A REVIEW OF Ceratocystis sensu stricto WITH SPECIAL REFERENCE TO THE SPECIES COMPLEXES C. coerulescens AND C. fimbriata

Mauricio Marín Montoya 1 y Michael J. Wingfield 2 ______

ABSTRACT

The genus Ceratocystis sensu stricto Ellis & Halst . includes many economically important plant pathogens of both angiosperms and gymnosperms, worldwide. Diseases caused by these fungi include vascular wilts, sap stains on logs and lumber, stem cankers and rots of roots, stems and fruits. Most Ceratocystis species are well adapted to dispersal by insects. Many species produce volatile metabolites with fruity odors that attract a wide range of insects to infected tissues. However, the degree of this association between insects and Ceratocystis species is highly variable, ranging from a mutualistic relationship such as that between C. polonica , C. laricicola and C. rufipennis and their specific bark beetle vectors, to non-specific associations, as are found in the case of C. paradoxa , C. fagacearum and C. fimbriata, with nitidulid beetles, flies and ambrosia beetles. The high degree of morphological similarity found amongst these fungi probably results from convergent evolution driven by selection for insect dispersal, and has made it difficult to clearly define the boundaries between species of Ceratocystis . During the course of the last decade, the use of phylogenetic studies based on comparisons of DNA sequence data has contributed substantially to clarify the taxonomy of this group of fungi. These studies have led to the conclusion that some Ceratocystis species thought to be single entities in the past actually represent complexes of cryptic species. This review is primarily intended to provide an introduction to experimental studies presented on species of Ceratocystis sensu stricto . However, in order to provide a firm background to this fungal genus, a brief outline is presented on related fungi that can broadly be referred to as the ophiostomatoid fungi.

Key words: Ophiostomatoid fungi, phylogenetic analysis, cryptic species, forest pathology.

1 Profesor Asistente, Universidad Nacional de Colombia, Sede Medellín. Escuela de Biociencias. A.A. 3840, Medellín, Colombia. 2 Director. Forestry and Agricultural Biotechnology Institute (FABI). Department of Microbiology and Plant Pathology. University of Pretoria, Pretoria, South Africa.

Recibido: Agosto 18 de 2005; aceptado: Febrero 16 de 2006.

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RESUMEN

REVISIÓN DE Ceratocystis sensu stricto CON ESPECIAL REFERENCIA A LOS COMPLEJOS DE LAS ESPECIES C. coerulescens Y C. fimbriata

El género Ceratocystis sensu stricto incluye un alto número de hongos fitopatógenos de plantas angiospermas y gimnospermas en diversas regiones del mundo. Entre las principales enfermedades causadas por estos hongos se destacan los marchitamientos vasculares, manchado de maderas, chancros y pudriciones radiculares, de tallos y frutos. Muchas especies producen metabolitos volátiles con olores que atraen una amplia variedad de insectos a los tejidos vegetales infectados, sin embargo, el grado de asociación entre los insectos y las diferentes especies de Ceratocystis es altamente variable, presentandose asociaciones mutualistas tales como aquellas entre C. polonica, C. laricicola y C. rufipenni e insectos escolítidos, así como también relaciones no específicas como en los casos de C. paradoxa , C. fagacearum y C. fimbriata con nitidúlidos, moscas y diversos coleópteros. El alto grado de similitud morfológica encontrada entre estos hongos hace difícil la definición de los límites entre las especies de Ceratocystis . Durante la pasada década, la utilización de estudios filogenéticos basados en comparaciones de DNA ha contribuido sustancialmente a clarificar la taxonomía de este grupo de hongos, así por ejemplo, dichos estudios han permitido concluir que algunas especies de Ceratocystis realmente representan complejos de especies crípticas. Esta revisión tiene como objetivo principal proveer una introducción a los estudios experimentales desarrollados para las especies de Ceratocystis sensu stricto y brevemente discutir aspectos relacionados con los denominados hongos ophiostomatoides.

Palabras claves: Hongos ophiostomatoides, análisis filogenético, especies cripticas, patología forestal. ______

The ophiostomatoid fungi include species are agents of sap stain on more than 100 species of ascomyce- conifers and hardwood trees, while tes that share morphological charac- others are aggressive pathogens of teristics and adaptation to dispersal economically important agronomic by insects and other arthropods crops (e.g. sweet potato, tobacco, (Wingfield et al. 1993, Harrington coffee, citrus, cacao, pineapple, 1993a, Kile 1993). These fungi are sugarcane, rubber) or forest trees found on a wide variety of substrates (e.g. oak, elm, eucalyptus and plane in tropical, subtropical and tem- trees) (Upadhyay 1981 1993, perate regions of the world. Ecologi- Wingfield et al . 1993). In addition, cally, they occupy a wide range of several ophiostomatoid fungi cause niches, ranging from saprotrophs to virulent systemic diseases in humans primary pathogens of both angios- and animals (Summerbell et al . perm and gymnosperm plants. Some 1993).

