Ceratocystis

Ellis & Halst., New Jersey Agric. Coll. Exp. Sta. Bull. 76: 14. 1890.

• Synonym: Rostrella Zimm., Meded. Lands Plantentuin 37: 24, 41. 1900.
• Classification: Sordariomycetes, Hypocreomycetidae, Microascales, Ceratocystidaceae. 
• Type species: Ceratocystis fimbriata Ellis & Halst. Neotype: BPI 595863.
• DNA barcodes (genus): 60S, LSU, mcm7.
• DNA barcodes (species): ITS, bt1, tef1, rpb2, ms204.

Ascomata perithecial, scattered or gregarious, immersed, partially embedded or superficial on the substrate; bases subglobose to globose or obpyriform, brown to black, covered with undifferentiated hyphae; ostiolar necks central, long, tapering towards apex; ascomatal apex straight or undulate, unbranched or branched, brown to black and becoming paler; ostiolar hyphae divergent or convergent, non-septate, straight, tapering towards apex, hyaline to light brown. Asci evanescent. Ascospores hyaline, 1-celled, ellipsoidal with gelatinous sheath which gives hat-shaped impression, accumulating in white, creamy to yellow masses at tips of necks. Conidiophores branched, straight or flexuous, hyaline to pale brown. Conidiogenous cells endophialidic, flask-shaped (lageniform) producing various shapes of cylindrical conidia or tubular-form producing barrel-shaped (doliiform) conidia, either lageniform alone or both forms present. Conidia hyaline, 1-celled, doliiform to cylindrical. Aleurioconidia (in some literature as chlamydospores) absent or present, pale brown to dark brown, pyriform, ellipsoidal to globose, singly or in chains.

Culture characteristics:

Colonies showing circular growth with undulate margins, mycelium submerged to aerial, colour ranging from moderate yellowish brown to greyish or brownish olive when mature, releasing sweet fruity aroma. No growth on cycloheximide.

Optimal media and cultivation conditions: 2 % MEA incubated at 25 °C. Addition of thiamin stimulates the development of sexual morph.

Distribution:

Worldwide.

Hosts:

Herbaceous root crops, Ipomea batatas (sweet potato), wounds or larval tunnels of woody angiosperms, Acacia, Annona, Carya, Citrus, Coffea, Colocacia, Colophospermum, Combretum, Corymbia, Cunninghamia, Dalbergia, Eucalyptus, Coffea, Mangifera, Platanus, Populus, Prosopis, Punica, Quercus, Rapanea, Saccharum, Schizolobium, Schotia, Styrax, Syzygium, Terminalia, Theobroma. Some known to be vectored by flies (Diptera), non-specific ambrosia beetles (Scolytinae), or nitidulid beetles (Nitidulidae), but without specific insect associates.

Disease symptoms:

Root rot, cankers and vascular stain.

Notes:

Ceratocystis sensu lato included a heterogeneous group of fungi classified under this generic name due to similar morphology resulting from convergent evolution, despite diverse ecological and biological features (Upadhyay 1981). The group has recently been divided into seven more defined and homogeneous genera, supported by multigene phylogenies, morphological similarities and ecological resemblance (Wingfield et al. 2013a, De Beer et al. 2014). The family Ceratocystidaceae includes nine genera, namely Ambrosiella, Ceratocystis, Chalaropsis, Davidsoniella, Endoconidiophora, Huntiella, Thielaviopsis, Meredithiella and Phialophoropsis (De Beer et al. 2014, Mayers et al. 2015). The genus Ceratocystis sensu stricto is now restricted to those species producing ascomata with smooth bases, ascospores with hat-shaped sheaths, and thielaviopsis-like asexual states, which differentiate them from other genera (De Beer et al. 2014). Within Ceratocystis, morphological differences between species are insignificant and phylogenies based on multiple gene regions are used to distinguish them from each other (Fourie et al. 2015). The ITS region, the universal barcode marker for fungi, has been widely used for delimiting species of Ceratocystis (Schoch et al. 2012). However, discovery of multiple ITS types within single species in the genus (Al Adawi et al. 2013, Naidoo et al. 2013, Harrington et al. 2014) raised an awareness that the ITS region alone should not be applied to draw species boundaries in Ceratocystis, and that additional gene regions should also be considered. Loci such as bt1 and tef1 do not provide good species resolution on their own, but provide strong support in combination with ITS (Fourie et al. 2015). The loci rpb2 and ms204 give stronger resolution than tef1 and bt1, but also need to be used in combination with ITS (Fourie et al. 2015).

