黑腹果蝇对高盐的产卵避性反应及其生物学意义
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摘要
【目的】研究黑腹果蝇Drosophila melanogaster对高盐的产卵避性,并通过高盐下后代生存率和发育历期的变化来揭示这一现象的生物学意义。【方法】应用产卵双选择装置,检测黑腹果蝇和雅库巴果蝇D. yakuba雌成虫分别对含有0. 25和1 mol/L NaCl的培养基的产卵选择性;利用产卵装置,检测黑腹果蝇对1 mol/L NaCl的位置效应;通过强迫产卵实验检测钠盐胁迫下黑腹果蝇的产卵能力;通过毛细管摄食法和观察口器延伸,检测钠盐胁迫下黑腹果蝇的摄食行为。利用黑暗条件和突变体Orco2分别探究视觉和嗅觉对高盐的产卵选择性。通过外科手术法摘除黑腹果蝇前足部分味觉感受器,并使用咸味突变体Ionotropic Receptor 76b (IR76b),研究介导该行为的感觉系统。在含有不同浓度NaCl (0,0. 25,0. 50,0. 75和1 mol/L)的培养基上培养黑腹果蝇,探究NaCl对黑腹果蝇后代的发育历期和存活率的影响。【结果】雌性黑腹果蝇产卵对高盐产生避性反应,对0. 25和1 mol/L NaCl的产卵偏嗜指数分别为-0. 45和-0. 59;雅库巴果蝇对高盐的反应与黑腹果蝇相同,对0. 25和1 mol/L NaCl的产卵偏嗜指数分别为-0. 78和-0. 99;并且两种果蝇均对0. 25和1 mol/L KCl和CaCl2产生产卵避性反应。黑腹果蝇避开含0. 25和1 mol/L NaCl培养基,位置指数分别为-0. 74和-0. 88。高盐不影响黑腹果蝇的生育能力,其对0,0. 25和1 mol/L NaCl的产卵指数分别为5. 59,6. 63和5. 41。黑腹果蝇对0. 25和1 mol/L NaCl摄食产生明显排斥反应,摄食指数分别为-0. 37和-0. 41,且随浓度增大食欲越低。同时在黑暗条件下,黑腹果蝇对0. 25和1 mol/L NaCl仍产生了显著的避性反应,产卵偏嗜指数分别为-0. 49和-0. 59,摘除前足的黑腹果蝇对0. 25 mol/L NaCl的产卵偏嗜指数为-0. 05,IR76b突变体对高盐的产卵避性反应消失,对0. 25和1 mol/L NaCl的产卵偏嗜指数分别为0. 46和0. 39。0. 25 mol/L NaCl明显延长了后代成蛹时间0. 40 d,后代幼虫存活率降低了16. 5%,而在1 mol/L NaCl上后代卵完全不能形成蛹和成虫。【结论】黑腹果蝇雌成虫通过咸味感觉器官感知高盐而产生产卵避性反应,以促进后代的生长发育和提高后代的幼虫存活率。
【Aim】To study the oviposition avoidance of Drosophila melanogaster to high salt,and to explore the biological significance of this phenomenon by the changes of the survival rate and developmental duration of the offspring under high salt. 【Methods】The oviposition preference of female adults of D. melanogaster and D. yakuba to culture media containing 0. 25 and 1 mol/L NaCl was assayed by the two-choice apparatus. The location effect of 1 mol/L NaCl on D. melanogaster adults was detected with oviposition apparatus. The oviposition ability of D. melanogaster adults under salt stress was detected with forced oviposition assay. The feeding behavior of D. melanogaster under salt stress was examined with capillary feeding and mouthpart extension assays. The visional and olfactory perceptions of oviposition selection were carried out in darkness and with Orco2 mutant,respectively. The sensory system mediating this behavior was studied by surgically removing the partial taste receptor of D.melanogaster forelegs and using the saline taste mutant Ionotropic Receptor 76 b(IR76 b). D. melanogaster was cultured on the media containing a serial of concentrations of NaCl(0,0. 25,0. 50,0. 75 and 1 mol/L),and the effects of NaCl on the developmental duration and survival rate of the offspring of D.melanogaster were investigated. 【Results】The female adults of D. melanogaster avoided to lay eggs on the media containing 0. 25 and 1 mol/L NaCl,with the oviposition indexes of-0. 45 and-0. 59,respectively. D. yakuba adults created similar response to high salt,with the oviposition preference indexes of-0. 78 and-0. 99,respectively. Both species tested showed oviposition avoidance to high concentration of KCl and CaCl2. D. melanogaster avoided to stay at the media containing 0. 25 and1 mol/L NaCl,with the location indexes of-0. 74 and-0. 88,respectively. There were comparable numbers of eggs laid on the media containing 0,0. 25 and 1 mol/L NaCl. D. melanogaster adults rejected 0. 25 and 1 mol/L NaCl,with the feeding indexes of-0. 37 and-0. 41,respectively,and their appetite decreased as the concentration increased. Under darkness,D. melanogaster adults still showed a significant avoidance response to 0. 25 and 1 mol/L NaCl,with the oviposition indexes of-0. 49 and-0. 59,respectively. After the forelegs of D. melanogaster adults were removed,the oviposition avoidance response of flies to 0. 25 mol/L NaCl was impaired,with the oviposition index of-0. 05. The oviposition avoidance response of IR76 b mutant to 0. 25 and 1 mol/L NaCl was compromised,with the oviposition indexes of 0. 