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Deep sequencing analysis of a strain of pecan mosaic-associated virus infecting Atractylodes macrocephala Koidz

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Abstract

Leaves of Atractylodes macrocephala Koidz with virus-like symptoms were collected in Shanxi Province, China. The strain Am of the Potyvirus species, pecan mosaic-associated virus (PMaV-Am), was discovered through the assembly of virus derived small interfering RNAs (vsiRNAs) that were isolated from symptomatic samples. The complete genome of PMaV-Am was determined to be 9310 nucleotides (nt) in length, including a large open reading frame encoding a polyprotein. Phylogenetic analysis showed that PMaV-Am is clustered together and most closely related to strain PMaV-LA from pecan. Sequence alignments of PMaV-Am complete genomic RNAs with PMaV-LA showed 98.78% nucleotide sequence homology and 96.53% amino acid identity, respectively. Further analyses of the vsiRNA profile showed that the most abundant PMaV from A. macrocephala (PMaV-Am) vsiRNAs were 21 nt long and biased for A at their 5′ terminal residue. Polarity distribution revealed that vsiRNAs were nearly equal amount of sense and antisense strands and hotspot was distributed in the HC-Pro coding region of the PMaV-Am genome. These results might provide an insight into the host RNA silencing defense induced by PMaV-Am, and provide guidelines on designing antiviral strategies using RNAi against PMaV-Am.

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References

  • Adams MJ, Antoniw JF, Beaudoin F (2005) Overview and analysis of the polyprotein cleavage sites in the family Potyviridae. Mol Plant Pathol 6:471–487

    Article  PubMed  CAS  Google Scholar 

  • Bologna NG, Voinnet O (2014) The diversity, biogenesis, and activities of endogenous silencing small RNAs in Arabidopsis. Annu Rev Plant Biol 65:473–503

    Article  PubMed  CAS  Google Scholar 

  • Bouché N, Lauressergues D, Gasciolli V, Vaucheret H (2006) An antagonistic function for Arabidopsis DCL2 in development and a new function for DCL4 in generating viral siRNAs. EMBO J 25:3347–3356

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Deleris A, Gallego-Bartolome J, Bao J, Kasschau KD, Carrington JC, Voinnet O (2006) Hierarchical action and inhibition of plant dicer-like proteins in antiviral defense. Science 313:68–71

    Article  PubMed  CAS  Google Scholar 

  • Fernández A, Guo HS, Sáenz P, Simón-Buela L, Gómez de Cedrón M, García JA (1997) The motif V of plum pox potyvirus CI RNA helicase is involved in NTP hydrolysis and is essential for virus RNA replication. Nucleic Acids Res 25:4474–4480

    Article  PubMed  PubMed Central  Google Scholar 

  • Garcia-Ruiz H, Takeda A, Chapman EJ, Sullivan CM, Fahlgren N, Brempelis KJ, Carrington JC (2010) Arabidopsis RNA-dependent RNA polymerases and dicer-like proteins in antiviral defense and small interfering RNA biogenesis during turnip mosaic virus infection. Plant Cell 22:481–496

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hagen C, Frizzi A, Kao J, Jia L, Huang M, Zhang Y, Huang S (2011) Using small RNA sequences to diagnose, sequence, and investigate the infectivity characteristics of vegetable-infecting viruses. Arch Virol 156:1209–1216

    Article  PubMed  CAS  Google Scholar 

  • Kiso Y, Tohkin M, Hikino H (1985) Mechanism of antihepatotoxic activity of atractylenolide I: effect on free radical generation and lipid peroxidation. Planta Med 2:97–100

    Article  Google Scholar 

  • Kreuze JF, Perez A, Untiveros M, Quispe D, Fuentes S, Barker I, Simon R (2009) Complete viral genome sequence and discovery of novel viruses by deep sequencing of small RNAs: a generic method for diagnosis, discovery and sequencing of viruses. Virology 388:1–7

