Characterization and pathogenicity of fungal trunk pathogens associated with declining of neem (Azadirachta indica A. Juss) trees in Iran

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

Begoude BAD, Slippers B, Wingfield MJ, Roux J (2010) Botryosphaeriaceae associated with Terminalia catappa in Cameroon, South Africa and Madagascar. Mycol Prog 9:101–123

Bhat SS, Sateesh MK, Devaki NS (1998) A new destructive disease of neem (Azadirachta indica) incited by Phomopsis azadirachtae. Curr Sci 74:17–19

Burgess T, Wingfield MJ, Wingfield BD (2003) Development and characterization of microsatellite loci for the tropical tree pathogen Botryosphaeria rhodina. Mol Ecol Notes 3:91–94

Canale MC, Nunes Nesi C, Falkenbach BR, Hunhoff da Silva CA, Brugnara EC (2019) Pleurostomophora richardsiae associated with olive tree and grapevine decline in Southern Brazil. Phytopathol Mediterr 58(1):201–205

Carbone I, Kohn LM (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91:553–556

Carlucci A, Raimondo ML, Cibelli F, Phillips AJL, Lops F (2013) Pleurostomophora richardsiae, Neofusicoccum parvum and Phaeoacremonium aleophilum associated with a decline of olives in southern Italy. Phytopathol Mediterr 52:517–527

Carlucci A, Cibelli F, Lops F, Phillips AJL, Ciccarone C, Raimondo ML (2015) Pleurostomophora richardsiae associated with trunk diseases of grapevines in southern Italy. Phytopathol Mediterr 54:109–123

Carroll GC, Carroll FE (1978) Studies on the incidence of coniferous needle endophytes in the Pacific Northwest. Can J Bot 56:3034–3043

Chicau G, Aboim-Inglez M, Cabral S, Cabral JPS (2000) Phaeoacremonium chlamydosporum and Phaeoacremonium angustius associated with esca and grapevine decline in northwest Portugal. Phytopathol Mediterr 39:80–86

Choueiri E, Jreijiri F, Chlela P, Mayet V, Comont G, Liminana JM, Mostert L, Fischer M, Lecomte P (2014) Fungal community associated with grapevine wood lesions in Lebanon. J Int des Sci la Vigne du Vin 48(4):293–302

Cilliers A (1993) A review of Lasiodiplodia theobromae with particular reference to its occurrence on coniferous seeds. S Afr For J 166:47–52

Cloete M, Fourie PH, Damm U, Crous PW, Mostert L (2011) Fungi associated with dieback symptoms of apple and pear trees with a special reference to grapevine trunk disease pathogens. Phytopathol Mediterr 50:176–190

Crous PW, Phillips AJL, Baxter AP (2000) Phytopathogenic fungi from South Africa. University of Stellenbosch, Department of Plant Pathology Press, University of Stellenbosch Printers, Stellenbosch, South Africa

Crous PW, Gams W, Wingfield MJ, van Wyk PS (1996) Phaeoacremonium gen. nov. associated with wilt and decline diseases of woody hosts and human infections. Mycologia 88:786–796

De Errasti A, Carmarán C, Novas MV (2010) Diversity and significance of fungal endophytes from living stems of naturalized trees from Argentina. Fungal Divers 41:29–40

Deng TJ, Li QL, Chen XL, Huang SP, Guo TX, Mo JY, Wei JM, Hsiang T (2015) First report of Lasiodiplodia theobromae associated with stem canker of Cassia fistula in Guangxi, South China. Plant Dis 99:288

Dupont J, Laloui W, Roquebert MF (1998) Partial ribosomal DNA sequences show an important divergence between Phaeoacremonium species isolated from Vitis vinifera. Mycol Res 102:631–637

Eskalen A, Rooney-Latham S, Gubler WD (2005) Occurrence of Togninia fraxinopennsylvanica on esca-diseased grapevines (Vitis vinifera) and declining ash trees (Fraxinus latifolia) in California. Plant Dis 89:528

Farr DF, Rossman AY (2018) Fungal Databases, U.S. National Fungus Collections, ARS, USDA. https://nt.ars-grin.gov/fungaldatabases

