RNA-Seq定量分析盐肤木对铅胁迫的响应
|
摘要
为探究重金属污染地生态修复先锋植物——盐肤木对重金属胁迫的分子响应机制,设置3个铅胁迫水平(0、250、1000mg·kg~(-1)),应用Illumina HiSeq~(TM)2000进行盐肤木根系的转录组测序,并通过Gene Ontology(GO)与Pathway功能显著富集分析方法,分析说明盐肤木响应不同铅胁迫水平下的差异表达基因。结果表明,盐肤木在遭受轻度铅胁迫时,主要有4类水解酶与2类磷酸酶相关基因显著富集,说明盐肤木主要通过调节细胞内水解酶与磷酸酶相关基因来抵御胁迫,而在重度铅胁迫下,主要有6类氧化还原酶相关基因出现显著富集,此时氧化还原酶相关基因起到主要调节作用;盐肤木在铅胁迫下细胞受损,在轻、重度铅胁迫下,分别有24、16类细胞相关基因显著富集,但其自身可通过调节细胞内细胞器、细胞质等相关的细胞运动以应对逆境;核糖体代谢通路是盐肤木适应铅胁迫的主要代谢通路。研究表明,核糖体相关基因是盐肤木响应铅胁迫的主要应答与调节基因。
Rhus chinensis is one of the pioneer plants for ecological restoration of heavy-metal-polluted areas. Since this species shows good tolerance to heavy metals such as lead and chromium, exploring its molecular response mechanism to heavy metal stress can provide a reference for the ecological restoration of heavy-metal pollution. In this study, we exposed R. chinensis to three concentrations of lead, corresponding to no, mild, and severe lead stress, respectively(0, 250, 1000 mg·kg~(-1)), and performed transcriptome sequencing of the roots on the Illumina HiSeq~(TM)2000 system. Significant enrichment analysis was performed for Gene Ontology(GO)and Pathway functions, and the differentially expressed genes in response to the different lead concentrations were analyzed. Four types of hydrolases and two types of phosphatase-related genes were found to be differentially expressed in the mild lead-stress condition, which indicated that R. chinensis was mainly regulated by intracellular hydrolase and phosphatase-related genes. Under severe lead stress, six types of oxidoreductase-related genes were significantly enriched and played a major regulatory role. The cells were damaged under lead stress, and 24 and 16 cell-related genes were significantly enriched under mild and severe lead stress, respectively. However, R. chinensis could cope with this adversity by regulating cellular movements such as the movement of organelles and cytoplasm in cells. The ribosomal metabolic pathway was found to be the main metabolic pathway for salt tolerance and adaptation to lead stress, and ribosome-associated genes appeared to be the major regulatory genes induced in response to lead stress in R. chinensis.
Rhus chinensis is one of the pioneer plants for ecological restoration of heavy-metal-polluted areas. Since this species shows good tolerance to heavy metals such as lead and chromium, exploring its molecular response mechanism to heavy metal stress can provide a reference for the ecological restoration of heavy-metal pollution. In this study, we exposed R. chinensis to three concentrations of lead, corresponding to no, mild, and severe lead stress, respectively(0, 250, 1000 mg·kg~(-1)), and performed transcriptome sequencing of the roots on the Illumina HiSeq~(TM)2000 system. Significant enrichment analysis was performed for Gene Ontology(GO)and Pathway functions, and the differentially expressed genes in response to the different lead concentrations were analyzed. Four types of hydrolases and two types of phosphatase-related genes were found to be differentially expressed in the mild lead-stress condition, which indicated that R. chinensis was mainly regulated by intracellular hydrolase and phosphatase-related genes. Under severe lead stress, six types of oxidoreductase-related genes were significantly enriched and played a major regulatory role. The cells were damaged under lead stress, and 24 and 16 cell-related genes were significantly enriched under mild and severe lead stress, respectively. However, R. chinensis could cope with this adversity by regulating cellular movements such as the movement of organelles and cytoplasm in cells. The ribosomal metabolic pathway was found to be the main metabolic pathway for salt tolerance and adaptation to lead stress, and ribosome-associated genes appeared to be the major regulatory genes induced in response to lead stress in R. chinensis.
