佛手低温胁迫相关基因的差异表达
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摘要
佛手(Citrus medica L.var.sarcodactylis Swingle)是药用及观赏价值都很高的经济植物,但它对低温反应敏感,容易发生冻害现象。因此,了解其冷敏感机制对提高抗寒性起着重要的作用。以佛手为试材,-4℃低温处理24 h后,采用mRNA差异显示技术(DDRT-PCR)和半定量RT-PCR技术,分析和鉴定与冷敏感相关的差异表达基因。DDRT结果获得差异片段121个,经生物信息学分析,差异表达序列中有33条为功能已知序列,88条为未知序列(其中5条具有开放性阅读框);半定量结果获得34个阳性基因片段,其中上调基因片段29个,下调基因片段5个。除了3个基因功能未知外,其余基因主要涉及植物防御/应激反应,细胞壁的修饰,信号转导,代谢,氨基酸转运,氧化损伤,转录和蛋白质的合成,其中与植物防御/应激反应和光合作用有关的基因可能是造成佛手寒敏感的主要原因。
Low temperature is one of the most common environmental stresses causing severe economic losses of most crops.Plants adapation to low temperature is mediated by differential gene expression,Investigation of the transcriptome profiling stressed by low temperature is important to unveil the mechanism of plant adapation to the stress.Multiple mechanisms are involved this process including differential expression of dehydrins and antifreeze proteins,chaperones and detoxification enzymes,as well as variations of biosynthetic enzymes producing the low molecular weight compounds.Regulatory proteins such as transcription factors,protein kinases and phospholipases are known to be differentially regulated under cold stress.However,few literatures were available on gene express correlated with cold-sensitivity in fingered citron. Fingered citron(Citrus medica L.var.sarcodactylis Swingle)has high values due to its medicinal properties and ornamental potential.However,high sensitivity of fingered citron to low temperature resulted in significant reduction of its production.Fingered citron′s maximum freezing tolerance,considered as the semilethal temperatures(LT50),is-4℃,and 24 h was considered as a critical period for cold stress.It is thus important to understand possible mechanisms involved in cold sensitivity of this plants species,as to promote its tolerance of cold stress. In the present study,the mRNA differential display reverse transcriptase polymerase chain reaction(DDRT-PCR) was used to analyze gene expression patterns involved in the cold sensitivity of Fingered Citrons.The plants were subjected to low temperature(-4℃) for 24 h,and alterations of gene expression patterns were analyzed.One hundred and twenty-one putative differentially expressed DNA fragments were cloned,sequenced,and analyzed.Thirty-eight genes with changed transcript levels were left after the exclusion of repeated sequences,33 of which are genes of known functions and 5 unknown through BLAST analyses.Expression analysis by semiquantitative RT-PCR(sqRT-PCR) showed that twenty-nine genes were up-regulated and five genes were down-regulated under cold stress.No significant variation of remaining four genes were observed,and considered to be false positives. Among the 34 differentially expressed fragments,eight genes were related to plant defense/stress responses,including hepicidin-like precursor,DNA-damage-repair/toleration protein(DRT),26S proteasome regulatory subunit,Retrotransposon-like protein,Avirulence protein(Avr),Ac-like transposase protein,Rhodanese domain protein and β-1,3-glucanase;Eight of nine metabolism-related genes are photosynthesis-related genes includes Abl interactor-like protein-2、3,cytochrome f,P700,plastocyanin-like protein,γ-type carbonic anhydrase protein,ATP synthase CF0 subunit I,Chlorophyllase-1 and phototropins;and 17 other genes are associated with cell wall modification,signal transduction,metabolism,amino acid transport,oxidative damage,transcription and protein synthesis.These data provide a new insight into molecular mechanisms underlying cold regulation of plant defense/stress responses and photosynthesis in Fingered Citrons,which is important to improve the cold tolerance of the citrus species.
