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High molecular diversity and divergent subpopulations of the begomovirus cnidoscolus mosaic leaf deformation virus associated with Cnidoscolus urens

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Abstract

Begomoviruses have circular, single-stranded DNA genomes encapsidated into twinned quasi-icosahedral particles and are transmitted by whiteflies of the Bemisia tabaci sibling group. Begomoviruses infect cultivated and non-cultivated plants, causing great losses in economically important crops worldwide. To better understand the genetic diversity of begomoviruses infecting the non-cultivated host Cnidoscolus urens, leaf samples exhibiting virus-like symptoms were collected in different localities in the state of Alagoas, Brazil, during 2015 and 2016. Forty-two complete DNA-A sequences were cloned and sequenced by the Sanger method. Based on nucleotide sequence comparisons, the 42 new isolates were identified as the bipartite begomovirus cnidoscolus mosaic leaf deformation virus (CnMLDV). The CnMLDV isolates were clustered in two phylogenetic groups (clusters I and II) corresponding to their sampling areas, and the high value of Wright’s F fixation index observed for the DNA-A sequences suggests population structuring. At least seven independent intraspecies recombination events were predicted among CnMLDV isolates, with recombination breakpoints located in the common region (CR) and in the CP and Rep genes. Also, a high per site nucleotide diversity (π) was observed for CnMLDV isolates, with CP being significantly more variable than Rep. Despite the high genetic variability, strong negative or purifying selection was identified as the main selective force acting upon CP and Rep.

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Data availability

The sequences described in this study were deposited in the GenBank database under accession numbers MW600734-MW600775.

References

  1. Brown JK, Zerbini FM, Navas-Castillo J, Moriones E, Ramos-Sobrinho R, Silva JCF, Fiallo-Olive E, Briddon RW, Hernandez-Zepeda C, Idris A, Malathi VG, Martin DP, Rivera-Bustamante R, Ueda S, Varsani A (2015) Revision of Begomovirus taxonomy based on pairwise sequence comparisons. Arch Virol 160:1593–1619. https://doi.org/10.1007/s00705-015-2398-y

    Article  CAS  PubMed  Google Scholar 

  2. Gilbertson RL, Batuman O, Webster CG, Adkins S (2015) Role of the insect supervectors Bemisia tabaci and Frankliniella occidentalis in the emergence and global spread of plant viruses. Annu Rev Virol 2:67–93. https://doi.org/10.1146/annurev-virology-031413-085410

    Article  CAS  PubMed  Google Scholar 

  3. Varsani A, Roumagnac P, Fuchs M, Navas-Castillo J, Moriones E, Idris A, Briddon RW, Rivera-Bustamante R, Zerbini FM, Martin DP (2017) Capulavirus and Grablovirus: two new genera in the family Geminiviridae. Arch Virol 162:1819–1831. https://doi.org/10.1007/s00705-017-3268-6

    Article  CAS  PubMed  Google Scholar 

  4. Zerbini FM, Briddon RW, Idris A, Martin DP, Moriones E, Navas-Castillo J, Rivera-Bustamante R, Roumagnac P, Varsani A, ICTV Report C (2017) ICTV virus taxonomy profile: Geminiviridae. J Gen Virol 98:131–133. https://doi.org/10.1099/jgv.0.000738

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Inoue-Nagata AK, Lima MF, Gilbertson RL (2016) A review of geminivirus diseases in vegetables and other crops in Brazil: current status and approaches for management. Hortic Bras 34:8–18. https://doi.org/10.1590/S0102-053620160000100002

    Article  CAS  Google Scholar 

  6. Morales FJ, Anderson PK (2001) The emergence and dissemination of whitefly-transmitted geminiviruses in Latin America. Arch Virol 146:415–441. https://doi.org/10.1007/s007050170153

    Article  CAS  PubMed  Google Scholar 

  7. Navas-Castillo J, Fiallo-Olive E, Sanchez-Campos S, VanAlfen NK, Bruening G, Leach JE (2011) Emerging virus diseases transmitted by whiteflies. Annu Rev Phytopathol 49:219–248. https://doi.org/10.1146/annurev-phyto-072910-095235

