Skip to main content
Top
Published in: Virology Journal 1/2019

Open Access 01-12-2019 | Research

Functional analysis of apple stem pitting virus coat protein variants

Authors: Xiaofang Ma, Ni Hong, Peter Moffett, Yijun Zhou, Guoping Wang

Published in: Virology Journal | Issue 1/2019

Login to get access

Abstract

Background

Although the canonical function of viral coat protein (CP) is to encapsidate the viral genome, they have come to be recognized as multifunctional proteins, involved in almost every stage of the viral infection cycle. However, CP functions of Apple stem pitting virus (ASPV) has not been comprehensively documented. This study aimed to characterize the functions of ASPV CP and any functional diversification caused by sequence diversity of six ASPV CP variants and studied their biological, serological, pathogenic and viral suppressor of RNA silencing (VSR) functions.

Methods

Six ASPV CP variants that have previously been shown to belong to different subgroups were selected here to study their diversity functions. Agrobacterium mediated infiltration (Agroinfiltration) was used to express YFP-ASPV-CPs in Nicotiana. benthamiana and infect Nicotiana. occidental with PVX-ASPV-CPs in. Confocal microscopy was used to detect YFP-ASPV-CPs florescence. CPs expressed in Escherichia coli BL21 (DE3) were induced by IPTG.

Results

In this study, we showed that recombinant CPs expressed in Escherichia coli BL21 (DE3) had different levels of serological reactivity to three anti-ASPV antibodies used to detect ASPV. Furthermore, fusion CPs with YFP (YFP-CPs) expressed in N. benthamiana cells differed in their ability to form aggregates. We also showed that ASPV isolates that harbour these CPs induced different biological symptoms on its herbaceous host N. occidentalis. At the same time, we found that all six CPs when expressed in PVX vector showed similar VSR activity and produced similar symptoms in N. occidentalis, despite their differences in amino acids.

