Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

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.
ADVANCED SEARCH
Log in
Top
Virology Journal
Published in: Virology Journal 1/2018

Open Access 01-12-2018 | Research

De novo transcriptomic assembly and mRNA expression patterns of Botryosphaeria dothidea infection with mycoviruses chrysovirus 1 (BdCV1) and partitivirus 1 (BdPV1)

Authors: Lihua Wang, Hui Luo, Wangcheng Hu, Yuekun Yang, Ni Hong, Guoping Wang, Aiming Wang, Liping Wang

Published in: Virology Journal | Issue 1/2018

Login to get access

Abstract

Background

Pear ring rot, caused by Botryosphaeria species, is responsible for substantial economic losses by causing severe recession of pear tree growth in China. Mycovirus-mediated hypovirulence in plant pathogenic fungi is a crucial biological method to control fungal diseases.

Methods

We conducted a large-scale and comprehensive transcriptome analysis to identify mRNA in B. dothidea in response to mycovirus. De novo sequencing technology from four constructed libraries of LW-C (Botryosphaeria dothidea chrysovirus 1, BdCV1), LW-P (Botryosphaeria dothidea partitivirus 1, BdPV1), LW-CP (LW-1 strain infection with BdCV1 and BdPV1), and Mock (free virus) was used to investigate and compare gene expression changes in B.dothidea strains infected with mycovirus.

Results

In total, 30,058 Unigenes with an average length of 2128 bp were obtained from 4 libraries of B. dothidea strains. These were annotated to specify their classified function. We demonstrate that mRNAs of B. dothidea strains in response to mycovirus are differentially expressed. In total, 5598 genes were up-regulated and 3298 were down-regulated in the LW-CP group, 4468 were up-regulated and 4291 down-regulated in the LW-C group, and 2590 were up-regulated and 2325 down-regulated in the LW-P group. RT-qPCR was used to validate the expression of 9 selected genes. The B. dothidea transcriptome was more affected by BdCV1 infection than BdPV1. We conducted GO enrichment analysis to characterize gene functions regulated by B. dothidea with mycovirus infection. These involved metabolic process, cellular process, catalytic activity, transporter activity, signaling, and other biological pathways. KEGG function analysis demonstrated that the enriched differentially expressed genes are involved in metabolism, transcription, signal transduction, and ABC transport. mRNA is therefore involved in the interaction between fungi and mycovirus. In addition, changes in differential accumulation levels of cp and RdRp of BdCV1 and BdPV1 in B. dothidea strains were evaluated, revealing that the accumulation of BdCV1 and BdPV1 is related to the phenotype and virulence of B. dothidea strain LW-1.