Low temperature is one of the most common environmental stresses causing severe economic losses of most crops.Plants adapation to low temperature is mediated by differential gene expression,Investigation of the transcriptome profiling stressed by low temperature is important to unveil the mechanism of plant adapation to the stress.Multiple mechanisms are involved this process including differential expression of dehydrins and antifreeze proteins,chaperones and detoxification enzymes,as well as variations of biosynthetic enzymes producing the low molecular weight compounds.Regulatory proteins such as transcription factors,protein kinases and phospholipases are known to be differentially regulated under cold stress.However,few literatures were available on gene express correlated with cold-sensitivity in fingered citron. Fingered citron(Citrus medica L.var.sarcodactylis Swingle)has high values due to its medicinal properties and ornamental potential.However,high sensitivity of fingered citron to low temperature resulted in significant reduction of its production.Fingered citron′s maximum freezing tolerance,considered as the semilethal temperatures(LT50),is-4℃,and 24 h was considered as a critical period for cold stress.It is thus important to understand possible mechanisms involved in cold sensitivity of this plants species,as to promote its tolerance of cold stress. In the present study,the mRNA differential display reverse transcriptase polymerase chain reaction(DDRT-PCR) was used to analyze gene expression patterns involved in the cold sensitivity of Fingered Citrons.The plants were subjected to low temperature(-4℃) for 24 h,and alterations of gene expression patterns were analyzed.One hundred and twenty-one putative differentially expressed DNA fragments were cloned,sequenced,and analyzed.Thirty-eight genes with changed transcript levels were left after the exclusion of repeated sequences,33 of which are genes of known functions and 5 unknown through BLAST analyses.Expression analysis by semiquantitative RT-PCR(sqRT-PCR) showed that twenty-nine genes were up-regulated and five genes were down-regulated under cold stress.No significant variation of remaining four genes were observed,and considered to be false positives. Among the 34 differentially expressed fragments,eight genes were related to plant defense/stress responses,including hepicidin-like precursor,DNA-damage-repair/toleration protein(DRT),26S proteasome regulatory subunit,Retrotransposon-like protein,Avirulence protein(Avr),Ac-like transposase protein,Rhodanese domain protein and β-1,3-glucanase;Eight of nine metabolism-related genes are photosynthesis-related genes includes Abl interactor-like protein-2、3,cytochrome f,P700,plastocyanin-like protein,γ-type carbonic anhydrase protein,ATP synthase CF0 subunit I,Chlorophyllase-1 and phototropins;and 17 other genes are associated with cell wall modification,signal transduction,metabolism,amino acid transport,oxidative damage,transcription and protein synthesis.These data provide a new insight into molecular mechanisms underlying cold regulation of plant defense/stress responses and photosynthesis in Fingered Citrons,which is important to improve the cold tolerance of the citrus species.
引文
[1]Zhang C K,Lang P,Dane F,Ebel R C,Singh N K,Locy R D,Dozier W A.Cold acclimation induced genes of trifoliate orange(Poncirus trifoliata).Plant Cell Reports,2005,23(10/11):764-769.
[2]Hughes M A,Dunn M A.The molecular biology of plant acclimation to low temperature.Journal of Experimental Botany,1996,47(3):291-305.
[3]Weiser C J.Cold resistance and injury in woody plants.Science,1970,169(3952):1269-1278.
[4]Chen X B,Zhang A P,Yao Q H.Advances in researches on Gene engineering of plant for cold resistance.Biotechnology Information,2001,(4):14-20.
[5]Guo W D,Zhang Z Z,Jiang X W,Chen M G,Zheng J S,Chen W R.Semilethal temperature of Fingered Citron(Citrus medica var.sarcodactylis Swingle)under low temperature stress and evaluation on their Cold Resistance.Acta Horticulturae Sinica,2009,36(1):81-86.
