Skip to main content
SpringerLink
Log in

Yield losses of asymptomatic strawberry plants infected with Strawberry mild yellow edge virus

European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

After successive vegetative propagation cycles, strawberry (Fragaria × ananassa Duch.) plants often accumulate multiple virus species that result in viral symptoms and losses in yield and quality. However, strawberry plants infected by a single virus species usually remain asymptomatic with unknown effects on fruit production and quality. In this context, the effect of Strawberry mild yellow edge virus (SMYEV) on fruit production was studied in strawberry plants, cultivar Camarosa, over two years. Asymptomatic SMYEV-infected plants showed a significant reduction in total and marketable fruit number and weight compared with healthy plants. These reductions ranged between 28% and 63%, depending on the parameter measured and the production cycle. Fluctuations in SMYEV concentration in the plants was detected throughout the crop cycle, suggesting that samples for virus diagnosis should be taken when the plant has the highest virus concentration; in this study, this occurred at the end of the crop cycle. These results show that analyzing symptomless strawberry plants should be part of a virus disease management plant and an important component to control the quantitative and qualitative impacts of SMYEV on strawberry yield.

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

Access this article

Log in via an institution

Price includes VAT (Finland)

Instant access to the full article PDF.

Institutional subscriptions

References

  • Babovic, M. V. (1976). Changes in the yield and quality of strawberry fruit infected by Strawberry crinkle virus. Acta Horticulturae, 66, 25–28.

    Article  Google Scholar 

  • Barritt, B. H., & Loo, H. Y. S. (1973). Effects of mottle, crinkle, and mild yellow-edge viruses on growth and yield of hood and northwest strawberries. Canadian Journal of Plant Science, 53, 605–607.

    Article  Google Scholar 

  • Bernardi, D., Garcia, M. S., Botton, M., & Nava, D. E. (2012). Biology and fertility life table of the green aphid Chaetosiphon fragaefolli on strawberry cultivars. Journal of Insect Science, 12, 1–8. https://doi.org/10.1673/031.012.2801.

    Article  Google Scholar 

  • Bijaisoradat, M., & Kuhn, C. W. (1985). Nature of resistance in soybean to cowpea chlorotic mottle virus. Phytopathology, 75, 351–355.

    Article  Google Scholar 

  • Bolton, A. T. (1974). Effects of three virus diseases and their combination on fruit yield of strawberries. Canadian Journal of Plant Science, 54, 271–275.

    Article  Google Scholar 

  • Chang, L., Zhang, Z., Yang, H., Li, H., & Dai, H. (2007). Detection of strawberry RNA and DNA viruses by RT-PCR using total nucleic acid as a template. Journal of Phytopathology, 155, 431–436. https://doi.org/10.1111/j.1439-0434.2007.01254.x.

    Article  CAS  Google Scholar 

  • Chinestra, S. C., Facchinetti, C., Curvetto, N. R., & Marinangeli, P. A. (2010). Detection and frequency of lily viruses in Argentina. Plant Disease, 94, 1188–1194.

    Article  Google Scholar 

  • Cho, J. D., Choi, G. S., Chung, B. N., Kim, J. S., & Choi, H. S. (2011). Strawberry mild yellow edge potexvirus from strawberry in Korea. The Plant Patholology Journal, 27, 187–190.

    Article  Google Scholar 

  • Conci, V. C., Lunello, P., Buraschi, D., Italia, R. R., & Nome, S. F. (2002). Variations of Leek yellow stripe virus concentration in garlic and its incidence in Argentina. Plant Disease, 86, 1085–1088.

    Article  Google Scholar 

  • Conci, V. C., Canavelli, A., Lunello, P., Di Rienzo, J., Nome, S. F., Zumelzu, G., & Italia, R. (2003). Yield losses associated with virus-infected garlic plants during five successive years. Plant Disease, 87, 1411–1415.

    Article  Google Scholar 

  • Conci, V. C., Torrico, A. K., Cafrune, E., Quevedo, V., Baino, O., Ramallo, J. C., Borquez, A. M., Mollinedo, V. A., Agüero, J. J., & Kirschbaum, D. (2009). First report of Strawberry mild yellow edge virus in Argentina. Acta Horticulturae, 842, 303–306.

