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A Survey on Plant Viruses in Natural Brassicaceae Communities Using RNA-Seq

  • Plant Microbe Interactions
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Abstract

Studies on plant viruses are biased towards crop diseases and little is known about viruses in natural vegetation. We conducted extensive surveys of plant viruses in wild Brassicaceae plants occurring in three local plant communities in central Japan. We applied RNA-Seq with selective depletion of rRNA, which allowed us to detect infections of all genome-reported viruses simultaneously. Infections of Turnip mosaic virus (TuMV), Cucumber mosaic virus (CMV), Brassica yellows virus, Pelargonium zonate spot virus, and Arabidopsis halleri partitivirus 1 were detected from the two perennial species, Arabidopsis halleri subsp. gemmifera and Rorippa indica. De novo assembly further detected partial sequences of a putative novel virus in Arabis fragellosa. Virus species composition and infection rate differed depending on site and plant species. Viruses were most frequently detected from the perennial clonal plant, A. halleri, in which a high clonal transmission rate of viruses across multiple years was confirmed. Phylogenetic analysis of TuMV and CMV showed that virus strains from wild Brassicaceae were included as a major clade of these viruses with other reported strains from crop plants, suggesting that viruses were shared among wild plants and crops. Our studies indicated that distribution of viruses in natural plant populations are determined by the combinations of life histories of viruses and hosts. Revealing viral distribution in the natural plant communities improves our knowledge on the ecology of plant viruses.

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References

  1. Tomlinson JA, Carter AL, Dale WT, Simpson CJ (1970) Weed plants as sources of cucumber mosaic virus. Ann Appl Biol 66:11–16. https://doi.org/10.1111/j.1744-7348.1970.tb04597.x

    Article  Google Scholar 

  2. Mueller EE, Groves RL, Gratton C (2011) Crop and non-crop plants as potential reservoir hosts of alfalfa mosaic virus and cucumber mosaic virus for spread to commercial snap bean. Plant Dis 96:506–514. https://doi.org/10.1094/PDIS-02-11-0089

    Article  Google Scholar 

  3. Roossinck MJ (2012) Plant virus metagenomics: biodiversity and ecology. Annu Rev Genet 46:359–369. https://doi.org/10.1146/annurev-genet-110711-155600

    Article  CAS  PubMed  Google Scholar 

  4. Aranda MA, Freitas-Astúa J (2017) Ecology and diversity of plant viruses, and epidemiology of plant virus-induced diseases. Ann Appl Biol 171:1–4. https://doi.org/10.1111/aab.12361

    Article  Google Scholar 

  5. Islam W, Zhang J, Adnan M, Noman A, Zainab M, Jian W (2017) Plant virus ecology: a glimpse of recent accomplishments. Appl Ecol Environ Res 15:691–705. https://doi.org/10.15666/aeer/1501_691705

    Article  Google Scholar 

  6. May RM, Anderson RM (1983) Epidemiology and genetics in the coevolution of parasites and hosts. Proc R Soc Lond B Biol Sci 219:281–313. https://doi.org/10.1098/rspb.1983.0075

    Article  CAS  PubMed  Google Scholar 

  7. Prendeville HR, Ye X, Morris TJ, Pilson D (2012) Virus infections in wild plant populations are both frequent and often unapparent. Am J Bot 99:1033–1042. https://doi.org/10.3732/ajb.1100509

    Article  PubMed  Google Scholar 

  8. Li L, Liu J, Zhang Q, Fu R, Zhu X, Li C, Chen J (2016) Seed-borne viral dsRNA elements in three cultivated Raphanus and Brassica plants suggest three cryptoviruses. Can J Microbiol 62:287–295. https://doi.org/10.1139/cjm-2015-0788

    Article  CAS  PubMed  Google Scholar 

  9. Alexander HM, Bruns E, Schebor H, Malmstrom CM (2017) Crop-associated virus infection in a native perennial grass: reduction in plant fitness and dynamic patterns of virus detection. J Ecol 105:1021–1031. https://doi.org/10.1111/1365-2745.12723

    Article  Google Scholar 

  10. Pagán I, Montes N, Milgroom MG, García-Arenal F (2014) Vertical transmission selects for reduced virulence in a plant virus and for increased resistance in the host. PLoS Pathog 10:e1004293. https://doi.org/10.1371/journal.ppat.1004293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Bottenberg H, Irwin ME (1992) Using mixed cropping to limit seed mottling induced by soybean mosaic virus. Plant Dis 76:304–306. https://doi.org/10.1094/PD-76-0304

