Effect of asymptomatic infection with southern tomato virus on tomato plants

  • Toshiyuki FukuharaEmail author
  • Midori Tabara
  • Hisashi Koiwa
  • Hideki Takahashi
Original Article


Southern tomato virus (STV) is often found infecting healthy tomato plants (Solanum lycopersicum). In this study, we compared STV-free and STV-infected plants of cultivar M82 to determine the effect of STV infection on the host plant. STV-free plants exhibited a short and bushy phenotype, whereas STV-infected plants were taller. STV-infected plants produced more fruit than STV-free plants, and the germination rate of seeds from STV-infected plants was higher than that of seeds from STV-free plants. This phenotypic difference was also observed in progeny plants (siblings) derived from a single STV-infected plant in which the transmission rate of STV to progeny plants via the seeds was approximately 86%. These results suggest that the interaction between STV and host plants is mutualistic. Transcriptome analysis revealed that STV infection affects gene expression in the host plant and results in downregulation of genes involved in ethylene biosynthesis and signaling. STV-infected tomato plants might thus be artificially selected due to their superior traits as a crop.



We thank Dr. Tomohide Natsuaki, Utsunomiya University, for valuable discussions, and the National BioResource Project of Japan, Tsukuba University, for providing tomato seeds. We acknowledge support received from the Gene Research Center at Tokyo University of Agriculture and Technology, the NGS core facility of the Genome Information Research Center at the Research Institute for Microbial Diseases of Osaka University, and the Human Genome Center at the Institute of Medical Science of the University of Tokyo.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.


This work was supported by the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan (Scientific Research on Innovative Areas [nos. 16H06435, 16H06429, and 16H21723] to T.F. and  H.T.) and the Global Innovation Research Organization of Tokyo University of Agriculture and Technology (to T.F.), and the Japan Society for the Promotion of Science (JSPS) through the JSPS Core-to-Core Program (Advanced Research Networks) entitled “Establishment of international agricultural immunology research-core for a quantum improvement in food safety” (to H.T.).

Supplementary material

705_2019_4436_MOESM1_ESM.pptx (2.3 mb)
Supplementary material 1 (PPTX 2306 kb)
705_2019_4436_MOESM2_ESM.doc (40 kb)
Supplementary material 2 (DOC 39 kb)


