Sensory experience and sensory activity regulate chemosensory receptor gene expression in Caenorhabditis elegans - PubMed (original) (raw)

Sensory experience and sensory activity regulate chemosensory receptor gene expression in Caenorhabditis elegans

E L Peckol et al. Proc Natl Acad Sci U S A. 2001.

Abstract

Changes in the environment cause both short-term and long-term changes in an animal's behavior. Here we show that specific sensory experiences cause changes in chemosensory receptor gene expression that may alter sensory perception in the nematode Caenorhabditis elegans. Three predicted chemosensory receptor genes expressed in the ASI chemosensory neurons, srd-1, str-2, and str-3, are repressed by exposure to the dauer pheromone, a signal of crowding. Repression occurs at pheromone concentrations below those that induce formation of the alternative dauer larva stage, suggesting that exposure to pheromones can alter the chemosensory behaviors of non-dauer animals. In addition, ASI expression of srd-1, but not str-2 and str-3, is induced by sensory activity of the ASI neurons. Expression of two receptor genes is regulated by developmental entry into the dauer larva stage. srd-1 expression in ASI neurons is repressed in dauer larvae. str-2 expression in dauer animals is induced in the ASI neurons, but repressed in the AWC neurons. The ASI and AWC neurons remodel in the dauer stage, and these results suggest that their sensory specificity changes as well. We suggest that experience-dependent changes in chemosensory receptor gene expression may modify olfactory behaviors.

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Figures

Figure 1

Figure 1

Chemosensory receptor expression is altered in the dauer stage. Promoter-GFP fusion genes were used to monitor expression of three chemosensory receptors, srd-1, str-2, and_str-3_ in adult (A, B, and_C_) and dauer (D, E, and_F_) animals. The head region is shown in a lateral view. White arrows denote ASI cell bodies. Adults express_srd-1_ and str-3 strongly and_str-2_ weakly in ASI (not detectable in_B_). Dauer larvae express str-2 and_str-3_ but not srd-1 in ASI. Yellow arrow in B denotes AWC cell body, which expresses_str-2_ in adults but not dauer larvae. The ASI neuron pair is bilaterally symmetric; in most panels, only one ASI is apparent, but in E the contralateral ASI neuron is visible. Each neuron extends a dendrite to the tip of the nose and a single U-shaped axon. Anterior is at left and dorsal is up. (Scale bars, 10 μM.)

Figure 2

Figure 2

Dauer pheromone suppresses srd-1, str-2, and str-3 expression. The expression of GFP fusion genes with srd-1 (A), str-2 (B), str-3 (C), and_daf-7_ (D) was examined in animals exposed to different amounts of crude dauer pheromone: 0 μl (dark bars), 50 μl (gray bars), and 100 μl (white bars) in 2 ml of agar. These dauer pheromone levels are lower than those that induce the dauer stage, so no dauer larvae were formed at any concentration. Dauer pheromone suppressed chemosensory receptor expression (A, B, and C) but not_daf-7_ expression (D) in both larvae and adults, and this suppression was dose-dependent with 100 μl suppressing more than 50 μl. Percentages of animals expressing any GFP, regardless of brightness, were tabulated for each strain. For each column, at least 50 animals were scored and error bars represent standard error of proportion. Adults were not examined for_str-2_ or daf-7 expression.

Figure 3

Figure 3

Low levels of dauer pheromone repress str-2 expression in ASI. (A) str-2 expression in ASI was increased in daf-22 mutants, which fail to produce pheromone (daf-22 alone, n = 89). In addition to the increased percentage of animals expressing_str-2_ (compare with Fig. 2_B_), GFP expression in ASI was also much stronger in daf-22 compared with wild-type (data not shown). When daf-22 animals were cocultivated with wild-type, pheromone-producing animals,str-2 expression in ASI was suppressed (daf-22 with wild type, n = 55). (B) As an assay for ASI remodeling, dauer larvae were exposed to the vital dye DiI, which stains exposed ASI neurons.str-2 was highly expressed in dauer larvae that did not stain with DiI (n = 132) and not expressed in dauer larvae that filled with DiI (n = 42).srd-1 and str-3 expression were unaltered in daf-22 mutants compared with wild type (data not shown).

Figure 4

Figure 4

Sensory activity regulates srd-1 expression. Animals with sensory defects were examined for alterations in chemosensory receptor expression. srd-1∷GFP was not expressed in_che-3_ mutant animals, which have defects in their sensory cilia (B), or in tax-2 mutants, which are defective in sensory signal transduction (C).str-3∷GFP expression was similar in wild-type (D), che-3 (E), and_tax-2_ (F) mutant animals.str-2∷GFP expression in ASI was similar in wild-type, che-3, and tax-2 animals (data not shown). White arrows denote ASI cell bodies. (Scale bars, 10 μm.)

Figure 5

Figure 5

Model for chemosensory receptor regulation. Pheromone suppresses expression of srd-1, str-2, and_str-3_ in ASI. Sensory activity is required for_srd-1_ expression. Under standard conditions, ASI expression of srd-1 and str-3 is high, whereas str-2 expression in ASI is suppressed by endogenous pheromone levels. As pheromone concentrations increase, expression of all three receptors decreases, and if harsh conditions persist, dauer development occurs. One consequence of dauer development is the retraction of the ASI cilia from the pore, relieving pheromone repression. Although this derepression is sufficient for_str-2_ and str-3 to be expressed, the reduction in ASI activity prevents expression of_srd-1._

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