植物小RNA在病毒致病过程中的作用研究进展
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摘要
目前,我国正遭受多种外来有害生物的入侵,给我国的农业生产以及生态环境造成了严重影响。其中检疫性植物病毒危害大、隐蔽性强,是重要的外来生物。掌握病毒致病的相关机制是有效防控入侵病毒病害的基础。微小RNA(microRNA,miRNA)以及病毒小干扰RNA(small interfering RNA,siRNA)是植物体内重要的非编码小RNA,在病毒致病过程中扮演着重要角色。病毒在侵染过程中,可以利用植物抗病毒免疫反应产生的siRNA进行致病,同时可以直接或间接干扰miRNA的代谢途径,导致相关症状的产生。本文根据植物小RNA的近期研究进展,对miRNA和病毒siRNA的产生途径、生物学特性以及作用分子机制进行了综述,并对其在病毒侵染过程中的作用进行了探讨,初步从小RNA的角度阐述了植物病毒的致病机制,以期为检疫性病毒病害的防控提供理论基础。
At present, China is suffering from a variety of invasive species, which seriously influences the agricultural products and ecological environment. The quarantine plant viruses are the important exotic species, as their damages are great and usually hard to be detected. It is essential to understand the related mechanisms of viral diseases for effectively preventing and controlling plant viruses. The microRNA(miRNA) and viral small interfering RNA(siRNA) are both very important non-encoding small RNAs in plants and play important roles during viral infection. The viruses use the siRNAs that are produced during the plant anti-virus immunity response to induce diseases, and also interfere in the metabolic pathways of miRNAs directly or indirectly. Based on recent research advances in small RNAs in plants, the production pathway, the biological characteristics and the molecular mechanisms of viral siRNAs and miRNAs were summarized, and the roles of small RNAs during viral infection were also discussed, which preliminarily explored the pathogenic mechanisms of plant viruses from the perspectives of plant small RNAs and provided the theoretical basis for the prevention and control of quarantine viruses.
At present, China is suffering from a variety of invasive species, which seriously influences the agricultural products and ecological environment. The quarantine plant viruses are the important exotic species, as their damages are great and usually hard to be detected. It is essential to understand the related mechanisms of viral diseases for effectively preventing and controlling plant viruses. The microRNA(miRNA) and viral small interfering RNA(siRNA) are both very important non-encoding small RNAs in plants and play important roles during viral infection. The viruses use the siRNAs that are produced during the plant anti-virus immunity response to induce diseases, and also interfere in the metabolic pathways of miRNAs directly or indirectly. Based on recent research advances in small RNAs in plants, the production pathway, the biological characteristics and the molecular mechanisms of viral siRNAs and miRNAs were summarized, and the roles of small RNAs during viral infection were also discussed, which preliminarily explored the pathogenic mechanisms of plant viruses from the perspectives of plant small RNAs and provided the theoretical basis for the prevention and control of quarantine viruses.