[6]Cao Y B,Shi R,Chen W R,Guo W D.Comparative analysis of expression changes of ethylene response factor6(ERF6)in Fingered Citron and Trifoliate Orange under cold stress.Acta Horticulturae Sinica,2011,38(10):1873-1882.
[7]Shi R,Cao Y B,Chen W R,Guo W D.On cDNA cloning and expression analysis of GRAS gene in Fingered Citron.Journal of Zhejiang Normal University:Natural Sciences,2011,34(4):446-451.
[8]Sanchez-Ballesta M T,Lafuente M T,Zacarias L,Granell A.Involvement of phenylalanine ammonia-lyase in the response of Fortune mandarin fruits to cold temperature.Physiologia Plantarum,2000,108(4):382-389.
[9]Downton J,Slatyer R O.Temperature dependence of photosynthesis in cotton.Plant Physiology,1972,50(4):518-522.
[10]Shi X B,Wei J M,Shen Y G.Insights into the subunit interactions of the chloroplast ATP synthase.Chinese Science Bulletin,2002,47(1):58-62.
[11]Cheeseman J M.Mechanisms of salinity tolerance in plants.Plant Physiology,1998,87(3):547-550.
[12]Pang Q,Hays J B,Rajagopal I,Schaefer T S.Selection of Arabidopsis cDNAs that partially correct phenotypes of Escherichia coli DNA-damage-sensitive mutants and analysis of two plant cDNAs that appear to express UV-specific dark repair activities.Plant Molecular Biology,1993,22(3):411-426.
[13]Lloyd R G.Conjugational recombination in resolvase-deficient ruvC mutants of Escherichia coli K-12depends on recG.Journal of Bacteriology,1991,173(17):5414-5418.
[14]Breusing N,Grune T.Regulation of proteasome-mediated protein degradation during oxidative stress and aging.Biological Chemistry,2008,389(3):203-209.
[15]Fu H,Girod P A,Doelling J H,van Nocker S,Hochstrasser M,Finley D,Vierstra R D.Structure and functional analysis of the26S proteasome subunits from plants.Plant Molecular Biology Reporter,1999,26(7):137-146.
[16]Lommel L,Chen L,Madura K.The26S proteasome negatively regulates the level of overall genomic nucleotide excision repair.Nucleic Acids Research,2000,28(24):4839-4845.
[17]Peng Z H,Staub J M,Serino G.The cellular level of PR500,a protein complex related to the19S regulatory particle of the proteasome,is regulated in response to stresses in plants.Molecular Biology of the Cell,2001,12(2):383-392.
[18]Picton R,Eggo M C,Merrill G A,Langman M J S,Singh S.Mucosal protection against sulphide:importance of the enzyme rhodanese.Gut,2002,50(2):201-205.
[19]Lamb C J,Zhang D P.A ligand-receptor mechanism in plant-pathogen recognition.Science,1996,274(5295):2038-2039.
[20]Holt B F,Belkhadir Y,Dangl J L.Antagonistic control of disease resistance protein stability in the plant immune system.Science,2005,309(5736):929-932.
[21]Zhang S,Gu Y Q,Singh J,Coleman-Derr D,Brar D S,Jiang N,Lemaux P G.New insights into Oryza genome evolution:high gene colinearity and differential retrotransposon amplification.Plant Molecular Biology,2007,64(5):589-600.
[22]Ansari K I,Walter S,Brennan J M,Lemmens M,Kessans S,McGahern A,Egan D,Doohan F M.Retrotransposon and gene activation in wheat in response to mycotoxigenic and non-mycotoxigenic-associated Fusarium stress.Theoretical and Applied Genetics,2007,114(5):927-937.
[23]Steward N,Ito M,Yamaguchi Y,Koizumi N,Sano H.Periodic DNA methylation in maize nucleosomes and demethylation by environmental stress.Journal of Biological Chemistry,2002,277(40):37741-37746.