    Article  CAS  PubMed  Google Scholar 

  8. Rocha CS, Castillo-Urquiza GP, Lima ATM, Silva FN, Xavier CAD, Hora-Júnior BT, Beserra EA, Malta AWO, Martin DP, Varsani A, Alfenas-Zerbini P, Mizubuti ESG, Zerbini FM (2013) Brazilian begomovirus populations are highly recombinant, rapidly evolving, and segregated based on geographical location. J Virol 87:5784–5799. https://doi.org/10.1128/JVI.00155-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Lima ATM, Ramos-Sobrinho R, Gonzalez-Aguilera J, Rocha CS, Silva SJC, Xavier CAD, Silva FN, Duffy S, Zerbini FM (2013) Synonymous site variation due to recombination explains higher genetic variability in begomovirus populations infecting non-cultivated hosts. J Gen Virol 94:418–431. https://doi.org/10.1099/vir.0.047241-0

    Article  CAS  PubMed  Google Scholar 

  10. Ramos-Sobrinho R, Xavier CAD, Pereira HMB, Lima GSA, Assunção IP, Mizubuti ESG, Duffy S, Zerbini FM (2014) Contrasting genetic structure between two begomoviruses infecting the same leguminous hosts. J Gen Virol 95:2540–2552. https://doi.org/10.1099/vir.0.067009-0

    Article  CAS  Google Scholar 

  11. Ferro CG, Silva JP, Xavier CAD, Godinho MT, Lima ATM, Mar TB, Lau D, Zerbini FM (2017) The ever increasing diversity of begomoviruses infecting non-cultivated hosts: new species from Sida spp. and Leonurus sibiricus, plus two New World alphasatellites. Ann Appl Biol 170:204–218. https://doi.org/10.1111/aab.12329

    Article  CAS  Google Scholar 

  12. Brown JK, Fauquet CM, Briddon RW, Zerbini FM, Moriones E, Navas-Castillo J (2012) Family Geminiviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy. Ninth Report of the International Committee on Taxonomy of Viruses. Elsevier/Academic Press, London, pp 351-373

  13. Seal S, VandenBosch F, Jeger M (2006) Factors influencing begomovirus evolution and their increasing global significance: implications for sustainable control. Crit Rev Plant Sci 25:23–46. https://doi.org/10.1080/07352680500365257

    Article  Google Scholar 

  14. Alabi OJ, Ogbe FO, Bandyopadhyay R, Lava Kumar P, Dixon AG, Hughes J, Naidu RA (2008) Alternate hosts of African cassava mosaic virus and East African cassava mosaic Cameroon virus in Nigeria. Arch Virol 153:1743–1747. https://doi.org/10.1007/s00705-008-0169-8

    Article  CAS  PubMed  Google Scholar 

  15. García-Andrés S, Monci F, Navas-Castillo J, Moriones E (2006) Begomovirus genetic diversity in the native plant reservoir Solanum nigrum: Evidence for the presence of a new virus species of recombinant nature. Virology 350:433–442. https://doi.org/10.1016/j.virol.2006.02.028

    Article  CAS  PubMed  Google Scholar 

  16. Monde G, Walangululu J, Winter S, Bragard C (2010) Dual infection by cassava begomoviruses in two leguminous species (Fabaceae) in Yangambi, Northeastern Democratic Republic of Congo. Arch Virol 155:1865–1869. https://doi.org/10.1007/s00705-010-0772-3

    Article  CAS  PubMed  Google Scholar 

  17. Stewart C, Kon T, Rojas M, Graham A, Martin D, Gilbertson R, Roye M (2014) Mixed infection of Sida jamaicensis in Jamaica reveals the presence of three recombinant begomovirus DNA A components. Arch Virol 159:2509–2512. https://doi.org/10.1007/s00705-014-2063-x

    Article  CAS  PubMed  Google Scholar 

  18. Vaghi-Medina CG, Martin DP, López Lambertini PM (2015) Tomato mottle wrinkle virus, a recombinant begomovirus infecting tomato in Argentina. Arch Virol 160:581–585. https://doi.org/10.1007/s00705-014-2216-y