Fathima SK (2004) Investigations on the biology and management of Phomopsis azadirachtae on neem. Dissertation, University of Mysore, Mysore, India

García-Benavides P, Martin-Zamorano P, Ocete-Pérez CA, Maistrello L, Ocete R (2013) Biodiversity of pathogenic wood fungi isolated from Xylotrechus arvicola (Olivier) galeries in vine shoots. J Int Sci Vigne Vin 47:73–81

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

Gramaje D, Mostert L, Groenewald JZ, Crous PW (2015) Phaeoacremonium: From esca disease to phaeohyphomycosis. Fungal Biol 119:759–783. https://doi.org/10.1016/j.funbio.2015.06.004

Groenewald M, Kang J-C, Crous PW, Gams W (2001) ITS and beta-tubulin phylogeny of Phaeoacremonium and Phaeomoniella species. Mycol Res 105:651–657

Hall T (2006) Bioedit 7.5.0.3. Department of Microbiology, North CarolinaState University. Retrieved from http://www.mbio. ncsu.edu/BioEdit/ Bioedit.html

Halleen F, Crous PW, Petrini O (2003) Fungi associated with healthy grapevine cuttings in nurseries, with special reference to pathogens involved in the decline of young vines. Australas Plant Pathol 32:47–52

Halleen F, Mostert L, Crous PW (2007) Pathogenicity testing of lesser known vascular fungi of grapevines. Australas Plant Pathol 36:277–285

Halliwell RS (1966) Association of Cephalosporium with a decline of oak in Texas. Plant Dis Rep 50:75–78

Hashemi H, Mohammadi H (2016) Identification and characterization of fungi associated with internal wood lesions and decline disease of willow and poplar trees in Iran. For Pathol 46:341–352. https://doi.org/10.1111/efp.12269

Hashemi H, Mohammadi H, Abdollahzadeh J (2017) Symptoms and fungi associated with elm trees decline in Iran. Eur J For Res 136(5–6):857–879. https://doi.org/10.1007/s10342-017-1075-y

Hausner G, Eyjólfsdóttir G, Reid J (1992) Two additional species of the genus Togninia. Can J Bot 70:724–734

Hawksworth DL, Gibson IAS, Gams W (1976) Phialophora parasitica associated with disease conditions in various trees. Trans Br Mycol Soc 66:427–431

Houbraken J, Verweij PE, Rijs AJ, Borman AM, Samson RA (2010) Identification of Paecilomyces variotii in clinical samples and settings. J Clin Microbiol 48:2754–2276

Jena SK, Tayung K (2013) Endophytic fungal communities associated with two ethno-medicinal plants of Similipal Biosphere Reserve, India and their antimicrobial prospective. J Appl Pharm Sci 3:7

Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol Biol Evol 30:772–780

Kazemzadeh Chakusary M, Mohammadi H, Khodaparast A (2017) Decline-associated Phaeoacremonium species occurring on forest trees in the north of Iran. For Pathol 47:e12368. https://doi.org/10.1111/efp.12368

Kazemzadeh Chakusary M, Mohammadi H, Khodaparast SA (2019) Diversity and pathogenicity of Botryosphaeriaceae species on forest trees in the north of Iran. Eur J For Res 138:685–704. https://doi.org/10.1007/s10342-019-01200-7

Khalil O (2012) Lasiodiplodia theobromae associated with gummosis in neem tree (Azadirachta indica A. Juss.) in the Sudan. S Afr J Sci 2:105–117

Kumaran RS, Hur BK (2009) Screening of species of the endophytic fungus Phomopsis for the production of the anticancer drug taxol. Biotechnol Appl Bioc 54:21–30

Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary enetics analysis across computing platforms. Mol Biol Evol 5(6):1547–1549

Kuntzmann P, Villaume S, Larignon P, Bertsch C (2010) Esca, BDA and Eutypiosis: Foliar symptoms, trunk lesions and fungi observed in diseased vinestocks in two vineyards in Alsace. Vitis 49:71–76

Li JT, Fu JF, Yan XR, Li HC, Zhou RJ (2006) Analysis of temporal dynamics of Curvularia leaf spot of maize (Curvularia lunata) epidemic and yield loss. J Shenyang Agric Univ 37(6):835