[24]Mhiri C,Morel J B,Vernhettes S,Casacuberta J M,Lucas H,Grandbastien M A.The promoter of the tobacco Tnt1retrotransposon is induced by wounding and by abiotic stress.Plant Molecular Biology,1997,33(2):257-266.
[25]Thimmapuram J,Korban S S.Characterization and expression ofβ-1,3-glucanase genes in peach.Molecular Genetics and Genomics,2001,265(3):469-479.
[26]McCollum T G,Doostdar H,Burkhart M D,Neidz R P,Mayer R T,McDonald R E.Biochemical and molecular characterization of aβ-1,3-endoglucanase from Valencia Orange Callus.HortScience,1996,31(4):614-614.
[27]Sanchez-Ballesta M T,Gosalbes M J,Rodrigo M J,Granell A,Zacarias L,Lafuente M T.Characterization of aβ-1,3-glucanase from citrus fruit as related to chilling-induced injury and ethylene production.Postharvest Biology and Technology,2006,40(2):133-140.
[28]Domingo C,Conejero V,Vera P.Genes encoding acidic and basic class IIIβ-1,3-glucanases are expressed in tomato plants upon viroid infection.Plant Molecular Biology,1994,24(5):725-732.
[29]Nogueira F T S,De Rosa V E Jr,Menossi M,Ulian E C,Arruda P.RNA expression profiles and data mining of sugarcane response to low temperature.Plant Physiology,2003,132(4):1811-1824.
[30]Tessitori M,Maria G,Capasso C,Catara G,Rizza S,de Luca V,Catara A,Capasso A,Carginale V.Differential display analysis of gene expression in Etrog citron leaves infected by Citrus viroid III.Biochimica et Biophysica Acta(BBA)-Gene Structure and Expression,2007,1769(4),228-235.
[31]Ding B L,Tan H H,Zhu S Q.Advances on research of the relationship between stresses and plant cell wall.Journal of Guangxi Academy of Sciences,2001,17(2):87-90.
[32]Weiser R L,Wallner S J,Waddell J W.Cell wall and extensin mRNA changes during cold acclimation of pea seedlings.Plant Physiology,1990,93(3):1021-1026.
[33]Purugganan M M,Braam J,Fry S C.The Arabidopsis TCH 4 xyloglucan endotransglycosylase(Substrate specificity,pH optimum,and cold tolerance).Plant Physiology,1997,115(1):181-190.
[34]Borutova R,Faix S,Placha I,Gresakova L,Cobanova K,Leng L.Effects of deoxynivalenol and zearalenone on oxidative stress and blood phagocytic activity in broilers.Archives of Animal Nutrition,2008,62(4):303-312.
[35]Cavalca L,Guerrieri N,Colombo M,Pagani S,Andreoni V.Enzymatic and genetic profiles in environmental strains grown on polycyclic aromatic hydrocarbons.Antonie van Leeuwenhoek,2007,91(4):315-325.
[36]Moussatova A,Kandt C,O'Mara M L,Tieleman D P.ATP-binding cassette transporters in Escherichia coli.Biochimica et Biophysica Acta,2008,1778(9):1757-1771.
[37]Hannivoort R A,Dunning S,Vander B S,Schroyen B,Woudenberg J,Oakley F,Buist-Homan M,van den Heuvel F A,Geuken M,Geerts A,Roskams T,Faber K N,Moshage H.Multidrug resistance-associated proteins are crucial for the viability of activated rat hepatic stellate cells.Hepatology,2008,48(2):624-634.
[38]Lu H,Klaassen C.Gender differences in mRNA expression of ATP-binding cassette efflux and bile acid transporters in kidney,liver,and intestine of5/6nephrectomized rats.Drug Metabolism and Disposition,2008,36(1):16-23.
[39]Locher K P.Structure and mechanism of ABC transporters.Current Opinion in Structural Biology,2004,14(4):426-431.
