Stress-reactivity and juvenile hormone degradation in Drosophila melanogaster strains having stress-related mutations

Insect Biochemistry and Molecular Biology 30 (2000) 775–783 www.elsevier.com/locate/ibmb

Stress-reactivity and juvenile hormone degradation in Drosophila melanogaster strains having stress-related mutations N.E. Gruntenko a

a,*

, T.G. Wilson b, M. Monastirioti c, I.Y. Rauschenbach

a

Institute of Cytology and Genetics, Russian Academy of Sciences, Siberian Division, Novosibirsk 630090, Russia b Department of Biology, Colorado State University, Fort Collins, CO 80523, USA c Institute of Molecular Biology and Biotechnology, FORTH, 711-10 Heraklion, Crete, Greece Received 31 October 1999; received in revised form 31 December 1999; accepted 25 January 2000

Abstract Juvenile hormone (JH) degradation was studied under normal and stress conditions in young and matured females of Drosophila melanogaster strains having mutations in different genes involved in responses to stress It was shown that (1) the impairment in heat shock response elicits an alteration in stress-reactivity of the JH system; (2) the impairment JH reception causes a decrease of JH-hydrolysing activity and of stress-reactivity in young females, while in mature ones stress reactivity is completely absent; (3) the absence of octopamine results in higher JH-hydrolysis level under normal conditions and altered JH stress-reactivity; (4) the higher dopamine content elicits a dramatic decrease of JH degradation under normal conditions and of JH stress-reactivity. Thus, the impairments in any component of the Drosophila stress reaction result in changes in the reponse of JH degradation system to stress. The role of JH in the development of the insect stress reaction is discussed.  2000 Elsevier Science Ltd. All rights reserved. Keywords: Drosophila melanogaster; ts403; Met; Tbh; ebony; Juvenile hormone; Stress reactivity

1. Introduction Juvenile hormone (JH), a sesquiterpenoid involved in the regulation of developmental transitions and reproduction in insects (reviews: Riddiford and Ashburner, 1991; Nijhout, 1994; Wyatt and Davey, 1996), is well known to play a main role in the development of the insect stress reaction (reviews: Cymborowski, 1991 Rauschenbach 1991, 1997). Two other important components of this multi-faceted response are the metabolism of biogenic amines, dopamine (DA) and octopamine (OA), and the heat shock response (HSR) (Orchard and Loughton, 1981; Davenport and Evans, 1984; Woodring et al., 1989; Hirashima et al., 1993, 1999; Rauschenbach et al. 1993, 1997; Rauschenbach, 1997; Sukhanova et al., 1997; Khlebodarova et al., 1998). We have previously shown that the JH metabolic sys-

* Corresponding author. Tel.: +383-2-333-526; fax: +383-2-331278. E-mail address: [email protected] (N.E. Gruntenko).

tem of wild type females of Drosophila melanogaster and D. virilis responds to stress conditions (termed here stressors) with a decrease in JH-hydrolysing activity. Males do not respond to stressors in this manner (Rauschenbach et al. 1995, 1996). The metabolic systems of DA and OA respond to stress, in both sexes, by an increase in the amine content and by a decrease in the activity of their synthetic enzymes (Rauschenbach et al., 1993; Hirashima et al., 1999). We have also demonstrated that a mutation disturbing the development of the stress reaction in D. virilis also elicits the impairment of HSR (Khlebodarova et al., 1998). How do impairments of the different components of the stress reaction, such as HSR and the metabolism of DA and OA, affect JH metabolism in D. melanogaster females under normal and stress conditions? Previous work has demonstrated that biogenic amines are involved in the regulation of JH biosynthesis and secretion by the corpora allata and that the expression of some HSR genes is JH dependent (Piulachs and Belles, 1989; Thompson et al., 1990; Berger et al., 1992; Granger et al., 1996).