46 and 0. 39,respectively. The time to puparium formation of the offspring on the media containing 0. 25 mol/L NaCl was significantly prolonged by 0. 40 d as compared to the control,and the larval survival rate of the offspring was decreased by 16. 5%. The eggs of the offspring completely failed to form pupa and adults on the medium containing 1 mol/L NaCl.【Conclusion】Female adults of D. melanogaster display the oviposition avoidance to high salt through salt taste perception,thus promoting the development and larval survival of the offspring.
【Aim】To study the oviposition avoidance of Drosophila melanogaster to high salt,and to explore the biological significance of this phenomenon by the changes of the survival rate and developmental duration of the offspring under high salt. 【Methods】The oviposition preference of female adults of D. melanogaster and D. yakuba to culture media containing 0. 25 and 1 mol/L NaCl was assayed by the two-choice apparatus. The location effect of 1 mol/L NaCl on D. melanogaster adults was detected with oviposition apparatus. The oviposition ability of D. melanogaster adults under salt stress was detected with forced oviposition assay. The feeding behavior of D. melanogaster under salt stress was examined with capillary feeding and mouthpart extension assays. The visional and olfactory perceptions of oviposition selection were carried out in darkness and with Orco2 mutant,respectively. The sensory system mediating this behavior was studied by surgically removing the partial taste receptor of D.melanogaster forelegs and using the saline taste mutant Ionotropic Receptor 76 b(IR76 b). D. melanogaster was cultured on the media containing a serial of concentrations of NaCl(0,0. 25,0. 50,0. 75 and 1 mol/L),and the effects of NaCl on the developmental duration and survival rate of the offspring of D.melanogaster were investigated. 【Results】The female adults of D. melanogaster avoided to lay eggs on the media containing 0. 25 and 1 mol/L NaCl,with the oviposition indexes of-0. 45 and-0. 59,respectively. D. yakuba adults created similar response to high salt,with the oviposition preference indexes of-0. 78 and-0. 99,respectively. Both species tested showed oviposition avoidance to high concentration of KCl and CaCl2. D. melanogaster avoided to stay at the media containing 0. 25 and1 mol/L NaCl,with the location indexes of-0. 74 and-0. 88,respectively. There were comparable numbers of eggs laid on the media containing 0,0. 25 and 1 mol/L NaCl. D. melanogaster adults rejected 0. 25 and 1 mol/L NaCl,with the feeding indexes of-0. 37 and-0. 41,respectively,and their appetite decreased as the concentration increased. Under darkness,D. melanogaster adults still showed a significant avoidance response to 0. 25 and 1 mol/L NaCl,with the oviposition indexes of-0. 49 and-0. 59,respectively. After the forelegs of D. melanogaster adults were removed,the oviposition avoidance response of flies to 0. 25 mol/L NaCl was impaired,with the oviposition index of-0. 05. The oviposition avoidance response of IR76 b mutant to 0. 25 and 1 mol/L NaCl was compromised,with the oviposition indexes of 0. 46 and 0. 39,respectively. The time to puparium formation of the offspring on the media containing 0. 25 mol/L NaCl was significantly prolonged by 0. 40 d as compared to the control,and the larval survival rate of the offspring was decreased by 16. 5%. The eggs of the offspring completely failed to form pupa and adults on the medium containing 1 mol/L NaCl.【Conclusion】Female adults of D. melanogaster display the oviposition avoidance to high salt through salt taste perception,thus promoting the development and larval survival of the offspring.