References:

• Hunt 1956, Upadhyay 1981 (morphology); Nag Raj & Kendrick 1975, Paulin-Mahady et al. 2002 (asexual morphs and species); Kile 1993, Van Wyk et al. 2013 (pathogenicity); De Beer et al. 2013a (higher classification); De Beer et al. 2013b (nomenclator); Wilken et al. 2013, Van der Nest et al. 2014a, b, Wingfield et al. 2015, 2016a, b (genomes); Wingfield et al. 2013a, De Beer et al. 2014 (generic definitions and phylogenetic relationships); Wingfield et al. 2013b (international spread).
• Al Adawi AO, Barnes I, Khan IA, et al. (2013). Ceratocystis manginecans associated with a serious wilt disease of two native legume trees in Oman and Pakistan. Australasian Plant Pathology 42: 179–193.
• De Beer ZW, Duong TA, Barnes I, et al. (2014). Redefining Ceratocystis and allied genera. Studies in Mycology 79: 187–219.
• De Beer ZW, Seifert KA, Wingfield MJ (2013a). The ophiostomatoid fungi: their dual position in the Sordariomycetes. In: The ophiostomatoid fungi: expanding frontiers. CBS Biodiversity Series 12 (Seifert KA, De Beer ZW, Wingfield MJ, eds). CBS-KNAW Fungal Biodiversity Centre, Utrecht, the Netherlands: 1–19.
• De Beer ZW, Seifert KA, Wingfield MJ (2013b). A nomenclator for ophiostomatoid genera and species in the Ophiostomatales and Microascales. In: The ophiostomatoid fungi: expanding frontiers. CBS Biodiversity Series 12 (Seifert KA, De Beer ZW, Wingfield MJ, eds). CBS-KNAW Fungal Biodiversity Centre, Utrecht, the Netherlands: 245–322.
• Fourie A, Wingfield MJ, Wingfield BD, et al. (2015). Molecular markers delimit cryptic species in Ceratocystis sensu stricto. Mycological Progress 14: 1–18.
• Harrington TC, Kazmi MR, Al-Sadi AM, et al. (2014). Intraspecific and intragenomic variability of ITS rDNA sequences reveals taxonomic problems in Ceratocystis fimbriata sensu stricto. Mycologia 106: 224–242.
• Hunt J (1956). Taxonomy of the genus Ceratocystis. Lloydia 19: 1–58.
• Kile GA (1993). Plant diseases caused by species of Ceratocystis sensu stricto and Chalara. In: Ceratocystis and Ophiostoma: Taxonomy, Ecology and Pathogenicity (Wingfield MJ, Seifert KA, Webber J, eds). APS Press, St. Paul, Minnesota, USA: 173–183.
• Mayers CG, Mcnew DL, Harrington TC, et al. (2015). Three genera in the Ceratocystidaceae are the respective symbionts of three independent lineages of ambrosia beetles with large, complex mycangia. Fungal Biology 119: 1075–1092.
• Nag Raj TR, Kendrick B (1975). A monograph of Chalara and allied genera. Wilfrid Laurier University Press, Waterloo, Canada.
• Naidoo K, Steenkamp E, Coetzee MPA, et al. (2013). Concerted evolution in the ribosomal RNA cistron. PLoS ONE 8: e59355.