    Article  PubMed  CAS  Google Scholar 

  • Langmead RBB, Trapnell C, Pop M, Salzberg LS (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li CQ, He LC, Dong HY, Jin JQ (2007) Screening for the anti-inflammatory activity of fractions and compounds from Atractylodes macrocephala Koidz. J Ethnopharmacol 114:212–217

    Article  PubMed  CAS  Google Scholar 

  • Lim S, Igori D, Zhao F, Ran HY, An TJ, Lim HS, Lee SH, Moon JS (2015) Complete genome sequence of a tentative new caulimovirus from the medicinal plant Atractylodes macrocephala. Arch Virol 160:3127–3131

    Article  PubMed  CAS  Google Scholar 

  • Llave C (2010) Virus-derived small interfering RNAs at the core of plant-virus interactions. Trends Plant Sci 15:701–707

    Article  PubMed  CAS  Google Scholar 

  • Lópezmoya JJ, Wang RY, Pirone TP (1999) Context of the coat protein DAG motif affects potyvirus transmissibility by aphids. J Gen Virol 80:3281

    Article  Google Scholar 

  • Mi S, Cai T, Hu Y, Chen Y, Hodges E, Ni F, Wu L, Li S, Zhou H, Long C (2008) Sorting of small RNAs into Arabidopsis Argonaute complexes is directed by the 5′ terminal nucleotide. Cell 133:116–127

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Moissiard G, Voinnet O (2006) RNA silencing of host transcripts by cauliflower mosaic virus requires coordinated action of the four Arabidopsis dicer-like proteins. Proc Natl Acad Sci U S A 103:19593–19598

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Molnár A, Csorba T, Lakatos L, Várallyay E, Lacomme C, Burgyán J (2005) Plant virus-derived small interfering RNAs originate predominantly from highly structured single-stranded viral RNAs. J Virol 79:7812–7818

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Niu Y, Shi X, Zhao H, Zhang X, Zhao B (2014) Molecular identification and partial sequence analysis of cucumber mosaic virus isolate from Atractylodes macrocephala Koidz. Acta Phytopathol Sin 44:357–362

    Google Scholar 

  • Niu Y, Shi X, Zhang X, Zhao H, Zhao B (2015) Molecular identification and sequence analysis of broad bean wilt virus 2 isolates from Atractylodes macrocephala Koidz. Chin J Virol 31:58–64

    CAS  Google Scholar 

  • Peng Y, Kadoury D, Gal-On A, Huet H, Wang Y, Raccah B (1998) Mutations in the HC-Pro gene of zucchini yellow mosaic potyvirus: effects on aphid transmission and binding to purified virions. J Gen Virol 79:897

    Article  PubMed  CAS  Google Scholar 

  • Qi XP, Bao FS, Xie ZX (2009) Small RNA deep sequencing reveals role for Arabidopsis thaliana RNA-dependent RNA polymerases in viral siRNA biogenesis. PLoS One 4:e4971

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Qu F, Ye X, Morris TJ (2008) Arabidopsis DRB4, AGO1, AGO7, and RDR6 participate in a DCL4-initiated antiviral RNA silencing pathway negatively regulated by DCL1. Proc Natl Acad Sci U S A 105:14732–14737

    Article  PubMed  PubMed Central  Google Scholar 

  • Rajamäki ML, Streng J, Valkonen JP (2014) Silencing suppressor protein VPg of a Potyvirus interacts with the plant silencing-related protein SGS3. Mol Plant-Microbe Interact 27:1199–1210

    Article  PubMed  CAS  Google Scholar 

  • Rohožková J, Navrátil M (2011) P1 peptidase – a mysterious protein of family Potyviridae. J Biosci 36:189–200

    Article  PubMed  CAS  Google Scholar 

  • Shiboleth YM, Haronsky E, Leibman D, Arazi T, Wassenegger M, Whitham SA, Gaba V, Gal-On A (2007) The conserved FRNK box in HC-Pro, a plant viral suppressor of gene silencing, is required for small RNA binding and mediates symptom development. J Virol 81:13135–13148

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Su X, Fu S, Qian Y, Xu Y, Zhou X (2015) Identification of Hop stunt viroid infecting Citrus limon in China using small RNAs deep sequencing approach. Virol J 12:103

