European Journal of Plant Pathology

, Volume 143, Issue 4, pp 737–752 | Cite as

Identification and distribution of Botryosphaeriaceae species associated with blueberry stem blight in China

Article

Abstract

Blueberry (Vaccinium corymbosum) has developed rapidly in China over the past 20 years because of its perceived health and nutritional benefits. Blueberry stem blight, caused by fungi in the family Botryosphaeriaceae, is the most destructive disease affecting blueberry production and quality worldwide. A field survey of 20 blueberry plantations in eight provinces across China was conducted to determine the occurrence and distribution of Botryosphaeriaceae species. In total, 69 Botryosphaeriaceae isolates associated with blueberry twig dieback and stem blight were identified based on morphological characteristics and analyses of nucleotide sequences of three genomic regions: the internal transcribed spacer region (ITS1-5.8S-ITS2), a partial sequence of the β-tubulin gene, and part of the translation elongation factor 1-α gene (EF1-α). Three species were identified, including: Botryosphaeria dothidea, Neofusicoccum parvum and Lasiodiplodia theobromae. Botryosphaeria dothidea and N. parvum were the most prevalent species and were widely distributed in all blueberry-growing regions. In contrast, L. theobromae was only found in southeastern regions. Koch’s postulates showed all three species to be pathogenic when inoculated with mycelial plugs on detached and intact blueberry stems (cv. Bluecrop). Pathogenicity tests showed N. parvum and L. theobromae to be more virulent than B. dothidea. To our knowledge, this study is the first comprehensive description for morphology, phylogenetic analysis, and distribution of Botryosphaeriaceae spp. as causal agents of blueberry stem blight in China.

Keywords

Blueberry (Vaccinium corymbosumStem blight Botryosphaeriaceae Pathogenicity Distribution 

References

  1. Abdollahzadeh, J., Javadi, A., Goltapeh, M. G., Zare, R., & Phillips, A. J. L. (2010). Phylogeny and morphology of four new species of Lasiodiplodia from Iran. Persoonia, 25, 1–10.PubMedCentralCrossRefPubMedGoogle Scholar
  2. 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, 98, 55–61.CrossRefGoogle Scholar
  3. Alves, A., Correia, A., & Phillips, A. J. L. (2006). Multi-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
  4. Alves, A., Crous, P. W., Correia, A., & Phillips, A. J. L. (2008). Morphological and molecular data reveal cryptic speciation in Lasiodiplodia theobromae. Fungal Diversity, 28, 1–13.Google Scholar
  5. Barr, M. E. (1987). Prodromus to Class Loculoascomycetes. Amherst: Hamilton I. Newell, Inc.Google Scholar
  6. Baskarathevan, J., Jaspers, M., & Jones, E. (2012). Genetic and pathogenic diversity of Neofusicoccum parvum in New Zealand vineyards. Fungal Biology, 116, 276–288.CrossRefPubMedGoogle Scholar
  7. Carbone, I., Anderson, J. B., & Kohn, L. M. (1999). A method for designing primer sets for the speciation studies in filamentous ascomycetes. Mycologia, 91, 553–556.CrossRefGoogle Scholar
  8. Chen, S. F., Morgan, D. P., Beede, R. H., & Michailides, T. J. (2013). First report of Lasiodiplodia theobromae associated with stem canker of almond in California. Plant Disease, 97(7), 994.CrossRefGoogle Scholar
  9. 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
  10. Choi, I. Y. (2011). First report of bark dieback on blueberry caused by Botryosphaeria dothidea in Korea. Plant Disease, 95(2), 227.CrossRefGoogle Scholar
  11. Crous, P. W., Slippers, B., Wingfield, M. J., Rheeder, J., Marasas, W. F. O., Philips, A. J. L., Alves, A., Burgess, T., Barber, P., & Groenwald, J. Z. (2006). Phylogenetic lineages in the Botryosphaeriaceae. Studies in Mycology, 55, 235–253.PubMedCentralCrossRefPubMedGoogle Scholar
  12. Denman, S., Crous, P. W., Taylor, J. E., Kang, J.-C., Pascoe, I., & Wingfield, M. J. (2000). An overview of the taxonomic history of Botryosphaeria, and a re-evaluation of its anamorphs based on morphology and ITS rDNA phylogeny. Studies in Mycology, 45, 129–140.Google Scholar
  13. Elfar, K., Torres, R., Díaz, G. A., & Latorre, B. A. (2013). Characterization of Diaporthe australafricana and Diaporthe spp. associated with stem canker of blueberry in Chile. Plant Disease, 97, 1042–1050.CrossRefGoogle Scholar
  14. Espinoza, J. G., Briceño, E. X., Keith, L. M., & Latorre, B. A. (2008). Canker and twig dieback of blueberry caused by Pestalotiopsis spp. and a Truncatella sp. in Chile. Plant Disease, 92, 1407–1414.CrossRefGoogle Scholar
  15. Espinoza, J. G., Briceño, E. X., Chávez, E. R., Úrbez-Torres, J. R., & Latorre, B. A. (2009). Neofusicoccum spp. associated with stem canker and dieback of blueberry in Chile. Plant Disease, 93, 1187–1194.CrossRefGoogle Scholar
  16. Glass, N. L., & Donldson, G. C. (1995). Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Applied and Environmental Microbiology, 61, 1323–1330.PubMedCentralPubMedGoogle Scholar
  17. Jacobs, K. A., & Rehner, S. A. (1998). Comparisons of cultural and morphological characters and ITS sequences in anamorphs of Botryosphaeria and related taxa. Mycologia, 90, 601–610.CrossRefGoogle Scholar
  18. Kong, C. S., Qiu, X. L., Yi, K. S., Yu, X. F., & Yu, L. (2010). First report of Neofusicoccum vitifusiforme causing blueberry blight of blueberry in China. Plant Disease, 94(11), 1373.CrossRefGoogle Scholar
  19. Li, L. M., & Wu, L. (2011). The research on development of blueberry industry in China. Beijing: China Agriculture Press.Google Scholar
  20. Marques, M. W., Lima, N. B., Morais, M. A., Jr., Barbosa, M. A. G., Souza, B. O., Michereff, S. J., Phillips, A. J. L., & Câmara, M. P. S. (2013). Species of Lasiodiplodia associated with mango in Brail. Fungal Diversity, 61, 181–193.CrossRefGoogle Scholar
  21. McDonald, V., & Eskalen, A. (2011). Botryosphaeriaceae species associated with avocado branch cankers in California. Plant Disease, 95, 1465–1473.CrossRefGoogle Scholar
  22. Milholland, R. D. (1972). Histopathology and pathogenicity of Botryosphaeria dothidea on blueberry stems. Phytopathology, 62, 654–660.CrossRefGoogle Scholar
  23. Moral, J., Muñoz-Díez, C., González, N., Trapero, A., & Michailides, T. J. (2010). Characterization and pathogenicity of Botryosphaeriaceae species collected from olive and other hosts in Spain and California. Phytopathology, 100, 1340–1351.CrossRefPubMedGoogle Scholar
  24. Pavlic, D., Slippers, B., Coutinho, T. A., & Wingfield, M. J. (2007). Botryosphaeriaceae occurring on native Syzygium cordatum in South Africa and their potential threat to Eucalyptus. Plant Pathology, 56, 624–636.CrossRefGoogle Scholar
  25. Phillips, A. J. L. (2002). Botryosphaeria species associated with diseases of grapevines in Portugal. Phytopathologia Mediterranea, 41, 3–18.Google Scholar
  26. Phillips, A. J. L., Oudemans, P. V., Correia, A., & Alves, A. (2006). Characterization and epitypification of Botryosphaeria corticis the cause of blueberry cane canker. Fungal Diversity, 21, 141–155.Google Scholar
  27. 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.PubMedCentralCrossRefPubMedGoogle Scholar
  28. 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.PubMedCentralCrossRefPubMedGoogle Scholar
  29. Punithalingam E. (1980). Plant diseases attributed to Botryodiplodia theobromae Pat. Cramer, Vaduz.Google Scholar
  30. Sambrook, J., & Russell, D. W. (2001). Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press. NY: Cold Spring Harbor.Google Scholar
  31. Slippers, B., & Wingfield, M. J. (2007). Botryosphaeriaceae as endophytes and latent pathogens of woody plants: diversity, ecology and impact. Fungal Biology Reviews, 21, 90–106.CrossRefGoogle Scholar
  32. Slippers, B., Crous, P. W., Denman, S., Coutinho, T. A., Wingfield, B. D., & Wingfield, M. J. (2004). Combined multiple gene genealogies and phenotypic characters differentiate several species previously identified as Botryosphaeria dothidea. Mycologia, 96, 83–101.CrossRefPubMedGoogle Scholar
  33. Slippers, B., Johnson, G. I., Crous, P. W., Coutinho, T. A., Wingfield, B. D., & Wingfield, M. J. (2005). Phylogenetic and morphological re-evaluation of the Botryosphaeria species causing diseased of Mangifera indica. Mycologia, 97, 99–110.CrossRefPubMedGoogle Scholar
  34. Slippers, B., Smit, W. A., Crous, P. W., Coutinho, 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, 56, 128–139.CrossRefGoogle Scholar
  35. 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
  36. Thomidis, T., Michailides, T. J., & Exadaktylou, E. (2011). Neofusicoccum parvum associated with fruit rot and shoot blight of peaches in Greece. European Journal of Plant Pathology, 131, 661–668.CrossRefGoogle Scholar
  37. Úrbez-Torres, J. R., Leavitt, G. M., Voegel, T., & Gubler, W. D. (2006). Identification and distribution of Botryosphaeria species associated with grapevine cankers in California. Plant Disease, 90, 1490–1503.CrossRefGoogle Scholar
  38. Úrbez-Torres, J. R., Leavitt, G. M., Guerrero, J. C., Guevara, J., & Gubler, W. D. (2008). Identification and pathogenicity of Lasiodiplodia theobromae and Diplodia seriata, the causal agents of bot canker disease of grapevines in Mexico. Plant Disease, 92, 519–529.CrossRefGoogle Scholar
  39. Wang, F., Zhao, L. N., Li, G. H., Huang, J. B., & Hsiang, T. (2011). Identification and characterization of Botryosphaeria spp. causing gummosis of peach trees in Hubei Province, central China. Plant Disease, 95, 1378–1384.CrossRefGoogle Scholar
  40. White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes forphylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, & T. J. White (Eds.), PCR Procotols: A Guide to Methods and Applications (pp. 315–322). New York: Academic.Google Scholar
  41. Wright, A. F., & Harmon, P. F. (2009). First report of Lasiodiplodia theobromae causing stem blight of southern high bush blueberries in Florida. Plant Disease, 93, 692.CrossRefGoogle Scholar
  42. Wright, A. F., & Harmon, P. F. (2010). Identification of species in the Botryosphaeriaceae family causing stem blight on southern highbush blueberry in Florida. Plant Disease, 94, 966–971.CrossRefGoogle Scholar
  43. Xu, C. N., Zhou, Z. S., Zhang, H. J., Wu, Y. X., & Chi, F. M. (2012). Identification of the pathogen causing stem canker of blueberry. Acta Phytopathologica Sinica, 42, 532–535.Google Scholar
  44. Xu, C. N., Zhou, Z. S., Chi, F. M., Wu, Y. X., Ji, Z. R., & Zhang, H. J. (2013). Research on the pathogen causing Botryosphaeria stem blight on blueberry. Acta Horticulture Sinica, 40, 231–236.Google Scholar
  45. Yan, J. Y., Xie, Y., Zhang, W., Wang, Y., Liu, J. K., Hyde, K. D., Seem, R. C., Zhang, G. Z., Wang, Z. Y., Yao, S. W., Bai, X. J., Dissanayake, A. J., Peng, Y. L., & Li, X. H. (2013). Species of Botryosphaeriaceae involved in grapevine dieback in China. Fungal Diversity, 61, 221–236.CrossRefGoogle Scholar
  46. Yu, L., Rasisara, I., Xu, S. G., Wu, X., & Zhao, J. R. (2012). First report of stem blight of blueberry caused by Botryosphaeria dothidea in China. Plant Disease, 96(11), 1697.CrossRefGoogle Scholar
  47. Yu, L., Impaprasert, R., Zhao, J. R., Xu, S. G., & Wu, X. (2013a). Stem dieback of high bush blueberries caused by Neofusicoccum parvum in China. New Disease Reports, 27, 3.CrossRefGoogle Scholar
  48. Yu, L., Zhao, J. R., Impaprasert, R., Xu, S. G., & Wu, X. (2013b). Identification of the pathogen causing twigs and stem dieback in blueberry. Acta Phytopathologica Sinica, 43, 421–425.Google Scholar
  49. Zhai, L., Zhang, M., Lv, G., Chen, X., Jia, N., Hong, N., & Wang, G. (2014). Biological and molecular characterization of four Botryosphaeria species isolated from pear plants showing stem wart and stem canker in China. Plant Disease, 98, 716–72.CrossRefGoogle Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2015

Authors and Affiliations

  1. 1.College of Plant ProtectionAgricultural University of HebeiBaodingPeople’s Republic of China
  2. 2.Research Institute of PomologyChinese Academy of Agricultural SciencesXingchengPeople’s Republic of China

Personalised recommendations