Skip to main content
Log in

Characterization of apple cultivar susceptibility to Neofusicoccum parvum Brazilian strains

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Due to climate change, Neofusicoccum parvum is currently emerging as a new pathogen of Rosaceae plant species. This increases the need of gaining knowledge on the pathogenicity of this fungus, particularly on apple cultivars of considerable economic importance. In this study, the virulence and temperature dependence of N. parvum isolates was assayed on ‘Gala’ and ‘Fuji’ apple fruit and wood. At 25 °C and 30 °C, ‘Gala’ fruits showed a higher susceptibility to all fungal strains than ‘Fuji’, whereas low infection severity was shown at 15 °C and 20 °C on both cultivars. Infrared spectroscopy revealed that ‘Fuji’ fruit tissues displayed a higher content of phenolic compounds and pectin esterification degree, as factors possibly correlated with fruit susceptibility. When strain virulence was assayed on wood, no significant difference in susceptibility was detected, as also shown by SEM analysis. The virulence of N. parvum was also tested by assaying the activity of lytic enzymes such as cellulase, polygalacturonase, polymethylgalacturonase, and xylanase.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abou-Mansour, E., Débieux, J. L., Ramírez-Suero, M., Bénard-Gellon, M., Magnin-Robert, M., Spagnolo, A., et al. (2015). Phytotoxic metabolites from Neofusicoccum parvum, a pathogen of Botryosphaeria dieback of grapevine. Phytochemistry. https://doi.org/10.1016/j.phytochem.2015.01.012.

    CAS  PubMed  Google Scholar 

  • Adesemoye, A. O., Mayorquin, J. S., Wang, D. H., Twizeyimana, M., Lynch, S. C., & Eskalen, A. (2014). Identification of species of Botryosphaeriaceae causing bot gummosis in citrus in California. Plant Disease. https://doi.org/10.1094/PDIS-05-13-0492-RE.

    CAS  PubMed  Google Scholar 

  • Amponsah, N. T., Jones, E. E., Ridgway, H. J., & Jaspers, M. V. (2008). Production of Botryosphaeria species conidia using grapevine green shoots. New Zealand Plant Protection, 61, 310–305.

    Google Scholar 

  • Amponsah, N. T., Jones, E. E., Ridgway, H. J., & Jaspers, M. V. (2011). Identifcation, potential inoculum sources and pathogenicity of species of the Botryosphaeriaceae associated with grapevine dieback disease in New Zealand. European Journal of Plant Pathology. https://doi.org/10.1071/AP05018.

    Google Scholar 

  • Ayers, W. A., Papavizas, G. C., Diem, A. F., Durrands, P. K., & Cooper, R. M. (1966). Polygalacturonate transeliminase and polyga-role of pectinases in vascular wilt disease as deterlacturonase production by Rhizoctonia solani. Phytopathology, 56, 1006–1011.

    CAS  Google Scholar 

  • Barros, A. S., Mafra, I., Ferreira, D., Cardoso, S., Reis, A., Lopes de Silva, J. A., et al. (2002). Determination of the degree of methyl esterification of pectic polysaccharides by FT-IR using an outer product PLS1 regression. Carbohydrate Polymers. https://doi.org/10.1016/S0144-8617(02)00017-6.

    CAS  Google Scholar 

  • Baskarathevan, J., Jaspers, M. V., Jones, E. E., & Ridgway, H. J. (2012). Development of isolate-specifc markers for Neofusicoccum parvum and N. luteum and their use to study rainwater splash dispersal in the vineyard. Plant Pathology. https://doi.org/10.1111/j.1365-3059.2012.02675.x.

    Google Scholar 

  • Beckman, T. G., & Reilly, C. C. (2005). Relative susceptibility of peach cultivars to fungal gummosis (Botryosphaeria dothidea). Journal of the American Pomological Society., 59, 111–116.