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Su X, Fu S, Qian Y, Zhang L, Xu Y, Zhou X (2016) Discovery and small RNA profile of Pecan mosaic-associated virus, a novel potyvirus of pecan trees. Sci Rep 6:26741

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Takeda A, Iwasaki S, Watanabe T, Utsumi M, Watanabe Y (2008) The mechanism selecting the guide strand from small RNA duplexes is different among argonaute proteins. Plant Cell Physiol 49:493–500

    Article  PubMed  CAS  Google Scholar 

  • Wang XB, Wu QF, Ito T, Cillo F, Li WX, Chen XM, Yu JL, Ding SW (2010) RNAi-mediated viral immunity requires amplification of virus-derived siRNAs in Arabidopsis thaliana. Proc Natl Acad Sci U S A 107:484–489

    Article  PubMed  Google Scholar 

  • Wu Q, Luo Y, Lu R, Lau N, Lai EC, Li WX, Ding SW (2010) Virus discovery by deep sequencing and assembly of virus-derived small silencing RNAs. Proc Natl Acad Sci U S A 107:1606–1611

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu Y, Huang L, Wang Z, Fu S, Che J, Qian Y, Zhou X (2014) Identification of Himetobi P virus in the small brown planthopper by deep sequencing and assembly of virus-derived small interfering RNAs. Virus Res 179:235–240

    Article  PubMed  CAS  Google Scholar 

  • Ye Y, Chao XJ, Wu JF, Cheng BC, Su T, Fu XQ, Li T, Guo H, Tse AK, Kwan HY (2015) ERK/GSK3β signaling is involved in atractylenolide I-induced apoptosis and cell cycle arrest in melanoma cells. Oncol Rep 34:1543–1548

    Article  PubMed  CAS  Google Scholar 

  • Yu R, Yu BX, Chen JF, Lv XY, Yan ZJ, Cheng Y, Ma Q (2016) Anti-tumor effects of Atractylenolide I on bladder cancer cells. J Exp Clin Cancer Res 35:40

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zerbino DR, Birney E (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821–829

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang X, Zhang X, Singh J, Li D, Qu F (2012) Temperature-dependent survival of turnip crinkle virus-infected Arabidopsis plants relies on an RNA silencing-based defense that requires DCL2, AGO2, and HEN1. J Virol 86:6847–6854

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang X, Shu M, Wang Y, Fu L, Li W, Deng B, Liang Q, Shen W (2014) Characterization of small interfering RNAs derived from sugarcane mosaic virus in infected maize plants by deep sequencing. PLoS One 9:e97013

    Article  CAS  Google Scholar 

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Acknowledgements

This study was supported by the National Natural Science Foundation of China (Grant No. 31540050 and Grant No. 31772130).

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Author notes

  1. Yanbing Niu and Xiaojing Pang contributed equally to this work and should be considered co-first authors

Authors and Affiliations

  1. College of Life Sciences, Shanxi Agricultural University, No.01. Mingxian Road, Taigu, 030801, China

    Yanbing Niu, Xiaojing Pang & Defu Wang

  2. Institute of Edible-Fungi, Shanxi Academy of Agricultural Sciences, Taiyuan, 030006, China

    Shang Guo

  3. Key Laboratory of Pest Management of Horticultural Crop of Hunan Province, Hunan Plant Protection Institute, Hunan Academy of Agricultural Science, Changsha, 410125, China

    Yong Liu

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  1. Yanbing Niu
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  2. Xiaojing Pang
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  3. Defu Wang
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  4. Shang Guo
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  5. Yong Liu
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Correspondence to Yanbing Niu.

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Niu, Y., Pang, X., Wang, D. et al. Deep sequencing analysis of a strain of pecan mosaic-associated virus infecting Atractylodes macrocephala Koidz. J Plant Pathol 100, 249–255 (2018). https://doi.org/10.1007/s42161-018-0072-4

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  • DOI: https://doi.org/10.1007/s42161-018-0072-4

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