引文
Adkar-Purushothama CR,Brosseau C,Giguere T,Sano T,Moffett P,Perreault JP.2015.Small RNA derived from the virulence modulating region of the Potato spindle tuber viroid silences callose synthase genes of tomato plants.Plant Cell,27(8):2178-2194
Adkar-Purushothama CR,Iyer PS,Perreault JP.2017.Potato spindle tuber viroid infection triggers degradation of chloride channel protein CLC-b-like and ribosomal protein S3a-like mRNAs in tomato plants.Scientific Reports,7(1):8341
Babu M,Gagarinova AG,Brandle JE,Wang AM.2008.Association of the transcriptional response of soybean plants with Soybean mosaic virus systemic infection.Journal of General Virology,89(4):1069-1080
Baldrich P,San Segundo B.2016.MicroRNAs in rice innate immunity.Rice,9(1):6
Bazzini AA,Hopp HE,Beachy RN,Asurmendi S.2007.Infection and coaccumulation of Tobacco mosaic virus proteins alter microR-NA levels,correlating with symptom and plant development.Proceedings of the National Academy Sciences of the United States of America,104(29):12157-12162
Borges F,Martienssen RA.2015.The expanding world of small RNAs in plants.Nature Reviews Molecular Cell Biology,16(12):727-741
Caplan JL,Mamillapalli P,Burch-Smith TM,Czymmek K,Dinesh-Kumar SP.2008.Chloroplastic protein NRIP1 mediates innate immune receptor recognition of a viral effector.Cell,132(3):449-462
Chapman EJ,Prokhnevsky AI,Gopinath K,Dolja VV,Carrington JC.2004.Viral RNA silencing suppressors inhibit the microRNApathway at an intermediate step.Genes&Development,18(10):1179-1186
Chellappan P,Vanitharani R,Fauquet CM.2005.MicroRNA-binding viral protein interferes with Arabidopsis development.Proceedings of the National Academy of Sciences of the United States of America,102(29):10381-10386
Coll NS,Epple P,Dangl JL.2011.Programmed cell death in the plant immune system.Cell Death and Differentiation,18(8):1247-1256
Csorba T,Kontra L,Burgyan J.2015.Viral silencing suppressors:tools forged to fine-tune host-pathogen coexistence.Virology,479/480:85-103
Dardick C.2007.Comparative expression profiling of Nicotiana benthamiana leaves systemically infected with three fruit tree viruses.Molecular Plant-Microbe Interactions,20(8):1004-1017
Diermann N,Matousek J,Junge M,Riesner D,Steger G.2010.Characterization of plant miRNAs and small RNAs derived from Potato spindle tuber viroid(PSTVd)in infected tomato.Biological Chemistry,391(12):1379-1390
Ding SW.2010.RNA-based antiviral immunity.Nature Reviews Immunology,10(9):632-644
Du ZY,Chen AZ,Chen WH,Westwood JH,Baulcombe DC,Carr JP.2014.Using a viral vector to reveal the role of microRNA159 in disease symptom induction by a severe strain of Cucumber mosaic virus.Plant Physiology,164(3):1378-1388
Feng JL,Liu SS,Wang MN,Lang QL,Jin CZ.2014.Identification of microRNAs and their targets in tomato infected with Cucumber mosaic virus based on deep sequencing.Planta,240(6):1335-1352
Finnegan EF,Pasquinelli AE.2013.MicroRNA biogenesis:regulating the regulators.Critical Reviews in Biochemistry and Molecular Biology,48(1):51-68
Fire A,Xu S,Montgomery MK,Kostas SA,Driver SE,Mello CC.1998.Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans.Nature,391(6669):806-811
German MA,Pillay M,Jeong DH,Hetawal A,Luo S,Janardhanan P,Kannan V,Rymarquis LA,Nobuta K,German R,et al.2008.Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends.Nature Biotechnology,26(8):941-946