    Article  Google Scholar 

  • Conci, V. C., Luciani, C. E., Celli, M. G., Perotto, M. C., Torrico, A. K., Pozzi, E., Strumia, G., Dughetti, A. C., Asinari, F., Conci, L. R., Fernandez, F. D., Salazar, S. M., Meneguzzi, N. G., & Kirschbaum, D. S. (2017). Advances in characterization and epidemiology of strawberry viruses and phytoplasmas in Argentina. Acta Horticulturae, 1156, 801–809. 10.17660/ActaHortic.2017.1156.118.

    Article  Google Scholar 

  • Converse, R. H. (1987). USDA agricultural handbook no. 631 (p. 277). Washington, D.C.: U.S. Department of Agriculture, Agricultural Research Service.

  • Coutts, B. A., Prince, R. T., & Jones, R. A. C. (2009). Quantifying effects of seedborne inoculum on virus spread, yield losses, and seed infection in the pea seed-borne mosaic virus-field pea pathosystem. Phytopathology, 99, 1156–1167. https://doi.org/10.1094/PHYTO-99-10-1156.

    Article  CAS  PubMed  Google Scholar 

  • Dal Zotto, A., Nome, S. F., Di Rienzo, J. A., & Docampo, D. M. (1999). Fluctuations of prunus necrotic ringspot virus (PNRSV) at various phenological stages in peach cultivars. Plant Disease, 83, 1055–1057.

    Article  Google Scholar 

  • Delfino, M. A. (2004). Afidos (Homoptera: Aphidoidea) de la Argentina. En: Cordo, H., Logarzo, G., Braun, K., & Di Iorio, O. (Eds.), Catálogo de los insectos fitófagos de la Argentina y sus plantas hospedadoras (1era ed, p.734). South American Biological Control Laboratory USDA-ARS, Sociedad Entomológica Argentina.

  • Delfino, M. A., Conci, V. C., & Dughetti, A. C. (2007). Áfidos transmisores de virus de frutilla en la Argentina. Horticultura Argentina, 26(61), 45.

    Google Scholar 

  • Di Rienzo, J. A., Casanoves, F., Balzarini, M. G., Gonzalez, L., Tablada, M., & Robledo, C. W. (2012). InfoStat versión 2012. Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. URL http://www.infostat.com.ar.

  • Dughetti, A. C., Conci, V. C., & Kirshbaum, D. (2017). Áfidos trasmisores de virus detectados en cultivos de frutilla en Argentina. Revista de Investigaciones Agropecuarias, 43, 36–50.

    Google Scholar 

  • FAO, Food and Agriculture Organization of the United Nations (2016). FAOSTAT agriculture data. http://faostat3.fao.org/download/Q/QC/E. Accessed May 2016.

  • Fernández, F. D., Conci, V. C., Kirschbaum, D. S., & Conci, L. R. (2013). Molecular characterization of a phytoplasma of the ash yellows group occurring in strawberry (Fragaria x ananassa Duch.) plants in Argentina. European Journal of Plant Pathology, 135, 1–4.

    Article  Google Scholar 

  • Fernández, F. D., Meneguzzi, N., Guzmán, F. A., Kirschbaum, D., Vilma, V. C., Nome, C., & Conci, L. R. (2015). Detection and identification of a novel 16SrXIII subgroup phytoplasma associated with strawberry red leaf disease in Argentina. International Journal of Systematic and Evolutionary Microbiology, 65, 2741–2747.

    Article  PubMed  Google Scholar 

  • Gibson, R. W., Mwanga, R. O. M., Kasule, S., Mpembe, I., & Carey, E. E. (1997). Apparent absence of viruses in most symptomless field-grown sweet potato in Uganda. Annals of Applied Biology, 130, 481–490.

    Article  Google Scholar 

  • Hane, D. C., & Hamm, P. B. (1999). Effects of seedborne Potato virus Y infection in two potato cultivars expressing mild disease symptoms. Plant Disease, 83, 43–45.