Conclusions

Different ASPV isolates induced different symptoms in N. occidentalis, however, ASPV CP variants expressed in PVX vector showed the same symptoms in N. occidentalis plants. Also, we showed that ASPV CP variants has the same level of VSR activity, but they have different abilities to aggregate in N. benthamiana.
Appendix
Available only for authorised users
Literature
1.
go back to reference Carstens EB. Ratification vote on taxonomic proposals to the international committee on taxonomy of viruses (2009). Arch Virol. 2010;155:133–46.PubMedCrossRef Carstens EB. Ratification vote on taxonomic proposals to the international committee on taxonomy of viruses (2009). Arch Virol. 2010;155:133–46.PubMedCrossRef
2.
go back to reference Jelkmann W. Nucleotide sequences of apple stem pitting virus and of the coat protein gene of a similar virus from pear associated with vein yellows disease and their relationship with potex- and carlaviruses. J Gen Virol. 1994;75:1535–42.PubMedCrossRef Jelkmann W. Nucleotide sequences of apple stem pitting virus and of the coat protein gene of a similar virus from pear associated with vein yellows disease and their relationship with potex- and carlaviruses. J Gen Virol. 1994;75:1535–42.PubMedCrossRef
3.
go back to reference Mathioudakis MM, Maliogka VI, Dovas CI, Vasilakakis M, Katis NI. First record of the apple stem pitting virus (ASPV) in quince in Greece. J Plant Pathol. 2006;88:225. Mathioudakis MM, Maliogka VI, Dovas CI, Vasilakakis M, Katis NI. First record of the apple stem pitting virus (ASPV) in quince in Greece. J Plant Pathol. 2006;88:225.
4.
go back to reference Mathioudakis MM, Maliogka VI, Katsiani AT, Katis NI. Incidence and molecular variability of apple stem pitting and apple chlorotic leaf spot viruses in apple and pear orchards in Greece. J Plant Pathol. 2010;92:139–47. Mathioudakis MM, Maliogka VI, Katsiani AT, Katis NI. Incidence and molecular variability of apple stem pitting and apple chlorotic leaf spot viruses in apple and pear orchards in Greece. J Plant Pathol. 2010;92:139–47.
5.
go back to reference Wu Z, Ku H, Su C, Chen I, Jan F. Molecular and biological characterization of an isolate of apple stem pitting virus causing pear vein yellows disease in Taiwan. J Plant Pathol. 2010;92:721–8. Wu Z, Ku H, Su C, Chen I, Jan F. Molecular and biological characterization of an isolate of apple stem pitting virus causing pear vein yellows disease in Taiwan. J Plant Pathol. 2010;92:721–8.
6.
go back to reference Moya A, Holmes EC, González-Candelas F. The population genetics and evolutionary epidemiology of RNA viruses. Nat Rev Microbiol. 2004;2:279.PubMedCrossRef Moya A, Holmes EC, González-Candelas F. The population genetics and evolutionary epidemiology of RNA viruses. Nat Rev Microbiol. 2004;2:279.PubMedCrossRef
7.
go back to reference Boulila M. Putative recombination events and evolutionary history of five economically important viruses of fruit trees based on coat protein-encoding gene sequence analysis. Biochem Genet. 2010;48:357–75.PubMedCrossRef Boulila M. Putative recombination events and evolutionary history of five economically important viruses of fruit trees based on coat protein-encoding gene sequence analysis. Biochem Genet. 2010;48:357–75.PubMedCrossRef
8.
9.
go back to reference Zhang X, Sun R, Guo Q, Zhang S, Meulia T, Halfmann R, Li D, Qu F. A self-perpetuating repressive state of a viral replication protein blocks superinfection by the same virus. PLoS Pathog. 2017;13:e1006253.PubMedPubMedCentralCrossRef Zhang X, Sun R, Guo Q, Zhang S, Meulia T, Halfmann R, Li D, Qu F. A self-perpetuating repressive state of a viral replication protein blocks superinfection by the same virus. PLoS Pathog. 2017;13:e1006253.PubMedPubMedCentralCrossRef