引文
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Chandrashekar J,Kuhn C,Oka Y,Yarmolinsky DA,Hummler E,Ryba NJ,Zuker CS,2010.The cells and peripheral representation of sodium taste in mice.Nature,464(7286):297-301.
Chatzigeorgiou M,Bang S,Hwang SW,Schafer WR,2013.tmc-1encodes a sodium-sensitive channel required for salt chemosensation in C.elegans.Nature,494(7435):95-99.
Frisoli TM,Schmieder RE,Grodzicki T,Messerli FH,2012.Salt and hypertension:is salt dietary reduction worth the effort?Am.J.Med.,125(5):433-439.
Hiroi M,Meunier N,Marion-Poll F,Tanimura T,2004.Two antagonistic gustatory receptor neurons responding to sweet-salty and bitter taste in Drosophila.J.Neurobiol.,61(3):333-342.
Huckesfeld S,Peters M,Pankratz MJ,2016.Central relay of bitter taste to the protocerebrum by peptidergic interneurons in the Drosophila brain.Nat.Commun.,7:12796-12804.
Ishimoto H,Tanimura T,2004.Molecular neurophysiology of taste in Drosophila.Cell.Mol.Life Sci.,61(1):10-18.
Ja WW,Carvalho GB,Mak EM,de la Rosa NN,Fang AY,Liong JC,Brummel T,Benzer S,2007.Prandiology of Drosophila and the CAFE assay.Proc.Natl.Acad.Sci.USA,104(20):8253-8256.
Joseph RM,Devineni AV,King IFG,Heberlein U,2009.Oviposition preference for and positional avoidance of acetic acid provide a model for competing behavioral drives in Drosophila.Proc.Natl.Acad.Sci.USA,106(27):11352-11357.
Kasischke ES,Johnstone JF,2005.Gustatory perception and behavior in Drosophila melanogaster.Curr.Biol.,15(17):673-684.
Kleinewietfeld M,Manzel A,Titze J,Kvakan H,Yosef N,Linker RA,Muller DN,Hafler DA,2013.Sodium chloride drives autoimmune disease by the induction of pathogenic TH17 cells.Nature,496(7446):518-522.
Knecht ZA,Silbering AF,Ni L,Klein M,Budelli G,Bell R,Abuin L,Ferrer AJ,Samuel AD,Benton R,Garrity PA,2016.Distinct combinations of variant ionotropic glutamate receptors mediate thermosensation and hygrosensation in Drosophila.e Life,5:44-60.
Knecht ZA,Silbering AF,Cruz J,Yang L,Croset V,Benton R,Garrity PA,2017.Ionotropic receptor-dependent moist and dry cells control hygrosensation in Drosophila.e Life,6:26654-26664.
Kristan WB,2008.Neuronal decision-making circuits.Curr.Biol.,18(19):928-932.
Larsson MC,Domingos AI,Jones WD,Chiappe ME,Amrein H,Vosshall LB,2004.Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction.Neuron,43(5):703-714.
Lee MJ,Sung HY,Jo H,Kim HW,Choi MS,Kwon JY,Kang KJ,2017.Ionotropic Receptor 76b is required for gustatory aversion to excessive Na+in Drosophila.Mol.Cells,40(10):787-795.
Ling F,Dahanukar A,Weiss LA,Kwon JY,Carlson JR,2014.The molecular and cellular basis of taste coding in the legs of Drosophila.J.Neurosci.,34(21):7148-7164.
Liu W,Jiang F,Bi X,Zhang YQ,2012.Drosophila FMRP participates in the DNA damage response by regulating G2/M cell cycle checkpoint and apoptosis.Hum.Mol.Genet.,21(21):4655-4668.
Liu W,Zhang K,Li Y,Su W,Hu K,Jin S,2017.Enterococci mediate the oviposition preference of Drosophila melanogaster through sucrose catabolism.Sci.Rep.,7(1):13420-13433.