Guo YS,Jia MA,Yang YM,Zhan LL,Cheng XF,Cai JY,Zhang J,Yang J,Liu T,Fu Q,et al.2017.Integrated analysis of tobacco miRNA and m RNA expression profiles under PVY infection provids insight into tobacco-PVY interactions.Scientific Reports,7(1):4895
Hadidi A,Flores R,Candresse T,Barba M.2016.Next-generation sequencing and genome editing in plant virology.Frontiers in Microbiology,7:1325
Islam W,Islam SU,Qasim M,Wang LD.2017.Host-pathogen interactions modulated by small RNAs.RNA Biology,14(7):891-904
Jones JDG,Dangl JL.2006.The plant immune system.Nature,444(7117):323-329
Khraiwesh B,Zhu JK,Zhu J.2012.Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants.Biochimica et Biophysica Acta,1819(2):137-148
Kumar R.2014.Role of microRNAs in biotic and abiotic stress responses in crop plants.Applied Biochemistry and Biotechnology,174(1):93-115
Lakatos L,Csorba T,Pantaleo V,Chapman EJ,Carrington JC,Liu YP,Dolja VV,Calvino LF,Lopez-Moya JJ,Burgyán J.2006.Small RNA binding is a common strategy to suppress RNA silencing by several viral suppressors.The EMBO Journal,25(12):2768-2780
Lee R,Feinbaum R,Ambros V.1993.The C.elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14.Cell,75(5):843-854
Li F,Pignatta D,Bendix C,Brunkard JO,Cohn MM,Tung J,Sun H,Kumar P,Baker B.2012.MicroRNA regulation of plant innate immune receptors.Proceedings of the National Academy Sciences of the United States of America,109(5):1790-1795
Li Y,Zhang QQ,Zhang JG,Wu L,Qi YJ,Zhou JM.2010b.Identification of microRNAs involved in pathogen-associated molecular pattern-triggered plant innate immunity.Plant Physiology,152(4):2222-2231
Li YF,Zheng Y,Addo-Quaye C,Zhang L,Saini A,Jagadeeswaran G,Axtell MJ,Zhang W,Sunkar R.2010a.Transcriptome-wide identification of microRNA targets in rice.The Plant Journal,62(5):742-759
Li YQ,Deng CL,Shang QX,Zhao XL,Liu XL,Zhou Q.2016.Characterization of siRNAs derived from Cucumber green mottle mosaic virus in infected cucumber plants.Archives of Virology,161(2):455-458
Liu SR,Zhou JJ,Hu CG,Wei C,Zhang JZ.2017.MicroRNA-mediated gene silencing in plant defense and viral counter-defense.Frontiers in Microbiology,8:1801
Llave C,Xie Z,Kasschau KD,Carrington JC.2002.Cleavage of scarecrow-like mRNA targets directed by a class of Arabidopsis miR-NA.Science,297(5589):2053-2056
Mandadi KK,Scholthof K-BG.2013.Plant immune responses against viruses:how does a virus cause disease?Plant Cell,25(5):1489-1505
Ma XX,Tang ZH,Qin JP,Meng YJ.2015.The use of high-throughput sequencing methods for plant microRNA research.RNA Biology,12(7):709-719
Mao W,Li Z,Xia X,Li Y,Yu J.2012.A combined approach of highthroughput sequencing and degradome analysis reveals tissue specific expression of microRNAs and their targets in cucumber.PLoS ONE,7(3):e33040
Moon JY,Park JM.2016.Cross-talk in viral defense signaling in plants.Frontiers in Microbiology,7:2068
Muthamilarasan M,Prasad M.2013.Plant innate immunity:an updated insight into defense mechanism.Journal of Biosciences,38(2):433-449
Napoli C,Lemieux C,Jorgensen R.1990.Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans.The Plant Cell,2(4):279-289
Navarro B,Gisel A,Rodio ME,Delgado S,Flores R,di Serio F.2012.Small RNAs containing the pathogenic determinant of a chloroplast-replicating viroid guide the degradation of a host m RNA as predicted by RNA silencing.The Plant Journal,70(6):991-1003
Pallas V,Garcia JA.2011.How do plant viruses induce disease?Interactions and interference with host components.Journal of General Virology,92(P12):2691-2705
