Black-foot disease of grapevine: an update on taxonomy, epidemiology and management strategies

245 www.fupress.com/pm ISSN (print): 0031-9465 © Firenze University Press ISSN (online): 1593-2095 Phytopathologia Mediterranea (2013) 52, 2, 245−261 Corresponding author: J. Armengol Fax: +34 963879269 E-mail: [email protected].es REVIEW Black-foot disease of grapevine: an update on taxonomy, epidemiology and management strategies Carlos aGUsTÍ-BrIsaCH and Josep arMeNGol Instituto Agroforestal Mediterráneo, Universidad Politécnica de Valencia, Camino de Vera s/n, 46022-Valencia, Spain Summary. Black-foot is one of the most destructive grapevine trunk diseases in nurseries and young vineyards, causing necrotic root lesions, wood necrosis of the rootstock base, and a gradual decline and death of grapevines. Causal agents of the disease are included into the genera Campylocarpon, “Cylindrocarpon”, Cylindrocladiella and Ilyonectria. Recent taxonomical studies of Neonectria and related genera with “Cylindrocarpon”-like anamorphs based on morphological and phylogenetic studies, divided Neonectria into five genera. Thus, the current taxonomical position and classification of the causal agents of black-foot disease, mainly “Cylindrocarpon”/Ilyonectria, comprises one of the main topics of this review. The review also provides an update on geographical distribution, epidemiology and management strategies of the disease. Key words: Campylocarpon, “Cylindrocarpon”, Cylindrocladiella, Ilyonectria, Vitis vinifera. Introduction Black-foot disease of grapevines is a serious disease in most wine and grape-producing regions of the world, particularly in nurseries and young vineyards (Halleen et al., 2006a). The causal agents are included into the genera Campylocarpon, “Cylindrocarpon”, Cylindrocladiella and Ilyonectria (Crous et al., 1993; Halleen et al. 2004; Halleen et al., 2006b; Schroers et al., 2008; Chaverri et al., 2011; Cabral et al., 2012a, c; Lombard et al., 2012). This disease was first described in 1961 (Grasso and Magnano Di San Lio, 1975), and over the last decade, its incidence has increased significantly in most grapevine production areas of the world (Halleen et al., 2006a; Alaniz et al., 2007). Although these pathogens usually manifest on mature grapevines, they have also been frequently isolated from symptomatic or asymptomatic rootstock mother-plants, rooted rootstock cuttings, bench-graft and young grafted vines in different grapevine production areas around the world, being considered the most common pathogenic fungi associated with young nursery vines (Rumbos and Rumbou, 2001; Halleen et al., 2003; Fourie and Halleen, 2004; Oliveira et al., 2004; Aroca et al., 2006; Dubrovsky and Fabritius, 2007; Halleen et al., 2007). Moreover, it is well known that these pathogens are common in the soil causing infection of grafted vines after some months of growth in nursery soils (Halleen et al. 2003, 2007; Chaverri et al., 2011). Characteristic symptoms of black-foot disease include a reduction in root biomass and root hairs with sunken and necrotic root lesions (Rego et al., 2000; Halleen et al., 2006a; Alaniz et al., 2007, 2009; Abreo et al., 2010). In some cases the rootstock diameter of older vines is thinner below the second tier. To compensate for the loss of functional roots, a second crown of horizontally growing roots is sometimes formed close to the soil surface. Removal of rootstock bark reveals black discoloration and necrosis of wood tissue which develops from the base of the rootstock (Figures 1A, 1B). The pith is also compacted and dis- Phytopathologia Mediterranea 246 C. Agustí-Brisach and J. Armengol colored (Scheck et al., 1998b; Larignon, 1999; Fourie and Halleen, 2001; Halleen et al., 2006a). External symptoms show reduced vigour with small-sized trunks, shortened internodes, uneven wood maturity, sparse foliage, and small leaves with interveinal chlorosis and necrosis (Figures 1C, 1D). Field symptoms of black-foot disease affected vines are frequently indistinguishable from those of caused by Petri disease (Scheck et al., 1998b; Rego et al., 2000; Halleen et al., 2006a; Alaniz et al., 2007, 2009; Abreo et al., 2010). When young vines are infected, death occurs quickly, nevertheless as the vine ages, infection results in a more gradual decline and death might only occur after a year (Gubler et al., 2004). Disease symptoms on mature vines (5 years and older) are noticed early in the growing season. Affected vines achieve poor new growth, fail to form shoots after winter dormancy, and die by mid-summer. Often shoots also dry and die during the summer. Vines with reduced vegetative growth also die during the subsequent dormant winter period (Halleen et al., 2006a). Causal agents Taxonomy and distribution The common name black-foot disease was proposed by Scheck et al. (1998b), to designate the disease caused by “Cylindrocarpon” destructans (Zinnsm.)          