[40]Toyoda Y,Hagiya Y,Adachi T,Hoshijima K,Kuo M T,Ishikawa T.MRP class of human ATP binding cassette(ABC)transporters:historical background and new research directions.Xenobiotica,2008,38(7/8):833-842.
[41]Wu S G,Ren X P.The relationship between Plant polyamine and several adverse stress.Journal of Shangqiu Vocational and Technical College,2005,4(2):58-59.
[4]陈香波,张爱平,姚泉洪.植物抗寒基因工程研究进展.生物技术通报,2001,(4):14-20.
[5]郭卫东,张真真,蒋小韦,陈民管,郑建树,陈文荣.低温胁迫下佛手半致死温度测定和抗寒性分析.园艺学报,2009,36(1):81-86.
[6]曹诣斌,石瑞,陈文荣,郭卫东.低温胁迫下佛手和枳乙烯应答因子6(ERF6)表达变化的比较分析.园艺学报,2011,38(10):1873-1882.
[7]石瑞,曹诣斌,陈文荣,郭卫东.佛手GRAS基因的克隆及表达分析.浙江师范大学学报:自然科学版,2011,34(4):446-451.
[10]石晓冰,魏家绵,沈允钢.叶绿体ATP合酶CF 1与CF 0亚基间的相互作用.科学通报,2001,46(18):1550-1554.
[31]丁宝莲,谈宏鹤,朱素琴.胁迫与植物细胞壁关系研究进展.广西科学院学报,2001,17(2):87-90.
[41]吴诗光,任雪平.植物多胺与几种逆境胁迫的关系.商丘职业技术学院学报,2005,4(2):58-59.
[2]Hughes M A,Dunn M A.The molecular biology of plant acclimation to low temperature.Journal of Experimental Botany,1996,47(3):291-305.
[3]Weiser C J.Cold resistance and injury in woody plants.Science,1970,169(3952):1269-1278.
[4]Chen X B,Zhang A P,Yao Q H.Advances in researches on Gene engineering of plant for cold resistance.Biotechnology Information,2001,(4):14-20.
[5]Guo W D,Zhang Z Z,Jiang X W,Chen M G,Zheng J S,Chen W R.Semilethal temperature of Fingered Citron(Citrus medica var.sarcodactylis Swingle)under low temperature stress and evaluation on their Cold Resistance.Acta Horticulturae Sinica,2009,36(1):81-86.
[6]Cao Y B,Shi R,Chen W R,Guo W D.Comparative analysis of expression changes of ethylene response factor6(ERF6)in Fingered Citron and Trifoliate Orange under cold stress.Acta Horticulturae Sinica,2011,38(10):1873-1882.
[7]Shi R,Cao Y B,Chen W R,Guo W D.On cDNA cloning and expression analysis of GRAS gene in Fingered Citron.Journal of Zhejiang Normal University:Natural Sciences,2011,34(4):446-451.
[8]Sanchez-Ballesta M T,Lafuente M T,Zacarias L,Granell A.Involvement of phenylalanine ammonia-lyase in the response of Fortune mandarin fruits to cold temperature.Physiologia Plantarum,2000,108(4):382-389.
[9]Downton J,Slatyer R O.Temperature dependence of photosynthesis in cotton.Plant Physiology,1972,50(4):518-522.
[10]Shi X B,Wei J M,Shen Y G.Insights into the subunit interactions of the chloroplast ATP synthase.Chinese Science Bulletin,2002,47(1):58-62.
[11]Cheeseman J M.Mechanisms of salinity tolerance in plants.Plant Physiology,1998,87(3):547-550.
[12]Pang Q,Hays J B,Rajagopal I,Schaefer T S.Selection of Arabidopsis cDNAs that partially correct phenotypes of Escherichia coli DNA-damage-sensitive mutants and analysis of two plant cDNAs that appear to express UV-specific dark repair activities.Plant Molecular Biology,1993,22(3):411-426.
[13]Lloyd R G.Conjugational recombination in resolvase-deficient ruvC mutants of Escherichia coli K-12depends on recG.Journal of Bacteriology,1991,173(17):5414-5418.