    Article  Google Scholar 

  • Hanzlíková-Vašková, D., Špak, J., & Petrzik, K. (2006). Variability in sequence of strawberry vein banding virus. Biologia Plantarum, 50, 660–666.

    Article  Google Scholar 

  • Hepp, R. F., & Martin, R. R. (1992). Occurrence of strawberry mild yellow-edge associated virus in wild Fragaria chiloensis in South America. Acta Horticulturae, 308, 57–59.

    Article  Google Scholar 

  • Hummer, K. E. (2008). Global conservation strategy for Fragaria (strawberry). Scripta Horticulturae (no. 6, p. 87). ISHS Secretariat, Leuven.

  • Jelkmann, W., Martin, R. R., Lesemann, D. E., Vetten, H. J., & Skelton, F. (1990). A new potexvirus associated with strawberry mild yellow edge disease. Journal of General Virology, 71, 1251–1258.

    Article  CAS  PubMed  Google Scholar 

  • Kirschbaum, D. S., & Hancock, J. F. (2000). The strawberry industry in South America. Hortscience, 35, 807–811.

    Google Scholar 

  • Klerks, M. M., Lindner, J. L., Vaskova, D., Spak, J., Thompson, J. R., Jelkmann, W., & Schoen, C. D. (2004). Detection and tentative grouping of Strawberry crinkle virus isolates. European Journal of Plant Pathology, 110, 45–52.

    Article  CAS  Google Scholar 

  • Lamprecht, S., & Jelkmann, W. (1997). Infectious cDNA clone used to identify strawberry mild yellow edge associated potexvirus as causal agent of the disease. Journal of General Virology, 78, 2347–2353.

    Article  CAS  PubMed  Google Scholar 

  • Leclercq-Le Quillec, F., Plantegenest, M., Riault, G., & Dedryver, C. A. (2000). Analyzing and modeling temporal disease progress of Barley yellow dwarf virus serotypes in barley fields. Phytopathology, 90, 860–866.

    Article  CAS  PubMed  Google Scholar 

  • Liu, H., Sears, J. L., & Morrison, R. H. (2003). Isolation and characterization of a carmo-like virus from calibrachoa plants. Plant Disease, 87, 167–171.

    Article  Google Scholar 

  • Lot, H., Chovelon, V., Souche, S., & Delecolle, B. (1998). Effects of Onion yellow dwarf and Leek yellow stripe viruses on symptomatology and yield loss of three french garlic cultivars. Plant Disease, 82, 1381–1385.

    Article  Google Scholar 

  • Luciani, C. E., Celli, M. G., Merino, M. C., Perotto, M. C., Pozzi, E., & Conci, V. C. (2016). First report of strawberry polerovirus 1 in Argentina. Plant Disease, 100, 1510.

    Article  Google Scholar 

  • Ma, X., Cui, H., Bernardy, M. G., Tian, L. N., Abbasi, P. A., & Wang, A. M. (2015). Molecular characterization of a Strawberry mild yellow edge virus isolate from Canada. Canadian Journal of Plant Pathology, 37, 369–375.

    Article  CAS  Google Scholar 

  • Maas, J. R. (1998). Compendium of strawberry virus diseases (2nd edition, p. 98). APS Press, St Paul.

  • Martin, R. R., & Tzanetakis, I. E. (2006). Characterisation and recent advances in detection of strawberry viruses. Plant Disease, 90, 384–396.

    Article  Google Scholar 

  • Mink, G. I. (1980). Identification of rugose mosaic-diseased cherry trees by enzymelinked immunosorbent assay. Plant Disease, 64, 691–694.

    Article  Google Scholar 

  • Mráz, I., Petrzik, K., Šíp, M., & Fránová-Honetšlegrová, J. (1998). Variability in coat protein sequence homology among American and European sources of Strawberry vein banding virus. Plant Disease, 82, 544–546 Retrieved from http://apsjournals.apsnet.org/doi/pdf/10.1094/PDIS.1998.82.5.544.

