The Effect of PPV Virus (Plum Pox Virus) on Phytohormonal Changes in Stone Fruit Trees: A Case Study of Peach, Apricot, Plum, and Almond

Document Type : Research Article

Authors

1 Research and Technology Institute of Plant Production, Afzalipour Research Institute, Shahid Bahonar University of Kerman

2 Department of Plant Breeding, CEBAS-CSIC, PO Box 164, E-30100 Espinardo, Murcia, Spain

Abstract

Sharka disease, caused by plum pox virus (PPV), is one of the most important and destructive viral diseases of stone fruit trees of the genus Prunus. This study aimed to investigate the effect of PPV infection on hormonal profile in stone fruit trees including peach, apricot, plum, and almond. The method of investigation included measurement of the concentration of some plant hormones using high-performance liquid chromatography (HPLC) techniques. The results showed that inoculation with PPV-D virus resulted in a decrease in cytokinin tZ concentration in all plants examined. This decrease was significant in "GF305" peach. Also, the concentration of isopentenyl adenine (iP) in "Real fino" apricot increased significantly after inoculation. GA1 concentration was observed only in the control "Pollizo" plum. GA3 concentrations significantly decreased in the inoculated "Garrigues" almonds and "Pollizo" plums. GA4 concentrations in "Rojo Pasión" apricot and "GF305" peach were lower in infected plants than in the control, but "Z506-7" apricot showed a significant increase after inoculation. "Garrigues" almond, "Z506-7" apricot and "GF305" peach showed a significant increase in IAA concentrations after inoculation. ABA concentrations in infected "Real fino" and "GF305" and SA concentrations in infected "Garrigues", "Real fino" and "Pollizo" significantly increased. In "GF305", JA concentration in the infected treatment was significantly reduced compared to the control treatment. Conversely, in "Garrigues" and "Pollizo", JA concentrations in the infected treatments was significantly increased. The results of this study showed that PPV infection can have different effects on the hormonal profile of stone fruit trees depending on the species