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Morphologically, the ophiostoma- fication. This confusion stems back to toid fungi are characterised by even 1891, when Halsted and spherical ascomatal bases with Fairchild misinterpreted the asco- elongated necks, deliquescent asci carps of the first described species, borne irregularly throughout the Ceratocystis fimbriata Ellis & Halst. as centrum of the ascocarps, and pycnidia (Nannfeldt 1932, Hunt single-celled ascospores that lack 1956, Griffin 1968, De Hoog 1974, germ-pores, often have ornamented Benny and Kimbrough 1980, sheaths and are produced in a Upadhyay 1981, De Hoog and mucilagenous matrix that exudes in Scheffer 1984, Von Arx and Van Der sticky droplets through ostioles at Walt 1988). Indeed the term the apices of the necks. The many "ophiostomatoid fungi" to some different anamorph states found extent illustrates this confusion and among the ophiostomatoid fungi all emerged from a meeting of scientists have holoblastic conidium deve- in 1990 who recognised that genera lopment, but display a variety of such as Ophiostoma and Ceratocystis conidiophore and conidial forms were phyologenetically unrelated but (Hunt 1956, Upadhyay 1981 1993, morphologically and ecologically si- Spatafora and Blackwell 1994). The milar (Wingfield et al . 1993). sticky spore masses (including the conidial masses produced by some Fifteen genera have historically been species) facilitate insect dispersal, as grouped within what are considered to they easily adhere to the insect be ophiostomatoid fungi. Some of bodies (Malloch and Blackwell these genera such as Ceratocystis Ellis 1993). The high degree of & Halstead and Ophiostoma H. & P. morphological similarity found Sydow, have been widely accepted, amongst these fungi is probably a whereas others have had limited re- result of convergent evolution, cognition and have later been consi- driven by selection for insect dered as synonyms or invalid genera dispersal (Spatafora and Blackwell (e.g. Ceratocystiopsis pad. & Kendrick, 1994). Endoconidiophora Münch, Europhium Parker) (Wingfield, Seifert and Webber The morphological similarity among 1993). To complicate matters further, the ophiostomatoid fungi made it more than 15 hyphomycete genera difficult to establish valuable taxo- with a wide range of conidiophores, nomic characters to delimitate them co-nidium ontogeny, and conidial at both lower (species, genera) and forms, have been linked to the higher (families, orders) taxonomic ophiosto-matoid fungi (Upadhyay and levels (Spatafora and Blackwell Kendrick 1975, Upadhyay 1981,1993). 1994). Consequently, controversial and often confusing taxonomic A major theme of the taxonomic debates have surrounded their classi- debates surrounding the ophiosto-

Rev.Fac.Nal.Agr.Medellín.Vol.59, No.1. p.3045-3075 2006. 3047 Marin, M.; Wingfield, M. matoid fungi has been whether they Thielaviopsis Went emend. Paulin, represent one or several genera, and Harrington et, McNew (Wingfield et more specifically whether Cerato- al . 1993, Paulin-Mahady, Harrington, cystis and Ophiostoma should be y McNew 2002). These anamorphs treated as congeneric (Hunt 1956, are distinguished by conidium Griffin 1968, Olchowecki and Reid development of ring wall building 1974, Upadhyay 1981 1993) or as (enteroblastic conidiogenesis) (Min- distinct genera (De Hoog 1974, De ter, Kirk y Sutton 1983, Minter 1987), Hoog and Scheffer 1984, Wingfield, and were recently transferred from Van Wyk y Marasas 1988). However, the genus Chalara (Corda) Rabenh. to more recent phylogenetic analyses Thielaviopsis based on analysis of based on DNA sequence comparisons sequence data from the ribosomal have demonstrated unequivocally RNA (rRNA) operon (Paulin-Mahady, that despite their morphologically Harrington y McNew 2002). Species similar teleomorphs, these genera are of Ceratocystis sensu stricto can also phylogenetically unrelated even at be distinguished from other ophios- the ordinal level, with Ceratocystis tomatoid fungi by the lack of residing in the Microascales and cellulose and rhamnose in their cell Ophiostoma being more closely rela- walls (Spencer and Gorin 1971, ted to species in the Diaporthales Jewell 1974, Weijman and De Hoog (Hausner et al . 1993a, b, Spatafora 1975) and their sensitivity to the and Blackwell 1994, Wingfield, antibiotic cycloheximide (Harrington Viljoen, y Wingfield 1999). Currently, 1981). five genera are accepted to belong to the wider group referred to as Ophiostoma. Fungi residing in the ophiostomatoid fungi. These include genus Ophiostoma are characterised Ceratocystis , Ophiostoma , Ceratocys- by having cellulose and rhamnose in tiopsis , Gondwanamyces Marais & their cell walls and being tolerant to Wingfield and Cornuvesica Viljoen & cycloheximide in culture (Harrington Winfield (Wingfield, Seifert and 1981, De Hoog and Scheffer 1984). Webber 1993, Upadhyay 1993, The anamorphs of these species are Marais et al . 1998, Viljoen, Wingfield accommodated in several hyphomy- and Wingfield 2000). This is despite cete genera, such as Leptographium the fact that they represent polyphy- Lagerberg & Melin, Pesotum Crane & letic lineages. Schocknecht, Sporothrix Hektoen & Perkins: Nicot & Mariat, Knoxdaviesia Ceratocystis. The name Ceratocystis Wingfield, van Wyk & Marasas and sensu lato has been used collectively Hyalorhinocladiella Upadhyay & Ken- for all the ophiostomatoid fungi, drick (Wingfield et al . 1993, Okada et while Ceratocystis sensu stricto is al . 1998, Hausner, Reid y Klassen used exclusively for species with 2000, Jacobs and Wingfield 2001). In anamorphs in the form-genus all these genera conidium develop-