引文
[1]徐军.植物促生细菌和EDTA对植物生长与富集土壤重金属的影响及机制研究[D].南京:南京农业大学,2012.XU Jun.Effects of plant growth-promoting bacteria and EDTA on the growth and heavy metal accmulation of plants[D].Nanjing:Nanjing Agricultural University,2012.
[2]Kumar G H,Kumari J P.Heavy metal lead influative toxicity and its assessment in phytoremediating plants:A review[J].Water,Air&Soil Pollution,2015,226(10):1-11.
[3]Bharwana S A,Shafaqat A,Farooq M A,et al.Influence of lead stress on growth,photosynthesis and lead uptake in the seedlings of cotton[J].International Journal of Agronomy and Plant Production,2013,4(10):2492-2501.
[4]施翔,王树凤,潘红伟,等.盐肤木幼苗对铅胁迫的生理响应[J].林业科学研究,2016,29(1):147-153.SHI Xiang,WANG Shu-feng,PAN Hong-wei,et al.Physiological responses of Rhus chinensis under lead stress[J].Forest Research,2016,29(1):147-153.
[5]张春荣,桑雪雨,渠萌,等.基于转录组测序揭示适度干旱胁迫对甘草根基因表达的调控[J].中国中药杂志,2015,40(24):4817-4823.ZHANG Chun-rong,SANG Xue-yu,QU Meng,et al.De novo sequencing and analysis of root transcriptome to reveal regulation of gene expression by moderate drought stress in Glycyrrhiza uralensis[J].China Journal of Chinese Medica,2015,40(24):4817-4823.
[6]Gong J M,Lee D A,Schroeder J I.Long-distance root-to-shoot transport of phytochelatins and cadmium in Arabidopsis[J].Proceedings of the National Academy of Sciences,2003,100(17):10118-10123.
[7]迟春宁,丁国华.植物耐重金属的分子生物学研究进展[J].生物技术通报,2017,33(3):6-11.CHI Chun-ning,DING Guo-hua.Research progress of the molecular biology in heavy metal tolerance of plants[J].Biotechnology Bulletin,2017,33(3):6-11.
[8]刘海琳,尹佟明.全基因组测序技术研究及其在木本植物中的应用[J].南京林业大学学报(自然科学版),2018,42(5):172-178.LIU Hai-lin,YIN Tong-ming.Progress on the whole genome sequencing and the application in woody plants[J].Journal of Nanjing Forestry University(Natural Science Edition),2018,42(5):172-178.
[9]陈晶,穆燕,陈明,等.盐肤木对重金属铬胁迫的生理生化反应研究[J].生态科学,2017,36(2):26-31.CHEN Jing,MU Yan,CHEN Ming,et al.Response of physiology and biochemistry of Rhus chinensis to heavy metal chromium stress[J].Ecological Science,2017,36(2):26-31.
[10]黄凯,张雪娇,冯媛,等.河南省尾矿库土壤重金属污染评价及优势植物重金属累积特征[J].黑龙江农业科学,2018(1):51-56.HUANG Kai,ZHANG Xue-jiao,FENG Yuan,et al.Evaluation of heavy metal pollution in soil of a tailings reservoir in Henan and accumulation of heavy metals in the dominant plants[J].Heilongjiang Agricultural Sciences,2018(1):51-56.
[11]Li Q T,Yang F J,Zhang B,et al.Biogeochemistry responses and spectral characteristics of Rhus Chinensis Mill under heavy metal contamination stress[J].Journal of Remote Sensing,2008,12(2):284-290.
[12]Marioni J C,Mason C E,Mane S M,et al.RNA-seq:An assessment of technical reproducibility and comparison with gene expression ar-387rays[J].Genome Research,2008,18(9):1509-1517.