10.
go back to reference Komorowska B, Siedlecki P, Kaczanowski S, Hasiów-Jaroszewska B, Malinowski T. Sequence diversity and potential recombination events in the coat protein gene of apple stem pitting virus. Virus Res. 2011;158:263–7.PubMedCrossRef Komorowska B, Siedlecki P, Kaczanowski S, Hasiów-Jaroszewska B, Malinowski T. Sequence diversity and potential recombination events in the coat protein gene of apple stem pitting virus. Virus Res. 2011;158:263–7.PubMedCrossRef
11.
go back to reference Liu N, Niu J, Zhao Y. Complete genomic sequence analyses of apple stem pitting virus isolates from China. Virus Genes. 2012;44:124–30.PubMedCrossRef Liu N, Niu J, Zhao Y. Complete genomic sequence analyses of apple stem pitting virus isolates from China. Virus Genes. 2012;44:124–30.PubMedCrossRef
12.
go back to reference Yoon JY, Joa JH, San Choi K, Do KS, Lim HC, Chung BN. Genetic diversity of a natural population of apple stem pitting virus isolated from apple in Korea. Plant Pathol J. 2014;30:195.PubMedPubMedCentralCrossRef Yoon JY, Joa JH, San Choi K, Do KS, Lim HC, Chung BN. Genetic diversity of a natural population of apple stem pitting virus isolated from apple in Korea. Plant Pathol J. 2014;30:195.PubMedPubMedCentralCrossRef
13.
go back to reference Ma X, Hong N, Moffett P, Wang G. Genetic diversity and evolution of apple stem pitting virus isolates from pear in China. Can J Plant Pathol. 2016;38:218–30.CrossRef Ma X, Hong N, Moffett P, Wang G. Genetic diversity and evolution of apple stem pitting virus isolates from pear in China. Can J Plant Pathol. 2016;38:218–30.CrossRef
14.
go back to reference Ivanov KI, Mäkinen K. Coat proteins, host factors and plant viral replication. Curr Opin Virol. 2012;2:712–8.PubMedCrossRef Ivanov KI, Mäkinen K. Coat proteins, host factors and plant viral replication. Curr Opin Virol. 2012;2:712–8.PubMedCrossRef
15.
go back to reference Voinnet O, Pinto YM, Baulcombe DC. Suppression of gene silencing: a general strategy used by diverse DNA and RNA viruses of plants. Proc Natl Acad Sci. 1999;96:14147–52.PubMedCrossRef Voinnet O, Pinto YM, Baulcombe DC. Suppression of gene silencing: a general strategy used by diverse DNA and RNA viruses of plants. Proc Natl Acad Sci. 1999;96:14147–52.PubMedCrossRef
16.
go back to reference Senshu H, Ozeki J, Komatsu K, Hashimoto M, Hatada K, Aoyama M, Kagiwada S, Yamaji Y, Namba S. Variability in the level of RNA silencing suppression caused by triple gene block protein 1 (TGBp1) from various potexviruses during infection. J Gen Virol. 2009;90:1014–24.PubMedCrossRef Senshu H, Ozeki J, Komatsu K, Hashimoto M, Hatada K, Aoyama M, Kagiwada S, Yamaji Y, Namba S. Variability in the level of RNA silencing suppression caused by triple gene block protein 1 (TGBp1) from various potexviruses during infection. J Gen Virol. 2009;90:1014–24.PubMedCrossRef
17.
go back to reference Morozov SY, Solovyev AG. Phylogenetic relationship of some “accessory” helicases of plant positive-stranded RNA viruses: toward understanding the evolution of triple gene block. Front Microbiol. 2015;6:508.PubMedPubMedCentralCrossRef Morozov SY, Solovyev AG. Phylogenetic relationship of some “accessory” helicases of plant positive-stranded RNA viruses: toward understanding the evolution of triple gene block. Front Microbiol. 2015;6:508.PubMedPubMedCentralCrossRef
18.
go back to reference Morozov SY, Solovyev AG. Triple gene block: modular design of a multifunctional machine for plant virus movement. J Gen Virol. 2003;84:1351–66.PubMedCrossRef Morozov SY, Solovyev AG. Triple gene block: modular design of a multifunctional machine for plant virus movement. J Gen Virol. 2003;84:1351–66.PubMedCrossRef
19.