3048 Rev.Fac.Nal.Agr.Medellín.Vol.59, No.1. p.3045-3075.2006. A review of Ceratocystis sensu... ment occurs exogenically through tocystiopsis falcata (Wright & Cain) apical wall building (holoblastic Upadhyay, which has a Chalara -like conidiogenesis) (Minter, Kirk y Sutton anamorph but is phylogenetically 1982). unrelated to Ceratocystis sensu stricto (Hausner, Reid y Klassen 1993- Ceratocystiopsis. The genus Cera- b , Viljoen, Wingfield y Wingfield tocystiopsis was established to 2000). accommodate ophiostomatoid fungi with elongate or falcate ascospores Ceratocystis sensu stricto. The surrounded by a falcate sheath with genus Ceratocystis sensu stricto attenuated ends (Upadhyay and includes many economically impor- Kendrick 1975, Upadhyay 1981, tant plant pathogens that especially Wingfield 1993). Anamorphs of these occur in tropical and sub-tropical species are formed by both en- regions of the world. Most species teroblastic and holoblastic conidio- require wounds in order to infect genesis and have included Spo- their hosts, and their pathogenicity rothrix, Hyalorhinocladiella, Chalara varies widely from weakly virulent and Knoxdaviesia states. However, fungi to very aggressive pathogens. the validity of this genus remains Some species have even a sapro- uncertain, as morphological and trophic life style ( Ceratocystis moni- molecular data have shown that liformis (Hedgc.) C. Moreau). Di- most species should be included seases caused by these fungi include within Ophiostoma (Wingfield vascular wilts, sap and lumber stains, 1993, Hausner, Reid y Klassen stem cankers and rots of roots, stems 1993a 1993 b) but that others with and fruits (Kile 1993, Harrington, Knoxdaviesia and Chalara ana- Wingfield and Kile 1996). morphs reside in genera such as Gondwanamyces and Cornuvesica , The most virulent Ceratocystis species respectively (Marais et al. 1998, generally cause vascular wilts and Viljoen et al . 2000) that are stem cankers of trees and other woo- unrelated to Ophiostoma . dy plants. For example, Ceratocystis fagacearum (Bretz) Hunt causes the Gondwanamyces and Cornuvesica. disease known as oak wilt of Quercus The genus Gondwanamyces was spp. in North America (Henry et al . recently established to accommodate 1944), Ceratocystis fimbriata causes two ophiostomatoid species with wilt and cankerstain diseases on a Knoxdaviesa anamorphs ( Ceratocys- wide range of hosts including cocoa tiopsis proteae Wingfield, Van Wyk & (Theobroma cacao L.) (Schieber Marasas and Ophiostoma capense 1969), coffee ( Coffea arabica L.) Wingfield & Van Wyk) (Marais et al . (Pontis 1951) and plane trees 1998). Cornuvesica was erected to (Platanus spp.) (Walter 1946, include the former species Cera- Panconesi 1981), Chalara autralis

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Walker & Kile cause a serious wilt Members of the genus Ceratocystis disease of Nothofagus cunninghamii have several means of transmission (Hook.) Oerst (Kile and Walker 1987) and dispersal, in addition to being and Ceratocystis polonica (Siemasz- vectored by insects. Species produ- ko) Moreau displays relatively high cing chlamydospores are usually soil- levels of virulence to Norway spruce borne (Rossetto and Ribeiro 1990, (Picea abies L. Karst.) and other Kile 1993), whereas those that spo- spruce species in Eurasia (Siemaszko rulate aerially are dispersed by wind 1939, Solheim 1986 1988, Krokene and water splash (Baker and Thomas and Solheim 1998, Kirisits 2001). 1946, Vigouroux and Stojadinovic 1990). Species that cause vascular Weaker pathogens include agents of wilts and woodstain can also be sap stain of lumber such as Cera- transmitted through root grafts tocystis coerulescens (Münch) Bakshi (Gibbs and French 1980, Accordi on conifers and Ceratocystis douglasii 1986) and by pruning tools. This is (Davidson) Wingfield & Harrington especially important for the spread of on Douglas-fir ( Pseudotsuga men- Ceratocystis pathogens in agricultural ziesii (Mirb.) Franco) (Münch 1907, crops and forest plantations (Walter, Harrington, Wingfield and Kile 1996, Rex and Schreiber 1952, Matasci and Wingfield, Harrington and Solheim Gessler 1997). 1997, Harrington and Wingfield 1998). Other weak pathogens include Most Ceratocystis species are well species producing lumber stain in adapted to dispersal by insects. Many hardwoods such as Ceratocystis vires- species produce volatile metabolites cens (Davidson) C. Moreau on maple with sweet fruity odours that attract (Acer saccharum Marsh.) (Davidson a wide range of insects to infected 1944) and Ceratocystis eucalypti tissues (Hanssen 1993, Kile 1993). Yuan & Kile on Eucalyptus spp. (Kile However, the intimacy ot the et al . 1996). association between insects and Ceratocystis species is highly variable. Likewise, various annual crop plants Species such as C. polonica, Cerato- are also seriously affected by Cerato- cystis laricicola Redfern & Minter and cystis species. Ceratocystis paradoxa Ceratocystis rufipenni Wingfield, (Dade) Moreau causes tissue rot on Harrington & Solheim, seem to have sugar cane ( Saccharum officinarum L.), a mutualistic relationship with their Musa spp. and Cocus nucifera L. (Kile bark beetle vectors (Redfern et al . 1993). Similarly, Ceratocystis adiposa 1987, Solheim 1988, Wingfield, (Hedgcock) Moreau incites tissue rot Harrington and Solheim 1997). On on sugar cane (Butler 1906) and the other hand, species such as C. Ceratocystis radicicola (Bliss) Moreau paradoxa (Chang and Jensen 1974), causes a root rot on date palms C. fagacearum (Juzwik and French (Phoenix dactylifera L.) (Bliss 1941). 1983, Appel, Kurdyla and Lewis