    Article  CAS  PubMed  Google Scholar 

  19. Hernández-Zepeda C, Idris AM, Carnevali G, Brown JK, Moreno-Valenzuela OA (2007) Preliminary identification and coat protein gene phylogenetic relationships of begomoviruses associated with native flora and cultivated plants from the Yucatan Peninsula of Mexico. Virus Genes 35:825–833. https://doi.org/10.1007/s11262-007-0149-1

    Article  CAS  PubMed  Google Scholar 

  20. Hussain K, Hussain M, Mansoor S, Briddon RW (2011) Complete nucleotide sequence of a begomovirus and associated betasatellite infecting croton (Croton bonplandianus) in Pakistan. Arch Virol 156:1101–1105. https://doi.org/10.1007/s00705-011-0993-0

    Article  CAS  PubMed  Google Scholar 

  21. Fernandes FR, Albuquerque LC, de Oliveira CL, Cruz AR, da Rocha WB, Pereira TG, Naito FY, Dias NM, Nagata T, Faria JC, Zerbini FM, Aragão FJ, Inoue-Nagata AK (2011) Molecular and biological characterization of a new Brazilian begomovirus, euphorbia yellow mosaic virus (EuYMV), infecting Euphorbia heterophylla plants. Arch Virol 156:2063–2069. https://doi.org/10.1007/s00705-011-1070-4

    Article  CAS  PubMed  Google Scholar 

  22. Fiallo-Olivé E, Chirinos DT, Geraud-Pouey F, Moriones E, Navas-Castillo J (2013) Complete genome sequences of two begomoviruses infecting weeds in Venezuela. Arch Virol 158:277–280. https://doi.org/10.1007/s00705-012-1451-3

    Article  CAS  PubMed  Google Scholar 

  23. Simmonds-Gordon RN, Collins-Fairclough AM, Stewart CS, Roye ME (2014) First report of a complete genome sequence for a begomovirus infecting Jatropha gossypifolia in the Americas. Arch Virol 159:2815–2818. https://doi.org/10.1007/s00705-014-2112-5

    Article  CAS  PubMed  Google Scholar 

  24. Melo AM, Silva SJC, Ramos-Sobrinho R, Ferro MMM, Assunção IP, Lima GSA (2016) Cnidoscolus mosaic leaf deformation virus: a novel begomovirus infecting euphorbiaceous plants in Brazil. Arch Virol 161:2605–2608. https://doi.org/10.1007/s00705-016-2919-3

    Article  CAS  PubMed  Google Scholar 

  25. Vaca-Vaca JC, Jara-Tejada F, Lopez-Lopez K (2018) Croton golden mosaic virus: a new bipartite begomovirus isolated from Croton hirtus in Colombia. Arch Virol 163:3199–3202. https://doi.org/10.1007/s00705-018-3989-1

    Article  CAS  PubMed  Google Scholar 

  26. Mar TB, Xavier CD, Lima ATM, Nogueira AM, Silva JCF, Ramos-Sobrinho R, Lau D, Zerbini FM (2017) Genetic variability and population structure of the New World begomovirus Euphorbia yellow mosaic virus. J Gen Virol 98(6):1537–1551. https://doi.org/10.1099/jgv.0.000784

    Article  CAS  PubMed  Google Scholar 

  27. Webster GL (1994) Synopsis of the genera and suprageneric taxa of Euphorbiaceae. Ann Mo Bot Gard 81(1):33–144. https://doi.org/10.2307/2399909

    Article  Google Scholar 

  28. Burger W, Huft M (1995) Flora Costaricencis: Euphorbiaceae. Fieldiana Bot 36:1–169

    Google Scholar 

  29. Melo AL, Sales MF (2008) O gênero Cnidoscolus Pohl (Crotonoideae-Euphorbiaceae) no Estado de Pernambuco, Brasil. Acta Bot Bras 22:806–827. https://doi.org/10.1590/S0102-33062008000300017

    Article  Google Scholar 

  30. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small amounts of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  31. Inoue-Nagata AK, Albuquerque LC, Rocha WB, Nagata T (2004) A simple method for cloning the complete begomovirus genome using the bacteriophage phi29 DNA polymerase. J Virol Methods 116:209–211. https://doi.org/10.1016/j.jviromet.2003.11.015

