Mutations in the larval foraging gene affect adult locomotory behavior after feeding in Drosophila melanogaster.

Pereira, H. Sofia; Sokolowski, Marla B.

doi:10.1073/pnas.90.11.5044

Cited by 160 publications

(165 citation statements)

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“…Larvae and adult flies with a rover allele (for R ) move greater distances while feeding than those with the sitter alleles (for s ) (Sokolowski, 1980;Pereira and Sokolowski, 1993). The for gene encodes a cGMP-dependent protein kinase (PKG) (Reaume and Sokolowski, 2009).…”

Section: Introductionmentioning

confidence: 99%

The locust foraging gene

Lucas

Kornfein

Chakaborty-Chatterjee

et al. 2010

Arch Insect Biochem Physiol

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Our knowledge of how genes act on the nervous system in response to the environment to generate behavioral plasticity is limited. A number of recent advancements in this area concern food-related behaviors and a specific gene family called foraging (for), which encodes a cGMPdependent protein kinase (PKG). The desert locust (Schistocerca gregaria) is notorious for its destructive feeding and long-term migratory behavior. Locust phase polyphenism is an extreme example of environmentally induced behavioral plasticity. In response to changes in population density, locusts dramatically alter their behavior, from solitary and relatively sedentary behavior to active aggregation and swarming. Very little is known about the molecular and genetic basis of this striking behavioral phenomenon. Here we initiated studies into the locust for gene by identifying, cloning, and studying expression of the gene in the locust brain. We determined the phylogenetic relationships between the locust PKG and other known PKG proteins in insects. FOR expression was found to be confined to neurons of the anterior midline of the brain, the pars intercerebralis. Our results suggest that differences in PKG enzyme activity are correlated to well-established phase-related behavioral differences. These results lay the groundwork for functional studies of the locust for gene and its possible relations to locust phase polyphenism.

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Section: Introductionmentioning

confidence: 99%

The locust foraging gene

Lucas

Kornfein

Chakaborty-Chatterjee

et al. 2010

Arch Insect Biochem Physiol

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“…PA and BUT were chosen, as they were unlikely to be odor equivalents; in larvae they are detected and processed by different combinations of peripheral and central structures (Kreher et al 2005). In addition, we found that larvae of the natural rover (for R ), sitter (for s ), and sitter mutant (for s2 ) strain, which was generated on a rover genetic background (de Belle et al 1989;Pereira and Sokolowski 1993), do not differ significantly in their response to these odors (below).…”

Section: Resultsmentioning

confidence: 95%

Natural variation in Drosophila larval reward learning and memory due to a cGMP-dependent protein kinase

Kaun

Hendel²,

Gerber³

et al. 2007

Learn. Mem.