• Paulin-Mahady AE, Harrington TC, McNew D (2002). Phylogenetic and taxonomic evaluation of Chalara, Chalaropsis, and Thielaviopsis anamorphs associated with Ceratocystis. Mycologia 94: 62–72.
• Schoch CL, Seifert KA, Huhndorf S, et al. (2012). Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proceedings of the National Academy of Sciences (USA) 109: 6241–6246.
• Upadhyay HP (1981). A monograph of Ceratocystis and Ceratocystiopsis. University of Georgia Press, Athens, Georgia, USA.
• Van der Nest MA, Beirn LA, Crouch JA, et al. (2014a). Draft genomes of Amanita jacksonii, Ceratocystis albifundus, Fusarium circinatum, Huntiella omanensis, Leptographium procerum, Rutstroemia sydowiana, and Sclerotinia echinophila. IMA Fungus 5: 473–486.
• Van der Nest MA, Bihon W, De Vos L, et al. (2014b). Draft genome sequences of Diplodia sapinea, Ceratocystis manginecans, and Ceratocystis moniliformis. IMA Fungus 5: 135–140.
• Van Wyk M, Wingfield BD, Wingfield MJ (2013). Ceratocystis species in the Ceratocystis fimbriata complex. In: The Ophiostomatoid Fungi: Expanding Frontiers (Seifert KA, De Beer ZW, Wingfield MJ, eds). CBS-KNAW Fungal Biodiversity Centre, Utrecht, the Netherlands: 65–73.
• Wilken PM, Steenkamp ET, Wingfield MJ, et al. (2013). Draft nuclear genome sequence for the plant pathogen, Ceratocystis fimbriata. IMA Fungus 4: 357–358.
• Wingfield BD, Ambler JM, Coetzee MPA, et al. (2016a). Draft genome sequences of Armillaria fuscipes, Ceratocystiopsis minuta, Ceratocystis adiposa, Endoconidiophora laricicola, E. polonica and Penicillium freii DAOMC 242723. IMA Fungus 7: 217–227.
• Wingfield BD, Barnes I, De Beer ZW, et al. (2015). Draft genome sequences of Ceratocystis eucalypticola, Chrysoporthe cubensis, C. deuterocubensis, Davidsoniella virescens, Fusarium temperatum, Graphilbum fragrans, Penicillium nordicum, and Thielaviopsis musarum. IMA Fungus 6: 493–506.
• Wingfield BD, Duong TA, Hammerbacher A, et al. (2016b). Draft genome sequences for Ceratocystis fagacearum, C. harringtonii, Grosmannia penicillata, and Huntiella bhutanensis. IMA Fungus 7: 317–323.
• Wingfield BD, Van Wyk M, Roos H, et al. (2013a). Ceratocystis: emerging evidence for discrete generic boundaries. In: The Ophiostomatoid Fungi: Expanding Frontiers (Seifert KA, De Beer ZW, Wingfield MJ, eds).  CBS-KNAW Fungal Biodiversity Centre, Utrecht, the Netherlands: 57–64.
• Wingfield MJ, Roux J, Wingfield BD, et al. (2013b). Ceratocystis and Ophiostoma: International spread, new associations and plant health. In: The Ophiostomatoid Fungi: Expanding Frontiers (Seifert KA, de Beer ZW, Wingfield MJ, eds). CBS-KNAW Fungal Biodiversity Centre, Utrecht, the Netherlands: 191–200.