Keywords

References

  1. Ádám A.L., Nagy Z.Á., Kátay G., Mergenthaler E. and Viczián O. 2018. Signals of Systemic Immunity in Plants: Progress and Open Questions. International Journal of Molecular Science. 10;19(4):1146. doi: 10.3390/ijms19041146.
  2. Alazem M. and Lin S. 2015. Roles of plant hormones in the regulation of host-virus interactions. Molecular plant pathology 16(5):529-540. doi: 10.1111/mpp.12204.
  3. Albacete A., Ghanem M.E., Martínez-Andujar C., Acosta M., Sánchez-Bravo J., Martínez V., Lutts S., Dodd I.C. and Pérez-Alfocea F. 2008. Hormonal changes in relation to biomass partitioning and shoot growth impairment in salinized tomato plants. Journal of experimental botany 59: 4119-4131.
  4. Albacete A., Martínez-Andújar M.E., Ghanem M.E., Acosta M., Sánchez-Bravo J., Asins M.J., Cuarter J., Lutts I.C., Dodd I.C. and Pérez-Alfocea F. 2009. Rootstock-mediated changes in xylem ionic and hormonal status are correlated with delayed leaf senescence, and increased leaf area and crop productivity in salinized tomato. Plant, Cell and Environment 32: 958-938.
  5. Asensio, M., 1996. El virus de la Sharka (Plum pox virus). Caracterizacio´n, diagno´ stico y deteccio´n mediante anticuerpos monoclonales especı´ficos. Tesis Doctoral. Universidad Polite´cnica de Valencia, p. 223 (Spanish)
  6. Baebler Š., Witek K., Petek M., Stare K., Tušek-Žnidarič M., Pompe-Novak M., Renaut J., Szajko K., Strzelczyk-Żyta D., Marczewski W., Morgiewicz K., Gruden K. and Hennig J. 2014. Salicylic acid is an indispensable component of the Ny-1 resistance-gene-mediated response against Potato virus Y infection in potato. Journal of Experimental Botany 65(4):1095-1109. doi: 10.1093/jxb/ert447.
  7. Barba M., Ilardi V. and Pasquini G. 2015. Control of pome and stone fruit virus diseases. In Advances in virus research. Academic Press 91: 47-83.
  8. Bari R and Jones D. 2009. Role of plant hormones in plant defence responses. Plant molecular biology 69(4): 473-88. doi: 10.1007/s11103-008-9435-0.
  9. Bernhard R., Marénaud C. and Sutic D. 1969. Le pêcher GF305 indicateur polyvalent des virus des espèces à noyaux. Annual phytopathology 1: 603-617.
  10. Canton M., Forestan C., Bonghi C. and Varotto2021. Meta-analysis of RNA-Seq studies reveals genes with dominant functions during flower bud endo- to eco-dormancy transition in Prunus species. Science Reports 11, 13173. https://doi.org/10.1038/s41598-021-92600-6.  
  11. Chirkov S., Sheveleva A., Ivanov P. and Zakubanskiy A. 2018. Analysis of genetic diversity of Russian sour cherry plum pox virus isolates provides evidence of a new strain. Plant Disease 102: 569-575. https://doi.org/10. 1094/PDIS-07-17-1104-RE.
  12. Clarke J.D., Volko S.M., Ledford H., Ausubel F.M. and Dong X. 2014. Roles of salicylic Acid, jasmonic acid, and ethylene in CPR-induced resistance in Arabidopsis. The Plant Cell 12: 2175-2190.
  13. Collum T.D. and Culver J. 2016. The impact of phytohormones on virus infection and disease. Current Opinion in Virology 17: 25-31.
  14. Collum TD, Stone AL, Sherman DJ, Rogers EE, Dardick C and Culver JN. 2020. Translatome profiling of plum pox virus-infected leaves in European plum reveals temporal and spatial coordination of defense responses in phloem tissues. Molecular Plant Microbe interactions 33(1):66-77. doi: 10.1094/MPMI-06-19-0152-FI.
  15. Damsteegt V.D., Scorza R., Stone A.L., Schneider W.L., Webb K., Demuth M. and Gil-dow F.E. 2007. Prunus host range of Plum pox virus (PPV) in the United States by aphid and graft inoculation. Plant Disease 91: 18-23.
  16. Dehkordi A.N., Rubio M., Babaeian N., Albacete A. and Martínez-Gómez P. 2018. Phytohormone signaling of the resistance to plum pox virus (PPV, sharka disease) induced by almond (Prunus dulcis (Miller) Webb) grafting to peach (P. persica L. Batsch). Viruses 3;10(5):238. doi: 10.3390/v10050238.
  17. Denancé N., Sánchez-Vallet A., Goffner D. and Molina A. 2013. Disease resistance or growth: The role of plant hormones in balancing immune responses and fitness costs. Frontiers of plant science 24; 4:155. doi: 10.3389/fpls.2013.00155.
  18. Dermastia, Nikolic P., Chersicola M. and Gruden K. 2015. Transcriptional profiling in infected and recovered grapevine plant responses to’ Candidatus Phytoplasma solani’. Phytopathogenic Mollicutes 5. S123. 10.5958/2249-4677.2015.00053.5.
  19. Ding P. and Ding Y. 2020. Stories of Salicylic Acid: A Plant Defense Hormone. Trends Plant Science. 25(6):549-565. doi: 10.1016/j.tplants.2020.01.004.
