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Fungal Diversity

, Volume 67, Issue 1, pp 157–179 | Cite as

Botryosphaeriaceae and Diaporthaceae associated with panicle and shoot blight of pistachio in California, USA

  • Shuai Fei Chen
  • David P. Morgan
  • Themis J. Michailides
Article

Abstract

Botryosphaeria panicle and shoot blight was considered as one of the single greatest threats to the California pistachio industry in the last two decades. A large number of fungi with typical morphological characteristics of Botryosphaeriaceae and Diaporthe were collected from pistachios in 18 counties in California and deposited in our culture collection. The aims of this study were to identify these isolates, recognize the distribution of these fungal species and test their pathogenicity to pistachio cultivars. A total of 304 California isolates were identified based on comparisons of DNA sequence data of the ITS, TEF-1α and β-tubulin gene regions, and combined with the morphological features of the cultures and conidia. Research results showed that California isolates represent eight species of Botryosphaeriaceae and one species of Diaporthe. These species include Botryosphaeria dothidea, Diplodia seriata, Dothiorella iberica, Dot. sarmentorum, Lasiodiplodia citricola, L. gilanensis, Neofusicoccum mediterraneum, Neof. vitifusiforme and Diaporthe chamaeropis. Of the Botryosphaeriaceae, 86 % of the isolates were identified as Neof. mediterraneum, which distributed in all the sampled counties. On pistachio trees, in addition to isolates from California, Neof. mediterraneum from Arizona, Neof. australe from Australia, B. dothidea, Neof. parvum and Dia. viticola from Greece were also identified. Pathogenicity of the California fungi on pistachio cultivars, Kerman (female) and Peters (male), using a mycelium plug and conidial suspension inoculation methods showed that all these species are pathogenic to the two tested pistachio cultivars, with L. citricola, L. gilanensis being the most pathogenic species, followed by Neof. mediterraneum. This study represents the first comprehensive work on the species identification, distribution and pathogenicity of Botryosphaeriaceae and Diaporthe on pistachio in California.

Keywords

Botryosphaeria Diaporthe Diplodia Dothiorella Lasiodiplodia Neofusicoccum Phomopsis 

Notes

Acknowledgments

This research was funded by California Pistachio Research Board. We thank the colleagues of the University of California Cooperative Extension for sending some of the diseased samples. We are also grateful to Ryan Puckett and Avery Hiley for the valuable assistance in the field inoculations, and Ms. FeiFei Liu and GuoQing Li in the China Eucalypt Research Centre (CERC) for their assistance in the sequence submission.