Ni L,Klein M,Svec KV,Budelli G,Chang EC,Ferrer AJ,Benton R,Samuel AD,Garrity PA,2016.The Ionotropic Receptors IR21a and IR25a mediate cool sensing in Drosophila.e Life,5:13254-13265.
Niewalda T,Singhal N,Fiala A,Saumweber T,Wegener S,Gerber B,2008.Salt processing in larval Drosophila:choice,feeding,and learning shift from appetitive to aversive in a concentrationdependent way.Chem.Senses,33(8):685-692.
Oka Y,Butnaru M,von Buchholtz L,Ryba NJ,Zuker CS,2013.High salt recruits aversive taste pathways.Nature,494(7438):472-475.
Richmond RC,Gerking JL,1979.Oviposition site preference in Drosophila.Behav.Genet.,9(3):233-241.
Silbering AF,Rytz R,Grosjean Y,Abuin L,Ramdya P,Jefferis GS,Benton R,2011.Complementary function and integrated wiring of the evolutionarily distinct Drosophila olfactory subsystems.J.Neurosci.,31(38):13357-13375.
Stergiopoulos K,Cabrero P,Davies SA,Dow JA,2009.Salty dog,an SLC5 symporter,modulates Drosophila response to salt stress.Physiol.Genomics,37(1):1-11.
Tsugane S,Sasazuki S,Kobayashi M,Sasaki S,2004.Salt and salted food intake and subsequent risk of gastric cancer among middle-aged Japanese men and women.Br.J.Cancer,90(1):128-134.
Wang LL,Chen LR,Zhu JX,Wang ZG,Zhao ZH,Li ZF,Liu W,2017.Oviposition avoidance of Drosophila melanogaster to propionic acid and its biological significance.Acta Entomol.Sin.,60(12):1430-1438.[王璐璐,陈利荣,朱景新,王子光,赵梓涵,李曌芳,刘威,2017.黑腹果蝇对丙酸的产卵避性反应及其生物学意义.昆虫学报,60(12):1430-1438.
Yang CH,Belawat P,Hafen E,Jan LY,Jan YN,2008.Drosophila egglaying site selection as a system to study simple decision-making processes.Science,319(5870):1679-1683.
Zhang YV,Ni J,Montell C,2013.The molecular basis for attractive salt-taste coding in Drosophila.Science,340(6138):1334-1358.
Benton R,Vannice KS,Gomez-Diaz C,Vosshall LB,2009.Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila.Cell,136(1):149-162.
Chandrashekar J,Kuhn C,Oka Y,Yarmolinsky DA,Hummler E,Ryba NJ,Zuker CS,2010.The cells and peripheral representation of sodium taste in mice.Nature,464(7286):297-301.
Chatzigeorgiou M,Bang S,Hwang SW,Schafer WR,2013.tmc-1encodes a sodium-sensitive channel required for salt chemosensation in C.elegans.Nature,494(7435):95-99.
Frisoli TM,Schmieder RE,Grodzicki T,Messerli FH,2012.Salt and hypertension:is salt dietary reduction worth the effort?Am.J.Med.,125(5):433-439.
Hiroi M,Meunier N,Marion-Poll F,Tanimura T,2004.Two antagonistic gustatory receptor neurons responding to sweet-salty and bitter taste in Drosophila.J.Neurobiol.,61(3):333-342.
Huckesfeld S,Peters M,Pankratz MJ,2016.Central relay of bitter taste to the protocerebrum by peptidergic interneurons in the Drosophila brain.Nat.Commun.,7:12796-12804.
Ishimoto H,Tanimura T,2004.Molecular neurophysiology of taste in Drosophila.Cell.Mol.Life Sci.,61(1):10-18.
Ja WW,Carvalho GB,Mak EM,de la Rosa NN,Fang AY,Liong JC,Brummel T,Benzer S,2007.Prandiology of Drosophila and the CAFE assay.Proc.Natl.Acad.Sci.USA,104(20):8253-8256.
Joseph RM,Devineni AV,King IFG,Heberlein U,2009.Oviposition preference for and positional avoidance of acetic acid provide a model for competing behavioral drives in Drosophila.Proc.Natl.Acad.Sci.USA,106(27):11352-11357.
Kasischke ES,Johnstone JF,2005.Gustatory perception and behavior in Drosophila melanogaster.Curr.Biol.,15(17):673-684.