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In this work, we analysed the mutations ts403, Met, Tbh and ebony (e) with respect to the response of JHdegradation system to stress. The recessive temperature sensitive lethal mutation l(l)ts403 results in the failure of heat shock protein (HSP)83 and HSP35 to be expressed, and a number of HSP70 proteins are only partially expressed (Evgen’ev and Denisenko, 1990). Met27 is a null allele of the Methoprene-tolerant gene that shows resistance to the toxic effects of both JH and a JH analog, methoprene. The mechanism of the resistance appears to be altered JH reception(Wilson and Fabian, 1986; Shemshedini and Wilson, 1990). Met27 completely lacks Met transcript and is clearly a null allele (Wilson and Ashok, 1998). TbhnM18 is a null mutation at the Tyramine b-hydroxylase locus, which results in complete absence of the tyramine β-hydroxylase protein and blockage of octopamine biosynthesis (Monastirioti et al., 1996). e is postulated to be the mutation of N-b-alanyl dopamine synthetase gene, based on the fact that e has twice as much DA as normal (Hodgetts, 1972; Hodgetts and Konopka, 1973; Ramadan et al., 1993). Here we asked whether these mutations would affect the decrease in JH degradation occurring in D. melanogaster when stressed. In order to answer this question, we studied the JH degradation in individuals of ts403, n Met27, TbhnM18 and Ste strains (carring l(l)ts403, Met27, Tbh and e mutations, respectively), under normal and stress conditions, and compared their stress-reactivity (calculated as percent change in JH hydrolysis under stress compared to hydrolysis under normal conditions) with that in a number of wild type and laboratory strains. We demonstrated (1) that ts403 females respond to stress by a decrease in JH degradation, as occurs in wild type females, but that their stress-reactivity significantly differs from that of wild type; (2) that in young v Met27 females, similar to wild type flies, JH hydrolysis is decreased upon stress, but their stress-reactivity is significantly lower than in wild type; (3) that JH degradation is unaffected in older v Met27 females under stress; (4) that TbhnM18 females show a significantly higher JH-hydrolysis level and different stress-reactivity than does the wild type; and (5) that young Ste females demonstrate significantly lower JH-hydrolysis and stress-reactivity, compared to the wild type.

Met27 strain was derived; laboratory balancer strain In(2LR)Cy/L; In(3LR)D/Sb, carrying morphological mutations with recessive lethal action Curly, Lobe (chromosome 2) and Dichaete, Stubble (chromosome 3; hereafter termed CyLDSb); strain ts403 carrying the recessive temperature sensitive lethal mutation l(l)ts403 (Arking, 1975); strain n Met27 carrying a null allele of the Methoprene-tolerant gene (Wilson and Ashok, 1998); strain TbhnM18 carrying a null mutation at the Tyramine b-hydroxylase locus (Monastirioti et al., 1996); and the laboratory Ste strain carrying the e mutation. Cultures were raised on standard medium (Rauschenbach et al., 1987) at 25°C, and adults were synchronized by eclosion. Flies were subjected to stress at 38°C for 3 h, and were subsequently frozen in liquid nitrogen and stored at ⫺20°C.

2. Materials and methods

3. Results

2.1. Drosophila strains

3.1. JH degradation in 1-day old ts403 and Canton S females under normal and heat stress conditions

The following D. melanogaster strains were used: the wild type laboratory strain Canton S; wild type isofemale strain 921500 from a natural population of Gorno-Altaisk; laboratory balancer strain First Multiple Seven (FM7); vermilion (n) strain from which the n

2.2. JH hydrolysis JH hydrolysis was measured by the assay of Hammock and Sparks, 1977. A fly was homogenized on ice in 30 µl of 0.1 M Na-phosphate buffer, pH 7.4, containing 0.5 mM phenylthiourea. The homogenates were centrifuged for 5 min at 12,000 rpm, and samples of the supernatant (10 µl) were utilized for the reaction. A mixture consisting of 0.1 µg unlabeled JH-III (Sigma) and 12,500 dpm 3H labeled JH-III (17.4 Ci/mmol at C-10, NEN Research Products, Germany) was used as substrate. The reaction was carried out in siliconized tubes in 100 µl of incubation mixture for 3 h, and it was stopped by the addition of 250 µl heptane and 50 µl of a solution containing 5% ammonia and 50% methanol (V/V). The tubes were shaken vigorously and centrifuged at 12,000 rpm for 10 min. Samples (100 µl) of both aqueous and heptane phases were placed in vials containing dioxane scintillation fluid and counted. Control experiments have shown a linear substrate–reaction relationship (Gruntenko et al., 1999), as well as the fact that measured activity is proportional to homogenate (i.e. enzyme) concentration (Rauschenbach, 1991; unpublished data). The significance of the differences between the data sets was tested by Student’s t-test. Sample size varied from 12 to 28 individuals for each measurement in all experiments.