Park JH,Shin C.2015.The role of plant small RNAs in NB-LRR regulation.Briefings in Functional Genomics,14(4):268-274
Pumplin N,Voinnet O.2013.RNA silencing suppression by plant pathogens:defence,counter-defence and counter-counter-defence.Nature Reviews Microbiology,11(11):745-760
Qi X,Bao FS,Xie Z.2009.Small RNA deep sequencing reveals role for Arabidopsis thaliana RNA-dependent RNA polymerases in viral siRNA biogenesis.PLoS ONE,4(3):e4971
Qiu Y,Zhang Y,Hu F,Zhu S.2017.Characterization of siRNAs derived from Cucumber mosaic virus in infected tobacco plants.Archives of Virology,162(7):2077-2082
Ramirez-Prado JS,Abulfaraj AA,Rayapuram N,Benhamed M,Hirt H.2018.Plant immunity:from signaling to epigenetic control of defense.Trends in Plant Science,23(9):833-844
Reinhart B,Slack F,Basson M,Pasquinelli AE,Bettinger JC,Rougvie AE,Horvitz HR,Ruvkun G.2000.The 21-nucleotide let-7 RNAregulates developmental timing in Caenorhabditis elegans.Nature,403(6772):901-906
Rosa C,Kuo YW,Wuriyanghan H,Falk BW.2018.RNA interference mechanisms and applications in plant pathology.Annual Review of Phytopathology,56:581-610
Shi B,Lin L,Wang S,Guo Q,Zhou H,Rong L,Li J,Peng J,Lu Y,Zheng H,et al.2016.Identification and regulation of host genes related to Rice stripe virus symptom production.The New Phytologist,209(3):1106-1119
Shimura H,Pantaleo V,Ishihara T,Myojo N,Inaba J,Sueda K,Burgyan J,Masuta C.2011.A viral satellite RNA induces yellow symptoms on tobacco by targeting a gene involved in chlorophyll biosynthesis using the RNA silencing machinery.PLoSPathogens,7(5):e1002021
Silhavy D,Burgyan J.2004.Effects and side-effects of viral RNA silencing suppressors on short RNAs.Trends in Plant Science,9(2):76-83
Smith NA,Eamens AL,Wang MB.2011.Viral small interfering RNAs target host genes to mediate disease symptoms in plants.PLoSPathogens,7(5):e1002022
Sun YY,Niu XW,Fan M.2017.Genome-wide identification of Cucumber green mottle mosaic virus-responsive microRNAs in watermelon.Archives of Virology,162(9):2591-2602
Sun ZT,He YQ,Li JM,Wang X,Chen JP.2015.Genome-wide characterization of Rice black streaked dwarf virus-responsive microR-NAs in rice leaves and roots by small RNA and degradome sequencing.Plant and Cell Physiology,56(4):688-699
Tijsterman M,Ketting RF,Plasterk RHA.2002.The genetics of RNAsilencing.Annual Review of Genetics,36:489-519
Tong AZ,Yuan Q,Wang S,Peng JJ,Lu YW,Zheng HY,Lin L,Chen HR,Gong YF,Chen JP,et al.2017.Altered accumulation of osamiR171b contributes to Rice stripe virus infection by regulating disease symptoms.Journal of Experimental Botany,68(15):4357-4367
Wang JY,Tang YF,Yang YW,Ma N,Ling XT,Kan JL,He ZF,Zhang BL.2016.Cotton leaf curl multan virus-derived viral small RNAs can target cotton genes to promote viral infection.Frontiers in Plant Science,7:1162
Wang MB,Masuta C,Smith NA,Shimura H.2012.RNA silencing and plant viral diseases.Molecular Plant-Microbe Interactions,25(10):1275-1285
Xia ZH,Zhao ZX,Li MJ,Chen L,Jiao ZY,Wu YH,Zhou T,Yu WC,Fan ZF.2018.Identification of miRNAs and their targets in maize in response to Sugarcane mosaic virus infection.Plant Physiology and Biochemistry,125:143-152
Zhang XR,Yuan YR,Pei Y,Lin SS,Tuschl T,Patel DJ,Chua NH.2006.Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense.Genes&Development,20(23):3255-3268