Table 4. DNA barcodes of accepted Ceratocystis spp.

¹CBS: Westerdijk Fungal Biodiversity Institute, Utrecht, the Netherlands; MAFF: Ministry of Agriculture, Forestry and Fisheries, Tsukuba, Ibaraki, Japan. ^{T and PT} indicate ex-type and ex-paratype, respectively.

²ITS: internal transcribed spacers and intervening 5.8S nrDNA; bt1: partial β-tubulin gene; tef1: partial translation elongation factor 1-alpha gene, ms204: partial guanine nucleotide-binding protein subunit beta-like protein gene; rpb2: partial RNA polymerase II second largest subunit gene. ^*Multiple ITS types reported.

• Baker CJ, Harrington TC, Krauss U, et al. (2003). Genetic variability and host specialization in the Latin American clade of Ceratocystis fimbriata. Phytopathology 93: 1274–1284.
• Barnes I, Roux J, Wingfield BD, et al. (2003). Ceratocystis pirilliformis, a new species from Eucalyptus nitens in Australia. Mycologia 95: 865–871.
• Fourie A, Wingfield MJ, Wingfield BD, et al. (2015). Molecular markers delimit cryptic species in Ceratocystis sensu stricto. Mycological Progress 14: 1–18.
• Heath RN, Wingfield MJ, Wingfield BD, et al. (2009). Ceratocystis species on Acacia mearnsii and Eucalyptus spp. in eastern and southern Africa including six new species. Fungal Diversity 34: 41–68.
• Johnson JA, Harrington TC, Engelbrecht CJB (2005). Phylogeny and taxonomy of the North American clade of the Ceratocystis fimbriata complex. Mycologia 97: 1067–1092.
• Kamgan G, Jacobs K, De Beer ZW, et al. (2008). Ceratocystis and Ophiostoma species including three new taxa, associated with wounds on native South African trees. Fungal Diversity 29: 37–59.
• Kamgan Nkuekam G, Wingfield MJ, Mohammed C, et al. (2012). Ceratocystis species, including two new species associated with nitidulid beetles, on eucalypts in Australia. Antonie Van Leeuwenhoek 101: 217–241.
• Kajitani Y, Masuya H (2011). Ceratocystis ficicola sp. nov., a causal fungus of fig canker in Japan. Mycoscience 52: 349–353.
• Liu F, Mbenoun M, Barnes I, et al. (2015). New Ceratocystis species from Eucalyptus and Cunninghamia in South China. Antonie Van Leeuwenhoek 107: 1451–1473.
• Luchi N, Ghelardini L, Belbahri L, et al. (2013). Rapid detection of Ceratocystis platani inoculum by quantitative real-time PCR assay. Applied and Environmental Microbiology 79: 5394–5404.
• Marin M, Castro B, Gaitan A, et al. (2003). Relationships of Ceratocystis fimbriata isolates from Colombian coffee-growing regions based on molecular data and pathogenicity. Journal of Phytopathology 151: 395–405.
• Mbenoun M, Wingfield MJ, Begoude Boyogueno AD, et al. (2014). Molecular phylogenetic analyses reveal three new Ceratocystis species and provide evidence for geographic differentiation of the genus in Africa. Mycological Progress 13: 219–240.
• Rodas CA, Roux J, van Wyk M, et al. (2008). Ceratocystis neglecta sp. nov., infecting Eucalyptus trees in Colombia. Fungal Diversity 28: 73–84.
• Van Wyk M, Al-Adawi AO, Khan IA, et al. (2007). Ceratocystis manginecans sp. nov., causal agent of a destructive mango wilt disease in Oman and Pakistan. Fungal Diversity 27: 213–230.
• Van Wyk M, Al-Adawi AO, Wingfield BD, et al. (2005). DNA based characterization of Ceratocystis fimbriata isolates associated with mango decline in Oman. Australasian Plant Pathology 34: 587–590.
• Van Wyk M, Van der Merwe NA, Roux J, et al. (2006). Population genetic analyses suggest that the Eucalyptus fungal pathogen Ceratocystis fimbriata has been introduced into South Africa. South African Journal of Science 102: 259–263.
• Van Wyk M, Roux J, Barnes I, et al. (2004). Ceratocystis polychroma sp. nov., a new species from Syzygium aromaticum in Sulawesi. Studies in Mycology 50: 273–282.
• Van Wyk M, Roux J, Nkuekam GK, et al. (2012). Ceratocystis eucalypticola sp. nov. from Eucalyptus in South Africa and comparison to global isolates from this tree. IMA Fungus 3: 45–58.
• Van Wyk M, Wingfield BD, Al-Adawi AO, et al. (2011a). Two new Ceratocystis species associated with mango disease in Brazil. Mycotaxon 117: 381–404.
• Van Wyk M, Wingfield BD, Clegg PA, et al. (2009a). Ceratocystis larium sp. nov., a new species from Styrax benzoin wounds associated with incense harvesting in Indonesia. Persoonia 22: 75–82.
• Van Wyk M, Wingfield BD, Marin M, et al. (2010). New Ceratocystis species infecting coffee, cacao, citrus and native trees in Colombia. Fungal Diversity 40: 103–117.
• Van Wyk M, Wingfield BD, Mohali S, et al. (2009b). Ceratocystis fimbriatomima, a new species in the C. fimbriata sensu lato complex isolated from Eucalyptus trees in Venezuela. Fungal Diversity 34: 173–183.
• Van Wyk M, Wingfield BD, Wingfield MJ (2011b). Four new Ceratocystis spp. associated with wounds on Eucalyptus, Schizolobium and Terminalia trees in Ecuador. Fungal Diversity 46: 111–131.