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Animals must be able to find and evaluate food to ensure survival. The ability to associate a cue with the presence of food is advantageous because it allows an animal to quickly identify a situation associated with a good, bad, or even harmful food. Identifying genes underlying these natural learned responses is essential to understanding this ability. Here, we investigate whether natural variation in the foraging (for) gene in Drosophila melanogaster larvae is important in mediating associations between either an odor or a light stimulus and food reward. We found that for influences olfactory conditioning and that the mushroom bodies play a role in this for-mediated olfactory learning. Genotypes associated with high activity of the product of for, cGMP-dependent protein kinase (PKG), showed greater memory acquisition and retention compared with genotypes associated with low activity of PKG when trained with three conditioning trials. Interestingly, increasing the number of training trials resulted in decreased memory retention only in genotypes associated with high PKG activity. The difference in the dynamics of memory acquisition and retention between variants of for suggests that the ability to learn and retain an association may be linked to the foraging strategies of the two variants.Learned associations such as identifying odors as indicators of food, or showing preferences for food-related odors, are conserved across diverse taxa from humans and mice to slugs, honeybees, and fruit flies (Ache and Young 2005). The fruit fly Drosophila melanogaster can use odors as cues for the presence of both a food reward and an aversive stimulus (Tempel et al. 1983;Scherer et al. 2003;Schwaerzel et al. 2003;Margulies et al. 2005;McGuire et al. 2005;Kim et al. 2007). Identifying genes underlying these natural learned responses is essential to understanding this ability. Here, we use classical reward conditioning to investigate how natural variation in the foraging (for) gene affects acquisition and decay of memory in D. melanogaster larvae.for encodes a cGMP-dependent protein kinase (PKG) (Osborne et al. 1997). In mammals, PKG is important for proper induction of long-term potentiation (LTP) and long-term depression (LTD) (Hartell 1994;Zhuo et al. 1994;Lev-Ram et al. 1997;Arancio et al. 2001;Fiel et al. 2003Fiel et al. , 2005Kleppisch et al. 2003;Hofmann et al. 2006). Although LTP and LTD are thought to be important mechanisms underlying learning and memory (Whitlock et al. 2006), few studies have shown a direct role for PKG in learning and memory. This study aims to do this by investigating how learning differs between allelic variants of for in Drosophila larvae.for is an ideal candidate to study how natural genetic variation can affect learning and memory, since natural for variants exist that have subtle but significant variations in PKG activity (Osborne et al. 1997). The rover variants of for (for R ) have higher for transcript levels and higher PKG activities compared with the sitter variants of for (for s ) (Osb...

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“…Natural strains of these larvae exhibit one of two foraging patterns: 'rover' larvae travel further than 'sitter' larvae in a single patch of food and move more between food patches [18,22]. In adulthood, the strains retain their separate foraging strategies [23], and rovers also acquire an enhanced sensitivity to sucrose [24]. Notably, rover and sitter locomotion activities do not differ significantly in the absence of food.…”

Section: Identification Of the Foraging Gene In D Melanogastermentioning

confidence: 95%

The neurogenetics and evolution of food-related behaviour

Douglas

Dawson‐Scully

Sokolowski

2005

Trends in Neurosciences

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All organisms must acquire nutrients from the ambient environment to survive. In animals, the need to eat has driven the evolution of a rich array of complex foodrelated behaviours that ensure appropriate nutrient intake in diverse niches. Here, we review some of the neural and genetic components that contribute to the regulation of food-related behaviour in invertebrates, with emphasis on mechanisms that are conserved throughout various taxa and activities. We focus on synthesizing neurobiological and genetic approaches into a neurogenetic framework that explains foodrelated behaviour as the product of interactions between neural substrates, genes and internal and external environments.Introduction to food-related behaviours All life must acquire organic and inorganic substrates as fuel and raw material for energetic, metabolic and physiological processes. Whereas many plants synthesize their constituent organic compounds from carbon dioxide, water and sunlight, animals enact a heterotrophic strategy to gain necessary nutrients. In turn, they have evolved an impressive array of behaviours to detect, capture and ingest food. Broadly, food-related behaviour can be defined as actions elicited in response to hunger or the perception of food, therefore including food-searching activities, intake and post-ingestive behaviours. Multiple internal and external cues influence whether an animal is searching for food or eating at any given time. A major internal parameter is the level of hunger, which is governed by a milieu of regulatory factors interacting within an elaborate homeostatic system [1,2]. External factors include abundance and distribution of food, competitors, risk of predation, season and time of day. In humans, the decision to eat is complicated further by psychological and cultural factors. Owing to the breadth of contributing factors, food-related behaviour represents a rich interface that has been characterized from several different perspectives, including the ecological [3,4] A comprehensive description of any behaviour requires insight into the pattern and functioning of the neural circuits that underlie expression of the behaviour. Circuit output, which is often modifiable through experience, depends on parameters such as neuronal membrane

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Mutations in the larval foraging gene affect adult locomotory behavior after feeding in Drosophila melanogaster.

Cited by 160 publications

References 10 publications

The locust foraging gene

The locust foraging gene

Natural variation in Drosophila larval reward learning and memory due to a cGMP-dependent protein kinase

The neurogenetics and evolution of food-related behaviour

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