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

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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.

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References

  • Abdollahzadeh J, Javadi A, Mohammadi Goltapeh E, Zare R, Phillips AJL (2010) Phylogeny and morphology of four new species of Lasiodiplodia from Iran. Persoonia 25:1–10

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • 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 23:1–15

    Google Scholar 

  • Alves A, Crous PW, Correia A, Phillips AJL (2008) Morphological and molecular data reveal cryptic speciation in Lasiodiplodia theobromae. Fungal Divers 28:1–13

    Google Scholar 

  • Ashworth Jr LJ, Morgan DP, Surber E (1986) Verticillium wilt of pistachio. California Agriculture July-August:21–24

  • Brown EA II, Britton KO (1986) Botryosphaeria disease of apple and peach in the southeastern United States. Plant Dis 70:480–484

    Article  Google Scholar 

  • Carbone I, Anderson JB, Kohn LM (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 3:553–556

    Article  Google Scholar 

  • 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 103:1384–1410

    Article  PubMed  CAS  Google Scholar 

  • 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 60:739–751

    Article  CAS  Google Scholar 

  • 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 97:993

    Article  Google Scholar 

  • Chen SF, Morgan DP, Beede RH, Michailides TJ (2013b) First report of Lasiodiplodia theobromae associated with Stem Canker of Almond in California. Plant Dis 97:994

    Article  Google Scholar 

  • Chen SF, Morgan DP, Michailides TJ (2013c) First report of Lasiodiplodia citricola associated with stem canker of peach in California, USA. J Plant Pathol 95:659

    Google Scholar 

  • 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 

  • Crous WP, Wingfield MJ, Phillips AJL (2007) Neofusicoccum mediterraneum Crous, M.J.Wingf. & A.J.L. Phillips, sp. nov. Fungal Planet 19

  • Crous PW, Groenewald JZ, Shivas RG et al (2011) Fungal planet description sheets: 69–91. Persoonia 26:108–156

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • 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 99:664–680

    Article  PubMed  CAS  Google Scholar 

  • 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 61:1323–1330

    PubMed  CAS  PubMed Central  Google Scholar 

  • Gomes RR, Glienke C, Videira SIR, Lombard L, Groenewald JZ, Crous PW (2013) Diaporthe: a genus of endophytic, saprobic and plant pathogenic fungi. Persoonia 31:1–41

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Hou X, Dewdney MM, Fu YS, Chen GQ, Hyde KD, Li HY (2013) Diaporthe species occurring on citrus in China. Fungal Divers 61:237–250

    Google Scholar 

  • Inderbitzin P, Bostock RM, Trouillas FP, Michailides TJ (2010) A six locus phylogeny reveals high species diversity in Botryosphaeriaceae from California almond. Mycologia 102:1350–1368

    Article  PubMed  CAS  Google Scholar 

  • Johnson JA, Gill RF, Valero KA, May SA (1996) Survival of Navel Orange worm (Lepidoptera: Pyralidae) during pistachio processing. J Econ Entomol 89:197–203

    Google Scholar 

  • 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 30:3059–3066

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Liu JK, Phookamsak R, Doilom M et al (2012) Towards a natural classification of Botryosphaeriales. Fungal Divers 57:149–210

    Article  Google Scholar 

  • Ma Z, Michailides TJ (2002) A PCR-based technique for identification of Fusicoccum sp. from pistachio and other hosts in California. Plant Dis 86:515–520

    Article  CAS  Google Scholar 

  • Ma Z, Boehm EWA, Luo Y, Michailides TJ (2001a) Population structure of Botryosphaeria dothidea from pistachio and other hosts in California. Phytopathology 91:665–672

    Article  PubMed  CAS  Google Scholar 

  • Ma Z, Morgan DP, Michailides TJ (2001b) Effects of water stress on Botryosphaeria blight of pistachio caused by Botryosphaeria dothidea. Plant Dis 85:745–749

    Article  Google Scholar 

  • 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 61:181–193

    Google Scholar 

  • 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 93:967

    Article  Google Scholar 

  • Mehl JWM, Slippers B, Roux J, Wingfield MJ (2011) Botryosphaeriaceae associated with Pterocarpus angolensis (kiaat) in South Africa. Mycologia 103:534–553

    Article  PubMed  Google Scholar 

  • Michailides TJ (1991) Pathogenicity, distribution, sources of inoculum, and infection courts of Botryosphaeria dothidea on pistachio. Phytopathology 81:566–573