    Article  Google Scholar 

  12. Jones RAC, Ferris DG (2000) Suppressing spread of alfalfa mosaic virus in grazed legume pasture swards using insecticides and admixture with grass, and effects of insecticides on numbers of aphids and three other pasture pests. Ann Appl Biol 137:259–271. https://doi.org/10.1111/j.1744-7348.2000.tb00067.x

    Article  CAS  Google Scholar 

  13. Hooks CRR, Fereres A (2006) Protecting crops from non-persistently aphid-transmitted viruses: a review on the use of barrier plants as a management tool. Virus Res 120:1–16. https://doi.org/10.1016/j.virusres.2006.02.006

    Article  CAS  PubMed  Google Scholar 

  14. Pedersen AB, Fenton A (2007) Emphasizing the ecology in parasite community ecology. Trends Ecol Evol 22:133–139. https://doi.org/10.1016/j.tree.2006.11.005

    Article  PubMed  Google Scholar 

  15. Callaway RM (1995) Positive interactions among plants. Bot Rev 61:306–349. https://doi.org/10.1007/BF02912621

    Article  Google Scholar 

  16. Seabloom EW, Borer ET, Gross K, Kendig AE, Lacroix C, Mitchell CE, Mordecai EA, Power AG (2015) The community ecology of pathogens: coinfection, coexistence and community composition. Ecol Lett 18:401–415. https://doi.org/10.1111/ele.12418

    Article  PubMed  Google Scholar 

  17. Filipe J, Maule M (2004) Effects of dispersal mechanisms on spatio-temporal development of epidemics. J Theor Biol 226:125–141. https://doi.org/10.1016/S0022-5193(03)00278-9

    Article  CAS  PubMed  Google Scholar 

  18. Gibson G (1997) Investigating mechanisms of spatiotemporal epidemic spread using stochastic models. Phytopathology 87:139–146. https://doi.org/10.1094/PHYTO.1997.87.2.139

    Article  CAS  PubMed  Google Scholar 

  19. Barba M, Czosnek H, Hadidi A (2014) Historical perspective, development and applications of next-generation sequencing in plant virology. Viruses 6:106–136. https://doi.org/10.3390/v6010106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Kamitani M, Nagano AJ, Honjo MN, Kudoh H (2016) RNA-Seq reveals virus-virus and virus-plant interactions in nature. FEMS Microbiol Ecol 92. https://doi.org/10.1093/femsec/fiw176

  21. Palukaitis P, Roossinck MJ, Dietzgen RG, Francki RI (1992) Cucumber mosaic virus. Adv Virus Res 41:281–348

    Article  CAS  PubMed  Google Scholar 

  22. Ohshima K, Yamaguchi Y, Hirota R, Hamamoto T, Tomimura K, Tan Z, Sano T, Azuhata F, Walsh JA, Fletcher J, Chen J, Gera A, Gibbs A (2002) Molecular evolution of turnip mosaic virus: evidence of host adaptation, genetic recombination and geographical spread. J Gen Virol 83:1511–1521. https://doi.org/10.1099/0022-1317-83-6-1511

    Article  CAS  PubMed  Google Scholar 

  23. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652. https://doi.org/10.1038/nbt.1883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Morlan JD, Qu K, Sinicropi DV (2012) Selective depletion of rRNA enables whole transcriptome profiling of archival fixed tissue. PLoS One 7:e42882. https://doi.org/10.1371/journal.pone.0042882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Rice P, Longden I, Bleasby A (2000) EMBOSS: the European molecular biology open software suite. Trends Genet 16:276–277. https://doi.org/10.1016/s0168-9525(00)02024-2

    Article  CAS  PubMed  Google Scholar 

  26. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara R, Simpson GL, Solymos P, Stevens MHH, Wagner H (2015) Vegan: community ecology package. R package version 2.3-5. 2016

  27. Roossinck MJ, Zhang L, Hellwald KH (1999) Rearrangements in the 5′ nontranslated region and phylogenetic analyses of cucumber mosaic virus RNA 3 indicate radial evolution of three subgroups. J Virol 73:6752–6758

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Bashir NS, Kalhor MR, Zarghani SN (2006) Detection, differentiation and phylogenetic analysis of cucumber mosaic virus isolates from cucurbits in the northwest region of Iran. Virus Genes 32:277–288. https://doi.org/10.1007/s11262-005-6912-2