JH-hydrolysing activity in 1-day old females of strains Canton S and ts403 under normal and stress conditions are shown in Fig. 1. The data indicate that under normal conditions, JH-hydrolysing activity in ts403 females

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lower JH-hydrolysing activity than do n females. Exposure to 38°C causes females of both n and Met27 strains to show a significant (P⬍0.001) decrease in JHhydrolysis level, compared to control females kept at 25°C. 3.3. JH degradation in 1-day-old TbhnM18 and Ste females under normal conditions and under heat stress

Fig. 1. Hydrolysis of [3H]JH-III in 1-day-old females of Canton S and ts403 strains of D. melanogaster under normal and stress (38°C, 3 h) conditions. Means±SE.

does not differ from that in Canton S ones. The data of Fig. 1 also demonstrate that ts403 females respond to stress as well as Canton S do: exposure to 38°C evokes in females of both strains a significant (P⬍0.001) decrease in JH-hydrolysing activity compared to control females maintained at 25°C.

The levels of JH-hydrolysing activity in 1-day-old females of TbhnM18 and Ste strains under normal and stress conditions are shown in Fig. 3, together with that of Canton S. The data reveal that under normal conditions, the level of JH degradation in females of TbhnM18 strain is significantly higher than that in Canton S (P⬍0.001). In contrast, Ste females are distinguished by a lower level of JH-hydrolysing activity compared to Canton S (P⬍0.001). The data in Fig. 3 also show that TbhnM18 and Ste females respond to heat stress as do Canton S: exposure to 38°C elicits in females of all three strains a decrease in the level of JH degradation compared to control females (P⬍0.001).

3.2. JH degradation in 1-day old n Met27 and n females under normal conditions and under heat stress JH-hydrolysis in 1-day old females of both n and n Met27 strains under normal and stress conditions are shown in Fig. 2. They indicate that under normal conditions n Met27 females show a significantly (P⬍0.01)

Fig. 2. Hydrolysis of [3H]JH-III in 1-day-old females of n and n Met27 strains of D. melanogaster under normal and stress (38°C 3 h) conditions. Means±SE.

Fig. 3. Hydrolysis of [3H]JH-III in 1-day-old females of Canton S, TbhnM18 and Ste strains of D. melanogaster under normal and stress (38°C 3 h) conditions. Means±SE.

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3.4. JH degradation under normal and stress conditions in l-day-old females of wild type (both Canton S and strain 921500) and laboratory (FM7, n and CyLDSb) strains It can be seen in Fig. 4 that 1-day-old females of Canton S strain are characterized by a level of JH degradation similar to that of the iso-female strain 921500 and of laboratory strains FM7, n and CyLDSb, which have no mutations relating with any components of the stress reaction (differences between Canton S and other strains are insignificant). Heat treatment of females of all these strains results in a significant (P⬍0.001) lowering of the level of JH degradation (compared to control females kept at 25°C). 3.5. JH degradation in 6-day-old Canton S and ts403 females under normal conditions and under heat stress Since JH degradation can control Drosophila reproduction under normal and heat stress conditions (Rauschenbach et al., 1996), we further measured the level of JH-hydrolysing activity in 6-day-old females of Canton S and ts403 strains. As seen in Fig. 5, under normal conditions the JH-hydrolysing activity in mature ts403 females does not differ from that of Canton S. Females of both strains show lower JH degradation (0.01) after heat stress (38°C, 3 h). 3.6. JH degradation under normal and stress conditions in 5-day-old n Met27 and n females Under normal conditions, the level of JH degradation in 5-day-old n Met27 females is the same as that in n

Fig. 5. Effect of short term heat stress (38°C, 3 h) on JH-hydrolysing activity in 6-day-old females of ts403 and Canton S strains of D. melanogaster. Means±SE.

females. After heat stress, mature n Met27 females show no changes in the level of JH metabolism compared with mature n females (Fig. 6) which respond to stress with a significant decrease in JH-hydrolysing activity (P⬍0.001). 3.7. JH degradation in 6-day old TbhnM18 and Canton S females under normal conditions and under heat stress Under normal conditions, the level of JH degradation in females of the TbhnM18 strain is significantly higher

Fig. 4. Hydrolysis of [3H]JH-III in l-day-old females of 921500, Canton S, FM7, n and CyLDSb strains of D. melanogaster under normal and stress (38°C, 3 h) conditions. Means±SE.