References

  1. Abdollahzadeh J, Javadi A, Mohammadi Goltapeh E, Zare R, Phillips AJL (2010) Phylogeny and morphology of four new species of Lasiodiplodia from Iran. Persoonia 25:1–10PubMedCrossRefPubMedCentralGoogle Scholar
  2. Alves A, Correia A, Phillips AJL (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 Divers 23:1–15Google Scholar
  3. Alves A, Crous PW, Correia A, Phillips AJL (2008) Morphological and molecular data reveal cryptic speciation in Lasiodiplodia theobromae. Fungal Divers 28:1–13Google Scholar
  4. Ashworth Jr LJ, Morgan DP, Surber E (1986) Verticillium wilt of pistachio. California Agriculture July-August:21–24Google Scholar
  5. Brown EA II, Britton KO (1986) Botryosphaeria disease of apple and peach in the southeastern United States. Plant Dis 70:480–484CrossRefGoogle Scholar
  6. Carbone I, Anderson JB, Kohn LM (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 3:553–556CrossRefGoogle Scholar
  7. Chen SF, Gryzenhout M, Roux J, Xie YJ, Wingfield MJ, Zhou XD (2011a) Novel species of Celoporthe from Eucalyptus and Syzygium trees in China and Indonesia. Mycologia 103:1384–1410PubMedCrossRefGoogle Scholar
  8. Chen SF, Pavlic D, Roux J, Xie YJ, Wingfield MJ, Zhou XD (2011b) Characterization of Botryosphaeriaceae from plantation-grown Eucalyptus species in South China. Plant Pathol 60:739–751CrossRefGoogle Scholar
  9. Chen SF, Fichtner E, Morgan DP, Michailides TJ (2013a) First report of Lasiodiplodia citricola and Neoscytalidium dimidiatum causing death of graft union of english Walnut in California. Plant Dis 97:993CrossRefGoogle Scholar
  10. Chen SF, Morgan DP, Beede RH, Michailides TJ (2013b) First report of Lasiodiplodia theobromae associated with Stem Canker of Almond in California. Plant Dis 97:994CrossRefGoogle Scholar
  11. Chen SF, Morgan DP, Michailides TJ (2013c) First report of Lasiodiplodia citricola associated with stem canker of peach in California, USA. J Plant Pathol 95:659Google Scholar
  12. Chen SF, Morgan D, Hasey JK, Anderson K, Michailides TJ (2013d) Phylogeny, morphology, distribution, and pathogenicity of Botryosphaeriaceae and Diaporthaceae from English walnut in California. Plant Dis. doi: 10.1094/PDIS-07-13-0706-RE Google Scholar
  13. Crous WP, Wingfield MJ, Phillips AJL (2007) Neofusicoccum mediterraneum Crous, M.J.Wingf. & A.J.L. Phillips, sp. nov. Fungal Planet 19Google Scholar
  14. Crous PW, Groenewald JZ, Shivas RG et al (2011) Fungal planet description sheets: 69–91. Persoonia 26:108–156PubMedCrossRefPubMedCentralGoogle Scholar
  15. Damm U, Crous PW, Fourie PH (2007) Botryosphaeriaceae as potential pathogens of Prunus in South Africa, with descriptions of Diplodia africana and Lasiodiplodia plurivora sp. nov. Mycologia 99:664–680PubMedCrossRefGoogle Scholar
  16. Glass NL, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous Ascomycetes. Appl Environ Microbiol 61:1323–1330PubMedPubMedCentralGoogle Scholar
  17. Gomes RR, Glienke C, Videira SIR, Lombard L, Groenewald JZ, Crous PW (2013) Diaporthe: a genus of endophytic, saprobic and plant pathogenic fungi. Persoonia 31:1–41PubMedCrossRefPubMedCentralGoogle Scholar
  18. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704PubMedCrossRefGoogle Scholar
  19. Hou X, Dewdney MM, Fu YS, Chen GQ, Hyde KD, Li HY (2013) Diaporthe species occurring on citrus in China. Fungal Divers 61:237–250Google Scholar
  20. Inderbitzin P, Bostock RM, Trouillas FP, Michailides TJ (2010) A six locus phylogeny reveals high species diversity in Botryosphaeriaceae from California almond. Mycologia 102:1350–1368PubMedCrossRefGoogle Scholar
  21. Johnson JA, Gill RF, Valero KA, May SA (1996) Survival of Navel Orange worm (Lepidoptera: Pyralidae) during pistachio processing. J Econ Entomol 89:197–203Google Scholar
  22. Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066PubMedCrossRefPubMedCentralGoogle Scholar