Zhou Y,Xu ZN,Duan CX,Chen YP,Meng QC,Wu JR,Hao ZF,Wang ZH,Li MS,Yong HJ,et al.2016.Dual transcriptome analysis reveals insights into the response to Rice black-streaked dwarf virus in maize.Journal of Experimental Botany,67(15):4593-4609
Adkar-Purushothama CR,Iyer PS,Perreault JP.2017.Potato spindle tuber viroid infection triggers degradation of chloride channel protein CLC-b-like and ribosomal protein S3a-like mRNAs in tomato plants.Scientific Reports,7(1):8341
Babu M,Gagarinova AG,Brandle JE,Wang AM.2008.Association of the transcriptional response of soybean plants with Soybean mosaic virus systemic infection.Journal of General Virology,89(4):1069-1080
Baldrich P,San Segundo B.2016.MicroRNAs in rice innate immunity.Rice,9(1):6
Bazzini AA,Hopp HE,Beachy RN,Asurmendi S.2007.Infection and coaccumulation of Tobacco mosaic virus proteins alter microR-NA levels,correlating with symptom and plant development.Proceedings of the National Academy Sciences of the United States of America,104(29):12157-12162
Borges F,Martienssen RA.2015.The expanding world of small RNAs in plants.Nature Reviews Molecular Cell Biology,16(12):727-741
Caplan JL,Mamillapalli P,Burch-Smith TM,Czymmek K,Dinesh-Kumar SP.2008.Chloroplastic protein NRIP1 mediates innate immune receptor recognition of a viral effector.Cell,132(3):449-462
Chapman EJ,Prokhnevsky AI,Gopinath K,Dolja VV,Carrington JC.2004.Viral RNA silencing suppressors inhibit the microRNApathway at an intermediate step.Genes&Development,18(10):1179-1186
Chellappan P,Vanitharani R,Fauquet CM.2005.MicroRNA-binding viral protein interferes with Arabidopsis development.Proceedings of the National Academy of Sciences of the United States of America,102(29):10381-10386
Coll NS,Epple P,Dangl JL.2011.Programmed cell death in the plant immune system.Cell Death and Differentiation,18(8):1247-1256
Csorba T,Kontra L,Burgyan J.2015.Viral silencing suppressors:tools forged to fine-tune host-pathogen coexistence.Virology,479/480:85-103
Dardick C.2007.Comparative expression profiling of Nicotiana benthamiana leaves systemically infected with three fruit tree viruses.Molecular Plant-Microbe Interactions,20(8):1004-1017
Diermann N,Matousek J,Junge M,Riesner D,Steger G.2010.Characterization of plant miRNAs and small RNAs derived from Potato spindle tuber viroid(PSTVd)in infected tomato.Biological Chemistry,391(12):1379-1390
Ding SW.2010.RNA-based antiviral immunity.Nature Reviews Immunology,10(9):632-644
Du ZY,Chen AZ,Chen WH,Westwood JH,Baulcombe DC,Carr JP.2014.Using a viral vector to reveal the role of microRNA159 in disease symptom induction by a severe strain of Cucumber mosaic virus.Plant Physiology,164(3):1378-1388
Feng JL,Liu SS,Wang MN,Lang QL,Jin CZ.2014.Identification of microRNAs and their targets in tomato infected with Cucumber mosaic virus based on deep sequencing.Planta,240(6):1335-1352
Finnegan EF,Pasquinelli AE.2013.MicroRNA biogenesis:regulating the regulators.Critical Reviews in Biochemistry and Molecular Biology,48(1):51-68
Fire A,Xu S,Montgomery MK,Kostas SA,Driver SE,Mello CC.1998.Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans.Nature,391(6669):806-811
German MA,Pillay M,Jeong DH,Hetawal A,Luo S,Janardhanan P,Kannan V,Rymarquis LA,Nobuta K,German R,et al.2008.Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends.Nature Biotechnology,26(8):941-946
Guo YS,Jia MA,Yang YM,Zhan LL,Cheng XF,Cai JY,Zhang J,Yang J,Liu T,Fu Q,et al.2017.Integrated analysis of tobacco miRNA and m RNA expression profiles under PVY infection provids insight into tobacco-PVY interactions.Scientific Reports,7(1):4895
