Expression responses of five cold tolerant related genes to two temperature dropping treatments in sea cucumber Apostichopus japonicus
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摘要
Environmental conditions,including ambient temperature,play important roles in survival,growth development,and reproduction of the Japanese sea cucumber,A postichopus japonicus. Low temperatures result in slowed growth and skin ulceration disease. In a previous study,we investigated the effect of low temperature on gene expression profiles in A. japonicus by suppression subtractive hybridization(SSH). Genes encoding Ferritin,Lysozyme,Hsp70,gp96,and AjToll were selected from a subtracted cDNA library of A. japonicus under acute cold stress. The transcriptional expression profiles of these genes were investigated in different tissues(coelomocyte,respiratory tree,intestine,longitudinal muscle) after exposure to acute and mild temperature dropping treatments. The results show that(1) the five cold-tolerance-related genes were found in all four tissues and the highest mRNA levels were observed in coelomocyte and respiratory tree;(2) under the temperature dropping treatments,three types of transcriptional regulation patterns were observed: primary suppression followed by up-regulation at-2°C,suppressed expression throughout the two treatments,and more rarely an initial stimulation followed by suppression; and(3) gene expression suppression was more severe under acute temperature dropping than under mild temperature dropping treatment. The five cold-tolerance-related genes that were distributed mainly in coelomocyte and respiratory tissues were generally down-regulated by low temperature stress but an inverse up-regulation event was found at the extreme temperature(-2°C).
Environmental conditions,including ambient temperature,play important roles in survival,growth development,and reproduction of the Japanese sea cucumber,A postichopus japonicus. Low temperatures result in slowed growth and skin ulceration disease. In a previous study,we investigated the effect of low temperature on gene expression profiles in A. japonicus by suppression subtractive hybridization(SSH). Genes encoding Ferritin,Lysozyme,Hsp70,gp96,and AjToll were selected from a subtracted cDNA library of A. japonicus under acute cold stress. The transcriptional expression profiles of these genes were investigated in different tissues(coelomocyte,respiratory tree,intestine,longitudinal muscle) after exposure to acute and mild temperature dropping treatments. The results show that(1) the five cold-tolerance-related genes were found in all four tissues and the highest mRNA levels were observed in coelomocyte and respiratory tree;(2) under the temperature dropping treatments,three types of transcriptional regulation patterns were observed: primary suppression followed by up-regulation at-2°C,suppressed expression throughout the two treatments,and more rarely an initial stimulation followed by suppression; and(3) gene expression suppression was more severe under acute temperature dropping than under mild temperature dropping treatment. The five cold-tolerance-related genes that were distributed mainly in coelomocyte and respiratory tissues were generally down-regulated by low temperature stress but an inverse up-regulation event was found at the extreme temperature(-2°C).
Environmental conditions,including ambient temperature,play important roles in survival,growth development,and reproduction of the Japanese sea cucumber,A postichopus japonicus. Low temperatures result in slowed growth and skin ulceration disease. In a previous study,we investigated the effect of low temperature on gene expression profiles in A. japonicus by suppression subtractive hybridization(SSH). Genes encoding Ferritin,Lysozyme,Hsp70,gp96,and AjToll were selected from a subtracted cDNA library of A. japonicus under acute cold stress. The transcriptional expression profiles of these genes were investigated in different tissues(coelomocyte,respiratory tree,intestine,longitudinal muscle) after exposure to acute and mild temperature dropping treatments. The results show that(1) the five cold-tolerance-related genes were found in all four tissues and the highest mRNA levels were observed in coelomocyte and respiratory tree;(2) under the temperature dropping treatments,three types of transcriptional regulation patterns were observed: primary suppression followed by up-regulation at-2°C,suppressed expression throughout the two treatments,and more rarely an initial stimulation followed by suppression; and(3) gene expression suppression was more severe under acute temperature dropping than under mild temperature dropping treatment. The five cold-tolerance-related genes that were distributed mainly in coelomocyte and respiratory tissues were generally down-regulated by low temperature stress but an inverse up-regulation event was found at the extreme temperature(-2°C).