[14]Breusing N,Grune T.Regulation of proteasome-mediated protein degradation during oxidative stress and aging.Biological Chemistry,2008,389(3):203-209.
[15]Fu H,Girod P A,Doelling J H,van Nocker S,Hochstrasser M,Finley D,Vierstra R D.Structure and functional analysis of the26S proteasome subunits from plants.Plant Molecular Biology Reporter,1999,26(7):137-146.
[16]Lommel L,Chen L,Madura K.The26S proteasome negatively regulates the level of overall genomic nucleotide excision repair.Nucleic Acids Research,2000,28(24):4839-4845.
[17]Peng Z H,Staub J M,Serino G.The cellular level of PR500,a protein complex related to the19S regulatory particle of the proteasome,is regulated in response to stresses in plants.Molecular Biology of the Cell,2001,12(2):383-392.
[18]Picton R,Eggo M C,Merrill G A,Langman M J S,Singh S.Mucosal protection against sulphide:importance of the enzyme rhodanese.Gut,2002,50(2):201-205.
[19]Lamb C J,Zhang D P.A ligand-receptor mechanism in plant-pathogen recognition.Science,1996,274(5295):2038-2039.
[20]Holt B F,Belkhadir Y,Dangl J L.Antagonistic control of disease resistance protein stability in the plant immune system.Science,2005,309(5736):929-932.
[21]Zhang S,Gu Y Q,Singh J,Coleman-Derr D,Brar D S,Jiang N,Lemaux P G.New insights into Oryza genome evolution:high gene colinearity and differential retrotransposon amplification.Plant Molecular Biology,2007,64(5):589-600.
[22]Ansari K I,Walter S,Brennan J M,Lemmens M,Kessans S,McGahern A,Egan D,Doohan F M.Retrotransposon and gene activation in wheat in response to mycotoxigenic and non-mycotoxigenic-associated Fusarium stress.Theoretical and Applied Genetics,2007,114(5):927-937.
[23]Steward N,Ito M,Yamaguchi Y,Koizumi N,Sano H.Periodic DNA methylation in maize nucleosomes and demethylation by environmental stress.Journal of Biological Chemistry,2002,277(40):37741-37746.
[24]Mhiri C,Morel J B,Vernhettes S,Casacuberta J M,Lucas H,Grandbastien M A.The promoter of the tobacco Tnt1retrotransposon is induced by wounding and by abiotic stress.Plant Molecular Biology,1997,33(2):257-266.
[25]Thimmapuram J,Korban S S.Characterization and expression ofβ-1,3-glucanase genes in peach.Molecular Genetics and Genomics,2001,265(3):469-479.
[26]McCollum T G,Doostdar H,Burkhart M D,Neidz R P,Mayer R T,McDonald R E.Biochemical and molecular characterization of aβ-1,3-endoglucanase from Valencia Orange Callus.HortScience,1996,31(4):614-614.
[27]Sanchez-Ballesta M T,Gosalbes M J,Rodrigo M J,Granell A,Zacarias L,Lafuente M T.Characterization of aβ-1,3-glucanase from citrus fruit as related to chilling-induced injury and ethylene production.Postharvest Biology and Technology,2006,40(2):133-140.
[28]Domingo C,Conejero V,Vera P.Genes encoding acidic and basic class IIIβ-1,3-glucanases are expressed in tomato plants upon viroid infection.Plant Molecular Biology,1994,24(5):725-732.
[29]Nogueira F T S,De Rosa V E Jr,Menossi M,Ulian E C,Arruda P.RNA expression profiles and data mining of sugarcane response to low temperature.Plant Physiology,2003,132(4):1811-1824.
[30]Tessitori M,Maria G,Capasso C,Catara G,Rizza S,de Luca V,Catara A,Capasso A,Carginale V.Differential display analysis of gene expression in Etrog citron leaves infected by Citrus viroid III.Biochimica et Biophysica Acta(BBA)-Gene Structure and Expression,2007,1769(4),228-235.