    Article  CAS  PubMed  Google Scholar 

  32. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410. https://doi.org/10.1016/s0022-2836(05)80360-2

    Article  CAS  PubMed  Google Scholar 

  33. Muhire BM, Varsani A, Martin DP (2014) SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PLoS ONE 9(9):e108277. https://doi.org/10.1371/journal.pone.0108277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Kumar S, Stecher G, Tamura K (2015) MEGA7: molecular evolutionary genetics analysis version 7. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054

    Article  CAS  Google Scholar 

  35. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312–1313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Gateway Computing Environments Workshop (GCE), New Orleans, LA, 2010. Ieee 1:8. https://doi.org/10.1109/GCE.2010.5676129

  37. Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16:1114–1116

    Article  CAS  Google Scholar 

  38. Shimodaira H (2002) An approximately unbiased test of phylogenetic tree selection. Syst Biol 51(3):492–508

    Article  PubMed  Google Scholar 

  39. Shimodaira H, Hasegawa M (2001) CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17(12):1246–1247. https://doi.org/10.1007/BF02338839

    Article  CAS  PubMed  Google Scholar 

  40. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14(8):2611–2620. https://doi.org/10.1111/j.1365-294x.2005.02553.x

    Article  CAS  PubMed  Google Scholar 

  42. Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4(2):359–361. https://doi.org/10.1007/s12686-011-9548-7

    Article  Google Scholar 

  43. Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354. https://doi.org/10.1111/j.1469-1809.1949.tb02451.x

    Article  CAS  PubMed  Google Scholar 

  44. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25(11):1451–1452. https://doi.org/10.1093/bioinformatics/btp187

    Article  CAS  PubMed  Google Scholar 

  45. R Core Team (2017) R: A language and environment for statistical computing. https://www.R-project.org/

  46. Lima ATM, Silva JCF, Silva FN, Castillo-Urquiza GP, Silva FF, Seah YM, Mizubuti ESG, Duffy S, Zerbini FM (2017) The diversification of begomovirus populations is predominantly driven by mutational dynamics. Virus Evol 3(1):vex005. https://doi.org/10.1093/ve/vex005

    Article  PubMed  PubMed Central  Google Scholar 

  47. Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267. https://doi.org/10.1093/molbev/msj030

    Article  CAS  PubMed  Google Scholar 

  48. Martin DP, Murrell B, Golden M, Khoosal A, Muhire B (2015) RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evol 1(1):vev003. https://doi.org/10.1093/ve/vev003

    Article  PubMed  PubMed Central  Google Scholar 

  49. Kosakovsky Pond SL, Frost SD (2005) Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21(10):2531–2533. https://doi.org/10.1093/bioinformatics/bti320

    Article  CAS  Google Scholar 

  50. Prasanna HC, Sinha DP, Verma A, Singh M, Singh B, Rai M, Martin DP (2010) The population genomics of begomoviruses: global scale population structure and gene flow. Virol J 7:220. https://doi.org/10.1186/1743-422X-7-220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. González-Aguilera J, Tavares SS, Ramos-Sobrinho R, Xavier CAD, Dueñas-Hurtado F, Lara-Rodrigues RM, da Silva DJH, Zerbini FM (2012) Genetic structure of a Brazilian population of the begomovirus Tomato severe rugose virus (ToSRV). Trop Plant Pathol 37:346–353. https://doi.org/10.1590/S1982-56762012000500007

    Article  Google Scholar 

  52. Silva SJC, Castillo-Urquiza GP, Hora-Júnior BT, Assunção IP, Lima GSA, Pio-Ribeiro G, Mizubuti ESG, Zerbini FM (2012) Species diversity, phylogeny and genetic variability of begomovirus populations infecting leguminous weeds in northeastern Brazil. Plant Pathol 61:457–467. https://doi.org/10.1111/j.1365-3059.2011.02543.x

    Article  Google Scholar 

  53. Ferro MMM, Ramos-Sobrinho R, Silva JT, Assunção IP, Lima GSA (2017) Genetic structure of populations of the begomoviruses Tomato mottle leaf curl virus and Sida mottle Alagoas virus infecting tomato (Solanum lycopersicum) and Sida spp., respectively. Trop Plant Pathol 42:39–45. https://doi.org/10.1007/s40858-016-0119-z