Conclusions

The identification and analysis of mRNAs from B. dothidea was first reported at the transcriptome level. Our analysis provides further insight into the interaction of B. dothidea strains infection with chrysovirus 1 (BdCV1) and partitivirus 1 (BdPV1) at the transcriptome level.
Appendix
Available only for authorised users
Literature
1.
Al-Haq MI, Seo Y, Oshita S, Kawagoe Y. Disinfection effects of electrolyzed oxidizing water on suppressing fruit rot of pear caused by Botryosphaeria berengeriana. Food Res Int. 2002;35(7):657–64.CrossRef
2.
Zea-Bonilla T, González-Sánchez MA, Martín-Sánchez PM, Pérez-Jiménez RM. Avocado dieback caused by Neofusicoccum parvum in the Andalucia region. Spain Plant Dis. 2007;91(8):1052.CrossRefPubMed
3.
Guo LY, Li JY, Li BH, Zhang XZ, Zhou ZQ, Li GX, Wang YZ, Li XJ, Huang LL, Sun GY, Wen YD. Investigation on the occurrence and chemical control of Botryosphaeria canker of apple in China. Plant Prot. 2009;35:120–3.
4.
Zhai LF, Zhang MX, Lv G, Chen XR, Jia NN, Hong N, Wang GP. Biological and molecular characterization of four Botryosphaeria species isolated from pear plants showing stem wart and stem canker in China. Plant Dis. 2014;98(8):716–26.CrossRefPubMed
5.
Wang LH, Luo H, Wang GP, Wang LP. Effect of Botryosphaeria dothidea Chrysovirus 1 isolate belonging to the Chrysoviridae family on growth and pathogenity of the B. dothidea strain infection in pears. J Fruit Science. 2017;34(10):1330–9.
6.
Xie JT, Jiang DH. New insights into mycoviruses and exploration for the biological control of crop fungal diseases. Annu Rev Phytopathol. 2014;52(1):45–68.CrossRefPubMed
7.
Ghabrial SA, Suzuki N. Viruses of plant pathogenic fungi. Annu Rev Phytopathol. 2009;47(1):353–84.CrossRefPubMed
8.
Chiba S, Salaipeth L, Sasaki A, Kanemastu S, Suzuki N. A novel bipartite dsRNA mycovirus from the white root rot fungus Roselia necatrix: molecular and biological characterization, taxonomic consideration, and potential for biological control. J Virol. 2009;83(24):128801–12.CrossRef
9.
Yu X, Li B, Fu YP, Xie JT, Cheng JS, Ghabrial SA, Li GQ, Yi XH, Jiang DH. Extracellular transmission of a DNA mycovirus and its use as a natural fungicide. Proc Natl Acad Sci U S A. 2013;110(4):1452–7.CrossRefPubMedPubMedCentral
10.
11.
Nuss DL. Biological control of chestnut blight: an example of virus-mediated attenuation of fungal pathogenesis. Microbiol Rev. 1992;56(4):561–76.PubMedPubMedCentral
12.
Nuss DL. Hypovirulence: mycoviruses at the fungal-plant interface. Nat Rev Microbiol. 2005;3(8):632–42.CrossRefPubMed
13.
Pearson MN, Beever RE, Boine B, Arthur K. Mycoviruses of filamentous fungi and their relevance to plant pathology. Mol Plant Pathol. 2009;10(1):115–28.CrossRefPubMed
14.
Zhai LF, Hong N, Zhang MX, Wang GP. Complete dsRNA sequence of a novel victorivirus isolated from the pear stem wart fungus Botryosphaeria dothidea. Arch Virol. 2015;160(2):613–6.CrossRefPubMed
15.
Zhai LF, Xiang J, Zhang MX, Fu M, Yang ZK, Hong N, Wang GP. Characterization of a novel double-stranded RNA mycovirus conferring hypovirulence from the phytopathogenic fungus Botryosphaeria dothidea. Virology. 2016;493:75–85.CrossRefPubMed
16.
Wang LP, Jiang JJ, Wang YF, Hong N, Zhang F, Xu WX, Wang GP. Hypovirulence of the phytopathogenic fungus Botryosphaeria dothidea: association with a coinfecting chrysovirus and a partitivirus. J Virol. 2014;88(13):7517–27.CrossRefPubMedPubMedCentral
17.
Allen TD, Nuss DL. Specific and common alterations in host gene transcript accumulation following infection of the chestnut blight fungus by mild and severe hypoviruses. J Virol. 2004;78(8):4145–55.CrossRefPubMedPubMedCentral
18.
Lee KM, Cho WK, Yu J, Son M, Choi H, Min K, Lee YW, Kim KH. A comparison of transcriptional patterns and mycological phenotypes following infection of Fusarium graminearum by four mycoviruses. PLoS One. 2014;9(6):e100989.CrossRefPubMedPubMedCentral
19.
Allen TD, Dawe AL, Nuss DL. Use of cDNA microarrays to monitor transcriptional responses of the chestnut blight fungus Cryphonectria parasitica to infection by virulence-attenuating hypoviruses. Eukaryot Cell. 2003;2:1253–65.CrossRefPubMedPubMedCentral
20.