[31]Ding B L,Tan H H,Zhu S Q.Advances on research of the relationship between stresses and plant cell wall.Journal of Guangxi Academy of Sciences,2001,17(2):87-90.
[32]Weiser R L,Wallner S J,Waddell J W.Cell wall and extensin mRNA changes during cold acclimation of pea seedlings.Plant Physiology,1990,93(3):1021-1026.
[33]Purugganan M M,Braam J,Fry S C.The Arabidopsis TCH 4 xyloglucan endotransglycosylase(Substrate specificity,pH optimum,and cold tolerance).Plant Physiology,1997,115(1):181-190.
[34]Borutova R,Faix S,Placha I,Gresakova L,Cobanova K,Leng L.Effects of deoxynivalenol and zearalenone on oxidative stress and blood phagocytic activity in broilers.Archives of Animal Nutrition,2008,62(4):303-312.
[35]Cavalca L,Guerrieri N,Colombo M,Pagani S,Andreoni V.Enzymatic and genetic profiles in environmental strains grown on polycyclic aromatic hydrocarbons.Antonie van Leeuwenhoek,2007,91(4):315-325.
[36]Moussatova A,Kandt C,O'Mara M L,Tieleman D P.ATP-binding cassette transporters in Escherichia coli.Biochimica et Biophysica Acta,2008,1778(9):1757-1771.
[37]Hannivoort R A,Dunning S,Vander B S,Schroyen B,Woudenberg J,Oakley F,Buist-Homan M,van den Heuvel F A,Geuken M,Geerts A,Roskams T,Faber K N,Moshage H.Multidrug resistance-associated proteins are crucial for the viability of activated rat hepatic stellate cells.Hepatology,2008,48(2):624-634.
[38]Lu H,Klaassen C.Gender differences in mRNA expression of ATP-binding cassette efflux and bile acid transporters in kidney,liver,and intestine of5/6nephrectomized rats.Drug Metabolism and Disposition,2008,36(1):16-23.
[39]Locher K P.Structure and mechanism of ABC transporters.Current Opinion in Structural Biology,2004,14(4):426-431.
[40]Toyoda Y,Hagiya Y,Adachi T,Hoshijima K,Kuo M T,Ishikawa T.MRP class of human ATP binding cassette(ABC)transporters:historical background and new research directions.Xenobiotica,2008,38(7/8):833-842.
[41]Wu S G,Ren X P.The relationship between Plant polyamine and several adverse stress.Journal of Shangqiu Vocational and Technical College,2005,4(2):58-59.
[4]陈香波,张爱平,姚泉洪.植物抗寒基因工程研究进展.生物技术通报,2001,(4):14-20.
[5]郭卫东,张真真,蒋小韦,陈民管,郑建树,陈文荣.低温胁迫下佛手半致死温度测定和抗寒性分析.园艺学报,2009,36(1):81-86.
[6]曹诣斌,石瑞,陈文荣,郭卫东.低温胁迫下佛手和枳乙烯应答因子6(ERF6)表达变化的比较分析.园艺学报,2011,38(10):1873-1882.
[7]石瑞,曹诣斌,陈文荣,郭卫东.佛手GRAS基因的克隆及表达分析.浙江师范大学学报:自然科学版,2011,34(4):446-451.
[10]石晓冰,魏家绵,沈允钢.叶绿体ATP合酶CF 1与CF 0亚基间的相互作用.科学通报,2001,46(18):1550-1554.
[31]丁宝莲,谈宏鹤,朱素琴.胁迫与植物细胞壁关系研究进展.广西科学院学报,2001,17(2):87-90.
[41]吴诗光,任雪平.植物多胺与几种逆境胁迫的关系.商丘职业技术学院学报,2005,4(2):58-59.