go back to reference Song Y, Hong N, Wang L, Hu H, Tian R, Xu W, Ding F, Wang G. Molecular and serological diversity in apple chlorotic leaf spot virus from sand pear (Pyrus pyrifolia) in China. Eur J Plant Pathol. 2011;130:183–96.CrossRef Song Y, Hong N, Wang L, Hu H, Tian R, Xu W, Ding F, Wang G. Molecular and serological diversity in apple chlorotic leaf spot virus from sand pear (Pyrus pyrifolia) in China. Eur J Plant Pathol. 2011;130:183–96.CrossRef
20.
go back to reference Li R, Mock R, Huang Q, Abad J, Hartung J, Kinard G. A reliable and inexpensive method of nucleic acid extraction for the PCR-based detection of diverse plant pathogens. J Virol Methods. 2008;154:48–55.PubMedCrossRef Li R, Mock R, Huang Q, Abad J, Hartung J, Kinard G. A reliable and inexpensive method of nucleic acid extraction for the PCR-based detection of diverse plant pathogens. J Virol Methods. 2008;154:48–55.PubMedCrossRef
21.
go back to reference Ali S, Magne M, Chen S, Côté O, Stare BG, Obradovic N, Jamshaid L, Wang X, Bélair G, Moffett P. Analysis of putative apoplastic effectors from the nematode, Globodera rostochiensis, and identification of an expansin-like protein that can induce and suppress host defenses. PLoS One. 2015;10:e115042. Ali S, Magne M, Chen S, Côté O, Stare BG, Obradovic N, Jamshaid L, Wang X, Bélair G, Moffett P. Analysis of putative apoplastic effectors from the nematode, Globodera rostochiensis, and identification of an expansin-like protein that can induce and suppress host defenses. PLoS One. 2015;10:e115042.
22.
go back to reference Xu ZY, Hong N, Xing B, Wang GP. Partial molecular characterization of a Chinese isolate of grapevine leafroll-associated virus 2 and production of antisera to recombinant viral proteins. J Plant Pathol. 2006;88:89–94. Xu ZY, Hong N, Xing B, Wang GP. Partial molecular characterization of a Chinese isolate of grapevine leafroll-associated virus 2 and production of antisera to recombinant viral proteins. J Plant Pathol. 2006;88:89–94.
23.
go back to reference Moffett P. In plant immunity: fragment complementation and co-immunoprecipitation assays for understanding R protein structure and function. Cham: Springer; 2011. p. 9–20.CrossRef Moffett P. In plant immunity: fragment complementation and co-immunoprecipitation assays for understanding R protein structure and function. Cham: Springer; 2011. p. 9–20.CrossRef
24.
go back to reference Geourjon C, Deleage G. SOPMA: significant improvements in protein secondary structure prediction by consensus prediction from multiple alignments. Comput Appl Biosci. 1995;11:681–4.PubMed Geourjon C, Deleage G. SOPMA: significant improvements in protein secondary structure prediction by consensus prediction from multiple alignments. Comput Appl Biosci. 1995;11:681–4.PubMed
25.
go back to reference Sheludko YV, Sindarovska YR, Gerasymenko IM, Bannikova MA, Kuchuk NV. Comparison of several Nicotiana species as hosts for high-scale agrobacterium-mediated transient expression. Biotechnol Bioeng. 2007;96:608–14.PubMedCrossRef Sheludko YV, Sindarovska YR, Gerasymenko IM, Bannikova MA, Kuchuk NV. Comparison of several Nicotiana species as hosts for high-scale agrobacterium-mediated transient expression. Biotechnol Bioeng. 2007;96:608–14.PubMedCrossRef
26.
go back to reference Voinnet O, Lederer C, Baulcombe DC. A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana. Cell. 2000;103:157–67.PubMedCrossRef Voinnet O, Lederer C, Baulcombe DC. A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana. Cell. 2000;103:157–67.PubMedCrossRef
27.
go back to reference Voinnet O. Induction and suppression of RNA silencing: insights from viral infections. Nat Rev Genet. 2005;6:206.PubMedCrossRef Voinnet O. Induction and suppression of RNA silencing: insights from viral infections. Nat Rev Genet. 2005;6:206.PubMedCrossRef