[13]Nagalakshmi U,Wang Z,Waern K,et al.The transcriptional landscape of the yeast genome defined by RNA sequencing[J].Science,2008,320(5881):1344-1349.
[14]祁云霞,刘永斌,荣威恒.转录组研究新技术:RNA-Seq及其应用[J].遗传,2011,33(11):1191-1202.QI Yun-xia,LIU Yong-bin,RONG Wei-heng.RNA-Seq and its applications:A new technology for transcriptomics[J].Hereditas,2011,33(11):1191-1202.
[15]鲁如坤.土壤农业化学分析方法[M].北京:中国农业科技出版社,2000.LU Ru-kun.Soil argrochemistry analysis protocoes[M].Beijing:China Agricultural Science and Technology Press,2000.
[16]吴凯朝,黄诚梅,李杨瑞,等.Trizol试剂法快速高效提取3种作物不同组织总RNA[J].南方农业学报,2012,43(12):1934-1939.WU Kai-chao,HUANG Cheng-mei,LI Yang-rui,et al.Fast and effective total RNA extraction from different tissues in 3 crops through the Trizol reagent method[J].Journal of Southern Agriculture,2012,43(12):1934-1939.
[17]Benjamini Y,Hochberg Y.Controlling the false discovery rate:Apractical and powerful approach to multiple testing[J].Journal of the Royal Statistical Society,1995,57(1):289-300.
[18]Kanehisa M,Araki M,Goto S,et al.KEGG for linking genomes to life and the environment[J].Nucleic Acids Research,2007,36(Suppl1):D480-D484.
[19]Li R,Yu C,Li Y,et al.SOAP2:An improved ultrafast tool for short read alignment[J].Bioinformatics,2009,25(15):1966-1967.
[20]Benjamini Y,Yekutieli D.The control of the false discovery rate in multiple testing under dependency[J].Annals of Statistics,2001,29(4):1165-1188.
[21]刘家佳.工业大麻盐胁迫转录组学研究[D].昆明:云南大学,2016.LIU Jia-jia.RNA-Seq analysis of industrial hemp under salt stress[D].Kunming:Yunnan University,2016.
[22]叶珊.利用差异显示与RNA-Seq技术进行萝卜铬胁迫响应相关基因鉴定[D].南京:南京农业大学,2013.YE Shan.Identification of genes involved in response to chromium stress with DD-PCR and RNA-SEQ in radish(Raphanus sativus L.)[D].Nanjing:Nanjing Agricultural University,2013.
[23]Cosgrove,Daniel J.Growth of the plant cell wall[J].Nature Reviews Molecular Cell Biology,2005,6(11):850-861.
[24]Catala C,Rose J K C,York W S,et al.Characterization of a Lycopersicon esculentum Mill.xyloglucan endotransglycosylase gene that is down-regulated by auxin in etiolated hypocotyls[J].Plant Physiology,2001,127(3):1180-1192.
[25]Cho S K,Kim J E,Park J A,et al.Constitutive expression of abiotic stress-inducible hot pepper CaXTH3,which encodes a xyloglucan endotransglucosylase/hydrolase homolog,improves drought and salt tolerance in transgenic Arabidopsis plants[J].Febs Letters,2006,580(13):3136-3144.
[26]Choi J Y,Seo Y S,Su J K,et al.Constitutive expression of CaXTH3,a hot pepper xyloglucan endotransglucosylase/hydrolase,enhanced tol-20197RNA-Seq erance to salt and drought stresses without phenotypic defects in Lycopersicon esculentum Mill.plants(Solanum lycopersicum cv.Dotaerang)[J].Plant Cell Reports,2011,30(5):867-877.
[27]Tomassoni M L,Amori D,Magni M V.Changes of nuclear membrane lipid composition affect RNA nucleocytoplasmic transport[J].Biochem Biophys Res Commun,1999,258(2):476-481.