  20. DolgovV., Kulikov I.M. and Burmenko Y.V. 2022. Modern bioengineering approaches to creating resistance to the Plum pox virus in stone fruit crops. Horticulture and Viticulture DOI:10.31676/0235-2591-2022-2-6-13.
  21. El-Sharkawy , Sherif S., Abdulla M. and Jayasankar S. 2017. Plum fruit development occurs via gibberellin-sensitive and -insensitive DELLA repressors. PLoS One 11;12(1): e0169440. doi: 10.1371/journal.pone.0169440.
  22. EPPO (2022) https://gd.eppo.int/taxon/PPV000/distribution.
  23. Espinoza C., Bascou B., Calvayrac C. and Bertrand C. 2021. Deciphering Prunus responses to PPV Infection: A way toward the use of metabolomics approach for the diagnostic of sharka disease. Metabolites 11(7), 465.‏ doi: 10.3390/metabo11070465.
  24. García J.A., Glasa M., Cambra M. and Candresse T. 2014. Plum pox virus and sharka: a model potyvirus and a major disease. Molecular plant pathology 15: 226-241.
  25. Ilardi V. and Tavazza M. 2015. Biotechnological strategies and tools for Plum pox virus resistance: Trans-, intra-, cis-genesis, and beyond. Frontiers of plant science. 8; 6:379. doi: 10.3389/fpls.2015.00379. 
  26. James D., Varga A. and Sanderson D. 2013. Genetic diversity of plum pox virus: Strains, disease and related challenges for control. Canadian Journal of Plant Pathology 35: 431-441. https://doi.org/10.1080/07060661.2013. 828100.
  27. Kazan and Manners J.M. 2009. Linking development to defense: auxin in plant-pathogen interactions. Trends in Plant Science 14(7): 373-82. doi: 10.1016/j.tplants.2009.04.005.
  28. Kumar , Khurana A. and Sharma A.K. 2014. Role of plant hormones and their interplay in development and ripening of fleshy fruits. Journal of Experimental Botany 65(16): 4561-75. doi: 10.1093/jxb/eru277.
  29. Martínez-Gómez P., Dicenta F. and Audergon J.M. 2000. Behaviour of apricot (Prunus armeniaca L.) cultivars in presence of sharka (plum pox virus): a review. Agronomie 20: 407-422
  30. Milošević T., Milošević N., Mladenović J. and Jevremović, D. 2019. Impact of Sharka disease on tree growth, productivity and fruit quality of apricot (Prunus armeniaca). Scientia Horticulturae 244: 270-276.‏
  31. Nachappa , Challacombe J., Margolies D.C., Nechols J.R., Whitfield A.E. and Rotenberg D. 2020. Tomato spotted wilt virus benefits its thrips vector by modulating metabolic and plant defense pathways in tomato. Frontiers of plant science 18;11:575564. doi: 10.3389/fpls.2020.575564.
  32. Naseem , Kaltdorf M. and Dandekar T. 2015. The nexus between growth and defence signalling: auxin and cytokinin modulate plant immune response pathways. Journal of experimental botany 66(16): 4885-96. doi: 10.1093/jxb/erv297.
  33. Nikbakht-Dehkordi A., Rubio, M., Babaeian, N., Albacete, A., & Martínez-Gómez, P. (2018). Phytohormone signaling of the resistance to plum pox virus (PPV, sharka disease) induced by almond (Prunus dulcis (Miller) Webb) grafting to peach (P. persica L. Batsch). Viruses, 10(5), 238.‏ doi: 3390/v10050238.
  34. Nikbakht-Dehkordi, A., & Martínez-Gómez, P. (2024). Phytohormones and Plant Defense. Journal of Plant Molecular Breeding, (2), -. doi: 10.22058/jpmb.2024.2045628.1313.
  35. Nwugo C., Lin H., Duan Y. and Civerolo E.L. 2013. The effect of 'Candidatus Liberibacter asiaticus' infection on the proteomic profiles and nutritional status of pre-symptomatic and symptomatic grapefruit (Citrus paradisi) plants. BMC Plant biology 11; 13:59. doi: 10.1186/1471-2229-13-59.
  36. Ozga J. and Reinecke 2003. Hormonal Interactions in Fruit Development. Journal of Plant Growth Regulation 22: 73-81.
  37. Park Y.D., Boe A.A. and Ehlenfeldt M.K. 1992. Effect of indole acetic acid (IAA) and zeatin riboside on shoot induction from solanum tuberosum l. leaf disks cultured in vitro and variation of the regenerated plants. Hortscience 27(6): 695d-695
  38. Pedrelli A., Panattoni A. and Cotrozzi L. 2024. The sharka disease on stone fruits in Italy: a review, with a focus on Tuscany. European Journal of Plant Pathology 169: 287-300.‏
  39. Pertry , Václavíková K., Depuydt S., Galuszka P., Spíchal L., Temmerman W., Stes E., Schmülling T., Kakimoto T., Van Montagu M.C., Strnad M., Holsters M., Tarkowski P. and Vereecke D. 2009. Identification of Rhodococcus fascians cytokinins and their modus operandi to reshape the plant. Proceedings of the National Academy of Sciences of the United States of America 106(3): 929-934. doi: 10.1073/pnas.0811683106.