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Junior 1990), C. fimbriata (Crone and switching (Harrington and McNew Bachelder 1961, Hinds 1972) and C. 1997,1998). In these species, selffer- moniliformis (Hinds and Davidson tile strains that contain both mating 1972) have non-specific associations type idiomorphs give rise to both with fungivorous or sap-feeding in- selffertile and self-sterile strains. The sects such as nitidulid beetles latter contain only the MAT-1 gene, (Coleoptera: Nitidulidae), flies (Dipte- and these MAT-1 strains can cross ra: Drosophilae) and ambrosia bee- with the selffertile strains. Progeny of tles (Peplinski and Merril 1974, Kile selfing and crossing events segregate 1993). in a 1:1 ratio, with half the ascor- pores being selffertile (MAT-1 and Different modes of reproduction are MAT-2) and the other half selfsterile found among Ceratocystis species, (MAT-1). It has been shown that self including heterothallism, homotha- sterile strains are produced as the llism and exclusive asexual repro- result of a deletion of the MAT-2 duction (Harrington, Steimel and Kile idiomorph, which then results in the 1998). Genetic studies have shown expression of only the MAT-1 mating that sexuality in these species is type (Witthuhn et al . 2000). controlled by two mating-type genes designated MAT-1 and MAT-2 The close morphological similarity (Harrington and McNew 1997,1998). between many Ceratocystis species In strictly heterothallic species, such contributes to poorly defined species as C. eucalypti and C. fagacearum , boundaries within the genus sexual progeny are only produced (Harrington, Wingfield and Kile 1996). upon mating of strains representing Phylogenetic studies using DNA se- different mating types (Kile et al . quence data from the rRNA operon 1996, Harrington, Steimel and Kile (Wingfield et al . 1994, Visser et al . 1998). Other species, such as Ch. 1995, Wingfield et al . 1996, Witthuhn australis and Chalara neocaledoniae et al . 1998, 1999, Barnes et al . 2003), Kiffer & Delon, are known only by mating type genes (Witthuhn et al . their anamorph states, and suppo- 2000, Harrington et al . 2002) and sedly only reproduce asexually (Kile microsatellite DNA regions (Barnes et et al . 1996, Harrington, Steimel and al . 2001) have suggested that some Kile 1998). However, most Cerato- Ceratocystis species that have been cystis species, including among regarded as single entities in the past, others, C. fimbriata , C. coerulescens , actually represent complexes of cryptic C. virescens , C. polonica and Cera- species. Two of these species comple- tocystis pinicola Harrington & Wing- xes, the C. coerulescens and C. field , are homothallic and also fimbriata complex, are treated in more undergo unidirectional mating type detail below (Figure 1).

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C. fimbriata

C. virescens (C74) (Quercus) 7 C. virescens (C251) (Acer) 54 Ch. australis ( Nothofagus ) C. virescens (C69) 1 100, d6 C. virescens (C203) 3 3 61, d3 C. eucalypti ( Eucalyptus ) 59, d1 Ch. neocaledoniae ( Coffea )

11 9 C. douglasii (Pseudotsuga ) 2 2 96, d5 C. coerulescens sp. A ( Pinus ) 2 62, 3 d1 6 10 C. coerulescens sp. B ( Picea )

5 98, d3 C. laricicola (Larix) C. polonica ( Picea ) 85, d1

1 C. coerulescens sp. C (C50) 1 C. coerulescens sp. C (C662) 71 C. coerulescens sp. C (C666) d1 50, d1

4 C. rufipenni (C609) (Picea ) C.rufipenni (C610) 90, d3 C. rufipenni (C612 )

Figure 1. Phylogeny of the Ceratocystis coerulescens species complex and its relationship with Ceratocystis fimbriata . The phylogenetic tree was produced from the DNA sequence of a 565 bp region of the ribosomal RNA operon using PAUP (Witthuhn et al. 1998).

Ceratocystis coerulescens com- operon and MAT-2 HMG box have plex. Eleven species have been shown that the species occurring on grouped in the Ceratocystis coeru- conifers form a single monophyletic lescens complex. These species have clade, with the hardwood species as similar morphology and are closely their basal ancestor (Witthuhn et al . related based on DNA sequence data 1998, 2000). It has thus been sug- and isozyme profiles (Harrington, gested that adaptation to conifer Wingfield and Kile 1996, Harrington hosts occurred once in the evolu- and Wingfield 1998, Witthuhn et al . tionary history of Ceratocystis 1999, 2000). Seven species cause sap (Witthuhn et al . 1998, 2000). stain on conifers in the family Pinaceae, while four species are Ceratocystis coerulescens was the pathogens or incite sap stain on first species described in the group hardwood trees. Phylogenetic ana- colonizing conifers (Münch 1907). lysis using sequences of the rRNA This fungus causes blue-stain of