28.
go back to reference Pallas V, García JA. How do plant viruses induce disease? Interactions and interference with host components. J Gen Virol. 2011;92:2691–705.PubMedCrossRef Pallas V, García JA. How do plant viruses induce disease? Interactions and interference with host components. J Gen Virol. 2011;92:2691–705.PubMedCrossRef
29.
go back to reference Weber PH, Bujarski JJ. Multiple functions of capsid proteins in (+) stranded RNA viruses during plant-virus interactions. Virus Res. 2015;196:140–9.PubMedCrossRef Weber PH, Bujarski JJ. Multiple functions of capsid proteins in (+) stranded RNA viruses during plant-virus interactions. Virus Res. 2015;196:140–9.PubMedCrossRef
30.
go back to reference Sonoda S, Koiwa H, Kanda K, Kato H, Shimono M, Nishiguchi M. The helper component-proteinase of sweet potato feathery mottle virus facilitates systemic spread of potato virus X in Ipomoea nil. Phytopathology. 2000;90:944–50.PubMedCrossRef Sonoda S, Koiwa H, Kanda K, Kato H, Shimono M, Nishiguchi M. The helper component-proteinase of sweet potato feathery mottle virus facilitates systemic spread of potato virus X in Ipomoea nil. Phytopathology. 2000;90:944–50.PubMedCrossRef
31.
go back to reference Te J, Melcher U, Howard A, Verchot-Lubicz J. Soilborne wheat mosaic virus (SBWMV) 19K protein belongs to a class of cysteine rich proteins that suppress RNA silencing. Virol J. 2005;2:18.PubMedPubMedCentralCrossRef Te J, Melcher U, Howard A, Verchot-Lubicz J. Soilborne wheat mosaic virus (SBWMV) 19K protein belongs to a class of cysteine rich proteins that suppress RNA silencing. Virol J. 2005;2:18.PubMedPubMedCentralCrossRef
32.
go back to reference Valli A, Dujovny G, García JA. Protease activity, self interaction, and small interfering RNA binding of the silencing suppressor P1b from cucumber vein yellowing ipomovirus. J Virol. 2008;82:974–86.PubMedCrossRef Valli A, Dujovny G, García JA. Protease activity, self interaction, and small interfering RNA binding of the silencing suppressor P1b from cucumber vein yellowing ipomovirus. J Virol. 2008;82:974–86.PubMedCrossRef
33.
go back to reference Martínez-Turiño S, Hernandez C. Inhibition of RNA silencing by the coat protein of Pelargonium flower break virus: distinctions from closely related suppressors. J Gen Virol. 2009;90:519–25.PubMedCrossRef Martínez-Turiño S, Hernandez C. Inhibition of RNA silencing by the coat protein of Pelargonium flower break virus: distinctions from closely related suppressors. J Gen Virol. 2009;90:519–25.PubMedCrossRef
34.
go back to reference Wang KD, Empleo R, Nguyen TTV, Moffett P, Sacco MA. Elicitation of hypersensitive responses in Nicotiana glutinosa by the suppressor of RNA silencing protein P0 from poleroviruses. Mol Plant Pathol. 2015;16:435–48.PubMedCrossRef Wang KD, Empleo R, Nguyen TTV, Moffett P, Sacco MA. Elicitation of hypersensitive responses in Nicotiana glutinosa by the suppressor of RNA silencing protein P0 from poleroviruses. Mol Plant Pathol. 2015;16:435–48.PubMedCrossRef
35.
go back to reference Hanssen IM, Thomma BP. Pepino mosaic virus: a successful pathogen that rapidly evolved from emerging to endemic in tomato crops. Mol Plant Pathol. 2010;11:179–89.PubMedCrossRef Hanssen IM, Thomma BP. Pepino mosaic virus: a successful pathogen that rapidly evolved from emerging to endemic in tomato crops. Mol Plant Pathol. 2010;11:179–89.PubMedCrossRef
36.
go back to reference Hu X, Nie X, He C, Xiong X. Differential pathogenicity of two different recombinant PVY NTN isolates in Physalis floridana is likely determined by the coat protein gene. Virol J. 2011;8:207.PubMedPubMedCentralCrossRef Hu X, Nie X, He C, Xiong X. Differential pathogenicity of two different recombinant PVY NTN isolates in Physalis floridana is likely determined by the coat protein gene. Virol J. 2011;8:207.PubMedPubMedCentralCrossRef