引文
Ali K S,Dorgai L,Abrahám M,Hermesz E.2003.Tissue-andstressor-specific differential expression of two hsc70genes in carp.B iochemical and B iophysical R esearchC ommunications,307:503-509.
Beck G,Ellis T W,Habicht G S,Schluter S F,Marchalonis J J.2002.Evolution of the acute phase response:iron releaseby echinoderm(Asterias forbesi)coelomocytes,andcloning of an echinoderm ferritin molecule.D evelopmentaland C omparative I mmunology,26:11-26.
Chang Y Q,Shi S B,Zhao C,Han Z H.2011.Characteristicsof papillae in wild,cultivated and hybrid sea cucumbers(Apostichopus japonicus).African Journal ofBiotechnology,10:13 780-13 788.
Chen B,Zhong D,Monteiro A.2006.Comparative genomicsand evolution of the HSP90 family of genes across allkingdoms of organisms.BMC Genomics,7:156-174.
Ciancio M,Chang E.2008.Do heat shock proteins play anyrole in gut inflammation?I nflammatory B owel D iseases,14:S102-3.
Dolmatov I Y,Ginanova T T.2009.Post-autotomy regenerationof respiratory trees in the holothurian A postichopusjaponicus(Holothuroidea,Aspidochirotida).C ell andT issue R esearch,336:41-58.
Dong Y W,Dong S L,Meng X L.2008.Effects of thermal andosmotic stress on growth,osmoregulation and Hsp70 insea cucumber(A postichopus japonicus Selenka).Aquaculture,276:179-186.
Dong Y W,Ji T T,Dong S L.2007.Stress responses to rapidtemperature changes of the juvenile sea cucumber(Apostichopus japonicus Selenka).J ournal of OceanUniversity of China,6:275-280.
Du H,Bao Z,Hou R,Wang S,Su H,Yan J,Tian M,Li Y,WeiW,Lu W,Hu X,Wang S,Hu J.2012.Transcriptomesequencing and characterization for the sea cucumberApostichopus japonicus(Selenka,1867).P lo S One,7:1-10.
Feder M,Hofmann G.1999.Heat shock proteins,molecularchaperones,and the stress response:evolutionary andecological physiology.A nnual Review of Physiology,61:23-82.
Gao F,Yang H,Xu Q,Wang F,Liu G.2009.Effect of watertemperature on digestive enzyme activity and gut mass insea cucumber Apostichopus japonicus(Selenka),withspecial reference to aestivation.C hinese Journal ofOceanology and Limnology,27:714-722.
Grorgi A,Mignogna G,Bellapadrona G,Gattoni M,Chiaraluce R,Consalvi V,Chiancone E,Stefanini S.2008.Theunusual co-assembly of H-and M-chains in the ferritinmolecule from the Antarctic teleosts T rematomusbernacchii and Trematomus newnesi.A rchives ofB iochemistry and B iophysics,478:69-74.
Gueguen Y,Cadoret J P,Flament D,Barreau-Roumiguière C,Girardot A L,Garnier J,Hoareau A,Bachère E,EscoubasJ M.2003.Immune gene discovery by expressed sequencetags generated from hemocytes of the bacteria-challengedoyster,Crassostrea gigas.Gene,303:139-145.
J i C L,Sun G H,Yang J M,Song Z L,Liu X Q,Wang W J.2011.Construction and analysis of the subtracted c DNAlibrary of Apostichopus Japonicus(Selenka)under hightemperature stress.O ceanologia e t Limnologia Sinica,42:60-66.(in Chinese with English abstract)
J i T,Dong Y,Dong S.2008.Growth and physiologicalresponses in the sea cucumber,A postichopus japonicusSelenka:aestivation and temperature.A quaculture,283:180-187.
J ohanson P T.1969.The coelomic elements of sea urchins(Strongylocentrotus)3.In vitro reaction to bacteria.J ournal of I nvertebrate P athology,13:42-62.