Linaldeddu BT, Alves A, Phillips AJL (2016) Sardiniella urbana gen. et sp. nov., a new member of the Botryosphaeriaceae isolated from declining Celtis australis trees in Sardinian streetscapes. Mycosphere 7(7):893–905. doi: org/https://doi.org/10.5943/mycos phere /si/1b/5

Luque J, Martos S, Aroca A, Raposo R, Garcia-Fihueres F (2009) Symptoms and fungi associated with declining mature grapevine plants in northeast Spain. J Plant Pathol 91:381–390

Maher N, Piot J, Bastien S, Vallance J, Rey P, Guérin-Dubrana L (2012) Wood necrosis in esca-affected vines: types, relationships and possible links with foliar symptom expression. OENO One 46(1):15–27

Mahesh B, Tejesvi MV, Nalini MS, Prakash HS, Kini KR, Subbiah V, Hunthrike SS (2005) Endophytic mycoflora of inner bark of Azadirachta indica A Juss. Curr Sci 88:218–219

Markakis EA, Kavroulakis N, Ntougias S, Koubouris GC (2017) Characterization of fungi associated with wood decay of tree species and grapevine in Greece. Plant Dis 10(11):1929–1940

Mayorquin JS, Eskalen A, Downer AJ, Hodel DR, Liu A (2012) First report of multiple species of the Botryosphaeriaceae causing bot canker disease of Indian laurel-leaf fig in California. Plant Dis 96:459

Mehl JWM, Slippers B, Roux J, Wingfield MJ (2014) Botryosphaeriaceae associated with die-back of Schizolobium parahyba trees in South Africa and Ecuador. For Pathol 44(5):396–408

Mirabdollahi Shamsi M, Akbarinia M, Mirabolfathy M, Manzari S, Ahmadikhah A (2019) Dieback and decline of wild almond (Amygdalus scoparia Spach) in the Harat protected forest of Yazd province, Iran. For Pathol e12538. doi: org/https://doi.org/10.1111/efp.12538

Mohali S, Burgess TI, Wingfield MJ (2005) Diversity and host association of the tropical tree endophyte Lasiodiplodia theobromae revealed using simple sequence repeat markers. For Pathol 35:385–396

Mohammadi H, Sharifi S (2016) Association of Botryosphaeriaceae and Phaeoacremonium species with insect-damaged quince shoots. J Plant Pathol 98:31–38

Mohammadi H, Kazemi S, Farahmand H (2014) Phaeoacremonium and Botryosphaeriaceae species associated with cypress (Cupressus sempervirens L.) decline in Kerman province (Iran). Phytopathol Mediterr 53:27–39. doi: https://doi.org/10.14601/Phytopathol_Mediterr-12717

Mohammadi H, Sarcheshmehpour M, Mafi E (2015) Fungal trunk pathogens associated with wood decay of pistachio trees in Iran. Span J Agric Res 13:e1007

Moreno-Sanz P, Lucchetta G, Zanzotto A, Loureiro MD, Suarez B, Angelini E (2013) Fungi associated to grapevine trunk diseases in young plants in Asturias (Northern Spain). Hort Sci (Prague) 40:138–144

Mostert L, Groenwald JZ, Summerbell RC, Robert V, Sutton DA, Padhye AA, Crous PW (2005) Species of Phaeoacremonium associated with infections in humans and environmental reservoirs in infected woody plants. J Clin Microbiol 43:1752–1767

Mostert L, Groenewald JZ, Summerbell RC, Gams W, Crous PW (2006) Taxonomy and pathology of Togninia (Diaporthales) and its Phaeoacremonium anamorphs. Stud Mycol 54:1–115

Nazmadini S, Mohammadi H, Kazemzadeh Chakusary M (2018) First report of Phaeoacremonium venezuelense and Neoscytalidium hyalinum from Calligonum amoenum in Iran. In: 23rd Iran. Plant Protec. Cong, 27–30 August, 2018. Gorgan University of Agricultural Sciences and Natural Resources, Gorgan. 391 pp