  40. Pieterse C.M.J., van der Does D., Zamioudis C., León-Reyes A. and van Wees S.C.M. 2012. Hormonal Modulation of Plant Immunity. Annual Review of Cell and Developmental Biology 28: 489-521.
  41. Porcel L., Picca C., Fuentes C. and Ojeda E. 2018. Plum pox virus (PPV) dispersion in plum trees (Prunus domestica. L) CV. D’Agen. Journal of Pharmacy and Pharmacology 6: 268-273.‏
  42. Robert-Seilaniantz, Grant M. and Jones J.D. 2011. Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annual review of phytopathology 49: 317-43.
  43. Robischon 2015. Do cytokinins function as two-way signals between plants and animals? Cytokinins may not only mediate defence reactions via secondary compounds, but may directly interfere with developmental signals in insects. BioEssays 37(4): 356-63. doi: 10.1002/bies.201400099.
  44. Rodamilans B., Valli A. and García, J.A. 2020. Molecular plant-plum pox virus interactions. Molecular Plant-Microbe Interactions 33(1): 6-17.‏
  45. Rubio M., García-Ibarra A., Martínez-Gómez P. and Dicenta F. 2009. Analysis of the main factors involved in the evaluation of Prunus resistance to Plum pox virus (Sharka) in control greenhouse conditions. Scientia horticulturae 123: 46-50.
  46. Rubio M., Martínez-García P.J., Martinez-Gomez, P. and Dicenta, F. 2024. Plum pox virus (sharka) resistance in peach by grafting 'Garrigues' almond as interstock. Scientia Horticulturae 338, DOI:1016/j.scienta.2024.113749.
  47. Rubio, Martínez-Gómez P. and Dicenta F. 2003. Resistance of almond cultivars to Plum pox virus (sharka). Plant Breeding. 122: 462-464.
  48. Rubio, Martinez-Gomez P., Marais A., Sánchez-Navarro J., Pallás V. and Candresse T. 2017. Recent advances and prospects in Prunus virology. Annals of Applied Biology 171. 10.1111/aab.12371.
  49. Rubio, M., Martínez-García, P. J., Nikbakht-Dehkordi, A., Prudencio, Á. S., Gómez, E. M., Rodamilans, B., Dicenta, F., García, J. A., & Martínez-Gómez, P. (2021). Gene Expression Analysis of Induced Plum pox virus(Sharka) Resistance in Peach (Prunus persica) by Almond ( dulcis) Grafting. International Journal of Molecular Sciences, 22(7), 3585. https://doi.org/10.3390/ijms22073585
  50. Sheveleva A., Ivanov P., Gasanova T., Osipov G. and Chirkov S. 2018. Sequence analysis of plum pox virus strain C isolates from Russia revealed prevalence of the D96E Mutation in the universal epitope and interstrain recombination events. Viruses 10, 450. https://doi.org/10.3390/ v10090450.
  51. Sidorova T., Mikhailov R., Pushin A., Miroshnichenko D. and Dolgov S. 2019. Agrobacterium-mediated transformation of russian commercial plum cv. "Startovaya" (Prunus domestica) with virus-derived hairpin rna construct confers durable resistance to PPV infection in mature plants. Front Plant Sci. 12; 10:286. doi: 10.3389/fpls.2019.00286.
  52. Sidorova T., Mikhailov R.V., Pushin A.S., Miroshnichenko D. and Dolgov S.V. 2022. Interference inhibition of Plum pox virus, induced by a hairpin-RNA of viral origin, provides long-term resistance to PPV infection in adult plants of the Startovaya (Prunus domestica) variety. Horticulture and viticulture.
  53. Sutaoney P, Pandey D, Joshi V, Vyas A, Joshi N, Shah K, Chauhan NS (2023) Use of plant-defense hormones against pathogen diseases. In Hormonal Cross-Talk, Plant Defense and Development (pp. 305-334). Academic Press.‏
  54. Vlot C., Dempsey D.A. and Klessig D.F. 2009. Salicylic Acid, a multifaceted hormone to combat disease. Annual review of phytopathology 47: 177-206.
  55. Wang L., Li H. and Ecker J.R. 2002. Ethylene biosynthesis and signaling networks. The Plant Cell 14 Suppl(Suppl):S131-51. doi: 10.1105/tpc.001768.
  56. Wasternack C. and Hause 2013. Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Annals of Botany 111 (6): 1021-1058, https://doi.org/10.1093/aob/mct067.
  57. Yand Y.X., Ahammed G.J., Wu C., Fan S. and Zhou Y.H. 2015. Crosstalk among jasmonate, salicylate and ethylene signaling pathways in plant disease and immune responses. Current Protein and Peptide Science 16: 450-461.
  58. Zhang , Zhang F., Melotto M., Yao J. and He S.Y. 2017. Jasmonate signaling and manipulation by pathogens and insects. Journal of Experimental Botany 68(6):1371-1385. doi: 10.1093/jxb/erw478.
Iranian Journal of Plant Pathology
Volume 60, Issue 1
April 2025
Pages 60-78

Files

Share

How to cite

Statistics