Ju Z,Dunham R A,Liu Z.2002.Differential gene expressionin the brain of channel catfish(Ictalurus punctatus)inresponse to cold acclimation.M olecular M enetics andG enomics,268:87-95.
K awai T,Akira S.2010.The role of pattern-recognitionreceptors in innate immunity:update on Toll-likereceptors.N ature I mmunology,11:373-384.
Kulkeaw K,Ishitani T,Kanemaru T,Ivanovski O,NakagawaM,Mizuochi C,Horio Y,Sugiyama D.2011.Coldexposure down-regulates zebrafish pigmentation.G enesCells,16:358-367.
Li C Z,Wang X Y,Ding J,Chang Y Q.2013.Constuction andanalysis of subtracted c DNA library of sea cucumberApostichopus japonicus under low temperature stress.Journal of Dalian Ocean University,28:522-527.(inChinese with English abstract)
Liao Y L.1980.The aspidochirote holothurians of China witherection of a new genus in echinoderms:present and past.In:Jangoux M ed.Proceedings of the EuropeanColloquium on Echinoderms.Brussels September 1979,Rotterdam,Balkema.p.115-120.
Liu G,Yang H,Liu S.2010.Effects of rearing temperature anddensity on growth,survival and development of seacucumber larvae,A postichopus japonicus(Selenka).Chinese Journal of Oceanology and Limnology,28:842-848.
Liu W,Chang Y Q,Ding J.2013.A preliminary study of effectof mild and acute drop of temperature on serum nonspecific immunity in‘Shuiyuan No.1’sea cucumberpopulations and the cultured sea cucumber populations.Journal of Fisheries of China,37:1 342-1 348.(inChinese with English abstract)
Long Y,Li L,Li Q,He X,Cui Z.2012.Transcriptomiccharacterization of temperature stress responses in larvalzebrafish.P los One,7:e37209.
Mignogna G,Chiaraluce R,Consalvi V,Cavallo S,Stefanini S,Chiancone E.2002.Ferritin from the spleen of theAntarctic teleost T rematomus bernacchii is an M-typehomopolymer.E uropean J ournal of B iochemistry,269:1 600-1 606.
Minagawa S,Hikima J,Hirono I,Aoki T,Mori H.2001.Expression of Japanese flounder c-type lysozyme c DNAin insect cells.D evelopmental and C omparativeI mmunology,25:439-445.
Moseley P.1998.Heat shock proteins and the inflammatoryresponse.A nnals of the N ew Y ork A cademy of S ciences,29:206-213.
Nakano K,Iwama G K.2002.The 70-k Da heat shockproteinresponse in two intertidal sculpins,O ligocottus maculosusand O.snyderi:relationship of hsp70 and thermaltolerance.C omparative B iochemistry and P hysiology Amolecular&I ntegrative P hysiology,133:79-94.
Pascoli F,Lanzano G S,Negrato E,Poltronieri C,Trocino A,Radaelli G,Bertotto D.2011.Seasonal effects onhematological and innate immune parameters in sea bassDicentrarchus labrax.F ish&S hellfish I mmunology,31:1 081-1 087.
Picard D.2002.Heat-shock protein 90:a chaperone for foldingand regulation.C ellular and M olecular L ife S ciences,59:1 640-1 648.
Ramírez-Gómez F,Aponte-Rivera F,Méndez-Castaner L,García-Arrarás J E.2010.Changes in holothuriancoelomocyte populations following immune stimulationwith different molecular patterns.F ish and S hellfishI mmunology,29:175-185.
Sepp?l?O,Jokela J.2011.Immune defence under extremeambient temperature.B iology L etters,7:119-122.
Sonna L A,Fujita J,Gaff in S L,Lilly C M.1985.Invitedreview:effects of heat and cold stress on mammalian geneexpression.J ournal of A pplied P hysiology,92:1 725-1 742.