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Fig. 6. Effect of short term heat stress (38°C 3 h) on JH-hydrolyzing activity in 5-day-old females of n and n Met27 strains of D. melanogaster. Means± SE.

(P⬍0.001) than that of Canton S (Fig. 7). It is clear that mature TbhnM18 females respond to heat stress by a sharp decrease in JH-hydrolysing activity (P⬍0.001). 3.8. The stress-reactivity of the JH degradation system in young and mature D. melanogaster females To characterize the stress-reactivity of the JH degradation system, we calculated the percent decrease of JHhydrolysing activity for each stressed female relative to the value under normal conditions (every experiment value was related to the average value for the control group, since it is impossible to determine the JHhydrolysing activity of the same individual under both control and stress conditions). As seen in Fig. 8, 1-dayold females of wild type (921500 and Canton S) and laboratory (FM7, n and CyLDSb) strains have similar stress-reactivity (the differences between strains are not significant). On the other hand, it is also apparent from the data of Fig. 8, that 1-day-old females having stressrelated mutations (ts403, n Met27, TbhnM18 and Ste) have lower levels of stress-reactivity (P⬍0.05 for ts403, P⬍0.01 for n Met27 and P⬍0.001 for TbhnM18 and Ste). We further analysed the stress-reactivity in mature females (6-day-old Canton S, ts403 and TbhnM18 strains and 5-day-old FM7, n and n Met27 strains). It is clear from the data in Fig. 9 that the stress-reactivity of mature TbhnM18 and ts403 females is significantly higher than that of wild type (Canton S) and laboratory (FM7 and n) strains (P⬍0.001 for ts403 and P⬍0.05 for TbhnM18). The stress-reactivity of n Met27 females is insignificant.

Fig. 7. Effect of short term heat stress (38°C, 3 h) on JH-hydrolysing activity in 6-day-old females of TbhnM18 and Canton S strains of D. melanogaster. Means ±SE.

4. Discussion In adult female insects, JH controls reproduction by regulation of the growth of previtellogenic and/or vitellogenic follicles, maturation of ovaries, stimulation and maintenance of vitellogenesis, uptake of vitellogenins from hemolymph to oocytes, and oviposition (Shapiro et al., 1986; Roe et al., 1987; Adams and Filipi, 1988; Bownes 1989, 1994; Khlebodarova et al., 1996; Rauschenbach et al., 1996; Soller et al., 1999). JH must be present at high levels to initiate maturation of ovaries and stimulate vitellogenesis, and then at lower levels to maintain vitellogenesis (Jowett and Postlethwait, 1981; Raikhel and Lea, 1985; Postlethwait and Parker, 1987; Bownes, 1989; Soller et al., 1999). For completion of normal egg development and for the onset of oviposition, the JH titer must be decreased in some insects (Riddiford, 1970; Temin et al., 1986;

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Fig. 8. Stress-reactivity of JH-degradation system in young females of 921500, Canton S, FM7, n, CyLDSb, ts403, n Met27, TbhnM18 and Ste strains of D. melanogaster. Means ±SE.

Fig. 9. Stress-reactivity of JH degradation system in matured females of Canton S, FM7, n, ts403, n Met27 and TbhnM18 strains of D. melanogaster. Means±SE.

Shapiro et al., 1986; Khlebodarova et al., 1996; Rauschenbach et al., 1996; Soller et al., 1999). The n Met27 characteristics revealed earlier and in the present study are consistent with this requirement. Indeed, n Met27 flies have reduced oogenesis (Wilson and Ashok, 1998) and decreased fertility (Gruntenko et al., 2000) under normal

conditions. It is possible that n Met27 females have an elevated JH level resulting from decreased JH-hydrolysing activity (see Figs. 2 and 6) or that the impaired JH reception in this strain may prevent JH-titre-mediated regulation of both the JH degradation system and oogenesis. In both cases fertility would be disturbed. We believe that our data obtained on TbhnM18 females in this study also agree with the idea that a high JH titre impedes ovipositon. Earlier it was shown that TbhnM18 females are sterile: although they mate, they retain fully developed eggs (Monastirioti et al., 1996). It was suggested that this phenotype is connected with the fact that in the absence of OA the function of oviductal muscle is impaired (Monastirioti et al., 1996) based on the finding that OA modulates activity of the oviductal muscle in two orthopteran species (Kalogianni and Theophilidis, 1993). The experiments of Thompson et al. (1990) demonstrated that OA inhibits JH biosynthesis in the adult female cockroach, Diploptera punctata. If a similar situation exists in D. melanogaster, the absence of OA in TbhnM18 females would result in the increased JH synthesis. Such an absence of down regulation of JH production by OA should result in higher JH production, which would elicit an increase in JH-hydrolysing activity for maintenance of the JH titre. Indeed, TbhnM18 females were shown to have levels of JH degradation almost twice those in Canton S (see Figs. 3 and 7), although the increased JH-hydrolysing activity is not enough to lower the JH titer to alevel permitting oviposition. On

