PubMed Lemaitre B , Miguel-Aliaga I . 2013 . The digestive tract of Drosophila melanogaster . Annu Rev Genet . 47 : 377 – 404 . Google Scholar CrossRef Search ADS PubMed Miyamoto T , Slone J , Song X , Amrein H . 2012 . A fructose receptor functions as a nutrient sensor in the Drosophila brain . Cell . 151 : 1113 – 1125 . Google Scholar CrossRef Search ADS PubMed Sakaguchi H , Suzuki MG . 2013 . Drosophila melanogaster larvae control amylase secretion according to the hardness of food . Front Physiol . 4 : 200 . Google Scholar CrossRef Search ADS PubMed Shepherd SJ , Lomer MC , Gibson PR . 2013 . Short-chain carbohydrates and functional gastrointestinal disorders . Am J Gastroenterol . 108 : 707 – 717 . Google Scholar CrossRef Search ADS PubMed Smith J . 1985 . Comprehensive insect physiology, biochemistry and pharmacology. Volume 4, Regulation: digestion, nutrition, excretion . Oxford [Oxfordshire] : Perganom Press . Stewart S , Koh TW , Ghosh AC , Carlson JR . 2015 . Candidate ionotropic taste receptors in the Drosophila larva . Proc Natl Acad Sci U S A . 112 : 4195 – 4201 . Google Scholar CrossRef Search ADS PubMed Stoffolano JG Jr , Haselton AT . 2013 . The adult Dipteran crop: a unique and overlooked organ . Annu Rev Entomol . 58 : 205 – 225 . Google Scholar CrossRef Search ADS PubMed Treherne JE . 1958 . The absorption and metabolism of some sugars in the locust, Schistocerca gregaria (Forsk.) . J Exp Biol . 35 : 611 – 625 . Widdowson EM , McCance RA . 1935 . The available carbohydrate of fruits: Determination of glucose, fructose, sucrose and starch . Biochem J . 29 : 151 – 156 . Google Scholar CrossRef Search ADS PubMed © The Author(s) 2018. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com

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Chemical SensesOxford University Press

Published: Mar 13, 2018

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