[28]贤加欢,张美萍,孙春玉,等.可溶性焦磷酸酶的研究进展[J/OL].基因组学与应用生物学.(2018-10-20).http//kns.cnki.net/kcms/detail/45.1369.Q.20181020.1613.006.html.XIAN Jia-huan,ZHANG Mei-ping,SUN Chun-yu,et al.Review on soluble pyrophosphatase[J/OL].Genomics and Applied Biology.(2018-10-20).http//kns.cnki.net/kcms/detail/45.1369.Q.20181020.1613.006.html.
[29]Park S,Li J,Pittman J K,et al.Up-regulation of a H+-pyrophosphatase(H+-PPase)as a strategy to engineer drought-resistant crop plants[J].Proceedings of the National Academy of Sciences,2005,102(52):18830-18835.
[30]Eckstein M,Thomas Dau?mann,Kragl U.Recent developments in NAD(P)H regeneration for enzymatic reductions in one-and twophase systems[J].Biocatalysis,2004,22(2):89-96.
[31]王晚晴.拟南芥FHY3/FAR1转录因子调控四吡咯合成与植物免疫的机理研究[D].北京:中国科学院大学,2014.WANG Wan-qing.Mechanism of Arabidopsis thaliana FHY3/FAR1transcription factor regulating tetrapyrrole synthesis and plant immunity[D].Beijing:University of Chinese Academy of Sciences,2014.
[32]Souza R D S,Adrián L d A S,Anjos d S L,et al.Lead tolerance and phytoremediation potential of Brazilian leguminous tree species at the seedling stage[J].Journal of Environmental Management,2012,110(4):299-307.
[33]梁前进.细胞器不依赖于DNA的复制:中心体自主复制解读[J].科学通报,2017,62(13):1333-1345.LIANG Qian-jin.Organellic replication that is independent of DNA:Unscrambling the autonomous centrosomal replication[J].Chinese Science Bulletin,2017,62(13):1333-1345.
[34]Yao Y X,Dong Q L,Zhai H,et al.The functions of an apple cytosolic malate dehydrogenase gene in growth and tolerance to cold and salt stresses[J].Plant Physiology&Biochemistry,2011,49(3):257-264.
[35]Komili S,Farny N G,Roth F P,et al.Functional specificity among ribosomal proteins regulates gene expression[J].Cell,2007,131(3):557-571.
[36]Barakat A,Szick-Miranda K,Chang I F,et al.The organization of cytoplasmic ribosomal protein genes in the Arabidopsis genome[J].Plant Physiology,2001,127(2):398-415.
[37]靳聪聪,侯名语,潘延云.拟南芥核糖体蛋白生物学功能研究进展[J].植物生理学报,2018,54(2):203-212.JIN Cong-cong,HOU Ming-yu,PAN Yan-yun.Research progress of ribosomal protein function in Arabidopsis thaliana[J].Plant Physiology Journal,2018,54(2):203-212.
[38]Zhou C,Huang M,Ren H,et al.Bioaccumulation and detoxification mechanisms for lead uptake identified in Rhus chinensis Mill.seedlings[J].Ecotoxicology&Environmental Safety,2017,142:59-68.
[39]李跃建,梁根云,刘小俊,等.黄瓜嫁接苗和自根苗的蛋白质组学研究[J].园艺学报,2009,36(8):1147-1152.LI Yue-jian,LIANG Gen-yun,LIU Xiao-jun,et al.Proteomic study on grafted and non-grafted cucumber(Cucumis sativus L.)[J].Acta Horticulturae Sinica,2009,36(8):1147-1152.
[40]姚广,高辉远,王未未,等.铅胁迫对玉米幼苗叶片光系统功能及光合作用的影响[J].生态学报,2009,29(3):1162-1169.YAO Guang,GAO Hui-yuan,WANG Wei-wei,et al.The effects of Pb-stress on functions of photosystems and photosynthetic rate in maize seedling leaves[J].Acta Ecologica Sinica,2009,29(3):1162-1169.