37.
go back to reference Mahajan SK, Chisholm ST, Whitham SA, Carrington JC. Identification and characterization of a locus (RTM1) that restricts long-distance movement of tobacco etch virus in Arabidopsis thaliana. Plant J. 1998;14:177–86.PubMedCrossRef Mahajan SK, Chisholm ST, Whitham SA, Carrington JC. Identification and characterization of a locus (RTM1) that restricts long-distance movement of tobacco etch virus in Arabidopsis thaliana. Plant J. 1998;14:177–86.PubMedCrossRef
38.
go back to reference Decroocq V, Salvador B, Sicard O, Glasa M, Cosson P, Svanella-Dumas L, Revers F, García JA, Candresse T. The determinant of potyvirus ability to overcome the RTM resistance of Arabidopsis thaliana maps to the N-terminal region of the coat protein. Mol Plant Microbe In. 2009;22:1302–11.CrossRef Decroocq V, Salvador B, Sicard O, Glasa M, Cosson P, Svanella-Dumas L, Revers F, García JA, Candresse T. The determinant of potyvirus ability to overcome the RTM resistance of Arabidopsis thaliana maps to the N-terminal region of the coat protein. Mol Plant Microbe In. 2009;22:1302–11.CrossRef
39.
go back to reference Carbonell A, Maliogka VI, Pérez JDJ, Salvador B, León DS, García JA, Simón-Mateo C. Diverse amino acid changes at specific positions in the N-terminal region of the coat protein allow plum pox virus to adapt to new hosts. Mol Plant Microbe In. 2013;26:1211–24.CrossRef Carbonell A, Maliogka VI, Pérez JDJ, Salvador B, León DS, García JA, Simón-Mateo C. Diverse amino acid changes at specific positions in the N-terminal region of the coat protein allow plum pox virus to adapt to new hosts. Mol Plant Microbe In. 2013;26:1211–24.CrossRef
40.
go back to reference Wileman T. Aggresomes and pericentriolar sites of virus assembly: cellular defense or viral design? Annu Rev Microbiol. 2007;61:149–67.PubMedCrossRef Wileman T. Aggresomes and pericentriolar sites of virus assembly: cellular defense or viral design? Annu Rev Microbiol. 2007;61:149–67.PubMedCrossRef
41.
go back to reference Gorovits R, Moshe A, Ghanim M, Czosnek H. Recruitment of the host plant heat shock protein 70 by tomato yellow leaf curl virus coat protein is required for virus infection. PLoS One. 2013;8:e70280.PubMedPubMedCentralCrossRef Gorovits R, Moshe A, Ghanim M, Czosnek H. Recruitment of the host plant heat shock protein 70 by tomato yellow leaf curl virus coat protein is required for virus infection. PLoS One. 2013;8:e70280.PubMedPubMedCentralCrossRef
42.
go back to reference Yelina NE, Savenkov EI, Solovyev AG, Morozov SY, Valkonen JP. Long-distance movement, virulence, and RNA silencing suppression controlled by a single protein in hordei-and potyviruses: complementary functions between virus families. J Virol. 2002;76:12981–91.PubMedPubMedCentralCrossRef Yelina NE, Savenkov EI, Solovyev AG, Morozov SY, Valkonen JP. Long-distance movement, virulence, and RNA silencing suppression controlled by a single protein in hordei-and potyviruses: complementary functions between virus families. J Virol. 2002;76:12981–91.PubMedPubMedCentralCrossRef
43.
go back to reference Dunoyer P, Pfeffer S, Fritsch C, Hemmer O, Voinnet O, Richards KE. Identification, subcellular localization and some properties of a cysteine-rich suppressor of gene silencing encoded by peanut clump virus. Plant J. 2002;29:555–67.PubMedCrossRef Dunoyer P, Pfeffer S, Fritsch C, Hemmer O, Voinnet O, Richards KE. Identification, subcellular localization and some properties of a cysteine-rich suppressor of gene silencing encoded by peanut clump virus. Plant J. 2002;29:555–67.PubMedCrossRef
