Effect of defective interfering RNAs on the vertical transmission of Tomato black ring virus


Pospieszny H., Hasiów-Jaroszewska B., Borodynko-Filas N., Elena S.F. (2020): Effect of defective interfering RNAs on the vertical transmission of Tomato black ring virus. Plant Protect. Sci., 56: 261–267.

download PDF

Viruses are thought to be the ultimate parasites, using host resources for multiplication. Interestingly, many viruses also have their own 'parasites', such as defective interfering RNAs (DI RNAs). One of the plant viruses whose infection can be accompanied by subviral RNAs is the Tomato black ring virus (TBRV). DI RNAs associated with the TBRV genome were generated de novo as a result of prolonged passages in one host. DI RNAs modulate the TBRV accumulation and the severity of the symptoms induced on the infected plants. In this study, we have addressed the question of whether DI RNAs can also affect TBRV vertical transmission through seeds. The experiments were conducted using the TBRV-Pi isolate and Chenopodium quinoa plants. C. quinoa plants were infected with TBRV-Pi with and without DI RNAs. Overall, 4 003 seeds were tested, and the analysis showed that the presence of DI RNAs made the TBRV-Pi seed transmission 44.76% more efficient. Moreover, for the first time, we showed that DI RNAs are being transferred from generation to generation.