Kleinewietfeld M,Manzel A,Titze J,Kvakan H,Yosef N,Linker RA,Muller DN,Hafler DA,2013.Sodium chloride drives autoimmune disease by the induction of pathogenic TH17 cells.Nature,496(7446):518-522.
Knecht ZA,Silbering AF,Ni L,Klein M,Budelli G,Bell R,Abuin L,Ferrer AJ,Samuel AD,Benton R,Garrity PA,2016.Distinct combinations of variant ionotropic glutamate receptors mediate thermosensation and hygrosensation in Drosophila.e Life,5:44-60.
Knecht ZA,Silbering AF,Cruz J,Yang L,Croset V,Benton R,Garrity PA,2017.Ionotropic receptor-dependent moist and dry cells control hygrosensation in Drosophila.e Life,6:26654-26664.
Kristan WB,2008.Neuronal decision-making circuits.Curr.Biol.,18(19):928-932.
Larsson MC,Domingos AI,Jones WD,Chiappe ME,Amrein H,Vosshall LB,2004.Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction.Neuron,43(5):703-714.
Lee MJ,Sung HY,Jo H,Kim HW,Choi MS,Kwon JY,Kang KJ,2017.Ionotropic Receptor 76b is required for gustatory aversion to excessive Na+in Drosophila.Mol.Cells,40(10):787-795.
Ling F,Dahanukar A,Weiss LA,Kwon JY,Carlson JR,2014.The molecular and cellular basis of taste coding in the legs of Drosophila.J.Neurosci.,34(21):7148-7164.
Liu W,Jiang F,Bi X,Zhang YQ,2012.Drosophila FMRP participates in the DNA damage response by regulating G2/M cell cycle checkpoint and apoptosis.Hum.Mol.Genet.,21(21):4655-4668.
Liu W,Zhang K,Li Y,Su W,Hu K,Jin S,2017.Enterococci mediate the oviposition preference of Drosophila melanogaster through sucrose catabolism.Sci.Rep.,7(1):13420-13433.
Ni L,Klein M,Svec KV,Budelli G,Chang EC,Ferrer AJ,Benton R,Samuel AD,Garrity PA,2016.The Ionotropic Receptors IR21a and IR25a mediate cool sensing in Drosophila.e Life,5:13254-13265.
Niewalda T,Singhal N,Fiala A,Saumweber T,Wegener S,Gerber B,2008.Salt processing in larval Drosophila:choice,feeding,and learning shift from appetitive to aversive in a concentrationdependent way.Chem.Senses,33(8):685-692.
Oka Y,Butnaru M,von Buchholtz L,Ryba NJ,Zuker CS,2013.High salt recruits aversive taste pathways.Nature,494(7438):472-475.
Richmond RC,Gerking JL,1979.Oviposition site preference in Drosophila.Behav.Genet.,9(3):233-241.
Silbering AF,Rytz R,Grosjean Y,Abuin L,Ramdya P,Jefferis GS,Benton R,2011.Complementary function and integrated wiring of the evolutionarily distinct Drosophila olfactory subsystems.J.Neurosci.,31(38):13357-13375.
Stergiopoulos K,Cabrero P,Davies SA,Dow JA,2009.Salty dog,an SLC5 symporter,modulates Drosophila response to salt stress.Physiol.Genomics,37(1):1-11.
Tsugane S,Sasazuki S,Kobayashi M,Sasaki S,2004.Salt and salted food intake and subsequent risk of gastric cancer among middle-aged Japanese men and women.Br.J.Cancer,90(1):128-134.
Wang LL,Chen LR,Zhu JX,Wang ZG,Zhao ZH,Li ZF,Liu W,2017.Oviposition avoidance of Drosophila melanogaster to propionic acid and its biological significance.Acta Entomol.Sin.,60(12):1430-1438.[王璐璐,陈利荣,朱景新,王子光,赵梓涵,李曌芳,刘威,2017.黑腹果蝇对丙酸的产卵避性反应及其生物学意义.昆虫学报,60(12):1430-1438.
Yang CH,Belawat P,Hafen E,Jan LY,Jan YN,2008.Drosophila egglaying site selection as a system to study simple decision-making processes.Science,319(5870):1679-1683.
Zhang YV,Ni J,Montell C,2013.The molecular basis for attractive salt-taste coding in Drosophila.Science,340(6138):1334-1358.
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