Niekerk JM, Groenewald JZ, Farr DF, Fourie PH, Halleen F, Crous PW (2005) Reassessment of Phomopsis species on grapevines. Australas Plant Pathol 34:1–13

O’Donnell K, Cigelnik E (1997) Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Mol Phylogen Evol 7:103–116

Olmo D, Armengol J, León M, Gramaje D (2015) Pathogenicity testing of lesser-known fungal trunk pathogens associated with wood decay of almond trees. Eur J Plant Pathol 143:607–611

Panahandeh S, Mohammadi H, Gramaje D (2019) Trunk disease fungi associated with Syzygium cumini in Iran. Plant Dis 103:711–720. doi: org/https://doi.org/10.1094/PDIS-06-18-0923-RE

Pavlic-Zupanca D, Malemea HM, Piškurc B, Wingfieldb BD, Wingfielda MJ, Slippers B (2017) Diversity, phylogeny and pathogenicity of Botryosphaeriaceae on nonnative Eucalyptus grown in an urban environment: A case study. Urban For Urban Green 26:139–148

Pelleteret P, Crovadore J, Cochard B, Pasche S, Bovigny PY, Chablais R, Lefort F (2017) Urban London plane tree dieback linked to fungi in the Botryosphaeriaceae. Urban For Urban Green 22:74–83

Pham CD, Purfield AE, Fader R, Pascoe N, Lockhart SR (2015) Development of a multilocus sequence typing system for medically relevant Bipolaris species. J Clin Microbiol 53:3239–3246

Phillips AJL, Alves A, Abdollahzadeh J, Slippers B, Wingfield MJ, Groenewald JZ, Crous PW (2013) The Botryosphaeriaceae: genera and species known from culture. Stud Mycol 76:51–167

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

Rajagopal R, Suryanarayanan TS (2000) Isolation of endophytic fungi from leaves of neem (Azadirachta indica). Curr Sci 78:1375–1378

Rodríguez-Gálvez E, Guerrero P, Barradas C, Crous PW, Alves A (2017) Phylogeny and pathogenicity of Lasiodiplodia species associated with dieback of mango in Peru. Fungal Biol 121:452–465

Rolshausen PE, U’rbez-Torres JR, Rooney-Latham S, Eskalen A, Smith RJ, Gubler WD (2010) Evaluation of pruning wound susceptibility and protection against fungi associated with grapevine trunk diseases. Am J Enol Vitic 61:113–119

Rooney-Latham S, Eskalen A, Gallegos LL, Gubler WD (2006) Potential alternate sources of inoculum for causal agents of esca (black measles) of grapevine in California. Phytopathology 96:S99–S100

Roxburgh W (1874) Description of Indian plants. Today and Tomorrows Printers and Publishers. New Delhi, India

Sabernasab M, Jamali S, Marefat A, Abbasi S (2019) Molecular and pathogenic characteristics of Paecilomyces formosus, a new causal agent of oak tree dieback in Iran. For Sci 65:743–750. https://doi.org/10.1093/forsci/fxz045

Sambrook J, Fritsch EG, Maniatis T (1989) Molecular cloning: a laboratory manual. Second edition. Cold Spring Harbor Laboratory Press, New York. USA

Sami S, Mohammadi H, Heydarnejad J (2014) Phaeoacremonium species associated with necrotic wood of pome fruit trees in Iran. J Plant Pathol 96:19–27

Samson RA, Houbraken J, Vaega J, Frisvad JC (2009) Polyphasic taxonomy of the heat resistant ascomycete genus Byssochlamys and its Paecilomyces anamorphs. Persoonia 22:14–27

Sateesh MK (1998) Microbiological investigations on die-back disease of neem (Azadirachta indica A. Juss.). Dissertation, University of Mysore. Mysore, India

Scott EM, Carter RT (2014) Canine keratomycosis in 11 dogs: A case series (2000–2011). J Am Anim Hosp Assoc 50(2):112–118

Slippers B, Wingfield MJ (2007) The Botryosphaeriaceae as endophytes and latent pathogens of woody plants diversity, ecology and impact. Fungal Biol Rev 21:90–106