    Article  CAS  PubMed  Google Scholar 

  29. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Pallett D, Thurston M, Cortina-Borja M, Edwards ML, Alexander M, Mitchell E, Raybould A, Cooper J (2002) The incidence of viruses in wild Brassica rapa ssp. sylvestris in southern England. Ann Appl Biol 141:163–170. https://doi.org/10.1111/j.1744-7348.2002.tb00209.x

    Article  Google Scholar 

  31. Rist DL, Lorbeer JW (1989) Occurrence and overwintering of cucumber mosaic virus and broad bean wilt virus in weeds growing near commercial lettuce fields in New York. Phytopathology 79:65–69. https://doi.org/10.1094/Phyto-79-65

    Article  Google Scholar 

  32. Kamitani M, Nagano AJ, Honjo MN, Kudoh H (2017) First report of Pelargonium zonate spot virus from wild Brassicaceae plants in Japan. J Gen Plant Pathol 83:329–332. https://doi.org/10.1007/s10327-017-0727-6

    Article  CAS  Google Scholar 

  33. Lapidot M, Guenoune-Gelbart D, Leibman D, Holdengreber V, Davidovitz M, Machbash Z, Klieman-Shoval S, Cohen S, Gal-On A (2010) Pelargonium zonate spot virus is transmitted vertically via seed and pollen in tomato. Phytopathology 100:798–804. https://doi.org/10.1094/phyto-100-8-0798

    Article  CAS  PubMed  Google Scholar 

  34. Roossinck MJ (2010) Lifestyles of plant viruses. Philos Trans R Soc Lond Ser B Biol Sci 365:1899–1905. https://doi.org/10.1098/rstb.2010.0057

    Article  Google Scholar 

  35. Schliephake E, Graichen K, Rabenstein FF (1999) Investigations on the vector transmission of the Beet mild yellowing virus (BMYV) and the Turnip yellows virus (TuYV). Journal of Plant Diseases and Protection 107(1):81–87. http://www.jstor.org/stable/43215342.

  36. Whitfield AE, Falk BW, Rotenberg D (2015) Insect vector-mediated transmission of plant viruses. Virology 479-480:278–289. https://doi.org/10.1016/j.virol.2015.03.026

    Article  CAS  PubMed  Google Scholar 

  37. Choi SK, Yoon JY, Ryu KH, Choi JK, Palukaitis P, Park WM (2002) Systemic movement of a movement-deficient strain of cucumber mosaic virus in zucchini squash is facilitated by a cucurbit-infecting potyvirus. J Gen Virol 83:3173–3178. https://doi.org/10.1099/0022-1317-83-12-3173

    Article  CAS  PubMed  Google Scholar 

  38. Pruss G, Ge X, Shi XM, Carrington JC, Bowman Vance V (1997) Plant viral synergism: the potyviral genome encodes a broad-range pathogenicity enhancer that transactivates replication of heterologous viruses. Plant Cell 9:859–868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Kondo H, Hirano S, Chiba S, Andika IB, Hirai M, Maeda T, Tamada T (2013) Characterization of burdock mottle virus, a novel member of the genus Benyvirus, and the identification of benyvirus-related sequences in the plant and insect genomes. Virus Res 177:75–86. https://doi.org/10.1016/j.virusres.2013.07.015

    Article  CAS  PubMed  Google Scholar 

  40. Nibert ML, Ghabrial SA, Maiss E, Lesker T, Vainio EJ, Jiang D, Suzuki N (2014) Taxonomic reorganization of family Partitiviridae and other recent progress in partitivirus research. Virus Res 188:128–141. https://doi.org/10.1016/j.virusres.2014.04.007

    Article  CAS  PubMed  Google Scholar 

  41. Boccardo G, Lisa V, Luisoni E, Milne RG (1987) Cryptic plant viruses. Adv Virus Res 32:171–214. https://doi.org/10.1016/S0065-3527(08)60477-7

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank Dr. Y. Sato for his helpful comments on statistical analysis.

Funding

This work was supported by KAKENHI (JP26221106, 16H06171, JP16H01473), CREST (JPMJCR15O1, JPMJCR15O2), and Grant-in-Aid for JSPS Fellows (15J00628).

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Correspondence to Mari Kamitani or Hiroshi Kudoh.

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Kamitani, M., Nagano, A.J., Honjo, M.N. et al. A Survey on Plant Viruses in Natural Brassicaceae Communities Using RNA-Seq. Microb Ecol 78, 113–121 (2019). https://doi.org/10.1007/s00248-018-1271-4

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