Li H, Fu YP, Jiang DH, Li GQ, Ghabrial SA, Yi XH. Down-regulation of Sclerotinia sclerotiorum gene expression in response to infection with Sclerotinia sclerotiorum debilitation-associated RNA virus. Virus Res. 2008;135(1):95–106.CrossRefPubMed
21.
Kwon SJ, Cho SY, Lee KM, Yu J, Son M, Kim H. Proteomic analysis of fungal host factors differentially expressed by Fusarium graminearum infected with fusarium graminearum virus-DK21. Virus Res. 2009;144(1–2):96–106.CrossRefPubMed
22.
Cho WK, Yu J, Lee KM, Son M, Min K, Lee YW, Kim KH. Genome-wide expression profiling shows transcriptional reprogramming in Fusarium graminearum by fusarium graminearum virus 1-DK21 infection. BMC Genomics. 2012;13(1):173.CrossRefPubMedPubMedCentral
23.
Zhu WJ, Wei W, Fu YP, Cheng JS, Xie JT, Li GQ, Yi XH, Kang ZS, Dickman MB, Jiang DH. A secretory protein of necrotrophic fungus Sclerotinia sclerotiorum that suppresses host resistance. PLoS One. 2013;8(1):e53901.CrossRefPubMedPubMedCentral
24.
özkan S, Mohorianu I, Xu P, Dalmay T, RHA C. Profiles and functional analysis of small RNAs derived from Aspergillus fumigatus infected with double-stranded RNA mycovirus. BMC Genomics. 2017;18(1):416.CrossRefPubMedPubMedCentral
25.
Parsley TB, Chen B, Geletka LM, Nuss DL. Differential modulation of cellular signaling pathways by mild and severe hypovirus strains. Eukaryot Cell. 2002;1(3):401–13.CrossRefPubMedPubMedCentral
26.
Liu Z, Lian S, Li B, Lu H, Dong X, Wang C. Draft genome sequence of Botryosphaeria dothidea, the pathogen of apple ring rot. Genome Announc. 2016;4(5):e01142–16.PubMedPubMedCentral
27.
Yan JY, Zhao WS, Chen Z, Xing QK, Zhang W, Chethana KWC, Xue MF, Ping J, Phillips AJL, Wang Y, et al. Comparative genome and transcriptome analyses reveal adaptations to opportunistic infection in woody plant degrading pathogens of Botryosphaeriaceae. DNA Res. 2018;25(1):87–102.CrossRefPubMed
28.
Stephen FA, Warren G, Webb M, Eugene WM, David JL. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–10.CrossRef
29.
Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005;21(18):3674–6.CrossRefPubMed
30.
Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, Lopez R. InterProScan: protein domains identifier. Nucleic Acids Res. 2005;33(Web Server issue):W116–20.CrossRefPubMedPubMedCentral
31.
Iseli C, Jongeneel CV, Bucher P. ESTScan: a program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. Proc Int Conf Intell Syst Mol Biol. 1999;99(2):138–48.
32.
33.
34.
Audic S, Claverie JM. The significance of digital gene expression profiles. Genome Res. 1997;7(10):986–95.CrossRefPubMed
35.
36.
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods. 2001;25(4):402–8.CrossRefPubMed
37.
Islam MS, Haque MS, Islam MM, Emdad EM, Halim A, Hossen QMM, Hossain MZ, Ahmed B, Rahim S, Rahman MS, et al. Tools to kill: genome of one of the most destructive plant pathogenic fungi Macrophomina phaseolina. BMC Genomics. 2012;13(1):493.CrossRefPubMedPubMedCentral
38.
Deng F, Allen TD, Hillman BI, Nuss DL. Comparative analysis of alterations in host phenotype and transcript accumulation following hypovirus and mycoreovirus infections of the chestnut blight fungus Cryphonectria parasitica. Eukaryot Cell. 2007;6(8):1286–98.CrossRefPubMedPubMedCentral
39.
Huang CJ, Cun YP, Yu HQ, Tong ZJ, Xiao BG, Song ZB, Wang BG, Li YP, Liu Y. Transcriptomic profile of tobacco in response to tomato zonate spot orthotospovirus infection. Virol J. 2017;14(1):153.CrossRefPubMedPubMedCentral
40.
Eusebio-Cope A, Sun LY, Tanaka T, Chiba S, Kasahara S, Suzuki N. The chestnut blight fungus for studies on virus/host and virus/virus interactions: from a natural to a model host. Virology. 2015;477:164–75.CrossRefPubMed
41.
Sun Q, Choi GH, Nuss DL. Hypovirus-responsive transcription factor gene pro1 of the chestnut blight fungus Cryphonectria parasitica is required for female fertility, asxual spore development, and stable maintenance of hypovirus infection. Eukaryot Cell. 2009;8(3):262–70.CrossRefPubMed
42.
Son H, Seo YS, Min K, Park AR, Lee J, Jin JM, Lin Y, Cao P, Hong SY, Kim EK, et al. A phenome-based functional analysis of transcription factors in the cereal head blight fungus fusarium graminearum. PLoS Pathog. 2011;7(10):e1002310.CrossRefPubMedPubMedCentral
43.
44.