    Google Scholar 

  • Bertsch, C., Ramirez-Suero, M., Magnin-Robert, M., Larignon, P., Chong, J., Abou-Mansour, E., et al. (2013). Grapevine trunk diseases: Complex and still poorly understood. Plant Pathology. https://doi.org/10.1111/j.1365-3059.2012.02674.x.

    Google Scholar 

  • Bonora, S., Francioso, O., Tugnoli, V., Prodi, A., Di Foggia, M., Righi, V., et al. (2009). Structural characteristics of ‘Hayward’ kiwifruit from elephantiasis-affected plants studied by DRIFT, FT-Raman, NMR, and SEM techniques. Journal of Agricultural and Food Chemistry. https://doi.org/10.1021/jf9002957.

    CAS  PubMed  Google Scholar 

  • Boyer, J., & Liu, R. H. (2004). Apple phytochemicals and their health benefits. Nutrition Journal. https://doi.org/10.1186/1475-2891-3-5.

  • Carlucci, A., Lops, F., Raimondo, M. L., Gentile, V., Mucci, M., & Frisullo, S. (2009). The Botryosphaeria species from vineyards of Apulia. Phytopathologia Mediterranea, 48, 180–180.

    Google Scholar 

  • Chen, S. F., Morgan, D. P., Hasey, J. K., Anderson, K., & Michailides, T. J. (2014). Phylogeny, morphology, distribution, and pathogenicity of Botryosphaeriaceae and Diaporthaceae from English walnut in California. Plant Disease. https://doi.org/10.1094/PDIS-07-13-0706-RE.

    PubMed  Google Scholar 

  • Coakley, S. M., Scherm, H., & Chakraborty, S. (1999). Climate change and plant disease management. Annual Review of Phytopathology. https://doi.org/10.1146/annurev.phyto.37.1.399.

    CAS  PubMed  Google Scholar 

  • Delgado-Cerrone, L., Mondino, P., & Alaniz, S. (2016). Botryosphariaceae species associated with stem canker, die-back and fruit rot on apple in Uruguay. European Journal of Plant Pathology, 146, 637–655. https://doi.org/10.1007/s10658-016-0949-z.

    Article  CAS  Google Scholar 

  • Di Francesco, A., Ugolini, L., D’Aquino, S., Pagnotta, E., & Mari, M. (2017). Biocontrol of Monilinia laxa by Aureobasidium pullulans strains: Insights on competition for nutrients and space. International Journal of Food Microbiology. https://doi.org/10.1016/j.ijfoodmicro.2017.02.007.

    CAS  PubMed  Google Scholar 

  • Di Francesco, A., Mari, M., & Roberti, R. (2018). Defense response against postharvest pathogens in hot water treated apples. Scientia Horticulturae. https://doi.org/10.1016/j.scienta.2017.09.039.

    CAS  Google Scholar 

  • Di Francesco, A., Cameldi, I., Neri, F., Barbanti, L., Folchi, A., Spadoni, A., & Baraldi, E. (2019). Effect of apple cultivars and storage periods on the virulence of Neofabraea spp. Plant Pathology. https://doi.org/10.1111/ppa.13074.

    CAS  Google Scholar 

  • Durrands, P. K., & Cooper, R. M. (1988). Selection and characterization of pectinase-deficient mutans of the vascular wilt pathogen Verticilliumablo-atrum. Physiological and Molecular Plant Pathology. https://doi.org/10.1016/S0885-5765(88)80029-8.

    CAS  Google Scholar 

  • Eriksson, K., & Petterson, B. (1975). Extracellular enzyme system utilized by the fungus Sporotrichum pulverulentum (Chrysosporium lignorum) for the breakdown of cellulose. European Journal of Biochemistry, 51, 193–206.

    CAS  PubMed  Google Scholar 

  • Esteves, A. C., Saraiva, M., Correia, A., & Alves, A. (2014). Botryosphaeriales fungi produce extracellular enzymes with 2 biotechnological potential. Canadian Journal of Microbiology. https://doi.org/10.1139/cjm-2014-0134.