    Article  Google Scholar 

  54. Venkataravanappa V, Prasanna HC, Reddy CNL, Reddy KM (2015) Evidence for two predominant viral lineages, recombination and subpopulation structure in begomoviruses associated with yellow vein mosaic disease of okra in India. Plant Pathol 64(3):508–518. https://doi.org/10.1111/ppa.12292

    Article  CAS  Google Scholar 

  55. García-Arenal F, Zerbini FM (2019) Life on the edge: geminiviruses at the interface between crops and wild plant hosts. Annu Rev Virol 6:411–433. https://doi.org/10.1146/annurev-virology-092818-015536

    Article  CAS  PubMed  Google Scholar 

  56. García-Arenal F, Fraile A, Malpica JM (2003) Variation and evolution of plant virus populations. Int Microbiol 6(4):225–232. https://doi.org/10.1007/s10123-003-0142-z

    Article  PubMed  Google Scholar 

  57. Zhou X, Liu Y, Calvert L, Munoz C, Otim-Nape GW, Robinson DJ, Harrison BD (1997) Evidence that DNA-A of a geminivirus associated with severe cassava mosaic disease in Uganda has arisen by interspecific recombination. J Gen Virol 78:2101–2211. https://doi.org/10.1099/0022-1317-78-8-2101

    Article  CAS  PubMed  Google Scholar 

  58. Monci F, Sánchez-Campos S, Navas-Castillo J, Moriones E (2002) A natural recombinant between the geminiviruses Tomato yellow leaf curl Sardinia virus and Tomato yellow leaf curl virus exhibits a novel pathogenic phenotype and is becoming prevalent in Spanish populations. Virology 303:317–326. https://doi.org/10.1006/viro.2002.1633

    Article  CAS  PubMed  Google Scholar 

  59. Lefeuvre P, Lett J-M, Reynaud B, Martin DP (2007) Avoidance of protein fold disruption in natural virus recombinants. PLoS Pathog 3:e181. https://doi.org/10.1371/journal.ppat.0030181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Lefeuvre P, Lett J-M, Varsani A, Martin DP (2009) Widely conserved recombination patterns among single-stranded DNA viruses. J Virol 83:2697–2707. https://doi.org/10.1128/JVI.02152-08

    Article  CAS  PubMed  Google Scholar 

  61. Prasanna HC, Rai M (2007) Detection and frequency of recombination in tomato-infecting begomoviruses of South and Southeast Asia. Virol J 4:111. https://doi.org/10.1186/1743-422X-4-111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Martin DP, Biagini P, Lefeuvre P, Golden M, Roumagnac P, Varsani A (2011) Recombination in eukaryotic single stranded DNA viruses. Viruses 3:1699–1738. https://doi.org/10.3390/v3091699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Hosseinzadeh MR, Shams-Bakhsh M, Osaloo SK, Brown JK (2014) Phylogenetic relationships, recombination analysis, and genetic variability among diverse variants of tomato yellow leaf curl virus in Iran and the Arabian Peninsula: further support for a TYLCV center of diversity. Arch Virol 159:485–497. https://doi.org/10.1007/s00705-013-1851-z

    Article  CAS  PubMed  Google Scholar 

  64. Briddon RW, Akbar F, Iqbal Z, Amrao L, Amin I, Saeed M, Mansoor S (2014) Effects of genetic changes to the begomovirus/betasatellite complex causing cotton leaf curl disease in South Asia post-resistance breaking. Virus Res 186:114–119. https://doi.org/10.1016/j.virusres.2013.12.008

    Article  CAS  PubMed  Google Scholar 

  65. Stanley J (1995) Analysis of African cassava mosaic virus recombinants suggests strand nicking occurs within the conserved nonanucleotide motif during the initiation of rolling circle DNA replication. Virology 206:707–712. https://doi.org/10.1016/s0042-6822(95)80093-x