3052 Rev.Fac.Nal.Agr.Medellín.Vol.59, No.1. p.3045-3075.2006. A review of Ceratocystis sensu... spruce and pine sapwood in Europe beetle Ips cembrae Heer in Europe and North America (Münch 1907, and Japan (Redfern et al . 1987, Harrington, Wingfield and Kile 1996, Yamaoka et al . 1998, Kirisits 2001, Harrington and Wingfield 1998). Stauffer et al . 2001). The remaining Ceratocystis pinicola occurs in Britain species in the conifer subgroup is C. and is an agent of blue-stain on pine polonica, which is a pathogen and logs and lumber (Gibbs 1993, agent of blue-stain on Norway spruce Harrington and Wingfield 1998). and other spruce species in Europe Ceratocystis rufipenni was described and Japan (Solheim 1986, Yamaoka from Engelmann spruce ( Picea et al . 1997). This Ceratocystis species engelmannii Parry ex Engelm.) and is primarily vectored by the aggre- white spruce ( Picea glauca (Moench) ssive bark beetle Ips typographus L. Voss) infested by the North American (Siemaszko 1939, Furniss, Solheim spruce bark beetle, Dendroctonus and Christiansen 1990) . In addition, rufipennis Kirby in British Columbia Ips typographus f. japo-nicus Niijima (Wingfield, Harrington and Solheim in Japan (Yamaoka et al . 1997) as 1997). It is virulent on Sitka spruce well as Ips amitinus Eichhoff (Kirisits (Picea sitchensis (Bong.) Carr.) and 2001) and Ips duplicatus Sahlberg can kill trees that have been (Krokene and Solheim 1996) in inoculated in sufficiently high do- Europe have recently been identified sages (Solheim and Safranyik 1997). as important vectors of C. polonica . Ceratocystis resinifera Harrington & Wingfield has been found in The four Ceratocystis species continental Europe and North occurring on hardwoods include C. America and colonizes wounds of live virescens that causes sapstreak in spruce trees (Harrington, Wingfield maple and other hardwood species in and Kile 1996, Harrington and eastern North America (Davidson Wingfield 1998). Ceratocystis dou- 1944, Harrington and Wingfield glasii has originally been recognized 1998), C. eucalypti that is a wound as a form of C. coerulescens colonist on Eucalyptus spp. in (Davidson 1953), but has sub- Tasmania and Victoria, Australia (Kile sequently been described as a new et al . 1996), and two asexual species species (Wingfield, Harrington and occurring in Australia, Ch. australis Solheim 1997). This fungus stains the and Ch. neocaledoniae . The first of sapwood of Douglas-fir in western these is a virulent pathogen causing North America, and appears to be myrtle wilt on Nothofagus restricted to the natural range f its cunninghamii in Tasmania (Kile et al . host (Wingfield, Harrington and 1996). The latter species produces a Solheim 1997, Harrington and Wing- vascular wilt disease on coffee (Coffea field 1998). Ceratocystis laricicola robusta Linden ex Wild.) and guava infests larch ( Larix spp.) and has a trees ( Psidium guajava L.) (Kile and mutualistic association with the bark Walker 1987).

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The Ceratocystis species occurring on and McNew 1998, Witthuhn et al . hardwoods and conifers can be 1998, 2000, Harrington and Wing- distinguished morphologically, based field 1998, Harrington et al . 2002). on conidiophore characteristics. The They have added considerable hardwood group has tapering and resolution to the taxonomy of nine of these species, but problems have proliferating phialides, while the co- remained in distinguishing between nifer species lack these phialide C. polonica and C. laricicola. characters (Harrington, Wingfield and Kile 1996). The conifer species Ceratocystis polonica was first isola- can be reliably subdivided into two ted from Norway spruce in Poland morphologically well-defined groups: and described by Siemaszko 1939 as C. coerulescens sensu lato, where the Ophiostoma polonicum. Visser et al . ascospores are surrounded by an 1995 reported the presence of a even sheath that is wider at the Chalara ( Thielaviopsis ) anamorph in ends than at the sides, and C. cultures of O. polonicum , and this characteristic, together with DNA se- polonica sensu lato , where quence comparisons, clearly showed ascospore sheaths are wider at the that this fungus is a species of Cera- sides than at the ends (Harrington tocystis . Ceratocystis laricicola , on and Wingfield 1998). Within the other hand, was correctly Ceratocystis coerulescens sensu lato described by Redfern et al . 1987. It on conifers, small morphological was, however, not compared with C. differences exist (Harrington and polonica, probably due to the fact Wingfield 1998), however, une- that C. polonica was not recognised quivocal separation of the entire as having a Chalara state at the time conifer colonizing species is when C. laricicola was described (Harrington and Wingfield 1998). practically only possible through Later studies showed the two species isozyme and DNA sequence were morphologically indistinguish- comparisons (Harrington, Wingfield able (Harrington and Wingfield and Kile 1996, Witthuhn et al . 1998, 1998), had identical ITS sequences 2000, Harrington et al . 2002). (Witthuhn et al . 1998), and a low level of isozyme variation (Harrington, Ceratocystis polonica sensu lato. Wingfield and Kile 1996). However, As discussed above, species in the C. they represent distinct ecological coerulescens complex have been entities (Siemaszko 1939, Solheim widely studied during the course of 1986, Redfern et al . 1987) and are true the past decade. These studies have biological species, as interspecific included several phenotypic and ge- crosses between MAT-1 and MAT-2 notypic characters (Harrington, strains of both species fail to produce Wingfield and Kile 1996, Harrington viable progeny (Harrington and

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McNew 1998, Harrington et al . has been introduced to Scotland and 2002). Denmark (Crooke and Bevan 1957, Redfern et al. 1987, Stauffer et al . These two fungi, together with C. 2001). This bark beetle is regarded as rufipenni are especially important for a secondary although important pest forestry, because they are associated of larch and plays a particularly with aggressive tree-killing bark important role in regions outside the beetles. Ceratocystis polonica is a natural range of European larch mutualistic associate of the Eurasian (Schimitschek 1931, Postner 1974, spruce bark beetle, I. typographus , Stauffer et al . 2001). For example, I. which is a highly destructive pest of cembrae and C. laricicola have Norway spruce throughout Eurasia become principal pests of larch in (Postner 1974, Chrisiansen and Bakke Scotland, after their introduction in 1988). Since the 18 th century I. 1955 with imported timber from typographus has caused large-scale Germany (Crooke and Bevan 1957, outbreaks with millions of killed Redfern et al . 1987). trees (Klimetzek and Yue 1997) in Scan-dinavia and central Europe Mass inoculation experiments that (Postner 1974, Christiansen and aim to mimic natural mass-attacks by Bakke 1988, Führer 1996, Kirisits bark beetles, have demonstrated that 2001). The most recent and still both C. polonica (Christiansen 1985, ongoing outbreak of I. typographus Solheim 1988, Kirisits 1998, Krokene in central and western Europe and Solheim 1998, Yamaoka, Taka- started around 1992 and has been hashi and Iguchi 2000, Kirisits and triggered by destructive wind- Offenthaler 2002) and C. laricicola throws, followed by years with (Redfern et al . 1987, Yamaoka et al . warm and dry climate (Führer 1996, 1998, Kirisits 2001) are able to kill Kirisits 2001). From 1985 to 1994, the their respective host trees. It is I. typographus – C. polonica complex thought that through the mutualistic has been responsible for losses of association between these bark about 14,1 million cubic meters of beetles and the specific Ceratocystis spruce wood in Austria, Switzerland spp. that they carry, the fungus and the German province Baden- increases the impact of each beetle Württemberg alone (Führer 1996). attack and thereby contributes to exhaust the host defences and makes Ceratocystis laricicola is vectored by the tree suitable for bark-beetle the eight spined larch bark beetle, I. reproduction (Whitney 1982, cembrae (Redfern et al . 1987, Harrington 1993b, Paine, Raffa and Yamaoka et al . 1998, Stauffer et al . Harrington 1997). Reciprocally, these 2001, Kirisits 2001), which is distri- fungi benefit by being dispersed and buted across continental Europe and introduced into suitable host trees by Asia (Postner 1974, Pfeffer 1995) and their beetle vectors (Whitney 1982,