[41]杜连彩.铅对苹果砧木平邑甜茶、八楞海棠的毒害机理及耐性比较研究[D].济南:山东师范大学,2006.DU Lian-cai.The study on mechanism of Pb toxicity apple stock M.hupehensis,M.micromalus and comparison of their tolerance[D].Jinan:Shandong Normal University,2006.
[2]Kumar G H,Kumari J P.Heavy metal lead influative toxicity and its assessment in phytoremediating plants:A review[J].Water,Air&Soil Pollution,2015,226(10):1-11.
[3]Bharwana S A,Shafaqat A,Farooq M A,et al.Influence of lead stress on growth,photosynthesis and lead uptake in the seedlings of cotton[J].International Journal of Agronomy and Plant Production,2013,4(10):2492-2501.
[4]施翔,王树凤,潘红伟,等.盐肤木幼苗对铅胁迫的生理响应[J].林业科学研究,2016,29(1):147-153.SHI Xiang,WANG Shu-feng,PAN Hong-wei,et al.Physiological responses of Rhus chinensis under lead stress[J].Forest Research,2016,29(1):147-153.
[5]张春荣,桑雪雨,渠萌,等.基于转录组测序揭示适度干旱胁迫对甘草根基因表达的调控[J].中国中药杂志,2015,40(24):4817-4823.ZHANG Chun-rong,SANG Xue-yu,QU Meng,et al.De novo sequencing and analysis of root transcriptome to reveal regulation of gene expression by moderate drought stress in Glycyrrhiza uralensis[J].China Journal of Chinese Medica,2015,40(24):4817-4823.
[6]Gong J M,Lee D A,Schroeder J I.Long-distance root-to-shoot transport of phytochelatins and cadmium in Arabidopsis[J].Proceedings of the National Academy of Sciences,2003,100(17):10118-10123.
[7]迟春宁,丁国华.植物耐重金属的分子生物学研究进展[J].生物技术通报,2017,33(3):6-11.CHI Chun-ning,DING Guo-hua.Research progress of the molecular biology in heavy metal tolerance of plants[J].Biotechnology Bulletin,2017,33(3):6-11.
[8]刘海琳,尹佟明.全基因组测序技术研究及其在木本植物中的应用[J].南京林业大学学报(自然科学版),2018,42(5):172-178.LIU Hai-lin,YIN Tong-ming.Progress on the whole genome sequencing and the application in woody plants[J].Journal of Nanjing Forestry University(Natural Science Edition),2018,42(5):172-178.
[9]陈晶,穆燕,陈明,等.盐肤木对重金属铬胁迫的生理生化反应研究[J].生态科学,2017,36(2):26-31.CHEN Jing,MU Yan,CHEN Ming,et al.Response of physiology and biochemistry of Rhus chinensis to heavy metal chromium stress[J].Ecological Science,2017,36(2):26-31.
[10]黄凯,张雪娇,冯媛,等.河南省尾矿库土壤重金属污染评价及优势植物重金属累积特征[J].黑龙江农业科学,2018(1):51-56.HUANG Kai,ZHANG Xue-jiao,FENG Yuan,et al.Evaluation of heavy metal pollution in soil of a tailings reservoir in Henan and accumulation of heavy metals in the dominant plants[J].Heilongjiang Agricultural Sciences,2018(1):51-56.
[11]Li Q T,Yang F J,Zhang B,et al.Biogeochemistry responses and spectral characteristics of Rhus Chinensis Mill under heavy metal contamination stress[J].Journal of Remote Sensing,2008,12(2):284-290.
[12]Marioni J C,Mason C E,Mane S M,et al.RNA-seq:An assessment of technical reproducibility and comparison with gene expression ar-387rays[J].Genome Research,2008,18(9):1509-1517.
[13]Nagalakshmi U,Wang Z,Waern K,et al.The transcriptional landscape of the yeast genome defined by RNA sequencing[J].Science,2008,320(5881):1344-1349.