Delmas S, Pullan ST, Gaddipati S, Kokolski M, Malla S, Blythe MJ, Ibbett R, Campbell M, Liddell S, Aboobaker A, et al. Uncovering the genome-wide transcriptional responses of the filamentous fungus aspergillus Niger to lignocellulose using RNA sequencing. PLoS Genet. 2012;8(8):e1002875.CrossRefPubMedPubMedCentral
45.
Soanes DM, Chakrabarti A, Paszkiewicz KH, Dawe AL, Talbot NJ. Genome-wide transcriptional profiling of appressorium development by the rice blast fungus Magnaporthe oryzae. PLoS Pathog. 2012;8(2):e1002514.CrossRefPubMedPubMedCentral
46.
Liu MM, Xing YM, Zhang DW, Guo SX. Transcriptome analysis of genes involved in defense response in Polyporus umbellatus with Armillaria mellea infection. Sci Rep. 2015;5(3):16075.CrossRefPubMedPubMedCentral
47.
Oghenekaro AO, Raffaello T, Kovalchuk A, Asiegbu FO. De novo transcriptomic assembly and profiling of Rigidoporus microporus during saprotrophic growth on rubber wood. BMC Genomics. 2016;17(1):234.CrossRefPubMedPubMedCentral
48.
Faruk MI, Eusebio-Cope A, Suzuki N. A host factor involved in hypovirus symptom expression in the chestnut blight fungus. J Virol. 2008;82(2):740–54.CrossRefPubMed
49.
50.
Campo S, Gillert KB, Carrington J. Small RNA-based antiviral defense in the phytopathogenic fungus Colletotrichum higginsianum. PLoS Pathog. 2016;12(6):e1005640.CrossRefPubMedPubMedCentral
51.
Chen Y, Gao QX, Huang MM, Liu Y, Liu ZY, Liu X, Ma ZH. Characterization of RNA silencing components in the plant pathogenic fungus Fusarium graminearum. Sci Rep. 2015;5:12500.CrossRefPubMedPubMedCentral
52.
Cogoni C, Macino G. Gene silencing in Neurospora crassa requires a protein homologous to RNA-dependent RNA polymerase. Nature. 1999;399(6732):166–9.CrossRefPubMed
53.
Zhang X, Segers GC, Sun Q, Deng F, Nuss DL. Characterization of hypovirus-derived small RNAs generated in the chestnut blight fungus by an inducible DCL-2-dependent pathway. J Virol. 2008;82(6):2613–9.CrossRefPubMedPubMedCentral
54.
Chiba S, Suzuki N. Highly activated RNA silencing via strong induction of dicer by one virus can interfere with the replication of an unrelated virus. Proc Natl Acad Sci U S A. 2015;112(35):4911–8.CrossRef
55.
Yaegashi H, Shimizu T, Ito T, Kanematsu S. Differential inductions of RNA silencing among encapsidated double-stranded RNA mycoviruses in the white root rot Fungs Rosellinia necatrix. J Virol. 2016;90(12):5677–92.CrossRefPubMedPubMedCentral
56.
Metadata
Title
De novo transcriptomic assembly and mRNA expression patterns of Botryosphaeria dothidea infection with mycoviruses chrysovirus 1 (BdCV1) and partitivirus 1 (BdPV1)
Authors
Lihua Wang
Hui Luo
Wangcheng Hu
Yuekun Yang
Ni Hong
Guoping Wang
Aiming Wang
Liping Wang
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2018
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-018-1033-4

Other articles of this Issue 1/2018

Virology Journal 1/2018 Go to the issue

Research

Comparison of enzyme-linked immunosorbent assay systems using rift valley fever virus nucleocapsid protein and inactivated virus as antigens

Review

The so far farthest reaches of the double jelly roll capsid protein fold

Research

Phylogenetic analysis of the wild-type strains of canine distemper virus circulating in the United States

Research

The detection of 3 ambiguous type 2 vaccine-derived polioviruses (VDPV2s) in Uganda

Research

High serum levels of pregenomic RNA reflect frequently failing reverse transcription in hepatitis B virus particles

Short Report

Reassessment of the capacity of the HIV-1 Env cytoplasmic domain to trigger NF-κB activation
Obesity Clinical Trial Summary

At a glance: The STEP trials

Read more

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

Pediatric Cardiology Video

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

Cardiopulmonary Comorbidity Video

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

Valvular Heart Disease Video

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

Heart Failure Video

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

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

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

Watch now

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits