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European Journal of Plant Pathology

, Volume 153, Issue 1, pp 211–225 | Cite as

Identification and characterization of Diplodia mutila, D. seriata, Phacidiopycnis washingtonensis and Phacidium lacerum obtained from apple (Malus x domestica) fruit rot in Maule Region, Chile

  • Gonzalo A. DíazEmail author
  • Bernardo A. Latorre
  • Enrique Ferrada
  • Mauricio Lolas
Article
  • 119 Downloads

Abstract

Two members of the family Botryosphaeriaceae (Diplodia mutila and D. seriata), one member of the family Bulgariaceae (Phacidiopycnis washingtonensis) and one member of the family Phacidiaceae (Phacidium lacerum) have been described as fungal plant pathogens causing apple rot during preharvest and/or postharvest. During a survey of apple rot in the commercial orchard cvs. Cripps Pink, Fuji and Gala that was conducted in the 2014–2015 and 2015–2016 seasons in the Maule Region, Chile, 820 isolates were obtained from 880 apple rot samples. Phylogenetic analyses of the internal transcribed spacer (ITS) region, portion of the β-tubulin gene (BT), large ribosomal subunit (LSU) region and small ribosomal subunit (SSU) region identified Diplodia mutila, D. seriata, Phacidiopycnis washingtonensis and Phacidium lacerum. Morphological features of isolates of D. mutila, D. seriata, Pha. washingtonensis and P. lacerum were similar to those described in the literature for the respective species. The isolates of D. mutila, D. seriata, Pha. washingtonensis and P. lacerum were sensitive to fludioxonil, pyrimethanil, tebuconazole and thiabendazole fungicides. The significant largest lesion on apple fruits cv. Cripps Pink were developed, when the fruits were inoculated from 15 days before harvest with Pha. washingtonensis while for D. mutila, D. seriata, P. lacerum was the same day of harvest. The fungal species Pha. washingtonensis and P. lacerum were the most important in developing apple rot (lesions) during cold storage. The specie D. seriata was the most predominant fungus obtained from apple fruit rot in the Maule Region, Chile. This study gives a better insight to the fungal species causing apple fruit rot in the Maule Region, Chile.

Keywords

Etiology Mycology Fungal rot pathogens 

Notes

Acknowledgements

We thank Marcela Cáceres, Catalina Espinosa, Constanza Catalan, Teresa Daza, Katherine Breve, María José Pichuante, Mauricio Gutierrez, and Claudia Pacheco for their invaluable technical support, and we are grateful to the apple commercial orchards of Agrícola San Clemente S. A., Verfrut S.A., Gonzagri S.A. Dole S. A. and Copefrut S.A and the experimental station of Panguilemo of the Universidad of Talca.

Compliance with ethical standards

Ethical approval

This manuscript is original and not published elsewhere. The author discussed the result, read and approved the final article. The authors confirm that there are no ethical issues in publication of the manuscript.

Conflict of interest

The author declare no conflict of interest.

Human and animals studies

This study does not contain studies with human participants or animals performed by any of the authors.

References

  1. Aguilar, C. G., Mazzola, M., & Xiao, C. L. (2017). Timing of apple fruit infection by Neofabraea perennans and Neofabraea kienholzii in relation to bull’s-eye rot development in storage apple fruit. Plant Disease, 101, 800–806.CrossRefGoogle Scholar
  2. Ali, E. Md., Pandit, L. K., Mulvaney, K. A., & Amiri, A. (2018). Sensitivity of Phacidiopycnis spp. isolates from pome fruit to six pre- and postharvest fungicides. Plant Disease, 102, 533–539.Google Scholar
  3. Alvarez, M., Pinilla, B., & Herrera, G. (2004). Enfermedades del manzano. First edition. INIA-La Platina, Ministerio de Agricultura, Santiago, Chile. 71 pp. (in Spanish).Google Scholar
  4. Alves, A., Correia, A., Luque, J., & Phillips, A. J. L. (2004). Botryosphaeria corticola, sp. nov. on Quercus species, with notes and description of Botryosphaeria stevensii and its anamorph, Diplodia mutila. Mycologia, 96, 598–613.CrossRefGoogle Scholar
  5. Alves, A., Correia, A., & Phillips, A. J. L. (2006). Multiple gene genealogies and morphological data support Diplodia cupressi sp. nov., previously recognized as D. pinea f. sp. cupressi, as a distinct species. Fungal Diversity, 23, 1–15.Google Scholar
  6. Arauz, L. F., & Sutton, T. B. (1990). Effect of interrupted wetness periods on spore germination and apple infection by Botryosphaeria obtusa. Phytopathology, 80, 1218–1220.CrossRefGoogle Scholar
  7. Belrose, Inc. (2016). World apple review (p. 2016). USA: Annual world review. Edn. Belrose, Inc. Pullman, WA.Google Scholar
  8. Biggs, A. R., & Miller, S. S. (2004). Relative susceptibility of selected apple cultivars to fruit rot caused by Botryosphaeria obtusa. Hort Science, 39, 303–306.Google Scholar
  9. Brown, E. A., II, & Britton, K. O. (1986). Botryosphaeria diseases of apple and peach in the southeastern United States. Plant Disease, 70, 480–484.CrossRefGoogle Scholar
  10. Cáceres, M., Lolas, M., Gutierrez, M., Ferrada, E., & Díaz, G. A. (2016). Severe outbreak of black rot in apple fruit cv. Fuji caused by Diplodia seriata during pre-harvest in Maule region, Chile. Plant Disease, 100, 2333.CrossRefGoogle Scholar
  11. 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, 98, 636–652.CrossRefGoogle Scholar
  12. Crespo, M., Moral, J., Michailides, T. J., & Trouillas, F. P. (2018). First report of black rot on apple fruit caused by Diplodia seriata in California. Plant Disease, 102, 824.CrossRefGoogle Scholar
  13. Crous, P. W., Slippers, B., Wingfield, M. J., Rheeder, J., Marasas, W. F. O., Phillips, A. J. L., Alves, A., Burgess, T., Barber, P., & Groenewald, J. Z. (2006). Phylogenetic lineages in the Botryosphaeriaceae. Studies in Mycology, 55, 235–253.CrossRefGoogle Scholar
  14. Crous, P. W., Quaedvlieg, W., Hansen, K., Hawksworth, D. L., & Groenewald, J. Z. (2014). Phacidium and Ceuthospora (Phacidiaceae) are congeneric: taxonopmic and nomenclatural implications. IMA Fungus, 5, 173–193.Google Scholar
  15. Delgado-Cerrone, L., Mondino-Hintz, P., & Alaniz-Ferro, S. (2016). Botryosphaeriaceae species associated with stem canker, die-back and fruit rot on apple in Uruguay. European Journal of Plant Pathology, 146, 637–655.CrossRefGoogle Scholar
  16. Díaz, G. A., & Latorre, B. A. (2014). Infection caused by Phaeomoniella chlamydospora associated with esca-like symptoms in grapevine in Chile. Plant Disease, 98, 351–360.CrossRefGoogle Scholar
  17. Díaz, G. A., Zoffoli, J. P., Lolas, M., Blanco, A., Latorre, B. A., Ferrada, E. E., Elfar, K., & Naranjo, P. (2016). Occurrence of Phacidiopycnis washingtonensis causing speck rot on stored pink lady apple fruit in Chile. Plant Disease, 100, 211–212.CrossRefGoogle Scholar
  18. Elfar, K., Zoffoli, J. P., & Latorre, B. A. (2018). Identification and characterization of Alternaria species associated with moldy core apple in Chile. Plant Disease, 102, 2158–2169.CrossRefGoogle Scholar
  19. Elliot, M., Chastagner, G. A., Coats, K. P., Sikdar, P., & Xiao, C. L. (2014). First report of a new leaf blight caused by Phacidiopycnis washingtonensis on Pacific madrone in wester Washington and Oregon. Plant Disease, 98, 1471.Google Scholar
  20. Ferrada, E. E., Lolas, M., Pacheco, C., & Díaz, G. A. (2017). Occurrence of severe outbreak of calyx-end rot associated with Botrytis cinerea in Malus × domestica cv. Cripps pink during harvest in the Maule Region, Chile. Plant Disease, 101, 2149.CrossRefGoogle Scholar
  21. FRAC, Fungicide Resistance Action Committee. (2018). FRAC code list 2018: Fungicides sorted by mode of action. http://www.frac.info. Accessed 15 Mar 2018.
  22. Garibaldi, A., Bertetti, D., Amatulli, M. T., & Gullino, M. L. (2010). First report of postharvest fruit rot in persimmon caused by Phacidiopycnis washingtonensis in Italy. Plant Disease, 94, 788.Google Scholar
  23. Giraud, M. (2009). Le black rot du pommier. Infos-Ctifl, 257, 36–41 (In French).Google Scholar
  24. Glass, N. L., & Donaldson, G. C. (1995). Development of primer set designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Applied and Environmental Microbiology, 61, 1323–1330.Google Scholar
  25. Henriquez, J. L. (2005). First report of apple rot caused by Neofabraea alba in Chile. Plant Disease, 89, 1360.CrossRefGoogle Scholar
  26. Jaklitsch, W. M., Checa, J., Blanco, M. N., Olariaga, I., Tello, S., & Voglmayr, H. (2018). A preliminary account of the Cucurbitariaceae. Studies in Mycology, 90, 71–118.CrossRefGoogle Scholar
  27. Kim, Y. K., & Xiao, C. L. (2006). A postharvest fruit rot in apple caused by Phacidiopycnis washingtonensis. Plant Disease, 90, 1376–1381.CrossRefGoogle Scholar
  28. Kim, Y. K., & Xiao, C. L. (2008). Distribution and incidence of Sphaeropsis rot in apple in Washington state. Plant Disease, 92, 940–946.CrossRefGoogle Scholar
  29. Kim, Y. K., Caiazzo, R., Sikdar, P., & Xiao, C. L. (2013). First report of Sphaeropsis rot of apple caused by Sphaeropsis pyriputrescens in New York. Plant Disease, 97, 1257.CrossRefGoogle Scholar
  30. Kim, Y. K., Curry, E. A., & Xiao, C. L. (2014). Infection of apple fruit by Sphaeropsis pyriputrescens in the orchard in relation to Sphaeropsis rot in storage. European Journal of Plant Pathology, 140, 133–143.CrossRefGoogle Scholar
  31. Kim, Y. K., Kwak, J. H., Aguilar, G., & Xiao, C. L. (2016). First report of black rot on apple fruit caused by Diplodia seriata in Washington State. Plant Disease, 100, 1499.CrossRefGoogle Scholar
  32. Kohn, F. C. J., & Hendrix, F. F. (1982). Temperature, free moisture, and inoculum concentrations effects on the incidence and development of white rot on apples. Phytopathology, 72, 313–316.Google Scholar
  33. Latorre, B. A. (2004). Enfermedades de plantas cultivadas, 6th Edition. Ediciones Universidad Católica de Chile. Santiago, Chile. 638pp. (in Spanish).Google Scholar
  34. Latorre, B. A., & Torres, R. (2012). Prevalence of isolates of Botrytis cinerea resistant to multiple fungicides in Chilean vineyards. Crops Protection , 40, 49–52.Google Scholar
  35. Liu, Q., & Xiao, C. L. (2009). Infection of d’Anjou pear fruit by Potebniamyces pyri in the orchard in relation to Phacidiopycnis rot during storage. Plant Disease, 93, 1059–1064.CrossRefGoogle Scholar
  36. Lolas, M., Contreras, J. M., Méndez, R., Cáceres, M., & Díaz, G. A. (2016). First report of Phytophthora fruit rot in apple caused by Phytophthora syringae during cold storage in Maule Region, Chile. Plant Disease, 100, 1507.CrossRefGoogle Scholar
  37. Phillips, A. J. L., Alves, A., Correia, A., & Luque, J. (2005). Two new species of Botryosphaeria with brown, 1-septate ascospores and Dothiorella anamorphs. Mycologia, 97, 513–529.CrossRefGoogle Scholar
  38. Phillips, A. J. L., Crous, P. W., & Alves, A. (2007). Diplodia seriata, the anamorph of Botryosphaeria obtusa. Fungal Diversity, 25, 141–155.Google Scholar
  39. Phillips, A. J. L., Alves, A., Pennycook, S. R., Johnston, P. R., Ramaley, A., Akulov, A., & Crous, P. W. (2008). Resolving the phylogenetic and taxonomic status of dark-spored teleomorph genera in the Botryosphaeriaceae. Persoonia, 21, 29–55.CrossRefGoogle Scholar
  40. Phillips, A. J. L., Alves, A., Abdollahzadeh, J., Slippers, B., Wingfield, M. J., Groenewald, J. Z., & Crous, P. W. (2013). The Botryosphaeriaceae: Genera and species known from culture. Studies in Mycology, 76, 51–167.CrossRefGoogle Scholar
  41. Sikdar, P., Mazzola, M., & Xiao, C. L. (2014). Infection courts and timing of infection of apples fruit by Phacidiopycnis washingtonensis in the orchard in relation to speck rot during storage. Plant Disease, 98, 1467–1475.CrossRefGoogle Scholar
  42. Slippers, B., Boissin, E., Phillips, A. J. L., Groenewald, J. Z., Lombard, L., Wingfield, M. J., Postma, A., Burgess, T., & Crous, P. W. (2013). Phylogenetic lineages in the Botryosphaeriales: A systematic and evolutionary framework. Studies in Mycology, 76, 31–49.CrossRefGoogle Scholar
  43. Slippers, B., Crous, P. W., Jami, F., Groenewald, J. Z., & Wingfield, M. J. (2017). Diversity in the Botryosphaeriales: Looking back, looking forward. Fungal Biology, 212, 307–321.CrossRefGoogle Scholar
  44. Sutton, T. B., Aldwinckle, H. S., Agnello, A. M., & Walgenbach, J. F. (2014). Compendium of apple and pear diseases and pest (Second ed.p. 218). USA: American Phytopathological Society Press, Minnesota.Google Scholar
  45. Tamura, K., Petersen, D., Petersen, N., Stecher, G., Nei, M., & Kumar, S. (2011). Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739.CrossRefGoogle Scholar
  46. Tang, W., Ding, Z., Zhou, Z. Q., Wang, Y. Z., & Guo, L. Y. (2012). Phylogenetic and pathogenic analyses show that the causal agent of apple ring rot in China is Botryosphaeria dothidea. Plant Disease, 96, 486–496.CrossRefGoogle Scholar
  47. Úrbez-Torres, J. R., Leavitt, G. M., Voegel, T. M., & Gubler, W. D. (2006). Identification and distribution of Botryosphaeria spp. associated with grapevine cankers in California. Plant Disease, 90, 1490–1503.CrossRefGoogle Scholar
  48. Úrbez-Torres, J. R., Peduto, F., Vossen, P. M., Krueger, W. H., & Gubler, W. D. (2013). Olive twig and branch dieback: Etiology, incidence, and distribution in California. Plant Disease, 97, 231–244.CrossRefGoogle Scholar
  49. USDA, United States Department of Agriculture. Foreing Agricultural Services. (2017). Chile: Fresh deciduos fruit annual. http://www.fas.usda.gov. Accessed 10 Dec 2017.
  50. Vilgalys, R., & Hester, M. (1990). Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology, 172, 4238–4246.CrossRefGoogle Scholar
  51. Weber, R. W. S. (2011). Phacidiopycnis washingtonensis, cause of new storage rot of apples in Northern Europe. Journal of Phytopathology, 159, 682–686.CrossRefGoogle Scholar
  52. Weber, R. W. S., & Dralle, N. (2013). Fungi associated with blossom-end rot of apples in Germany. European Journal of Horticultural Science, 78, 97–105.Google Scholar
  53. White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Snisky, & T. J. White (Eds.), PCR, a guide to methods and applications (pp. 315–322). San Diego: Academic Press.Google Scholar
  54. Wiseman, M. S., Dugan, F. M., Kim, Y. K., & Xiao, C. L. (2015). A postharvest fruit rot of apple caused by Lambertella corni-maris in Washington State. Plant Disease, 99, 201–206.CrossRefGoogle Scholar
  55. Wiseman, M. S., Kim, Y. K., Dugan, F. M., Rogers, J. D., & Xiao, C. L. (2016). A new postharvest fruit rot in apple and pear caused by Phacidium lacerum. Plant Disease, 100, 32–39.CrossRefGoogle Scholar
  56. Xiao, C. L., & Sitton, J. W. (2004). Effects of culture media and environmental factors on mycelial growth and pycnidial production of Potebniamyces pyri. Mycological Research, 108, 926–932.CrossRefGoogle Scholar
  57. Xiao, C. L., Rogers, J. D., & Boal, R. J. (2004). First report of a new postharvest fruit rot on apple caused by Sphaeropsis pyriputrescens. Plant Disease, 88, 223.CrossRefGoogle Scholar
  58. Xiao, C. L., Rogers, J. D., Kim, Y. K., & Liu, Q. (2005). Phacidiopycnis washingtonensis-a new species associated with pome fruit from Washington State. Mycologia, 97, 464–473.Google Scholar
  59. Xiao, C. L., Kim, Y. K., & Boal, R. J. (2009). A new canker disease of crabapple trees caused by Phacidiopycnis washingtonensis in Washington State. Plant Health Progress, 10, 43.  https://doi.org/10.1094/PHP-2009-0612-01-BR.CrossRefGoogle Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2018

Authors and Affiliations

  1. 1.Laboratorio de Patología Frutal, Departamento de Producción Agrícola, Facultad de Ciencias AgrariasUniversidad de TalcaTalcaChile
  2. 2.Departamento de Fruticultura y EnologíaPontificia Universidad Católica de ChileSantiagoChile
  3. 3.Instituto de Producción y Sanidad VegetalUniversidad Austral de ChileValdiviaChile

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