    CAS  PubMed  Google Scholar 

  • Fernandes, I., Alves, A., Correia, A., Devreese, B., & Esteves, A. C. (2014). Secretome analysis identifies potential virulence factors of Diplodia corticola, a fungal pathogen involved in cork oak (Quercus suber) decline. Fungal Biology. https://doi.org/10.1016/j.funbio.2014.04.006.

    CAS  PubMed  Google Scholar 

  • Hansen, J., Sato, M., Kharecha, P., Russell, G., Lea, D. W., Siddall, M. (2007). Climate change and trace gases. Philosophical transactions. Series A, mathematical, physical, and engineering sciences, https://doi.org/10.1098/rsta.2007.2052.

    CAS  Google Scholar 

  • Heneczowski, M., Kopacz, M., Nowak, D., & Kuzniar, A. (2001). Infrared spectrum analysis of some flavonoids. Acta Poloniae Pharmaceutica, 58, 415–420.

    Google Scholar 

  • Iotti, M., & Zambonelli, A. (2006). A quick and precise technique for identifying ectomycorrhizas by PCR. Mycological Research, 110, 60–65.

    CAS  PubMed  Google Scholar 

  • Javier-Alva, J., Gramaje, D., Alvarez, L. A., & Armengol, J. (2009). First report of Neofusicoccum parvum associated with dieback of mango trees in Peru. Plant Disease. https://doi.org/10.1094/PDIS-93-4-0426B.

    CAS  PubMed  Google Scholar 

  • Khon, F. C., & Hendrix, F. F. (1983). Influence of sugar content and pH on development of white rot on apples. Plant Disease, 67, 410–412.

    Google Scholar 

  • Kikot, G. E., Hours, R. A., & Alconada, T. M. (2009). Contribution of cell wall degrading enzymes to pathogenesis of Fusarium graminearum: A review. Journal of Basic Microbiology. https://doi.org/10.1002/jobm.200800231.

    CAS  PubMed  Google Scholar 

  • Lambert, C., Bisson, J., Waffo-Teguo, P., Papastamoulis, Y., Richard, T., Corio-Costet, M. F., et al. (2012). Phenolics and their antifungal role in grapevine wood decay: Focus on the Botryosphaeriaceae family. Journal of Agricultural and Food Chemistry. https://doi.org/10.1021/jf303290g.

    CAS  PubMed  Google Scholar 

  • Lionetti, V., Cervone, F., & Bellincampi, D. (2012). Methyl esterification of pectin plays a role during plant-pathogen interactions and affects plant resistance to diseases. Journal of Plant Physiology. https://doi.org/10.1016/j.jplph.2012.05.006.

    CAS  PubMed  Google Scholar 

  • Luque, J., Martos, S., Aroca, A., Raposo, R., & Garcia-Figueres, F. (2009). Symptoms and fungi associated with declining mature grapevine plants in Northeast Spain. Journal of Plant Pathology. https://doi.org/10.4454/jpp.v91i2.968.

  • Marques, M. W., Lima, N. B., Morais Jr., M. A., Barbosa, M. A. G., Souza, B. O., Michereff, S. J., et al. (2013). Species of Lasiodiplodia associated with mango in Brazil. Fungal Diversity. https://doi.org/10.1007/s13225-013-0231-z.

    Google Scholar 

  • Melzer, R. R., & Berton, O. (1986). Incidência de Botryosphaeria berengeriana cultura da macieira (Malus domestica) no estado de Santa Catarina, Brasil. Fitopatologia Brasileira., 11, 891–898.

    Google Scholar 

  • Molina-Gayosso, E., Silva-Rojas, H. V., García-Morales, S., & Avila-Quezada, G. (2012). First report of black spots on avocado fruit caused by Neofusicoccum parvum in Mexico. Plant Disease. https://doi.org/10.1094/PDIS-08-11-0699.

    CAS  PubMed  Google Scholar 

  • Mugnai, L., Surico, G., & Sfalanga, A. (1997). Produzione di enzimi esocellulari da parte di funghi del legno di viti colpite da “mal dell’esca”. Micologia italiana., 1, 11–22.