    Article  Google Scholar 

  • Nome, S. F., & Yossen, V. (1980). Identificación de virus de frutilla en Argentina. I. virus del moteado de la frutilla (Strawberry mottle virus) RIA. XV (pp. 245–257).

  • Ortego, J. (1997). Pulgones de la Patagonia Argentina con la descripción de Aphis intrusa sp. n. (Homoptera: Aphididae). Revista de la Facultad de Agronomía. La Plata, 102, 59–80.

    Google Scholar 

  • Perotto, M. C., Luciani, C., Celli, M. G., Torrico, A. K., & Conci, V. C. (2014). First report of Strawberry crinkle virus in Argentina. New Disease Report, 30, 5. https://doi.org/10.5197/j.20440588.2014.030.005.

    Article  Google Scholar 

  • Posthuma, K. I., Adams, A. N., Hong, Y., & Kirby, M. J. (2002). Detection of Strawberry crinkle virus in plants and aphids by RT-PCR using conserved L gene sequences. Plant Pathology, 51, 266–274. https://doi.org/10.1046/j.1365-3059.2002.00725.x.

    Article  CAS  Google Scholar 

  • Ramkat, R. C., Wangai, A. W., Ouma, J. P., Rapando, P. N., & Lelgut, D. K. (2008). Cropping system influences Tomato spotted wilt virus disease development, thrips population and yield of tomato (Lycopersicon Esculentum). Annals of Applied Biology, 153, 373–380. https://doi.org/10.1111/j.1744-7348.2008.00268.x.

    Article  Google Scholar 

  • Thompson, J. R., & Jelkmann, W. (2003). The detection and variation of Strawberry mottle virus. Plant Disease, 87, 385–390.

    Article  CAS  Google Scholar 

  • Torrico, A. K., Celli, M. G., Cafrune, E. E., Kirschbaum, D. S., & Conci, V. C. (2016). Genetic variability and recombination analysis of the coat protein gene of Strawberry mild yellow edge virus. Australasian Plant Patholology, 45, 401–409.

    Article  CAS  Google Scholar 

  • Xiang, Y., Bernardy, M., Bhagwat, B., Wiersma, P. A., DeYoung, R., & Bouthillier, M. (2015). The complete genome sequence of a new polerovirus in strawberry plants from eastern Canada showing strawberry decline symptoms. Archives of Virology, 160, 553–556.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by grants from the Instituto Nacional de Tecnología Agropecuaria (INTA), Agencia Nacional de Promoción Científica y Tecnológica through the Fondo para la Investigación Científica y Tecnológica (FONCyT), Argentina.

Author information

Author notes

  1. A. K. Torrico and S. M. Salazar contributed equally to this work

Authors and Affiliations

  1. Instituto de Patología Vegetal (IPAVE), Centro de Investigaciones Agropecuarias (CIAP), Instituto Nacional de Tecnología Agropecuaria (INTA), Córdoba, Argentina

    A. K. Torrico

  2. Estación Experimental Agropecuaria Famaillá, INTA, and Facultad de Agronomía y Zootecnia, Universidad Nacional de Tucumán, Tucumán, Argentina

    S. M. Salazar

  3. Estación Experimental Agropecuaria Famaillá, INTA, Tucumán, Argentina

    D. S. Kirschbaum

  4. Instituto de Patología Vegetal (IPAVE) CIAP-INTA, and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Córdoba, Argentina

    V. C. Conci

Authors
  1. A. K. Torrico
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. M. Salazar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. S. Kirschbaum
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. V. C. Conci
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to V. C. Conci.

Ethics declarations

Authors confirm that this manuscript has not been published elsewhere and is not under consideration by another journal. All authors have approved the manuscript and agree with submission to this Journal.

There are no conflicts of interest and the investigation did not involving human participants and/or animals.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Torrico, A.K., Salazar, S.M., Kirschbaum, D.S. et al. Yield losses of asymptomatic strawberry plants infected with Strawberry mild yellow edge virus . Eur J Plant Pathol 150, 983–990 (2018). https://doi.org/10.1007/s10658-017-1337-z

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-017-1337-z

Keywords

Search

Navigation