Sun H,Zhou Z,Dong Y,Yang A,Jiang B,Gao S,Chen Z,Guan X,Wang B,Wang X.2013.Identification andexpression analysis of two Toll-like receptor genes fromsea cucumber(A postichopus japonicus).F ish andS hellfish I mmunology,34:147-158.
Taro M,Fumiyuki G,Toshihiro Y,Toru E,Takashi S,ShinichiroK,Masamitsu S,Shigeru U.2007.Construction of homoand heteropolymers of plant ferritin subunits using an invitro protein expression system.P rotein Expression andPurification,56:237-246.
Tort L,Rotllant J,Rovira L.1998.Immunological suppressionin gilthead sea bream Sparus aurata of the North-WestMediterranean at low temperatures.C omparativeBiochemistry and Physiology,Part A,120:175-179.
Vornanen M,Hassinen M,Koskinen H,Krasnov A.2005.Steady-state effects of temperature acclimation on thetranscriptome of the rainbow trout heart.A mericanJ ournal of P hysiology-r egulatory I ntegrative andC omparative P hysiology,289:1 177-1 184.
Wang F,Yang H,Gabr H R,Gao F.2008a.Immune conditionof Apostichopus japonicus during aestivation.Aquaculture,285:238-243.
Wang F,Yang H,Gao F,Liu G.2008b.Effects of acutetemperature or salinity stress on the immune response insea cucumber,Apostichopus japonicus.C omparativeB iochemistry and P hysiology A-molecular&I ntegrativeP hysiology,151:491-498.
Wang P H,Liang J P,Gu Z H,Wan D H,Weng S P,Yu X Q,HeJ G.2012.Molecular cloning,characterization andexpression analysis of two novel Tolls(Lv Toll2 andLv Toll3)and three putative Spatzle-like Toll ligands(Lv Spz1-3)from Litopenaeus vannamei.D evelopmentaland C omparative I mmunology,36:359-371.
Wang X Y,Chang Y Q,Ding J,Liu W.2012.A preliminarystudy of temperature reduction on immune enzymes,soluble sugars and soluble proteins in sea cucumber.Journal of Agriculture,2:44-49.(in Chinese with Englishabstract)
Xue Q,Schey K,Volety A,Chu F,La P.2004.Purification andcharacterization of lysozyme from plasma of the easternoyster(Crassostrea virginica).C omparative B iochemistryand P hysiology B-biochemistry&M olecular B iology,139:11-25.
Yamashita M,Ojima N,Sakamoto T.1996.Molecular cloningand cold-inducible gene expression of ferritin H subunitisoforms in rainbow trout cells.J ournal of B iologicalC hemistry,271:26 908-26 913.
Yang A,Zhou Z,Dong Y,Jiang B,Wang X,Chen Z,Guan X,Wang B,Sun D.2010.Stability comparison of cytb andβ-actin genes expression in sea cucumber,A postichopusjaponicus.Journal of Agricultural Science and Techology,12:79-84.
Yang C,Zhang J,Li F,Ma H,Zhang Q,Jose Priya T A,ZhangX,Xiang J.2008.A toll receptor from Chinese shrimpFenneropenaeus chinensis is responsive to V ibrioanguillarum infection.F ish&S hellfish I mmunology,24:564-574.
Yang H,Yuan X,Zhou Y,Mao Y,Zhang T,Liu Y.2005.Effectsof body size and water temperature on food consumptionand growth in the sea cucumber A postichopus japonicus(Selenka)with special reference to aestivation.Aquaculture Research,36:1 085-1 092.
Yu J H,Song J H,Choi M C,Park S W.2009.Effects of watertemperature change on immune function in surf clams,Mactra veneriformis(Bivalvia:Mactridae).J ournal ofI nvertebrate P athology,102:30-35.
Yu M Z,Chang Y Q.2008.The effects of low temperature onsome physiological phenomena in different populationsof sea cucumber Apostichopus japonicas juveniles.Journal of Dalian Fisheries University,23:31-36.(inChinese with English abstract)
Zhao H,Yang H S,Zhao H L,Chen M Y.2011.Heat stressmediated gene expression in the body wall of the Japanesesea cucumber A postichopus japonicus.Aquatic Biology,12:23-31.