Brunt A.A., Crabtree K., Dallwitz M.J., Gibba A.J., Watson L. (1966): Viruses of Plants. Descriptions and Lists from the VIDE Database. Wallingford, CAB International.
Digiaro M.D., Yahyaoui E., Martelli T., Elbeaino T. (2015): The sequencing of the complete genome of Tomato black ring virus (TBRV) and of the RNA2 of three Grapevine chrome mosaic virus (GCMV) isolates from grapevine reveals the possible recombinant origin of GCMV. Virus Genes, 50: 165–171. https://doi.org/10.1007/s11262-014-1094-4
Gallitelli D., Rana G.L., Volvas C., Martelli G.P. (2004): Viruses of globe artichoke: An overview. Journal of Plant Pathology, 86: 267–281.
Galwey N.W. (1989): Quinoa. Biologist, 36: 267–274.
Graves M.V., Pogany J., Romero J. (1996): Defective interfering RNAs and defective viruses associated with multipartite RNA viruses of plants. Seminars in Virology, 7: 399–408. https://doi.org/10.1006/smvy.1996.0048
Hampton R.O., Francki R.I.B. (1992): RNA-1 dependent seed transmissibility of Cucumber mosaic virus in Phaseolus vulgaris. Phytopathology, 82: 127–130. https://doi.org/10.1094/Phyto-82-127
Hanada K., Harrison B.D. (1977): Effects of virus genotype and temperature on seed transmission of nepoviruses. Annals of Applied Biology, 85: 79–92. https://doi.org/10.1111/j.1744-7348.1977.tb00632.x
Harrison B.D., Mowat W.P., Taylor C.E. (1961): Transmission of a strain of Tomato black ring virus by Longidorus elongatus (Nematoda). Virology, 14: 480–485. https://doi.org/10.1016/0042-6822(61)90341-5
Hasiów-Jaroszewska B., Borodynko N., Figlerowicz M., Pospieszny H. (2012): Two types of defective RNAs arising from the Tomato black ring virus genome. Archives of Virology, 157: 569–572. https://doi.org/10.1007/s00705-011-1200-z
Hasiów-Jaroszewska B., Minicka J., Zarzyńska-Nowak A., Budzyńska D., Elena SF. (2018): Defective RNA particles derived from Tomato black ring virus genome interfere with the replication of parental virus. Virus Research, 250: 87–94. https://doi.org/10.1016/j.virusres.2018.04.010
Holland J.J., Semler B.L., Jones C., Perrault J., Reid L., Roux L. (1978): Role of DI, virus mutation, and host response in persistent infections by envelope RNA viruses. In: Stevens J.G., Todaro G.J., Fox C.P. (eds): Persistent Viruses. ICN-UCLA. Symposia on Molecular and Cellular Biology. XI. New York, Academic Press: 57–73.
Inoue-Nagata A.K., Kormelink R., Nagata T., Kitajima E.W., Goldbach R., Peters D. (1997): Effects of temperature and host on the generation of Tomato spotted wilt virus defective interfering RNAs. Phytopathology, 87: 1168–1173. https://doi.org/10.1094/PHYTO.1997.87.11.1168
Jacobsen S.E., Mujica A., Stolen O. (1998): Salt tolerance of quinoa during germination. Agronomia Tropical (Maracay), 48: 359–366.
Johansen E., Edwards M.C., Hampton R.O. (1994): Seed transmission of viruses: current perspectives. Annual Review of Phytopathology, 32: 363–386 https://doi.org/10.1146/annurev.py.32.090194.002051
Jończyk M., Borodynko N., Figlerowicz M., Pospieszny H. (2004): Small defective interfering RNAs arising from Tomato black ring virus (TBRV) genome. FEBS Journal, P2.2–01.
Ling K.S. (2008): Pepino mosaic virus on tomato seeds, virus location and mechanical transmission. Plant Disease, 92: 1701–1705. https://doi.org/10.1094/PDIS-92-12-1701
Lister R.M., Murant A.F. (1967): Seed-transmission of nematode-borne viruses. Annals of Applied Biology, 59: 49–62. https://doi.org/10.1111/j.1744-7348.1967.tb04416.x
Lukhovitskaya N.I., Thaduri S., Garushyants S.K., Torrance L., Savenkov E.I. (2013): Deciphering the mechanism of defective interfering RNA (DI RNA) biogenesis reveals that a viral protein and the DI RNA act antagonistically in virus infection. Journal of Virology, 87: 6091–6103. https://doi.org/10.1128/JVI.03322-12
Pathak K.N., Nagy P.D. (2009): Defective interfering RNAs: foes or viruses and friends of virologists. Viruses, 1: 859–919. https://doi.org/10.3390/v1030895
Paudel D.B., Sanfaçon H. (2018): Exploring the diversity of mechanisms associated with plant tolerance to virus infection. Frontiers of Plant Science, 9: 1575. doi: 10.3389/fpls.2018.01575 https://doi.org/10.3389/fpls.2018.01575
Pospieszny H., Borodynko-Filas N., Hasiów-Jaroszewska B., Czerwonka B., Elena S.F. (2020): An assessment of the transmission rate of the Tomato black ring virus through tomato seeds. Plant Protection Science, 56: 9–12. https://doi.org/10.17221/33/2019-PPS
Rymelska N., Borodynko N., Pospieszny H., Hasiów-Jaroszewska B. (2013): Analysis of the biological and molecular variability of the Polish isolates of Tomato black ring virus (TBRV). Virus Genes, 47: 338–346. https://doi.org/10.1007/s11262-013-0941-z
Sambrook J., Fritsh E.F., Maniatis T. (1989): Molecular Cloning: a Laboratory Manual, 2nd Ed. Cold Spring Harbor, Cold Spring Harbor Laboratory Press.
Simon A.E., Roossinick M.J., Havelda Z. (2004): Plant virus satellite and defective interfering RNAs: new paradigms for  https://doi.org/10.1146/annurev.phyto.42.040803.140402
a new century. Annual Review of Phytopathology, 42: 415–437.
Szittya G., Molnar A., Silhavy D., Hornyik C., Burgyan J. (2002): Short defective interfering RNAs of tombusviruses are not targeted but trigger post-transcriptional gene silencing against their helper virus. Plant Cell, 14: 359–372. https://doi.org/10.1105/tpc.010366
Wang D., Macfarlane S.A., Maule A.J. (1997): Viral determinants of Pea early browning virus seed transmission in pea. Virology, 234: 112–117. https://doi.org/10.1006/viro.1997.8637
download PDF

© 2020 Czech Academy of Agricultural Sciences | Prohlášení o přístupnosti