Hadidi A,Flores R,Candresse T,Barba M.2016.Next-generation sequencing and genome editing in plant virology.Frontiers in Microbiology,7:1325
Islam W,Islam SU,Qasim M,Wang LD.2017.Host-pathogen interactions modulated by small RNAs.RNA Biology,14(7):891-904
Jones JDG,Dangl JL.2006.The plant immune system.Nature,444(7117):323-329
Khraiwesh B,Zhu JK,Zhu J.2012.Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants.Biochimica et Biophysica Acta,1819(2):137-148
Kumar R.2014.Role of microRNAs in biotic and abiotic stress responses in crop plants.Applied Biochemistry and Biotechnology,174(1):93-115
Lakatos L,Csorba T,Pantaleo V,Chapman EJ,Carrington JC,Liu YP,Dolja VV,Calvino LF,Lopez-Moya JJ,Burgyán J.2006.Small RNA binding is a common strategy to suppress RNA silencing by several viral suppressors.The EMBO Journal,25(12):2768-2780
Lee R,Feinbaum R,Ambros V.1993.The C.elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14.Cell,75(5):843-854
Li F,Pignatta D,Bendix C,Brunkard JO,Cohn MM,Tung J,Sun H,Kumar P,Baker B.2012.MicroRNA regulation of plant innate immune receptors.Proceedings of the National Academy Sciences of the United States of America,109(5):1790-1795
Li Y,Zhang QQ,Zhang JG,Wu L,Qi YJ,Zhou JM.2010b.Identification of microRNAs involved in pathogen-associated molecular pattern-triggered plant innate immunity.Plant Physiology,152(4):2222-2231
Li YF,Zheng Y,Addo-Quaye C,Zhang L,Saini A,Jagadeeswaran G,Axtell MJ,Zhang W,Sunkar R.2010a.Transcriptome-wide identification of microRNA targets in rice.The Plant Journal,62(5):742-759
Li YQ,Deng CL,Shang QX,Zhao XL,Liu XL,Zhou Q.2016.Characterization of siRNAs derived from Cucumber green mottle mosaic virus in infected cucumber plants.Archives of Virology,161(2):455-458
Liu SR,Zhou JJ,Hu CG,Wei C,Zhang JZ.2017.MicroRNA-mediated gene silencing in plant defense and viral counter-defense.Frontiers in Microbiology,8:1801
Llave C,Xie Z,Kasschau KD,Carrington JC.2002.Cleavage of scarecrow-like mRNA targets directed by a class of Arabidopsis miR-NA.Science,297(5589):2053-2056
Mandadi KK,Scholthof K-BG.2013.Plant immune responses against viruses:how does a virus cause disease?Plant Cell,25(5):1489-1505
Ma XX,Tang ZH,Qin JP,Meng YJ.2015.The use of high-throughput sequencing methods for plant microRNA research.RNA Biology,12(7):709-719
Mao W,Li Z,Xia X,Li Y,Yu J.2012.A combined approach of highthroughput sequencing and degradome analysis reveals tissue specific expression of microRNAs and their targets in cucumber.PLoS ONE,7(3):e33040
Moon JY,Park JM.2016.Cross-talk in viral defense signaling in plants.Frontiers in Microbiology,7:2068
Muthamilarasan M,Prasad M.2013.Plant innate immunity:an updated insight into defense mechanism.Journal of Biosciences,38(2):433-449
Napoli C,Lemieux C,Jorgensen R.1990.Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans.The Plant Cell,2(4):279-289
Navarro B,Gisel A,Rodio ME,Delgado S,Flores R,di Serio F.2012.Small RNAs containing the pathogenic determinant of a chloroplast-replicating viroid guide the degradation of a host m RNA as predicted by RNA silencing.The Plant Journal,70(6):991-1003
Pallas V,Garcia JA.2011.How do plant viruses induce disease?Interactions and interference with host components.Journal of General Virology,92(P12):2691-2705
Park JH,Shin C.2015.The role of plant small RNAs in NB-LRR regulation.Briefings in Functional Genomics,14(4):268-274