Beck G,Ellis T W,Habicht G S,Schluter S F,Marchalonis J J.2002.Evolution of the acute phase response:iron releaseby echinoderm(Asterias forbesi)coelomocytes,andcloning of an echinoderm ferritin molecule.D evelopmentaland C omparative I mmunology,26:11-26.
Chang Y Q,Shi S B,Zhao C,Han Z H.2011.Characteristicsof papillae in wild,cultivated and hybrid sea cucumbers(Apostichopus japonicus).African Journal ofBiotechnology,10:13 780-13 788.
Chen B,Zhong D,Monteiro A.2006.Comparative genomicsand evolution of the HSP90 family of genes across allkingdoms of organisms.BMC Genomics,7:156-174.
Ciancio M,Chang E.2008.Do heat shock proteins play anyrole in gut inflammation?I nflammatory B owel D iseases,14:S102-3.
Dolmatov I Y,Ginanova T T.2009.Post-autotomy regenerationof respiratory trees in the holothurian A postichopusjaponicus(Holothuroidea,Aspidochirotida).C ell andT issue R esearch,336:41-58.
Dong Y W,Dong S L,Meng X L.2008.Effects of thermal andosmotic stress on growth,osmoregulation and Hsp70 insea cucumber(A postichopus japonicus Selenka).Aquaculture,276:179-186.
Dong Y W,Ji T T,Dong S L.2007.Stress responses to rapidtemperature changes of the juvenile sea cucumber(Apostichopus japonicus Selenka).J ournal of OceanUniversity of China,6:275-280.
Du H,Bao Z,Hou R,Wang S,Su H,Yan J,Tian M,Li Y,WeiW,Lu W,Hu X,Wang S,Hu J.2012.Transcriptomesequencing and characterization for the sea cucumberApostichopus japonicus(Selenka,1867).P lo S One,7:1-10.
Feder M,Hofmann G.1999.Heat shock proteins,molecularchaperones,and the stress response:evolutionary andecological physiology.A nnual Review of Physiology,61:23-82.
Gao F,Yang H,Xu Q,Wang F,Liu G.2009.Effect of watertemperature on digestive enzyme activity and gut mass insea cucumber Apostichopus japonicus(Selenka),withspecial reference to aestivation.C hinese Journal ofOceanology and Limnology,27:714-722.
Grorgi A,Mignogna G,Bellapadrona G,Gattoni M,Chiaraluce R,Consalvi V,Chiancone E,Stefanini S.2008.Theunusual co-assembly of H-and M-chains in the ferritinmolecule from the Antarctic teleosts T rematomusbernacchii and Trematomus newnesi.A rchives ofB iochemistry and B iophysics,478:69-74.
Gueguen Y,Cadoret J P,Flament D,Barreau-Roumiguière C,Girardot A L,Garnier J,Hoareau A,Bachère E,EscoubasJ M.2003.Immune gene discovery by expressed sequencetags generated from hemocytes of the bacteria-challengedoyster,Crassostrea gigas.Gene,303:139-145.
J i C L,Sun G H,Yang J M,Song Z L,Liu X Q,Wang W J.2011.Construction and analysis of the subtracted c DNAlibrary of Apostichopus Japonicus(Selenka)under hightemperature stress.O ceanologia e t Limnologia Sinica,42:60-66.(in Chinese with English abstract)
J i T,Dong Y,Dong S.2008.Growth and physiologicalresponses in the sea cucumber,A postichopus japonicusSelenka:aestivation and temperature.A quaculture,283:180-187.
J ohanson P T.1969.The coelomic elements of sea urchins(Strongylocentrotus)3.In vitro reaction to bacteria.J ournal of I nvertebrate P athology,13:42-62.
Ju Z,Dunham R A,Liu Z.2002.Differential gene expressionin the brain of channel catfish(Ictalurus punctatus)inresponse to cold acclimation.M olecular M enetics andG enomics,268:87-95.