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the other hand, it is also possible that altered JH metabolism in these flies is related to a hither to unidentified phenotype/process. Evidence supporting the regulation of JH metabolism by biogenic amines in Drosophila comes from our data on Ste strain. The flies carrying e mutation are known to have twice as much DA as wild type (Hodgetts, 1972; Hodgetts and Konopka, 1973; Ramadan et al., 1993). Because DA can influence JH secretion (Piulachs and Belles, 1989; Granger et al., 1996) we might expect the JH titre to be affected, with consequent changes in JHhydrolysing activity in females of Ste strain. Indeed, Ste females have a level of JH degradation almost a half that of Canton S (see Fig. 3). We cannot exclude the possibility that the differences between Ste, TbhnM18 and Canton S females in the level of JH-hydrolysis are the result of strain polymorphism. However, four strains without any stress-related mutations (921500, FM7, n and CyLDSb) were examined and were found to have JH-hydrolysing activity similar to that of Canton S, under normal conditions. Hence, the high JH-hydrolysis level in TbhnM18 females and low level in Ste apparently result from the corresponding mutations. The reason to investigate JH metabolism in the ts403 strain, with its impairment of HSR, was the existing evidence on the regulation of the expression of heat shock proteins (hsp) genes by the combined action of the hormones JH and 20-OH-ecdysone. Inhibition of the ecdysteroid peak at pupariation by a temperature shift of the conditionally ecdysteroid-deficient D. melanogaster strain ecd-1 results in a block of hsp26 RNA and a decline in hsp83 RNA level; subsequent addition of exogenous 20-OH-ecdysone restores expression of both genes (Thomas and Lengyel, 1986). JH was reported to inhibit in a dose-dependent manner the ecdysterone induction of the small hsp genes of Drosophila, expressed in cultured cells (Berger et al., 1992). Our data revealed that the block in HSR expression does not affect JH degradation under normal conditions (see Figs. 1 and 5). How do the mutations in the different components of the D. melanogaster stress-reaction effect the stressreactivity of the JH degradation system? We have previously demonstrated that exposure of Drosophila females to stress results in a sharp decrease of the JHhydrolysing activity and as a consequence, the onset of oviposition by young females is delayed 24 h, while mature females cease oviposition for two days (Rauschenbach et al. 1995, 1996). We have also shown that in certain D. virilis and D. melanogaster strains that do not respond to stress, the level of JH-hydrolysis in females was significantly lower compared to that of wild type. This level does not alter upon heat stress (Rauschenbach et al. 1995, 1996; Gruntenko et al., 1999).

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As the present data show, each of the mutations studied elicits some alteration in the stress reactivity of the JH degradation system. Mature females of wild type and laboratory strains without any disturbances in their stress-reaction demonstrate significantly lower stressreactivity than younger ones (see Figs. 8 and 9). In contrast, mature TbhnM18 females demonstrate higher stressreactivity than younger ones. Moreover, this response differs from that in wild type: in mature females it is higher (see Fig. 9) and in young ones, lower (see Fig. 8). The stress-reactivity in ts403 females does not change with age in contrast to wild-type (see Figs. 8 and 9). Young Ste females demonstrate the lowest stressreactivity (see Fig. 8). Young n Met27 females also have decreased stress-reactivity compared to Met27 flies of the same age (see Fig. 8). Mature n Met27 females show the most essential differencies from wild type: their stressreactivtity is insignificant (see Fig. 9). In summary this work suggests that JH may play the key role in the development of the insect stress-reaction.

Acknowledgements This study was supported by grants from the Russian Fundamental Research Foundation and the Siberian Branch of the Russian Academy of Sciences for Young Prominent Scientists. Dr. Gruntenko was the recipient of a travel award from the Organizing Committee of the Seventh International Conference on the Juvenile Hormones.

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