[14]祁云霞,刘永斌,荣威恒.转录组研究新技术:RNA-Seq及其应用[J].遗传,2011,33(11):1191-1202.QI Yun-xia,LIU Yong-bin,RONG Wei-heng.RNA-Seq and its applications:A new technology for transcriptomics[J].Hereditas,2011,33(11):1191-1202.
[15]鲁如坤.土壤农业化学分析方法[M].北京:中国农业科技出版社,2000.LU Ru-kun.Soil argrochemistry analysis protocoes[M].Beijing:China Agricultural Science and Technology Press,2000.
[16]吴凯朝,黄诚梅,李杨瑞,等.Trizol试剂法快速高效提取3种作物不同组织总RNA[J].南方农业学报,2012,43(12):1934-1939.WU Kai-chao,HUANG Cheng-mei,LI Yang-rui,et al.Fast and effective total RNA extraction from different tissues in 3 crops through the Trizol reagent method[J].Journal of Southern Agriculture,2012,43(12):1934-1939.
[17]Benjamini Y,Hochberg Y.Controlling the false discovery rate:Apractical and powerful approach to multiple testing[J].Journal of the Royal Statistical Society,1995,57(1):289-300.
[18]Kanehisa M,Araki M,Goto S,et al.KEGG for linking genomes to life and the environment[J].Nucleic Acids Research,2007,36(Suppl1):D480-D484.
[19]Li R,Yu C,Li Y,et al.SOAP2:An improved ultrafast tool for short read alignment[J].Bioinformatics,2009,25(15):1966-1967.
[20]Benjamini Y,Yekutieli D.The control of the false discovery rate in multiple testing under dependency[J].Annals of Statistics,2001,29(4):1165-1188.
[21]刘家佳.工业大麻盐胁迫转录组学研究[D].昆明:云南大学,2016.LIU Jia-jia.RNA-Seq analysis of industrial hemp under salt stress[D].Kunming:Yunnan University,2016.
[22]叶珊.利用差异显示与RNA-Seq技术进行萝卜铬胁迫响应相关基因鉴定[D].南京:南京农业大学,2013.YE Shan.Identification of genes involved in response to chromium stress with DD-PCR and RNA-SEQ in radish(Raphanus sativus L.)[D].Nanjing:Nanjing Agricultural University,2013.
[23]Cosgrove,Daniel J.Growth of the plant cell wall[J].Nature Reviews Molecular Cell Biology,2005,6(11):850-861.
[24]Catala C,Rose J K C,York W S,et al.Characterization of a Lycopersicon esculentum Mill.xyloglucan endotransglycosylase gene that is down-regulated by auxin in etiolated hypocotyls[J].Plant Physiology,2001,127(3):1180-1192.
[25]Cho S K,Kim J E,Park J A,et al.Constitutive expression of abiotic stress-inducible hot pepper CaXTH3,which encodes a xyloglucan endotransglucosylase/hydrolase homolog,improves drought and salt tolerance in transgenic Arabidopsis plants[J].Febs Letters,2006,580(13):3136-3144.
[26]Choi J Y,Seo Y S,Su J K,et al.Constitutive expression of CaXTH3,a hot pepper xyloglucan endotransglucosylase/hydrolase,enhanced tol-20197RNA-Seq erance to salt and drought stresses without phenotypic defects in Lycopersicon esculentum Mill.plants(Solanum lycopersicum cv.Dotaerang)[J].Plant Cell Reports,2011,30(5):867-877.
[27]Tomassoni M L,Amori D,Magni M V.Changes of nuclear membrane lipid composition affect RNA nucleocytoplasmic transport[J].Biochem Biophys Res Commun,1999,258(2):476-481.
[28]贤加欢,张美萍,孙春玉,等.可溶性焦磷酸酶的研究进展[J/OL].基因组学与应用生物学.(2018-10-20).http//kns.cnki.net/kcms/detail/45.1369.Q.20181020.1613.006.html.XIAN Jia-huan,ZHANG Mei-ping,SUN Chun-yu,et al.Review on soluble pyrophosphatase[J/OL].Genomics and Applied Biology.(2018-10-20).http//kns.cnki.net/kcms/detail/45.1369.Q.20181020.1613.006.html.