    Article  Google Scholar 

  • 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 82:1399–1406

    Article  Google Scholar 

  • Michailides TJ, Morgan DP (2004) Panicle and shoot blight of pistachio: a major threat to the California Pistachio Industry. January 2004, APSnet Feature

  • Michailides TJ, Morgan DP, Felts D (2002) First report of Botryosphaeria rhodina causing shoot blight of pistachio in California. Plant Dis 86:1273

    Article  Google Scholar 

  • Mila AL, Michailides TJ (2006) Use of Bayesian methods to improve prediction of panicle and shoot blight severity of pistachio in California. Phytopathology 96:1142–1147

    Article  PubMed  Google Scholar 

  • 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 95:926–932

    Article  PubMed  CAS  Google Scholar 

  • 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 100:1340–1351

    Article  PubMed  Google Scholar 

  • 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 93:1175–1181

    Article  Google Scholar 

  • Ntahimpera N, Driever GF, Felts D, Morgan DP, Michailides TJ (2002) Dynamics and pattern of infection by Botryosphaeria dothidea on pistachio buds. Plant Dis 86:282–287

    Article  Google Scholar 

  • Phillips A, Alves A, Correia A, Luque J (2005) Two new species of Botryosphaeria with brown, 1-septate ascospores and Dothiorella anamorphs. Mycologia 97:513–529

    Article  PubMed  Google Scholar 

  • Phillips AJL, Crous PW, Alves A (2007) Diplodia seriata, the anamorph of “Botryosphaeriaobtusa. Fungal Divers 25:141–155

    Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Rayner RW (1970) A mycological colour chart. Commonwealth Mycological Institute and British Mycological Society, Kew, p 34

    Google Scholar 

  • Rice RE, Uyemoto JK, Ogawa JM, Pemberton WM (1985) New findings on pistachio problems. Calif Agric 39:15–18

    Google Scholar 

  • Santos JM, Phillips AJL (2009) Resolving the complex of Diaporthe (Phomopsis) species occurring on Foeniculum vulgare in Portugal. Fungal Divers 34:111–125

    Google Scholar 

  • 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 114:255–270

    Article  PubMed  CAS  Google Scholar 

  • SAS Instatute Inc (2011) SAS/STAT Users Guide, Version 9.3. SAS Inc., Cary, NC

  • 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 96:83–101

    Article  PubMed  CAS  Google Scholar 

  • 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 96:1028–1039

    Google Scholar 

  • 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 85:1235–1240

    Article  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Tan YP, Edwards J, Grice KER, Shivas RG (2013) Molecular phylogenetic analysis reveals six new species of Diaporthe from Australia. Fungal Divers 61:251–260

    Google Scholar 

  • 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 50:189–225

    Article  Google Scholar 

  • Udayanga D, Liu X-Z, Crous PW, McKenzie EHC, Chukeatirote E, Hyde KD (2012) A multi-locus phylogenetic evaluation of Diaporthe (Phomopsis). Fungal Divers 56:157–171

    Article  Google Scholar 

  • Úrbez-Torres JR, Gubler WD (2009) Pathogenicity of Botryosphaeriaceae species isolated from grapevine cankers in California. Plant Dis 93:584–592

    Article  Google Scholar 

  • 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 92:519–529

    Article  Google Scholar 

  • Úrbez-Torres JR, Peduto F, Gubler WD (2010) First report of grapevine cankers caused by Lasiodiplodia crassispora and Neofusicoccum mediterraneum in California. Plant Dis 94:785

    Google Scholar 

  • 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 52:169–189

    Article  Google Scholar 

  • 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 97:231–244

    Article  Google Scholar 

  • Van Niekerk JM, Crous PW, Groenewald JZ, Fourie PH, Halleen F (2004) DNA phylogeny, morphology and pathogenicity of Botryosphaeria species on grapevines. Mycologia 96:781–798

    Article  PubMed  Google Scholar 

  • Van Niekerk JM, Groenewald JZ, Farr DF, Fourie PH, Halleen F, Crous PW (2005) Reassessment of Phomopsis species on grapevines. Australas Plant Pathol 34:27–39

    Article  Google Scholar 

  • 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 315–322

    Chapter  Google Scholar 

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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.

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Chen, S.F., Morgan, D.P. & Michailides, T.J. Botryosphaeriaceae and Diaporthaceae associated with panicle and shoot blight of pistachio in California, USA. Fungal Diversity 67, 157–179 (2014). https://doi.org/10.1007/s13225-014-0285-6

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