  23. Liu JK, Phookamsak R, Doilom M et al (2012) Towards a natural classification of Botryosphaeriales. Fungal Divers 57:149–210CrossRefGoogle Scholar
  24. Ma Z, Michailides TJ (2002) A PCR-based technique for identification of Fusicoccum sp. from pistachio and other hosts in California. Plant Dis 86:515–520CrossRefGoogle Scholar
  25. Ma Z, Boehm EWA, Luo Y, Michailides TJ (2001a) Population structure of Botryosphaeria dothidea from pistachio and other hosts in California. Phytopathology 91:665–672PubMedCrossRefGoogle Scholar
  26. Ma Z, Morgan DP, Michailides TJ (2001b) Effects of water stress on Botryosphaeria blight of pistachio caused by Botryosphaeria dothidea. Plant Dis 85:745–749CrossRefGoogle Scholar
  27. Marques MW, Lima NB, de Morais A, Jr M, Barbosa MAG, Souza BO, Michereff SJ, Phillips AJL, Câmara MPS (2013) Species of Lasiodiplodia associated with mango in Brazil. Fungal Divers 61:181–193Google Scholar
  28. McDonald V, Lynch S, Eskalen A (2009) First report of Neofusicoccum australe, N. luteum, and N. parvum associated with avocado branch canker in California. Plant Dis 93:967CrossRefGoogle Scholar
  29. Mehl JWM, Slippers B, Roux J, Wingfield MJ (2011) Botryosphaeriaceae associated with Pterocarpus angolensis (kiaat) in South Africa. Mycologia 103:534–553PubMedCrossRefGoogle Scholar
  30. Michailides TJ (1991) Pathogenicity, distribution, sources of inoculum, and infection courts of Botryosphaeria dothidea on pistachio. Phytopathology 81:566–573CrossRefGoogle Scholar
  31. Michailides TJ, Morgan DP (1992) Effects of temperature and wetness duration on infection of pistachio by Botryosphaeria dothidea and management of disease by reducing duration of irrigation. Phytopathology 82:1399–1406CrossRefGoogle Scholar
  32. Michailides TJ, Morgan DP (2004) Panicle and shoot blight of pistachio: a major threat to the California Pistachio Industry. January 2004, APSnet FeatureGoogle Scholar
  33. Michailides TJ, Morgan DP, Felts D (2002) First report of Botryosphaeria rhodina causing shoot blight of pistachio in California. Plant Dis 86:1273CrossRefGoogle Scholar
  34. Mila AL, Michailides TJ (2006) Use of Bayesian methods to improve prediction of panicle and shoot blight severity of pistachio in California. Phytopathology 96:1142–1147PubMedCrossRefGoogle Scholar
  35. Mila AL, Driever GF, Morgan DP, Michailides TJ (2005) Effects of latent infection, temperature, precipitation, and irrigation on panicle and shoot blight of pistachio in California. Phytopathology 95:926–932PubMedCrossRefGoogle Scholar
  36. Moral J, Muñoz-Díez C, González N, Trapero A, Michailides TJ (2010) Characterization and pathogenicity of Botryosphaeriaceae species collected from olive and other hosts in Spain and California. Phytopathology 100:1340–1351PubMedCrossRefGoogle Scholar
  37. Morgan DP, Driever GF, Felts D, Krueger WH, Michailides TJ (2009) Evaluation of two disease warning systems for Botryosphaeria panicle and shoot blight of California pistachio and efficient control based on early-season sprays. Plant Dis 93:1175–1181CrossRefGoogle Scholar
  38. Ntahimpera N, Driever GF, Felts D, Morgan DP, Michailides TJ (2002) Dynamics and pattern of infection by Botryosphaeria dothidea on pistachio buds. Plant Dis 86:282–287CrossRefGoogle Scholar
  39. Phillips A, Alves A, Correia A, Luque J (2005) Two new species of Botryosphaeria with brown, 1-septate ascospores and Dothiorella anamorphs. Mycologia 97:513–529PubMedCrossRefGoogle Scholar
  40. Phillips AJL, Crous PW, Alves A (2007) Diplodia seriata, the anamorph of “Botryosphaeriaobtusa. Fungal Divers 25:141–155Google Scholar
  41. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818PubMedCrossRefGoogle Scholar
  42. Rayner RW (1970) A mycological colour chart. Commonwealth Mycological Institute and British Mycological Society, Kew, p 34Google Scholar
  43. Rice RE, Uyemoto JK, Ogawa JM, Pemberton WM (1985) New findings on pistachio problems. Calif Agric 39:15–18Google Scholar
  44. Santos JM, Phillips AJL (2009) Resolving the complex of Diaporthe (Phomopsis) species occurring on Foeniculum vulgare in Portugal. Fungal Divers 34:111–125Google Scholar
  45. Santos JM, Correia VG, Phillips AJL (2010) Primers for mating-type diagnosis in Diaporthe and Phomopsis: their use in teleomorph induction in vitro and biological species definition. Fungal Biol 114:255–270PubMedCrossRefGoogle Scholar
  46. SAS Instatute Inc (2011) SAS/STAT Users Guide, Version 9.3. SAS Inc., Cary, NCGoogle Scholar
  47. Slippers B, Crous PW, Denman S, Coutinho TA, Wingfield BD, Wingfield MJ (2004a) Combined multiple gene genealogies and phenotypic characters differentiate several species previously identified as Botryosphaeria dothidea. Mycologia 96:83–101PubMedCrossRefGoogle Scholar
  48. Slippers B, Fourie G, Crous PW, Coutinho TA, Wingfield BD, Wingfield MJ (2004b) Multiple gene sequences delimit Botryosphaeria australis sp. nov. from B. lutea. Mycologia 96:1028–1039Google Scholar
  49. Smith DR, Michailides TJ, Stanosz GR (2001) Differentiation of a Fusicoccum species causing panicle and shoot blight on California pistachio trees from Botryosphaeria dothidea. Plant Dis 85:1235–1240CrossRefGoogle Scholar
  50. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedCrossRefGoogle Scholar
  51. Tan YP, Edwards J, Grice KER, Shivas RG (2013) Molecular phylogenetic analysis reveals six new species of Diaporthe from Australia. Fungal Divers 61:251–260Google Scholar
  52. Udayanga D, Liu X, McKenzie EHC, Chukeatirote E, Bahkali AHA, Hyde KD (2011) The genus Phomopsis: biology, applications, species concepts and names of common phytopathogens. Fungal Divers 50:189–225CrossRefGoogle Scholar
  53. Udayanga D, Liu X-Z, Crous PW, McKenzie EHC, Chukeatirote E, Hyde KD (2012) A multi-locus phylogenetic evaluation of Diaporthe (Phomopsis). Fungal Divers 56:157–171CrossRefGoogle Scholar
  54. Úrbez-Torres JR, Gubler WD (2009) Pathogenicity of Botryosphaeriaceae species isolated from grapevine cankers in California. Plant Dis 93:584–592CrossRefGoogle Scholar
  55. Úrbez-Torres JR, Leavitt GM, Guerrero JC, Guevara J, Gubler WD (2008) Identification and pathogenicity of Lasiodiplodia theobromae and Diplodia seriata, the causal agents of bot canker disease of grapevines in Mexico. Plant Dis 92:519–529CrossRefGoogle Scholar
  56. Úrbez-Torres JR, Peduto F, Gubler WD (2010) First report of grapevine cankers caused by Lasiodiplodia crassispora and Neofusicoccum mediterraneum in California. Plant Dis 94:785Google Scholar
  57. Úrbez-Torres JR, Peduto F, Striegler RK, Urrea-Romero KE, Rupe JC, Cartwright RD, Gubler WD (2012) Characterization of fungal pathogens associated with grapevine trunk diseases in Arkansas and Missouri. Fungal Divers 52:169–189CrossRefGoogle Scholar
  58. Úrbez-Torres JR, Peduto F, Vossen PM, Krueger WH, Gubler WD (2013) Olive twig and branch dieback: etiology, incidence, and distribution in California. Plant Dis 97:231–244CrossRefGoogle Scholar
  59. Van Niekerk JM, Crous PW, Groenewald JZ, Fourie PH, Halleen F (2004) DNA phylogeny, morphology and pathogenicity of Botryosphaeria species on grapevines. Mycologia 96:781–798PubMedCrossRefGoogle Scholar
  60. Van Niekerk JM, Groenewald JZ, Farr DF, Fourie PH, Halleen F, Crous PW (2005) Reassessment of Phomopsis species on grapevines. Australas Plant Pathol 34:27–39CrossRefGoogle Scholar
  61. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Snisky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic, San Diego, pp 315–322CrossRefGoogle Scholar

Copyright information

© Mushroom Research Foundation 2014

Authors and Affiliations

  1. 1.Department of Plant PathologyUniversity of California-Davis/Kearney Agricultural Research and Extension CenterParlierUSA
  2. 2.China Eucalypt Research Centre (CERC), Chinese Academy of Forestry (CAF)ZhanJiangChina

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