Skip to main content

Advertisement

SpringerLink
Log in

Molecular Evolutionary History of Sugarcane yellow leaf virus Based on Sequence Analysis of RNA-Dependent RNA Polymerase and Putative Aphid Transmission Factor-Coding Genes

  • Original Article
  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

RNA-dependent RNA polymerase (RdRp) encoded by ORF2 and putative aphid transmission factor (PATF) encoded by ORF5 of Sugarcane yellow leaf virus (SCYLV) were detected in six sugarcane cultivars affected by yellow leaf using RT-PCR and real-time RT-PCR assays. Expression of both genes varied among infected plants, but overall expression of RdRp was higher than expression of PATF. Cultivar H87-4094 from Hawaii yielded the highest transcript levels of RdRp, whereas cultivar C1051-73 from Cuba exhibited the lowest levels. Sequence comparisons among 25 SCYLV isolates from various geographical locations revealed an amino acid similarity of 72.1–99.4 and 84.7–99.8 % for the RdRp and PATF genes, respectively. The 25 SCYLV isolates were separated into three (RdRp) and two (PATF) phylogenetic groups using the MEGA6 program that does not account for genetic recombination. However, the SCYLV genome contained potential recombination signals in the RdRp and PATF coding genes based on the GARD genetic algorithm. Use of this later program resulted in the reconstruction of phylogenies on the left as well as on the right sides of the putative recombination breaking points, and the 25 SCYLV isolates were distributed into three distinct phylogenetic groups based on either RdRp or PATF sequences. As a result, recombination reshuffled the affiliation of the accessions to the different clusters. Analysis of selection pressures exerted on RdRp and PATF encoded proteins revealed that ORF 2 and ORF 5 underwent predominantly purifying selection. However, a few sites were also under positive selection as assessed by various models such as FEL, IFEL, REL, FUBAR, MEME, GA-Branch, and PRIME.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Aaziz R, Tepfer M (1999) Recombination in RNA viruses and in virus-resistant transgenic plants. J Gen Virol 80:1339–1346

    Article  CAS  PubMed  Google Scholar 

  • Abu Ahmad Y, Royer M, Daugrois JH, Costet L, Lett JM, Victoria JI, Girard JC, Rott P (2006) Geographical distribution of four Sugarcane yellow leaf virus genotypes. Plant Dis 90:1156–1160

    Article  CAS  Google Scholar 

  • Abu Ahmad Y, Costet L, Daugrois J-H, Nibouche S, Letourmy P, Girard J-C, Rott P (2007) Variation in infection capacity and in virulence exists between genotypes of Sugarcane yellow leaf virus. Plant Dis 91:253–259

    Article  Google Scholar 

  • Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723

    Article  Google Scholar 

  • Aljanabi S, Parmessur Y, Moutia Y, Saumtally S, Dookun A (2001) Further evidence of the association of a phytoplasma and a virus with yellow leaf syndrome in sugarcane. Plant Path 50:628–636

    Article  Google Scholar 

  • Atchley WR, Zhao J, Fernandes AD, Druke T (2005) Solving the protein sequence metric problem. PNAS 102:6395–6400

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Boulila M (2011) Selective constraints, molecular recombination structure and phylogenetic reconstruction of isometric plant RNA viruses of the families Luteoviridae and Tymoviridae. Biochimie 93:242–253

    Article  CAS  PubMed  Google Scholar 

  • Chao L (1988) Evolution of sex in RNA viruses. J Theor Biol 133:99–112

    Article  CAS  PubMed  Google Scholar 

  • Chao L (1997) Evolution of sex and the molecular clock in RNA viruses. Gene 205:301–308

    Article  CAS  PubMed  Google Scholar 

  • Chare ER, Holmes EC (2006) A phylogenetic survey of recombination frequency in plant RNA viruses. Arch Virol 15:933–946

    Article  Google Scholar 

  • Chay C, Smith DM, Vaughan R, Gray SM (1996) Diversity among isolates within the PAV serotype of barley yellow dwarf virus. Phytopathology 86:370–377

    Article  CAS  Google Scholar 

  • Chinnaraja C, Viswanathan R, Karuppaiah R, Bagyalakshmi K, Malathi P, Parameswari B (2013) Complete genome characterization of Sugarcane yellow leaf virus from India: Evidence for RNA recombination. Eur J Plant Pathol 135:335–349

    Article  CAS  Google Scholar 

  • Conant GC, Wagner GP, Stadler PF (2007) Modeling amino acid substitution pattern in orthologous genes. Mol Phyl Evol 42:298–307

    Article  CAS  Google Scholar 

  • Corpet F (1988) Multiple sequence alignment with hierarchical clustering. Nucl Acids Res 16:10881–10890

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cronjǐe P, Tymon A, Jones P, Bailey R (1998) Association of a phytoplasma with a yellow leaf syndrome of sugarcane in Africa. Ann Appl Biol 133:177–186

    Article  Google Scholar 

  • Delport W, Poon AFY, Frost SDW, Kosakovsky Pond SL (2010) Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 29:2455–2457