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Malloch and Blackwell 1993, Krokene infections, such as those reported in 1996). Ironically, the less virulent the forest tree pathogens Ophios- pathogenic Ophiostoma spp. associa- toma novoulmi (Rogers, Buck, and ted with these insects (Solheim 1986, Braiser 1987, Cole et al . 1998) and Krokene 1996, Krokene and Solheim Cryphonectria parasitica (Nuss 1992, 1998, Kirisits 2001, Viiri 2002) gain 2000), might have been involved but the same dispersal advantage, simply were not considered. by being present in this environment. Spruce trees infected by C. polonica Mechanisms of fungal colonization respond in several ways to contain and host responses have been the fungus. Responses such as particularly well studied in the C. cellular proliferation, mobilization of polonica – Norway spruce system. polyphenolic parenchyma cells, for- Fungal succession studies have mation of traumatic resin ducts, shown that C. polonica is the first lignification (Nagy et al . 2000, species to invade the sapwood after Evensen et al . 2000, Krokene, I. typographus has attacked a tree Solheim and Christiansen 2003) as (Solheim 1992). This is probably due well as translocation of starch re- to its rapid growth and its ability to serves (Christiansen and Ericsson tolerate the low oxygen levels found 1986) have been shown to be part of in living sapwood (Solheim 1991). the defence mechanisms. Further- However, not all isolates of C. more, experiments have shown that polonica have the same ability to kill preinoculation of spruce trees with trees and to induce intensive blue- non lethal dosages of C. polonica stain in the spwood of its host tree. inoculum induces disease resistance Isolates with low levels of virulence that protects trees against subse- have been reported from indepen- quent mass infections of the same dent mass inoculation experiments in fungus (Christiansen et al . 1999, Austria (Kirisits and Anglberger 1999, Krokene and Solheim 2001). The Baier et al . 2002) and Norway mechanisms underlying this induced (Krokene and Solheim 2001). Kirisits resistance differ from the systemic and Anglberger 1999 considered the acquired resistance (SAR) present in low level of virulence as a general angiosperms, since it is non-systemic characteristic of the particular isolate and non-specific (Krokene, Solheim used in their experiment. Likewise, in and Christiansen 2003). The induced the Norwegian study loss of patho- resistance of Norway spruce is due to genicity was attributed to senescence anatomical and biochemical reactions of the isolates after several transfers in the phloem and the sapwood, in of cultures during routine storage or, which polyphenolic parenchyma cells alternatively, to long periods of and traumatic resin ducts are in- storage of the isolates (Krokene and volved (Krokene, Solheim and Solheim 2001). However, mycoviral Christiansen 2003). Different ne-

3056 Rev.Fac.Nal.Agr.Medellín.Vol.59, No.1. p.3045-3075.2006. A review of Ceratocystis sensu... crotizing fungi, chemical elicitors and 1950 amendment, the name C. fim- even mechanical wounding can briata became widely accepted activate a similar defence response (Griffin 1968, Von Arx 1974, compared to that induced by pre- Upadhyay 1981). treatment with C. polonica (Christiansen et al . 1999, Krokene Morphologically, C. fimbriata is cha- and Solheim 2001, Franceschi, racterised by perithecia with long Krekling and Christiansen 2002). necks that taper towards the tips and terminate in 8 to 15 convergent The Ceratocystis fimbriata com- ostiolar hyphae. Perithecial bases are plex. Ceratocystis fimbriata was first dark and globose, surrounded by a reported causing rot of sweet potato dense network of hyphae. Asci are (Ipomoea batatas L.) in 1890 in New evanescent in the early stages of Jersey, USA (Halsted 1890). It is the development, while ascospores are type species of the genus Ce- characteristically hat-shaped and exu- ratocystis and as in the case of other ded through the perithecial necks in Ceratocystis species, its taxonomy sticky masses (Hunt 1956, Upadhyay was unclear for more than fifty years. 1981). The fungus also produces Saccardo 1892 reclassified this chains of cylindrical conidia and fungus as Sphaeronaema fim- aleurioconidia (chlamydospores) that briatum , while Zimmerman 1900 play an important role in the survival described a strain of C. fimbriata of this fungus in the soil (Pontis causing coffee canker in Java 1951, Webster and Butler 1967, (Indonesia) as a separate species, Accordi 1989). The anamorph of C. Rostrella coffea Zimmermann. Elliott fimbriata has for many years been 1923 renamed C. fimbriata as accommodated in Chalara (Hunt Ceratostomella fimbriata , but when 1956, Nag Raj and Kendrick 1975, Nannfeldt 1932 erected the family Upadhyay 1981), but recently, based Ophiostomataceae, the species was on a phylogenetic analysis of DNA transferred to the genus sequence data, has been recognised Ophiostoma , and later, based on the as best residing in Thielaviopsis presence of endoconida (now (Paulin-Mahady et al . 2002). recognised as the Thielaviopsis state) to Endoconidiophora (Davidson Ceratocystis fimbriata is one of the 1935). The name Ceratocystis fim- most aggressive plant pathogens in briata was recognized again by the genus Ceratocystis , causing wilt, Bakshi 1950, who revived the generic canker-stain diseases as well as tissue name Ceratocystis and considered rot on a wide variety of perennial as Ophiostoma , Endoconidiophora , well as agronomic crop plants, Rostrella , Linostoma and Gros- worldwide (Kile 1993). More than 30 mannia as synonyms of Ceratocystis . economically important plants are When Hunt 1956 accepted Bakshi’s attacked by this pathogen (Baker and