K awai T,Akira S.2010.The role of pattern-recognitionreceptors in innate immunity:update on Toll-likereceptors.N ature I mmunology,11:373-384.
Kulkeaw K,Ishitani T,Kanemaru T,Ivanovski O,NakagawaM,Mizuochi C,Horio Y,Sugiyama D.2011.Coldexposure down-regulates zebrafish pigmentation.G enesCells,16:358-367.
Li C Z,Wang X Y,Ding J,Chang Y Q.2013.Constuction andanalysis of subtracted c DNA library of sea cucumberApostichopus japonicus under low temperature stress.Journal of Dalian Ocean University,28:522-527.(inChinese with English abstract)
Liao Y L.1980.The aspidochirote holothurians of China witherection of a new genus in echinoderms:present and past.In:Jangoux M ed.Proceedings of the EuropeanColloquium on Echinoderms.Brussels September 1979,Rotterdam,Balkema.p.115-120.
Liu G,Yang H,Liu S.2010.Effects of rearing temperature anddensity on growth,survival and development of seacucumber larvae,A postichopus japonicus(Selenka).Chinese Journal of Oceanology and Limnology,28:842-848.
Liu W,Chang Y Q,Ding J.2013.A preliminary study of effectof mild and acute drop of temperature on serum nonspecific immunity in‘Shuiyuan No.1’sea cucumberpopulations and the cultured sea cucumber populations.Journal of Fisheries of China,37:1 342-1 348.(inChinese with English abstract)
Long Y,Li L,Li Q,He X,Cui Z.2012.Transcriptomiccharacterization of temperature stress responses in larvalzebrafish.P los One,7:e37209.
Mignogna G,Chiaraluce R,Consalvi V,Cavallo S,Stefanini S,Chiancone E.2002.Ferritin from the spleen of theAntarctic teleost T rematomus bernacchii is an M-typehomopolymer.E uropean J ournal of B iochemistry,269:1 600-1 606.
Minagawa S,Hikima J,Hirono I,Aoki T,Mori H.2001.Expression of Japanese flounder c-type lysozyme c DNAin insect cells.D evelopmental and C omparativeI mmunology,25:439-445.
Moseley P.1998.Heat shock proteins and the inflammatoryresponse.A nnals of the N ew Y ork A cademy of S ciences,29:206-213.
Nakano K,Iwama G K.2002.The 70-k Da heat shockproteinresponse in two intertidal sculpins,O ligocottus maculosusand O.snyderi:relationship of hsp70 and thermaltolerance.C omparative B iochemistry and P hysiology Amolecular&I ntegrative P hysiology,133:79-94.
Pascoli F,Lanzano G S,Negrato E,Poltronieri C,Trocino A,Radaelli G,Bertotto D.2011.Seasonal effects onhematological and innate immune parameters in sea bassDicentrarchus labrax.F ish&S hellfish I mmunology,31:1 081-1 087.
Picard D.2002.Heat-shock protein 90:a chaperone for foldingand regulation.C ellular and M olecular L ife S ciences,59:1 640-1 648.
Ramírez-Gómez F,Aponte-Rivera F,Méndez-Castaner L,García-Arrarás J E.2010.Changes in holothuriancoelomocyte populations following immune stimulationwith different molecular patterns.F ish and S hellfishI mmunology,29:175-185.
Sepp?l?O,Jokela J.2011.Immune defence under extremeambient temperature.B iology L etters,7:119-122.
Sonna L A,Fujita J,Gaff in S L,Lilly C M.1985.Invitedreview:effects of heat and cold stress on mammalian geneexpression.J ournal of A pplied P hysiology,92:1 725-1 742.
Sun H,Zhou Z,Dong Y,Yang A,Jiang B,Gao S,Chen Z,Guan X,Wang B,Wang X.2013.Identification andexpression analysis of two Toll-like receptor genes fromsea cucumber(A postichopus japonicus).F ish andS hellfish I mmunology,34:147-158.