    Article  Google Scholar 

  • Domingo E, Holland JJ (1997) RNA virus mutations and fitness for survival. Ann Rev Microb 51:151–178

    Article  CAS  PubMed  Google Scholar 

  • ElSayed AI (2013) Maize (Zea mays L.) constitutes a novel host to Sugarcane yellow leaf virus. Cana J Plant Pathol 35:68–74

    Article  CAS  Google Scholar 

  • ElSayed AI, Komor E (2012) Investigation of ORF0 as a sensitive alternative diagnostic segment to detect Sugarcane yellow leaf virus. J Gen Plant Path 78:207–216

    Article  Google Scholar 

  • ElSayed AI, Komor E (2013) Quantitative analysis of transcripts of the open reading frames of Sugarcane yellow leaf virus genome by one-multiplex RT-PCR: evidence for a high transcript level of suppressor gene in sink leaves. J Phytopathol 161:774–783

    Article  CAS  Google Scholar 

  • ElSayed AI, Weig A, Komor E (2011) Molecular characterization of Hawaiian Sugarcane yellow leaf virus genotypes and their phylogenetic relationship to strains from other sugarcane-growing countries. Eur J Plant Pathol 129:399–412

    Article  Google Scholar 

  • ElSayed AI, Boulila M, Komor E, Zhu YJ (2012) Putative recombination signature and significance of deletion/insertion events in RdRp coding region of Sugarcane yellow leaf virus. Biochimie 94:1764–1772

    Article  CAS  PubMed  Google Scholar 

  • Haenni A-L (2008) In: Roossinck MJ (ed) Virus evolution and taxonomy, plant virus evolution. Springer, Berlin, pp 205–217

    Chapter  Google Scholar 

  • Khishino H, Hasegawa M (1989) Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea. J Mol Evol 29:170–179

    Article  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Korber B (2000) HIV signatures and similarities. In: Rodrigo AG, Learn GH Jr (eds) Computational and evolutionary analysis of HIV molecular sequences. Kluwer Academic, Dordrecht, pp 55–72

    Google Scholar 

  • Kosakovsky Pond SL, Frost SDW (2005a) Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21:2531–2533

    Article  Google Scholar 

  • Kosakovsky Pond SL, Frost SDW (2005b) A genetic algorithm approach to detecting lineage-specific variation in selection pressure. Mol Biol Evol 22:478–485

    Article  Google Scholar 

  • Kosakovsky Pond SL, Frost SDW, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676–679

    Article  Google Scholar 

  • Kosakovsky Pond SL, Posada D, Gravenor MB, Woelk CH, Frost SDW (2006a) GARD: a genetic algorithm for recombination detection. Bioinformatics 22:3096–3098

    Article  PubMed  Google Scholar 

  • Kosakovsky Pond SL, Posada D, Gravenor MB, Woelk CH, Frost SDW (2006b) Automated phylogenetic detection of recombination using a genetic algorithm. Mol Biol Evol 23:1891–1901

    Article  PubMed  Google Scholar 

  • Kosakovsky Pond SL, Frost SD, Grossman Z, Gravenor MB, Richman DD, Brown AJ (2006c) Adaptation to different human populations by HIV-1 revealed by codon-based analyses. PLoS Comput Biol 2:530–538

    Article  Google Scholar 

  • Larkin MA, Blackshileds G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Lehrer AT, Komor E (2008) Symptom expression of yellow leaf disease in sugarcane cultivars with different degrees of infection by Sugarcane yellow leaf virus. Plant Pathol 57:178–189

    Google Scholar 

  • Lin YH, Gao SJ, Damaj MB, Fu HY, Chen RK, Mirkov TE (2014) Genome characterization of Sugarcane yellow leaf virus from China reveals a novel recombinant genotype. Arch Virol. doi:10.1007/s00705-013-1957-3

    PubMed Central  Google Scholar 

  • Lockhart BEL, Cronjǐe CPR (2000) Yellow leaf syndrome. In: Rott P, Bailey RA, Comstock JC, Croft BJ, Saumtally AS (eds) A guide to sugarcane diseases. CIRAD-ISSCT, Montpellier, France, pp 291–295

    Google Scholar 

  • Martin RR, Keese PK, Young JM, Waterhouse PM, Gerlach WL (1990) Evolution and molecular biology of luteoviruses. Ann Rev Phytopathol 28:341–363

    Article  CAS  Google Scholar 

  • Moonan F, Molina J, Mirkov TE (2000) Sugarcane yellow leaf virus: an emerging virus that has evolved by recombination between luteoviral and poleroviral ancestors. Virology 269:156–171

    Article  CAS  PubMed  Google Scholar 

  • Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Kosakovsky Pond SL (2012) Detecting individual sites subject to episodic diversifying selection. PLoS Genet 8:e1002764. doi:10.1371/journal.pgen.1002764

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Murrell B, Moola S, Mabona A, Weighill T, Sheward D, Kosakovsky Pond SL, Scheffler K (2013) FUBAR: A Fast, Unconstrained Bayesian AppRoximation for inferring selection. Mol Biol Evol 30:1196–1205