44.
go back to reference Senshu H, Yamaji Y, Minato N, Shiraishi T, Maejima K, Hashimto M, Miura C, Neriya Y, Namba S. A dual strategy for the suppression of host antiviral silencing: two distinct suppressors for viral replication and viral movement encoded by potato virus M. J Virol. 2011;11:5211–73. Senshu H, Yamaji Y, Minato N, Shiraishi T, Maejima K, Hashimto M, Miura C, Neriya Y, Namba S. A dual strategy for the suppression of host antiviral silencing: two distinct suppressors for viral replication and viral movement encoded by potato virus M. J Virol. 2011;11:5211–73.
45.
go back to reference Canizares MC, Taylor KM, Lomonossoff GP. Surface-exposed C-terminal amino acids of the small coat protein of cowpea mosaic virus are required for suppression of silencing. J Gen Virol. 2004;85:3431–5.PubMedCrossRef Canizares MC, Taylor KM, Lomonossoff GP. Surface-exposed C-terminal amino acids of the small coat protein of cowpea mosaic virus are required for suppression of silencing. J Gen Virol. 2004;85:3431–5.PubMedCrossRef
46.
go back to reference Karran RA, Sanfaçon H. Tomato ringspot virus coat protein binds to ARGONAUTE 1 and suppresses the translation repression of a reporter gene. Mol Plant Microbe In. 2014;27:933–43.CrossRef Karran RA, Sanfaçon H. Tomato ringspot virus coat protein binds to ARGONAUTE 1 and suppresses the translation repression of a reporter gene. Mol Plant Microbe In. 2014;27:933–43.CrossRef
47.
go back to reference Olspert A, Kamsol K, Sarmiento C, Gerassimenko J, Truve E. Cocksfoot mottle virus coat protein is dispensable for the systemic infection. Virol J. 2014;11:19.PubMedPubMedCentralCrossRef Olspert A, Kamsol K, Sarmiento C, Gerassimenko J, Truve E. Cocksfoot mottle virus coat protein is dispensable for the systemic infection. Virol J. 2014;11:19.PubMedPubMedCentralCrossRef
48.
go back to reference Mathioudakis MM, Rodríguez-Moreno L, Sempere RN, Aranda MA, Livieratos I. Multifaceted capsid proteins: multiple interactions suggest multiple roles for Pepino mosaic virus capsid protein. Mol Plant Microbe In. 2014;27:1356–69.CrossRef Mathioudakis MM, Rodríguez-Moreno L, Sempere RN, Aranda MA, Livieratos I. Multifaceted capsid proteins: multiple interactions suggest multiple roles for Pepino mosaic virus capsid protein. Mol Plant Microbe In. 2014;27:1356–69.CrossRef
50.
51.
go back to reference Wu J, Wang Z, Shi Z, Zhang S, Ming R, Zhu S, Khan MA, Tao S, Korban SS, Wang H. The genome of pear (Pyrus bretschneideri Rehd.). Genome Res. 2012;12:144112–311. Wu J, Wang Z, Shi Z, Zhang S, Ming R, Zhu S, Khan MA, Tao S, Korban SS, Wang H. The genome of pear (Pyrus bretschneideri Rehd.). Genome Res. 2012;12:144112–311.
52.
go back to reference Liu J, Zhang X, Zhang F, Hong N, Wang G, Wang A, Wang L. Identification and characterization of microRNAs from in vitro-grown pear shoots infected with apple stem grooving virus in response to high temperature using small RNA sequencing. BMC Genomics. 2015;16:945.PubMedPubMedCentralCrossRef Liu J, Zhang X, Zhang F, Hong N, Wang G, Wang A, Wang L. Identification and characterization of microRNAs from in vitro-grown pear shoots infected with apple stem grooving virus in response to high temperature using small RNA sequencing. BMC Genomics. 2015;16:945.PubMedPubMedCentralCrossRef
Metadata
Title
Functional analysis of apple stem pitting virus coat protein variants
Authors
Xiaofang Ma
Ni Hong
Peter Moffett
Yijun Zhou
Guoping Wang
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2019
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-019-1126-8

Other articles of this Issue 1/2019

Virology Journal 1/2019 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.