  1. 1.
    Natsuaki T, Yamashita S, Doi Y, Okuda S, Teranaka M (1983) Radish yellow edge virus, a seed-borne virus with double-stranded RNA, of a possible new group. Ann Phytopathol Soc Jpn 49:593–599. CrossRefGoogle Scholar
  2. 2.
    Dodds JA, Morris TJ, Jordan RL (1984) Plant viral double-stranded RNA. Annu Rev Phytopathol 22:151–168. CrossRefGoogle Scholar
  3. 3.
    Boccardo G, Lisa V, Luisini E, Milne RG (1987) Cryptic plant viruses. Adv Virus Res 32:171–214. CrossRefPubMedGoogle Scholar
  4. 4.
    Brown GG, Finnegan PM (1989) RNA plasmids. Int Rev Cytol 117:1–56. CrossRefPubMedGoogle Scholar
  5. 5.
    Gibbs MJ, Koga R, Moriyama H, Pfeiffer P, Fukuhara T (2000) Phylogenetic analysis of some large double-stranded RNA replicons from plants suggests they evolved from a defective single-stranded RNA virus. J Gen Virol 81:227–233. CrossRefPubMedGoogle Scholar
  6. 6.
    Fukuhara T, Koga R, Aoki N, Yuki C, Yamamoto N, Oyama N, Udagawa T, Horiuchi H, Miyazaki S, Higashi Y, Takeshita M, Ikeda K, Arakawa M, Matsumoto N, Moriyama H (2006) The wide distribution of endornaviruses, large double-stranded RNA replicons with plasmid-like properties. Arch Virol 151:995–1002. CrossRefPubMedGoogle Scholar
  7. 7.
    Roossinck MJ (2010) Lifestyles of plant viruses. Philos Trans R Soc B 365:1899–1905. CrossRefGoogle Scholar
  8. 8.
    Ghabrial SA, Nibert ML, Maiss E, Lesker T, Baker TS, Tao YJ (2012) Family Partitiviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy: ninth report of the International Committee on Taxonomy of Viruses. Elsevier, San Diego, pp 523–534Google Scholar
  9. 9.
    Fukuhara T, Gibbs MJ (2012) Family Endornaviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy: ninth report of the International Committee on Taxonomy of Viruses. Elsevier, San Diego, pp 519–521Google Scholar
  10. 10.
    Sabanadzovic S, Valverde RA, Brown JK, Martin RR, Tzanetakis IE (2009) Southern tomato virus: the link between the families Totiviridae and Partitiviridae. Virus Res 140:130–137. CrossRefPubMedGoogle Scholar
  11. 11.
    Wickner RB, Ghabrial SA, Nibert ML, Patterson JL, Wang CC (2012) Family Totiviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy: ninth report of the International Committee on Taxonomy of Viruses. Elsevier, San Diego, pp 639–650Google Scholar
  12. 12.
    Tzanetakis IE, Sabanadzovic S (2013) Establishment of the family Amalgaviridae, the genus Amalgavirus and inclusion of four species in the genus.
  13. 13.
    Krupovic M, Dolja VV, Koonin EV (2015) Plant viruses of the Amalgaviridae family evolved via recombination between viruses with double-stranded and negative-strand RNA genomes. Biol Direct 10:12. CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Nibert ML, Pyle JD, Firth AE (2016) A +1 ribosomal frameshifting motif prevalent among plant amalgaviruses. Virology 498:201–208. CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Candresse T, Marais A, Faure C (2013) First report of Southern tomato virus on tomatoes in southwest France. Plant Dis 97:1124. CrossRefPubMedGoogle Scholar
  16. 16.
    Iacono G, Hernandez-Llopis D, Alfaro-Fernandez A, Davino M, Font M, Panno S, Galipenso L, Rubio L, Davino S (2015) First report of Southern tomato virus in tomato crops in Italy. New Dis Rep 32:27. CrossRefGoogle Scholar
  17. 17.
    Padmanabhan C, Zheng Y, Li R, Sun SE, Zhang D, Liu Y, Fei Z, Ling KS (2015) Complete genome sequence of southern tomato virus identified in China using next-generation sequencing. Genome Announc 3:e01266–15. CrossRefGoogle Scholar
  18. 18.
    Padmanabhan C, Zheng Y, Li R, Fei Z, Ling KS (2015) Complete genome sequence of southern tomato virus naturally infecting tomatoes in Bangladesh. Genome Announc 3:e01522–15. CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Verbeek M, Dullemans A, Espino A, Botella M, Alfaro-Fernández A, Font M (2015) First report of Southern tomato virus in tomato in the Canary Islands, Spain. J Plant Pathol 97:392. CrossRefGoogle Scholar
  20. 20.
    Elvira-González L, Puchades AV, Carpino C, Alfaro-Fernandez A, Font-San-Ambrosio MI, Rubio L, Galipienso L (2017) Fast detection of Southern tomato virus by one-step transcription loop-mediated isothermal amplification (RT-LAMP). J Virol Methods 241:11–14. CrossRefPubMedGoogle Scholar
  21. 21.
    Puchades AV, Carpino C, Alfaro-Fernandez A, Font-San-Ambrosio MI, Davino S, Guerri J, Rubio L, Galipienso L (2017) Detection of Southern tomato virus by molecular hybridization. Ann Appl Biol 171:172–178. CrossRefGoogle Scholar
  22. 22.
    Turco S, Golyaev V, Seguin J, Gilli C, Farinelli L, Boller T, Schumpp O, Pooggin MM (2018) Small RNA-omics for virome reconstruction and antiviral defense characterization in mixed infections of cultivated Solanum plants. Mol Plant Microbe Interact 31:707–723. CrossRefPubMedGoogle Scholar
  23. 23.
    Alcalá-Briseño RI, Coşkan S, Londoño MA, Polston JE (2017) Genome sequence of Southern tomato virus in asymptomatic tomato ‘Sweet Hearts’. Genome Announc 5:e01374–16. CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Menda N, Semel Y, Peled D, Eshed Y, Zamir D (2004) In silico screening of a saturated mutation library of tomato. Plant J 38:861–872. CrossRefPubMedGoogle Scholar
  25. 25.
    Galpaz N, Wang O, Menda N, Zamir D, Hirschberg J (2008) Abscisic acid deficiency in the tomato mutant high pigment 3 leading to increased plastid number and higher fruit lycopene content. Plant J 53:717–730. CrossRefPubMedGoogle Scholar
  26. 26.
    Morris TJ, Dodds JA (1979) Isolation and analysis of double-stranded RNA from virus-infected plant and fungal tissue. Phytopathology 69:854–858. CrossRefGoogle Scholar