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Harrington 2000) including, among (Pontis 1951). The fungus is easily others, plane trees (Walter, Rex and transported on agricultural tools or Schreiber 1952, Panconesi 1981), with soil. Thus, a major factor asso- Eucalyptus spp. (Roux et al . 1999, ciated with spread of coffee canker in Roux et al . 2001), aspen ( Populus tre- Colombia is infection through muloides Michx.) (Zalasky 1965, Hinds wounds on the lower stems made by 1972), rubber ( Hevea brasiliensis the shoes of farmers needing to se- (Wiild: Juss.) Mull-Arg.) (Silveira et al . cure themselves on the steep slopes 1994), mango ( Mangifera indica L.) on which coffee is cultivated (Castro (Batista 1960), almond ( Prunus 1991). amygdalus Batsch.) (De Vay et al . 1968, Teviotdale and Harper 1991), Ceratocystis fimbriata was first re- Syngonium spp. (Walker et al . 1988) ported on cacao in Ecuador in 1918, and pimento trees ( Pimenta officinalis causing a serious wilt disease L.) (Leather 1966). (Desrosiers 1958). This disease was subsequently found in Venezuela Ceratocystis fimbriata is particularly (Malaguti 1952), Colombia (Idrobo important in Latin America, where it 1958), Trinidad (Goberdhan 1959), causes substantial losses in three of Costa Rica (Havord 1962) and the the main perennial crops that are Dominican Republic (Schieber 1969). grown in this region: coffee, cocoa Recently, cacao wilt disease has also and citrus ( Citrus spp.). Coffee canker been detected in Brazil, in plantations has been reported from Colombia from South Bahia (Bezerra 1997). (Obregon 1936), Venezuela (Pontis Cacao wilt is frequently associated 1951), Guatemala (Szkolnik 1951) with wounds made by machetes and and Costa Rica (Echandi and Segall other tools. The mycelium and spores 1956). Symptoms of diseased plants enter the xylem and ray parenchyma include yellowing of foliage, dieback cells through such fresh wounds, and and wilt. When the outer surface of cause dark reddish to purple staining the stem bark of infected trees is that may develop into a vascular wilt. removed, dark lesions are obvious Externally, the disease is easily recog- and these usually extend downwards nized because wilted leaves be-come towards the roots and girdle the dry, curled and remain attached to trunks, causing tree death (Pontis the trees for several weeks (Montes 1951, Castro 1991). Coffee canker de Oca 1975). The incidence of cacao has become one of the most impor- wilt has been reduced significantly in tant threats to coffee production in Latin America in recent years, Colombia, where more than 800000 especially because resistant varieties hectares of this crop are planted have become widely available for (Castro 1998). The principal mode of planting (Delgado and Echandi 1965, ingress for C. fimbriata into coffee Ocampo, Mafla and Victoria 1982, trunks is through mechanical wounds Simmonds 1994).

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The first report of C. fimbriata in tries such as Colombia and Costa citrus orchards was made in 1981, Rica, several native hosts (e.g. Inga when it caused serious dieback on sp., Herrania sp., Annona muricata L., lime trees ( Citrus aurantifolia Caryodendron orinocense Karst.) are (Christm.) Swing) in the central infected by this pathogen (Montes de region of Colombia (Instituto Oca 1975, Pardo-Cardona 1995 and Colombiano Agropecuario 1993). Buriticá 1999), but their role as Three years later, it was also found alternative hosts and sources of on lemon trees ( Citrus limon inoculum for susceptible agricultural Burmman) in Argentina (Contreras crops remains uncertain. and Marmelioz 1984). By 1994, about 10% of the citrus trees in Ceratocystis fimbriata has long been Colombia had been killed by the recognised as a variable fungus con- pathogen (Mourichon 1994). The sisting of distinct, host-specialized disease is characterised by a general strains (Webster and Butler 1967, yellowing of the foliage, followed by Harrington 2000). The best studied heavy defoliation and prominent of these host specific races is C. shoot proliferation. Internally, brown fimbriata forma specialis platani , to reddish lesions are evident in the which causes a canker stain disease stele of the trunk, and, as the disease of plane trees in the Northern hemis- progresses, lesions converge and be- phere (Walter, Rex and Schreiber come flame shaped, black in colour, 1952, Santini and Capretti 2000). and trees are eventually killed Similarly, reciprocal inoculation ex- (Mourichon 1994). periments have demonstrated the existence of host-specific isolates on The taxonomic complexity of what pimento (Leather 1966), sweet po- has been referred to as C. fimbriata tato (Kojima and Uritani 1976), in Latin America became evident in a Syngonium (Vogelzang and Scott recent study based on ITS sequence 1991) and cocoa (Baker and comparisons and microsatellite ana- Harrington 2000). Earlier genetic lysis (Barnes et al . 2001). Isolates of analyses indicated that such host- C. fimbriata from coffee in Colombia specialized isolates could represent were found to reside in two distinct, but closely related species genetically isolated groups that (Olsen and Martin 1949, Webster and might represent different species. Butler 1967). The view that the host However, apart from this study and is an important factor separating scattered information that is not strains of C. fimbriata sensu lato has widely available in the scientific recently also been confirmed based literature, very little is known on DNA sequence data (Wingfield et regarding the biology, ecology or al . 1996, Witthuhn et al . 1998, genetic background of C. fimbriata in Santini and Capretti 2000, Barnes et Latin America. For example, in coun- al . 2001 2003). Witthuhn et al . 1999

