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Clock Mutants of Drosophila Melanogaster (Eclosion/Circadian/Rhythms/X Chromosome) RONALD J

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Clock Mutants of Drosophila Melanogaster (Eclosion/Circadian/Rhythms/X Chromosome) RONALD J Proc. Nat. Acad. Sci. USA Vol. 68, No. 9, pp. 2112-2116, September 1971 Clock Mutants of Drosophila melanogaster (eclosion/circadian/rhythms/X chromosome) RONALD J. KONOPKA AND SEYMOUR BENZER Division of Biology, California Institute of Technology, Pasadena, Calif. 91109 Contributed by Seymour Benzer, July 2, 1971 ABSTRACT Three mutants have been isolated in dark period. In a few bottles, males emerged in approximately which the normal 24-hour rhythm is drastically changed. equal numbers during day and night. Each mutant candidate One mutant is arrhythmic; another has a period of 19 hr; a third has a period of 28 hr. Both the eclosion rhythm of a was examined in more detail by raising pupae in LD 12:12, population and the locomotor activity of individual flies then monitoring the adult eclosion rhythm in constant are affected. All these mutations appear to involve the darkness. From a total of about 2000 F1 males, three rhythm same functional gene on the X chromosome. mutants were obtained. Rhythmic variations in behavior are displayed by many Determination of eclosion and locomotor organisms, ranging from single cells to man (1). When the activity rhythms rhythm persists under constant conditions, and has a period Eclosion rhythms, free-running in constant darkness, were of around one day, depending little on temperature, the determined with automatic "bang boxes" (20), generously rhythm is called circadian (2). Many experiments have at- loaned by Dr. Colin Pittendrigh. Several hundred pupae, tempted to probe the mechanism (3), but the nature of the raised in LD 12:12, were transferred to the apparatus at the underlying oscillation remains unknown (4). Perturbations end of a light cycle. The apparatus was thereafter maintained by inhibitors of RNA or protein synthesis suggest that such in constant darkness. Fractions were collected every hour, molecules are involved (5-8). Biochemical systems that yielding an eclosion profile. oscillate with much shorter periods have been demonstrated Locomotor activity of individual adult flies was measured both in vivo and in vitro (9, 10), but their relation to circadian by monitoring their movement with infrared light, which does rhythms is not clear. not affect the Drosophila clock (21). The devices, designed An approach that has been successful in unravelling mecha- and built by Dr. Yoshiki Hotta, used a small incandescent nisms in some systems is the use of genetic alterations. Since lamp, a Wratten No. 87C filter transmitting only wavelengths the expression of a rhythm requires an integrated system, greater than 800 um, and a chamber (3 mm thick X 4 mm mutation of the genes responsible for development and func- wide X 45 mm high) containing the fly, some food, and a tion of the system could lead to abnormal rhythms. Various cotton plug. Two silicon solar cells were arranged so that one aspects of circadian rhythms have indeed been shown to be received light transmitted through the upper third of the sensitive to genetic makeup (11-18). For genetic dissection of chamber, the other the lower third; they were wired so that circadian rhythms in an organism having a nervous system, the output voltage was zero when equal light fell on both cells. Drosophila offers certain advantages. Much is already known As the fly moved into or out of the area monitored by either about the rhythm of eclosion (emergence of the adult fly from solar cell, the resulting imbalance was converted to an all-or- the pupa), and genetic methodology is readily available. none response registered on an event recorder. The sharpest This paper describes the first result of such an analysis. rhythms were obtained with young flies (within one week of eclosion) previously exposed to at least three cycles of LD MATERIALS AND METHODS 12:12. Isolation of mutants D. melanogaster of the C-S (Canton-Special) wild strain was Genetic mapping of rhythm mutants maintained on cornmeal medium. Mutagenesis by ethyl The rhythm mutants had normal morphology, but their methane sulfonate was according to Lewis and Bacher (19), abnormal eclosion patterns could be used as markers in re- the treated males being mated to virgin attached-X females, combination experiments. Males bearing an X-linked rhythm so that each F1 progeny male carri&Va treated X chromosome mutation were crossed to females homozygous for the visible received from his father. Each male was mated individually markers yellow-2, scute, vermilion, forked, and a wild-type to attached-X females, producing a stock of males bearing allele of yellow located near the centromere. These markers identical X chromosomes, plus normal-rhythm attached-X had no effect upon rhythm. F1 males, receiving