  27. 27.
    Okada R, Kiyota E, Moriyama H, Fukuhara T, Natsuaki T (2015) A simple and rapid method for viral dsRNA isolation from plant and fungal tissue. J Gen Plant Pathol 81:103–107. CrossRefGoogle Scholar
  28. 28.
    Langmead B, Salzberg S (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359. CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562–578. CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Shivaprasad PV, Dunn RM, Santos BA, Bassett A, Baulcombe DC (2012) Extraordinary transgressive phenotypes of hybrid tomato are influenced by epigenetics and small silencing RNAs. EMBO J 31:257–266. CrossRefPubMedGoogle Scholar
  31. 31.
    Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17:10–12. CrossRefGoogle Scholar
  32. 32.
    Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP (2011) Integrative genomics viewer. Nat Biotechnol 29:24–26. CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Wu HJ, Ma YK, Chen T, Wang M, Wang XJ (2012) PsRobot: a web-based plant small RNA meta-analysis toolbox. Nucleic Acids Res 40:W22–W28. CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Xu P, Chen F, Mannas JP, Feldman T, Sumner LW, Roossinck MJ (2008) Virus infection improves drought tolerance. New Phytol 180:911–921. CrossRefPubMedGoogle Scholar
  35. 35.
    Westwood JH, McCann L, Naish M, Dixon H, Murphy AM, Stancombe MA, Bennett MH, Powell G, Webb AA, Carr JP (2013) A viral RNA silencing suppressor interferes with abscisic acid-mediated signalling and induces drought tolerance in Arabidopsis thaliana. Mol Plant Pathol 14:158–170. CrossRefPubMedGoogle Scholar
  36. 36.
    Abeles S, Morgan PW, Saltveit ME (1992) Ethylene in plant biology, 2nd edn. Academic Press, San Diego.
  37. 37.
    Smalle J, Van Der Straeten D (1997) Ethylene and vegetative development. Physiol Plant 100:593–605. CrossRefGoogle Scholar
  38. 38.
    Jafari Z, Haddad R, Hosseini R, Garoosi G (2013) Cloning, identification and expression analysis of ACC oxidase gene involved in ethylene production pathway. Mol Biol Rep 40:1341–1350. CrossRefPubMedGoogle Scholar
  39. 39.
    Meng C, Yang D, Ma X, Zhao W, Liang X, Ma N, Meng Q (2016) Suppression of tomato SlNAC1 transcription factor delays fruit ripening. J Plant Physiol 193:88–96. CrossRefPubMedGoogle Scholar
  40. 40.
    Zhang H, Zhang D, Chen J, Yang Y, Huang Z, Huang D, Wang XC, Huang R (2004) Tomato stress-responsive factor TSRF1 interacts with ethylene responsive element GCC box and regulates pathogen resistance to Ralstonia solanacearum. Plant Mol Biol 55:825–834. CrossRefPubMedGoogle Scholar
  41. 41.
    Donaire L, Wang Y, Gonzalez-Ibeas D, Mayer KF, Aranda MA, Llave C (2009) Deep-sequencing of plant viral small RNAs reveals effective and widespread targeting of viral genomes. Virology 392:203–214. CrossRefPubMedGoogle Scholar
  42. 42.
    Ramesh SV, Williams S, Kappagantu M, Mitter N, Pappu HR (2017) Transcriptome-wide identification of host genes targeted by tomato spotted wilt virus-derived small interfering RNAs. Virus Res 238:13–23. CrossRefPubMedGoogle Scholar
  43. 43.
    Mi S, Cai T, Hu Y, Chen Y, Hodges E, Ni F, Wu L, Li S, Zhou H, Long C, Chen S, Hannon GJ, Qi Y (2008) Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5’ terminal nucleotide. Cell 133:116–127. CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Müller M, Munné-Bosch S (2015) Ethylene response factors: a key regulatory hub in hormone and stress signaling. Plant Physiol 169:32–41. CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Roossinck MJ (2011) The good viruses: viral mutualistic symbioses. Nat Rev Microbiol 9:99–108. CrossRefPubMedGoogle Scholar
  46. 46.
    Khankhum S, Valverde RA (2018) Physiological traits of endornavirus-infected and endornavirus-free common bean (Phaseolus vulgaris) cv Black Turtle Soup. Arch Virol 163:1051–1056. CrossRefPubMedGoogle Scholar
  47. 47.
    Xie WS, Antoniw JF, White RF, Jolliffee TH (1994) Effects of beet cryptic virus infection on sugar beet in field trials. Ann Appl Biol 124:451–459. CrossRefGoogle Scholar
  48. 48.
    Kieber JJ, Rothenberg M, Roman G, Feldmann KA, Ecker JR (1993) Ctr1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the Raf family of protein kinases. Cell 72:427–441. CrossRefPubMedGoogle Scholar
  49. 49.
    Khankhum S, Sela N, Osorno JM, Valverde RA (2016) RNAseq analysis of endornavirus-infected vs. endornavirus-free common bean (Phaseolus vulgaris) cultivar Black Turtle Soup. Front Microbiol 7:1905. CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Moriyama H, Horiuchi H, Koga R, Fukuhara T (1999) Molecular characterization of two endogenous double-stranded RNAs in rice and their inheritance by interspecific hybrids. J Biol Chem 274:6882–6888. CrossRefPubMedGoogle Scholar
  51. 51.
    Read AF (1994) The evolution of virulence. Trends Microbiol 2:73–76. CrossRefPubMedGoogle Scholar
  52. 52.
    Roossinck MJ (2015) Plants, viruses and the environment: ecology and mutualism. Virology 479–480:271–277. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Applied Biological SciencesTokyo University of Agriculture and TechnologyFuchuJapan
  2. 2.Institute of Global Innovation ResearchTokyo University of Agriculture and TechnologyFuchuJapan
  3. 3.Molecular and Environmental Plant Sciences, Vegetable and Fruit Improvement Center, Department of Horticultural SciencesTexas A&M UniversityCollege StationUSA
  4. 4.Graduate School of Agricultural ScienceTohoku UniversitySendaiJapan

Personalised recommendations