Rev.Fac.Nal.Agr.Medellín.Vol.59, No.1. p.3045-3075 2006. 3059 Marin, M.; Wingfield, M. found that isolates of C. fimbriata from this species in its pear-shaped from Populus spp., Prunus spp. and perithecial bases. Phylogenetic Platanus spp. could be separated analysis of the rRNA ITS regions also based on RFLP analysis of the ITS supported the definition of this regions of the rRNA operon. Similar fungus as a new Ceratocystis species results were obtained by Santini and (Barnes et al . 2003). Capretti 2000 and Barnes et al . 2001, using RAPD / minisatellite markers and microsatellite markers, res- CONCLUSIONS pectively. Thus, C. fimbriata strains from different hosts and geo- Selection pressure for insect disper- graphical regions grouped in sion has resulted in convergent separated clades in accordance with morphological characteristics in the their respective hosts and origins. ophiostomatoid fungi, which has made it difficult to establish reliable The view that C. fimbriata may taxonomic characters for this group represent a complex of cryptic of fungi. Thus, the classification of species has gained further support by these fungi has been the subject of the recent description of two new substantial debate since the first Ceratocystis species that probably ophiostomatoid species was descri- used to be treated within C. bed in 1890. In recent years, phylo- fimbriata . Ceratocystis albofundus genetic analyses using DNA sequence Wingfield, De Beer & Morris was data have provided new clarity to reported causing wilt and die-back of classification of these fungi and have Acacia mearnsii Wildeman in South facilitated more accurate identi- Africa (Morris, Wingfield and De Beer fication of them. 1993, De Beer 1994). Detailed mor- phological and molecular compari- The genus Ceratocystis sensu stricto sons showed that the fungus repre- is reserved for those ophiostomatoid sents a distinct Ceratocystis species fungi that have Thielaviopsis ana- that is characterised by light-co- morphs, that are intolerant to the loured perithecial bases, dark necks, antibiotic cycloheximide in culture divergent ostiolar hyphae and and that lack cellulose and rhamnose distinct ITS sequences (Wingfield et in their cell walls. Some of these al . 1996, Roux et al . 1999). The other species are economically important new species from wounds on plant pathogens of both agricultural Eucalyptus in Australia has recently crops and forest plantation trees. As been described as Ceratocystis piri- species of Ceratocystis have been lliformis Barnes & Wingfield (Barnes more intensively studied, it has et al . 2003). This species has hat- become evident that some of the shaped ascospores similar to those species in fact represent a complex of found in C. fimbriata , but differs several host-specialized forms and

3060 Rev.Fac.Nal.Agr.Medellín.Vol.59, No.1. p.3045-3075.2006. A review of Ceratocystis sensu... cryptic taxa. This has important impli- within this complex of important cations, especially in designing for plant pathogens. quarantine measures against these pathogens. Much literature has been generated for Ceratocystis sensu stricto . During Nine of the eleven species thus far the last decade, research dealing identified in the C. coerulescens with these fungi was especially complex have been unequivocally focused in understanding the phylo- delimited using a wide variety of genetic relationships amongst Cera- phenotypic and genotypic charac- tocystis species. However, a few teristics. Nevertheless, problems have studies deal with the population been experienced in separate C. biology of Ceratocystis species. The polonica and C. laricicola . This is knowledge of the level of variability because they are morphologically and degree of genetic structure of indistinguishable, have similar iso- natural populations of plant patho- zyme profiles and identical ITS gens is important to establish sequences. Both species are hypothesis regarding their origin, associated with aggressive conifer movement and reproduction stra- bark beetles and are able to kill their tegies. This information is likely to be hosts, which justifies a more required in the planning and intensive study of them. Improved implementation of management stra- taxonomy of these species and an tegies against diseases caused by extended knowledge regarding their species of Ceratocystis , including population characteristics would generation of resistant plant expand our understanding of their material, development of quarantine epidemiological relationships with strategies and appropriate use of insect vectors and host trees. chemical control measures.

Ceratocystis fimbriata represents one ACKNOWLEDGEMENTS of the most virulent and econo- mically important vascular pathogens We wish to express our gratitude to in many agricultural crops and forest Prof. Brenda Wingfield, Dr. Oliver trees. Genetic and pathological Preisig and Dr. Thomas Kirisits for studies have suggested that this their critic review of this manuscript. fungus comprises a complex of Financial support was provided by several host-specialized forms. Two the National Research Foundation of these “forms” have already been (NRF) of South Africa, the University described as new species based on of Pretoria, the Forestry and Agricul- molecular and detailed mor- tural Biotechnology Institute (FABI), phological comparisons. It is clear the members of the Tree Pathology that further investigations are Cooperative Program (TPCP), the required to delimitate other species National Center of Coffee Research

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(Cenicafé, Colombia) and the on cacao, sweet potato and sycamore. Institute of Forest Entomology, Forest In: Inoculum. Vol. 51, no. 6; p. 3-7. Pathology and Forest Protection, Universität für Bodenkultur Wien Baker, K. F. and Thomas, E. H. 2001. (IFFF-BOKU), Austria. Ceratocystis fimbriata. Available in Internet: http://www.public. iastate. edu/~tcharrin/CABIinfo.html.[Consult REFERENCES ed: October 2003]

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