    Google Scholar 

  • Mugnai, L., Graniti, A., & Surico, G. (1999). Esca (black measles) and brown wood streaking two old and elusive diseases of grapevines. Plant Disease. https://doi.org/10.1094/PDIS.1999.83.5.404.

    CAS  PubMed  Google Scholar 

  • Pérez, C. A., Wingfield, M. J., Slippers, B., Altier, N. A., & Blanchette, R. A. (2010). Endophytic and canker-associated Botryosphaeriaceae occurring on non-native Eucalyptus and native Myrtaceae trees in Uruguay. Fungal Diversity. https://doi.org/10.1007/s13225-009-0014-8.

    Google Scholar 

  • Phillips, A. J. L., Alves, A., Abdollahzadeh, J., Slippers, B., Wingfield, M. J., Groenewald, J. Z., et al. (2013). The Botryosphaeriaceae: Genera and species known from culture. Studies in Micology. https://doi.org/10.3114/sim0021.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Prodorutti, D., Cainelli, C., Gualandri, V., Profaizer, D., Dallago, A., Branz, A., et al. (2012). Moria e deperimento del melo in Trentino. Atti Giornate Fitopatologiche, 2, 619–620.

    Google Scholar 

  • Ramírez-Suero, M., Chong, J., Farine, S., Kiefe-Mazet, F., Pensec, F., Gacougnole, I., et al. (2012). Effect of Neofusicoccum parvum and Diplodia seriata extra-cellular compounds on defence gene expression in Vitis vinifera cv. Chardonnay and cv. Gewurztraminer. Phytopathologia Mediterranea, 51, 438–438.

    Google Scholar 

  • Sakalidis, M. L., Hardy, G. E. S. J., & Burgess, T. I. (2011). Class III endophytes, clandestine movement amongst hosts and habitats and their potential for disease; a focus on Neofusicoccum australe. Australasian Plant Pathology, 40, 510–521. https://doi.org/10.1007/s13313-011-0077-3.

    Article  Google Scholar 

  • Sakalidis, M. L., Slippers, B., Wingfield, B. D., G. E. St. J. Hardy, Burgess, T. I. (2013). The challenge of understanding the origin, pathways and extent of fungal invasions: global populations of the Neofusicoccum parvumN. ribis species complex. Diversity and Distributions, https://doi.org/10.1111/ddi.12030.

    Google Scholar 

  • Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH image to ImageJ: 25 years of image analysis. Nature Methods, 9, 671–675 PMID: 22930834.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schulz, H., & Baranska, M. (2007). Identification and quantification of valuable plant substances by IR and Raman spectroscopy. Vibrational Spectroscopy. https://doi.org/10.1016/j.vibspec.2006.06.001.

    CAS  Google Scholar 

  • Slippers, B., & Wingfield, M. J. (2007). Botryosphaeriaceae as endophytes and latent pathogens of woody plants: Diversity, ecology and impact. Fungal Biology Reviews. https://doi.org/10.1016/j.fbr.2007.06.002.

    Google Scholar 

  • Slippers, B., Smit, A., Crous, P. W., Countinho, T. A., Wingfield, B. D., & Wingfield, M. J. (2007). Taxonomy, phylogeny and identification of Botryosphaeriaceae associated with pome and stone fruit trees in South Africa and other regions of the world. Plant Pathology. https://doi.org/10.1111/j.1365-3059.2006.01486.x.

  • Slippers, B., Boissin, E., Phillips, A. J. L., Groenewald, J. Z., Wingfield, M. J., Postma, A., et al. (2013). Phylogenetic lineages in the Botryosphaeriales: A systematic and evolutionary framework. Studies in Mycology, https://doi.org/10.3114/sim0020.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Spagnolo, A., Marchi, G., Peduto, F., Phillips, A. J. L., & Surico, G. (2011). Detection of Botryosphaeriaceae species within grapevine woody tissues by nested PCR, with particular emphasis on the Neofusicoccum parvum/N. ribis complex. European Journal of Plant Pathology. https://doi.org/10.1007/s10658-010-9715-9.