Pumplin N,Voinnet O.2013.RNA silencing suppression by plant pathogens:defence,counter-defence and counter-counter-defence.Nature Reviews Microbiology,11(11):745-760
Qi X,Bao FS,Xie Z.2009.Small RNA deep sequencing reveals role for Arabidopsis thaliana RNA-dependent RNA polymerases in viral siRNA biogenesis.PLoS ONE,4(3):e4971
Qiu Y,Zhang Y,Hu F,Zhu S.2017.Characterization of siRNAs derived from Cucumber mosaic virus in infected tobacco plants.Archives of Virology,162(7):2077-2082
Ramirez-Prado JS,Abulfaraj AA,Rayapuram N,Benhamed M,Hirt H.2018.Plant immunity:from signaling to epigenetic control of defense.Trends in Plant Science,23(9):833-844
Reinhart B,Slack F,Basson M,Pasquinelli AE,Bettinger JC,Rougvie AE,Horvitz HR,Ruvkun G.2000.The 21-nucleotide let-7 RNAregulates developmental timing in Caenorhabditis elegans.Nature,403(6772):901-906
Rosa C,Kuo YW,Wuriyanghan H,Falk BW.2018.RNA interference mechanisms and applications in plant pathology.Annual Review of Phytopathology,56:581-610
Shi B,Lin L,Wang S,Guo Q,Zhou H,Rong L,Li J,Peng J,Lu Y,Zheng H,et al.2016.Identification and regulation of host genes related to Rice stripe virus symptom production.The New Phytologist,209(3):1106-1119
Shimura H,Pantaleo V,Ishihara T,Myojo N,Inaba J,Sueda K,Burgyan J,Masuta C.2011.A viral satellite RNA induces yellow symptoms on tobacco by targeting a gene involved in chlorophyll biosynthesis using the RNA silencing machinery.PLoSPathogens,7(5):e1002021
Silhavy D,Burgyan J.2004.Effects and side-effects of viral RNA silencing suppressors on short RNAs.Trends in Plant Science,9(2):76-83
Smith NA,Eamens AL,Wang MB.2011.Viral small interfering RNAs target host genes to mediate disease symptoms in plants.PLoSPathogens,7(5):e1002022
Sun YY,Niu XW,Fan M.2017.Genome-wide identification of Cucumber green mottle mosaic virus-responsive microRNAs in watermelon.Archives of Virology,162(9):2591-2602
Sun ZT,He YQ,Li JM,Wang X,Chen JP.2015.Genome-wide characterization of Rice black streaked dwarf virus-responsive microR-NAs in rice leaves and roots by small RNA and degradome sequencing.Plant and Cell Physiology,56(4):688-699
Tijsterman M,Ketting RF,Plasterk RHA.2002.The genetics of RNAsilencing.Annual Review of Genetics,36:489-519
Tong AZ,Yuan Q,Wang S,Peng JJ,Lu YW,Zheng HY,Lin L,Chen HR,Gong YF,Chen JP,et al.2017.Altered accumulation of osamiR171b contributes to Rice stripe virus infection by regulating disease symptoms.Journal of Experimental Botany,68(15):4357-4367
Wang JY,Tang YF,Yang YW,Ma N,Ling XT,Kan JL,He ZF,Zhang BL.2016.Cotton leaf curl multan virus-derived viral small RNAs can target cotton genes to promote viral infection.Frontiers in Plant Science,7:1162
Wang MB,Masuta C,Smith NA,Shimura H.2012.RNA silencing and plant viral diseases.Molecular Plant-Microbe Interactions,25(10):1275-1285
Xia ZH,Zhao ZX,Li MJ,Chen L,Jiao ZY,Wu YH,Zhou T,Yu WC,Fan ZF.2018.Identification of miRNAs and their targets in maize in response to Sugarcane mosaic virus infection.Plant Physiology and Biochemistry,125:143-152
Zhang XR,Yuan YR,Pei Y,Lin SS,Tuschl T,Patel DJ,Chua NH.2006.Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense.Genes&Development,20(23):3255-3268
Zhou Y,Xu ZN,Duan CX,Chen YP,Meng QC,Wu JR,Hao ZF,Wang ZH,Li MS,Yong HJ,et al.2016.Dual transcriptome analysis reveals insights into the response to Rice black-streaked dwarf virus in maize.Journal of Experimental Botany,67(15):4593-4609