their X females. The stocks were reared at constant temperature chromosomes from their mothers, were all y2 SC V f - y+, and under LD 12:12 (12 hr of 50 foot-candles or more of white the females were all heterozygous, having the rhythm muta- fluorescent light, 12 hr of darkness each day). tion on one X chromosome and y2 SC V f * y+ on the other. To detect X-linked rhythm mutants, the stocks were ex- These males and females were mated to each other. F2 males, amined for ones in which males emerged abnormally. The receiving X chromosomes that had an opportunity to undergo normal females in each bottle served as an internal control, recombination in their mothers, included various recombi- at least twice as many emerging during the light as during the nants for the rhythm mutation and the morphological markers. 2112 Downloaded by guest on September 29, 2021 Proc. Nat. Acad. Sci. USA 68 (1971) Clock Mutants of Drosophila 2113 A. F2 progeny were raised in LD 12:12 at 250C, collected in the normal pupal stage, and transferred to "bang boxes," as above. The morphological phenotype of each male fly was scored by 2 microscopic examination, and the eclosion profile was plotted for each parental and recombinant class. 10 Complementation tests on rhythm mutants Flies heterozygous (in the trans arrangement) for two rhythm 0 mutations were constructed as follows. Males bearing one of the mutations were crossed to females carrying the balancer X chromosome FM 7, which contains multiple inversions to suppress crossingover between the two X chromosomes, as well as the dominant marker Bar for identification (22). Virgin progeny females (mutant/FM 7) were crossed to males bearing the second rhythm mutation, and the double hetero- zygotes (identified by lack of the Bar marker) were selected. These were tested individually in the locomotor-activity meter. The same procedure was used for constructing flies hetero- 60 r zygous for rhythm mutations and various X-chromosome C. deletions. 401 short- period RESULTS Eclosion rhythms of normal and mutant strains 201 Fig. 1A shows the normal circadian rhythm of eclosion of adults. The data shown are for attached-X females (carrying the genetic markers yellow and forked), which were routinely used as internal controls in experiments involving mu- tants (see Methods). Their rhythm was indistinguishable from that of the C-S males from which the rhythm mu- tants were isolated. These eclosion peaks are somewhat broader than those reported for D. pseudoobscura (23). In pseudoobscura, the period of the eclosion rhythm has usually been determined with reference to the median point of each successive eclosion peak. For melanogaster, a more sharply de- finable point is the time at which the peak rises to half its DAYS maximum value. The average period for normal flies (Fig. 1A) is about 24 hr. FIG. 1. Eclosion rhythms, in constant darkness, for popula- tions of rhythmically normal and mutant flies, previously ex- Figs. 1B, 1C, and 1D show the rhythms for males of three posed to LD 12:12. T = 20°C. mutant types, each isolated by one-step mutation from the normal C-S strain. One mutant is essentially arrhythmic; another has a short period of about 19 hr; the third has a long Fig. 2A shows the activity, as registered on an event recorder, period of about 28 hr. These profiles are reproducible in re- for a rhythmically-normal female (yellow, forked, attached-X). peated runs for each strain and the properties of the mutants The fly was raised in LD 12:12, then placed in the monitoring have been hereditarily transmitted over many generations. device at the end of a light cycle. In these records, the offset Effect of temperature on the eclosion rhythms of activity was typically more abrupt than the onset, so that Between 18'C and 250C, the period of the eclosion rhythm the free-running period could be best determined by measure- of normal D. melanogaster remains constant to about 1 hr ment of the average drift in time of offset per day. The rhythm (the interval used in collecting fractions). The same is true shown in Fig. 2A, therefore, has a period of about 25 hr. for the short- and long-period mutants. The arrhythmic For 8 females studied, the average period was 24.5 4 0.4 hr. mutant remains arrhythmic in this temperature range. Fig. 2B shows the activity of a female homozygous for the arrhythmic mutation. The activity appears, by comparison, Locomotor activity rhythm in individual flies random in time. Thus, this mutation has indeed abolished the Eclosion occurs only once in a fly's lifetime; to study the clock locomotor rhythm in individual flies. Four females studied that controls eclosion, one must observe an entire population. gave similar results, with no evident periodicity. This raises a question for the apparently arrhythmic mutant: Fig. 2C shows the activity for a homozygous short-period Is the absence of an eclosion rhythm due to lack of expression female.
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