    Google Scholar 

  • Spagnolo, A., Larignon, P., Magnin-Robert, M., Hovasse, A., Cilindre, C., Van Dorsselaer, A., et al. (2014). Flowering as the most highly sensitive period of grapevine (Vitis vinifera L. cv Mourvèdre) to the Botryosphaeria dieback agents Neofusicoccum parvum and Diplodia seriata infection. International Journal of Molecular Sciences. https://doi.org/10.3390/ijms15069644.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Spotts, R. A., Cervantes, L. A., & Mielke, E. A. (1999). Variability in postharvest decay among apple cultivars. Plant Disease. https://doi.org/10.1094/PDIS.1999.83.11.1051.

    CAS  PubMed  Google Scholar 

  • Srivastava, P., Andersen, P. C., Marois, J. J., Wright, D. L., Srivastava, M., & Harmon, P. F. (2013). Effect of phenolic compounds on growth and ligninolytic enzyme production in Botryosphaeria isolates. Crop Protection. https://doi.org/10.1016/j.cropro.2012.09.015.

    CAS  Google Scholar 

  • St Leger, R. J., Joshi, L., & Roberts, D. W. (1997). Adaptation of proteases and carbohydrases of saprophytic: Phytopathogenic and entomopathogenic fungi to the requirements of their ecological niches. Microbiology, 143, 1983–1992.

    CAS  PubMed  Google Scholar 

  • Stempien, E. (2017). Grapevine Botryosphaeria dieback fungi have specific aggressiveness factor repertory involved in wood decay and stilbene metabolization. PLoS One. https://doi.org/10.1371/journal.pone.0188766.

    PubMed  PubMed Central  Google Scholar 

  • Synytsya, A., Copikova, J., Matejka, P., & Machovic, V. (2003). Fourier transform Raman and infrared spectroscopy of pectins. Carbohydrate Polymers. https://doi.org/10.1016/S0144-8617(03)00158-9.

    CAS  Google Scholar 

  • Taylor, A., Hardy, G. E. St. J., Wood, P., & Burgess, T. (2005). Identification and pathogenicity of Botryosphaeria species associated with grapevine decline in Western Australia. Australasian Plant Pathology. https://doi.org/10.1071/AP05018.

    Google Scholar 

  • Úrbez-Torres, J. R. (2011). The status of Botryosphaeriaceae species infecting grapevines. Phytopathologia Mediterranea. https://doi.org/10.14601/Phytopathol_Mediterr-9316.

  • Vallette-Collet, O., Cimerman, A., Reignault, P., Levis, C., & Boccara, M. (2003). Disruption of Botrytis cinerea pectin methyl esterase gene Bcpme I reduces virulence on several host plants. Molecular Plant-Microbe Interactions. https://doi.org/10.1094/MPMI.2003.16.4.360.

    CAS  PubMed  Google Scholar 

  • Yang, Y. L., Turner, J., Stephens, J., Campbell, R. E., & Walter, M. (2017). Comparison of in vitro and in planta sporogenesis in Neofusicoccum species from blueberry. New Zealand Plant Protection, 70, 203–208.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. Baraldi.

Ethics declarations

Conflict of interest

This work was not financed by grants. The authors declare no conflict of interest. This article does not contain any work conducted on animal or human participants.

Electronic supplementary material

ESM 1

(DOCX 171 kb)

ESM 2

(DOCX 343 kb)

ESM 3

(DOCX 39 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Di Francesco, A., Rusin, C., Di Foggia, M. et al. Characterization of apple cultivar susceptibility to Neofusicoccum parvum Brazilian strains. Eur J Plant Pathol 156, 939–951 (2020). https://doi.org/10.1007/s10658-020-01945-7

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-020-01945-7

Keywords

Navigation