    Article  CAS  PubMed  Google Scholar 

  66. Fauquet CM, Sawyer S, Idris AM, Brown JK (2005) Sequence analysis and classification of apparent recombinant begomoviruses infecting tomato in the Nile and Mediterranean basins. Phytopathology 95:549–555. https://doi.org/10.1094/phyto-95-0549

    Article  CAS  PubMed  Google Scholar 

  67. García-Andrés S, Accotto GP, Navas-Castillo J, Moriones E (2007) Founder effect, plant host, and recombination shape the emergent population of begomoviruses that cause the tomato yellow leaf curl disease in the Mediterranean basin. Virology 359:302–312. https://doi.org/10.1016/j.virol.2006.09.030

    Article  CAS  PubMed  Google Scholar 

  68. Silva SJC, Castillo-Urquiza GP, Hora Júnior BT, Assunção IP, Lima GS, Pio-Ribeiro G, Mizubuti ESG, Zerbini FM (2011) High genetic variability and recombination in a begomovirus population infecting the ubiquitous weed Cleome affinis in northeastern Brazil. Arch Virol 156:2205–2213. https://doi.org/10.1007/s00705-011-1119-4

    Article  CAS  PubMed  Google Scholar 

  69. Briddon RW, Pinner MS, Stanley J, Markham PG (1990) Geminivirus coat protein gene replacement alters insect specificity. Virology 177:85–94. https://doi.org/10.1016/0042-6822(90)90462-Z

    Article  CAS  PubMed  Google Scholar 

  70. Ohnesorge S, Bejarano ER (2009) Begomovirus coat protein interacts with a small heat-shock protein of its transmission vector (Bemisia tabaci). Insect Mol Biol 18:693–703. https://doi.org/10.1111/j.1365-2583.2009.00906.x

    Article  CAS  PubMed  Google Scholar 

  71. Rana VS, Singh ST, Priya NG, Kumar J, Rajagopal R (2012) Arsenophonus GroEL interacts with CLCuV and is localized in midgut and salivary gland of whitefly B. tabaci. PLoS ONE 7(8):e42168. https://doi.org/10.1371/journal.pone.0042168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Ilyina TV, Koonin EV (1992) Conserved sequence motifs in the initiator proteins for rolling circle DNA replication encoded by diverse replicons from eubacteria, eucaryotes and archaebacteria. Nucleic Acids Res 20(13):3279–3285. https://doi.org/10.1093/nar/20.13.3279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Heyraud-Nitschke F, Schumacher S, Laufs J, Schaefer S, Schell J, Gronenborn B (1995) Determination of the origin cleavage and joining domain of geminivirus Rep proteins. Nucleic Acids Res 23(6):910–916. https://doi.org/10.1093/nar/23.6.910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Orozco BM, Miller AB, Settlage SB, Hanley-Bowdoin L (1997) Functional domains of a geminivirus replication protein. J Biol Chem 272(15):9840–9846. https://doi.org/10.1074/jbc.272.15.9840

    Article  CAS  PubMed  Google Scholar 

  75. Nash TE, Dallas MB, Reyes MI, Buhrman GK, Ascencio-Ibañez JT, Hanley-Bowdoin L (2011) Functional analysis of a novel motif conserved across geminivirus Rep proteins. J Virol 85(3):1182–1192. https://doi.org/10.1128/JVI.02143-10

    Article  CAS  PubMed  Google Scholar 

  76. Patil BL, Fauquet CM (2009) Cassava mosaic geminiviruses: actual knowledge and perspectives. Mol Plant Pathol 10:685–701. https://doi.org/10.1111/j.1364-3703.2009.00559.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Alabi OJ, Kumar PL, Naidu RA (2011) Cassava mosaic disease: a curse to food security in Sub-Saharan Africa. APSnet Features. https://doi.org/10.1094/APSnetFeature-2011-0701

    Article  Google Scholar 

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Acknowledgements

The authors wish to thank the Brazilian agencies Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for supporting this research.

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Mendes, A.L.S.F., Melo, A.M., Ramos-Sobrinho, R. et al. High molecular diversity and divergent subpopulations of the begomovirus cnidoscolus mosaic leaf deformation virus associated with Cnidoscolus urens. Arch Virol 166, 3289–3299 (2021). https://doi.org/10.1007/s00705-021-05245-1

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