[29]Park S,Li J,Pittman J K,et al.Up-regulation of a H+-pyrophosphatase(H+-PPase)as a strategy to engineer drought-resistant crop plants[J].Proceedings of the National Academy of Sciences,2005,102(52):18830-18835.
[30]Eckstein M,Thomas Dau?mann,Kragl U.Recent developments in NAD(P)H regeneration for enzymatic reductions in one-and twophase systems[J].Biocatalysis,2004,22(2):89-96.
[31]王晚晴.拟南芥FHY3/FAR1转录因子调控四吡咯合成与植物免疫的机理研究[D].北京:中国科学院大学,2014.WANG Wan-qing.Mechanism of Arabidopsis thaliana FHY3/FAR1transcription factor regulating tetrapyrrole synthesis and plant immunity[D].Beijing:University of Chinese Academy of Sciences,2014.
[32]Souza R D S,Adrián L d A S,Anjos d S L,et al.Lead tolerance and phytoremediation potential of Brazilian leguminous tree species at the seedling stage[J].Journal of Environmental Management,2012,110(4):299-307.
[33]梁前进.细胞器不依赖于DNA的复制:中心体自主复制解读[J].科学通报,2017,62(13):1333-1345.LIANG Qian-jin.Organellic replication that is independent of DNA:Unscrambling the autonomous centrosomal replication[J].Chinese Science Bulletin,2017,62(13):1333-1345.
[34]Yao Y X,Dong Q L,Zhai H,et al.The functions of an apple cytosolic malate dehydrogenase gene in growth and tolerance to cold and salt stresses[J].Plant Physiology&Biochemistry,2011,49(3):257-264.
[35]Komili S,Farny N G,Roth F P,et al.Functional specificity among ribosomal proteins regulates gene expression[J].Cell,2007,131(3):557-571.
[36]Barakat A,Szick-Miranda K,Chang I F,et al.The organization of cytoplasmic ribosomal protein genes in the Arabidopsis genome[J].Plant Physiology,2001,127(2):398-415.
[37]靳聪聪,侯名语,潘延云.拟南芥核糖体蛋白生物学功能研究进展[J].植物生理学报,2018,54(2):203-212.JIN Cong-cong,HOU Ming-yu,PAN Yan-yun.Research progress of ribosomal protein function in Arabidopsis thaliana[J].Plant Physiology Journal,2018,54(2):203-212.
[38]Zhou C,Huang M,Ren H,et al.Bioaccumulation and detoxification mechanisms for lead uptake identified in Rhus chinensis Mill.seedlings[J].Ecotoxicology&Environmental Safety,2017,142:59-68.
[39]李跃建,梁根云,刘小俊,等.黄瓜嫁接苗和自根苗的蛋白质组学研究[J].园艺学报,2009,36(8):1147-1152.LI Yue-jian,LIANG Gen-yun,LIU Xiao-jun,et al.Proteomic study on grafted and non-grafted cucumber(Cucumis sativus L.)[J].Acta Horticulturae Sinica,2009,36(8):1147-1152.
[40]姚广,高辉远,王未未,等.铅胁迫对玉米幼苗叶片光系统功能及光合作用的影响[J].生态学报,2009,29(3):1162-1169.YAO Guang,GAO Hui-yuan,WANG Wei-wei,et al.The effects of Pb-stress on functions of photosystems and photosynthetic rate in maize seedling leaves[J].Acta Ecologica Sinica,2009,29(3):1162-1169.
[41]杜连彩.铅对苹果砧木平邑甜茶、八楞海棠的毒害机理及耐性比较研究[D].济南:山东师范大学,2006.DU Lian-cai.The study on mechanism of Pb toxicity apple stock M.hupehensis,M.micromalus and comparison of their tolerance[D].Jinan:Shandong Normal University,2006.