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nagai M, Sakoda Y, Mori M, Hayashi M, Kida H, Akashi H (2003) Insertion of a cellular sequence and RNA recombination in the structural protein coding region of cytopathogenic bovine viral diarrhea virus. J Gen Virol 84:447–452

    Article  CAS  PubMed  Google Scholar 

  • Ohta T (1973) Slightly deleterious mutant substitutions in evolution. Nature 246:96–98

    Article  CAS  PubMed  Google Scholar 

  • Ohta T (1974) Mutational pressure as the main cause of molecular evolution and polymorphism. Nature 252(29):351–354

    Article  CAS  Google Scholar 

  • Ohta T (1992) The nearly neutral theory of molecular evolution. Ann Rev Ecol Evol Syst 23:263–286

    Article  Google Scholar 

  • Pathak KB, Nagy PD (2009) Defective interfering RNAs: foes of viruses and friends of virologists. Viruses 1:895–919

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Power AG (2000) Insect transmission of plant viruses: a constraint on virus variability. Curr Opin Plant Biol 3:336–340

    Article  CAS  PubMed  Google Scholar 

  • Reanney DC (1982) The evolution of RNA viruses. Ann Rev Microb 13:47–73

    Article  Google Scholar 

  • Roossinck JM (1997) Mechanisms of plant virus evolution. Ann Rev Phytopathol 35:191–209

    Article  CAS  Google Scholar 

  • Rott P, Mirkov TE, Schenck S, Girard J-C (2007) Recent advances in research on Sugarcane yellow leaf virus, the causal agent of sugarcane yellow leaf. In: Proceedings international society of sugarcane technologists congress 26 (CD Rom).

  • Scheffler K, Martin DP, Seoighe C (2006) Robust inference of positive selection from recombining coding sequences. Bioinformatics 22:2493–2499

    Article  CAS  PubMed  Google Scholar 

  • Smith GR, Borg Z, Lockhart BEL, Braithwaite KS, Gibbs MJ (2000) Sugarcane yellow leaf virus: a novel member of the Luteoviridae that probably arose by inter-species recombination. J Gen Virol 81:1865–1869

    Article  CAS  PubMed  Google Scholar 

  • Tajima F (1989) Statistical-method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Viswanathan R (2004) Ratoon stunting disease infection favours severity of yellow leaf syndrome caused by Sugarcane yellow leaf virus in sugarcane. Sugarcane Inter 22:3–7

    Google Scholar 

  • Viswanathan R, Balamuralikrishnan M, Karuppaiah R (2008) Identification of three genotypes of Sugarcane yellow leaf virus causing yellow leaf disease from India and their molecular characterization. Virus Gen 37:368–379

    Article  CAS  Google Scholar 

  • Wang MQ, Zhou GH (2010) A near complete genome sequence of a distinct isolate of Sugarcane yellow leaf virus from China, representing a sixth new genotype. Virus Gen 41:268–272

    Article  CAS  Google Scholar 

  • Wang MQ, Xu DL, Li R, Zhou GH (2012) Genotype identification and genetic diversity of Sugarcane yellow leaf virus in China. Plant Pathol 61:986–993

    Article  Google Scholar 

  • Worobey M, Holmes EC (1999) Evolutionary aspects of recombination in RNA viruses. J Gen Virol 80:2535–2543

    Article  CAS  PubMed  Google Scholar 

  • Zaccomer B, Haenni AL, Macaya G (1995) The remarkable variety of plant RNA virus genomes. J Gen Virol 76:231–247

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Dr. Axel Lehrer (Hawaiian Agriculture Research Center, Aiea, USA) and to Dr. Isabel Medina Borges (Havana, Cuba) for the gift of sugarcane cultivars. This work was supported by the research fund from Zagazig University, Egypt.

Author information

Authors and Affiliations

  1. Biochemistry Department, Faculty of Agriculture, Zagazig University, Zagazig, 44519, Egypt

    Abdelaleim Ismail ElSayed

  2. Institut de l’Olivier, B.P. 14, 4061, Sousse Ibn-khaldoun, Tunisia

    Moncef Boulila

  3. Plant Pathology Department, Everglades Research & Education Center (EREC), Institute of Food and Agricultural Sciences, University of Florida, 3200 East Palm Beach Road, Belle Glade, FL, 33430-4702, USA

    Philippe Rott

Authors
  1. Abdelaleim Ismail ElSayed
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Moncef Boulila
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Philippe Rott
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Abdelaleim Ismail ElSayed.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

ElSayed, A.I., Boulila, M. & Rott, P. Molecular Evolutionary History of Sugarcane yellow leaf virus Based on Sequence Analysis of RNA-Dependent RNA Polymerase and Putative Aphid Transmission Factor-Coding Genes. J Mol Evol 78, 349–365 (2014). https://doi.org/10.1007/s00239-014-9630-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-014-9630-3

Keywords

Search

Navigation