Slippers B, Boissin E, Phillips AJL, Groenewald JZ, Lombard L, Wingfield MJ, Postma A, Burgess T, Crous PW (2013) Phylogenetic lineages in the Botryosphaeriales: a systematic and evolutionary framework. Stud Mycol 76:31–49

Slippers B, Fourie G, Crous PW, Coutinho TA, Wingfield BD, Carnegie AJ, Wingfield MJ (2004) Speciation and distribution of Botryosphaeria spp. on native and introduced Eucalyptus trees in Australia and South Africa. Stud Mycol 50:343–358

Smith H, Wingfield M, Crous PW, Coutinho TA (1996) Sphaeropsis sapinea and Botryosphaeria dothidea endophytic in Pinus spp. and Eucalyptus spp. in South Africa. S Afr J Bot 62:86–88

Sohrabi M, Mohammadi H, León M, Armengol J, Banihashemi Z (2020) Fungal pathogens associated with branch and trunk cankers of nut crops in Iran. Eur J Plant Pathol. https://doi.org/10.1007/s10658-020-01996-w

Soltaninejad N, Mohammadi H, Massumi H (2017) Isolation, identification and pathogenicity of Botryosphaeriaceae and Phaeoacremonium species associated with decline of Prunus species in Iran. J Plant Pathol 99:571–581

Spies CFJ, Moyo P, Halleen F, Mostert L (2018) Phaeoacremonium species diversity on woody hosts in the Western Cape Province of South Africa. Persoonia 40:26–62. doi: org/https://doi.org/10.3767/persoonia.2018.40.02

Tan Y, Crous PW, Shivas RG (2018) Cryptic species of Curvularia in the culture collection of the Queensland Plant Pathology Herbarium. MycoKeys 35:1–25

Tenguria RK, Khan FN (2011) Distribution of endophytic fungi in leaves of Azadirachta indica A. JUSS. (Neem) of panchmarhi biosphere reserve. Curr Bot 2:27–29

Úrbez-Torres JR, Leavitt GM, Voegel TM, Gubler WD (2006) Identification and distribution of Botryosphaeria spp. associated with grapevine cankers in California. Plant Dis 90:1490–1503

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

Van Niekerk JM, Fourie PH, Halleen F, Crous PW (2006) Botryosphaeria spp. as grapevine trunk disease pathogens. Phytopathol Mediterr 45:S43–S54

Van Niekerk JM, Bester W, Halleen F, Crous PW, Fourie PH (2011) The distribution and symptomatology of grapevine trunk disease pathogens are influenced by climate. Phytopathol Mediterr 50:S98–S111

Verma VC, Gond SK, Kumar A, Kharwar RN, Strobel G (2007) The endophytic mycoflora of bark, leaf and stem tissues of Azadirachta indica A. Juss (Neem) from Varanasi (India). Microb Ecol 54:119–125

Verma VC, Gond SK, Kumar A, Kharwar RN, Boulanger LA, Strobel GA (2011) Endophytic fungal flora from roots and fruits of an Indian neem plant Azadirachta indica A. Juss., and impact of culture media on their isolation. Indian J Microbiol 51:469–476

Vijaykrishna D, Mostert L, Jeewon R, Gams W, Hyde KD, Crous PW (2004) Pleurostomophora, an anamorph of Pleurostoma (Calosphaeriales), a new anamorph genus morphologically similar to Phialophora. Stud Mycol 50:387–395

Vu D, Groenewald M, de Vries M, Gehrmann T, Stielow B, Eberhardt U, Al-Hatmi A, Groenewald JZ, Cardinali G, Houbraken J, Boekhout T, Crous PW, Robert V, Verkley GJM (2019) Large-scale generation and analysis of filamentous fungal DNA barcodes boosts coverage for kingdom fungi and reveals thresholds for fungal species and higher taxon delimitation. Stud Mycol 92:135–154

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, Sninsky JJ, White TJ. PCR Protocols: A Guide to Methods and Applications. Ed. by San Diego, CA: Academic Press, pp 315–321

White CL, Halleen F, Mostert L (2011) Symptoms and fungi associated with esca in South African vineyards. Phytopathol Mediterr 50:S236–S246