Taro M,Fumiyuki G,Toshihiro Y,Toru E,Takashi S,ShinichiroK,Masamitsu S,Shigeru U.2007.Construction of homoand heteropolymers of plant ferritin subunits using an invitro protein expression system.P rotein Expression andPurification,56:237-246.
Tort L,Rotllant J,Rovira L.1998.Immunological suppressionin gilthead sea bream Sparus aurata of the North-WestMediterranean at low temperatures.C omparativeBiochemistry and Physiology,Part A,120:175-179.
Vornanen M,Hassinen M,Koskinen H,Krasnov A.2005.Steady-state effects of temperature acclimation on thetranscriptome of the rainbow trout heart.A mericanJ ournal of P hysiology-r egulatory I ntegrative andC omparative P hysiology,289:1 177-1 184.
Wang F,Yang H,Gabr H R,Gao F.2008a.Immune conditionof Apostichopus japonicus during aestivation.Aquaculture,285:238-243.
Wang F,Yang H,Gao F,Liu G.2008b.Effects of acutetemperature or salinity stress on the immune response insea cucumber,Apostichopus japonicus.C omparativeB iochemistry and P hysiology A-molecular&I ntegrativeP hysiology,151:491-498.
Wang P H,Liang J P,Gu Z H,Wan D H,Weng S P,Yu X Q,HeJ G.2012.Molecular cloning,characterization andexpression analysis of two novel Tolls(Lv Toll2 andLv Toll3)and three putative Spatzle-like Toll ligands(Lv Spz1-3)from Litopenaeus vannamei.D evelopmentaland C omparative I mmunology,36:359-371.
Wang X Y,Chang Y Q,Ding J,Liu W.2012.A preliminarystudy of temperature reduction on immune enzymes,soluble sugars and soluble proteins in sea cucumber.Journal of Agriculture,2:44-49.(in Chinese with Englishabstract)
Xue Q,Schey K,Volety A,Chu F,La P.2004.Purification andcharacterization of lysozyme from plasma of the easternoyster(Crassostrea virginica).C omparative B iochemistryand P hysiology B-biochemistry&M olecular B iology,139:11-25.
Yamashita M,Ojima N,Sakamoto T.1996.Molecular cloningand cold-inducible gene expression of ferritin H subunitisoforms in rainbow trout cells.J ournal of B iologicalC hemistry,271:26 908-26 913.
Yang A,Zhou Z,Dong Y,Jiang B,Wang X,Chen Z,Guan X,Wang B,Sun D.2010.Stability comparison of cytb andβ-actin genes expression in sea cucumber,A postichopusjaponicus.Journal of Agricultural Science and Techology,12:79-84.
Yang C,Zhang J,Li F,Ma H,Zhang Q,Jose Priya T A,ZhangX,Xiang J.2008.A toll receptor from Chinese shrimpFenneropenaeus chinensis is responsive to V ibrioanguillarum infection.F ish&S hellfish I mmunology,24:564-574.
Yang H,Yuan X,Zhou Y,Mao Y,Zhang T,Liu Y.2005.Effectsof body size and water temperature on food consumptionand growth in the sea cucumber A postichopus japonicus(Selenka)with special reference to aestivation.Aquaculture Research,36:1 085-1 092.
Yu J H,Song J H,Choi M C,Park S W.2009.Effects of watertemperature change on immune function in surf clams,Mactra veneriformis(Bivalvia:Mactridae).J ournal ofI nvertebrate P athology,102:30-35.
Yu M Z,Chang Y Q.2008.The effects of low temperature onsome physiological phenomena in different populationsof sea cucumber Apostichopus japonicas juveniles.Journal of Dalian Fisheries University,23:31-36.(inChinese with English abstract)
Zhao H,Yang H S,Zhao H L,Chen M Y.2011.Heat stressmediated gene expression in the body wall of the Japanesesea cucumber A postichopus japonicus.Aquatic Biology,12:23-31.
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