B C D A Figure 1. A, black discoloration and necrosis of wood tissue which develops from the base of the rootstock, characteristic of black-foot disease; B, longitudinal section of a rootstock showing dark-brown to black discoloration; C, Un-sprouted grapevine propagation material in a grapevine nursery; D, grapevine plants showing stunded growth, reduced vigour and retarded sprouting in a young plantation. 247 Vol. 52, No. 2, August, 2013 An update of black-foot disease of grapevine Scholten and “C.” obtusisporum (Cooke & Harkn.) Wollenw., which were the two species traditionally reported as the causal agents of basal rot or root necrosis on grapevines. Nevertheless, this disease was already named as “pied noir” in French language since 1969, because of the presence of black necrosis on the base of diseased rootstocks (Badour, 1969). The first report of “C.” destructans on grapevine was made in France in 1961 (Maluta and Larignon, 1991). Since then, it has been isolated from diseased vines in Italy (Grasso, 1984), Portugal (Rego, 1994), California (Scheck et al., 1998b), Argentina (Gatica et al., 2001), Germany (Fischer and Kassemeyer, 2003), Pennsylvania (Gugino and Travis, 2003), New Zealand and South Africa (Halleen et al., 2004), Brazil (Garrido et al., 2004) and Canada (Petit et al., 2011). “Cylindrocarpon” obtusisporum, has also been reported to produce black-foot symptoms on grapevine in Sicily (Grasso and Magnano di San Lio, 1975) and California (Scheck et al., 1998a). The generic name “Cylindrocarpon” was introduced in 1913 by Wollenweber for anamorphs belonging to Nectria section Willkommiotes Wollenw. This section included species without chlamydospores. Few years later, in 1917, Wollenweber expanded the concept of “Cylindrocarpon” to include species forming mycelial chlamydospores in culture, being “C.” destructans the most important member of this group (Brayford, 1993). In 1966, Booth split the genus into four groups based on the presence or absence of microconidia and chlamydospores: (i) “Cylindrocarpon” magnusianum (Sacc.) Wollenw., which was the anamorph of the type species of Neonectria, (ii) “C.” cylindroides Wollenw., which was the type species of the genus “Cylindrocarpon”, (iii) “C.” destructans, which was the anamorph of Neonectria radicicola, and (iv) members of “Cylindrocarpon” species predominantly connected with teleomorphs of the ‘Nectria’ mammoidea group (Brayford, 1993; Halleen et al., 2006a). “Cylindrocarpon” obtusisporum was originally described from the USA (California) as occurring on Acacia sp., where it was observed to form macroconidia and chlamydospores (Booth, 1966). “Cylindrocarpon” obtusisporum strains identified by Booth (1966) originated from a broad range of host plants in Europe, New Zealand, North America, and, at least partly, formed microconidia. Traditionally, representatives of all ‘Nectria’ groups with “Cylindrocarpon” anamorphs were transferred into Neonectria (Rossman et al., 1999; Mantiri et al., 2001; Brayford et al., 2004). Mantiri et al. (2001) and Brayford et al. (2004) analyzed mitochondrial small subunit (SSU) ribosomal DNA (rDNA) sequence data of some of the species and concluded that the Neonectria/“Cylindrocarpon” species grouped together by this reclassification were monophyletic. However, these authors also found that this overall Neonectria/“Cylindrocarpon” clade included distinct subclades corresponding to at least three of the four groups delineated by Booth (1966). Significant molecular variation among taxa with “Cylindrocarpon”- like anamorphs was found by Seifert et al. (2003) in a study on fungi causing root rot of ginseng (Panax quinquefolius L.) and other hosts. The dendrograms in this study, based on partial β-tubulin gene (TUB), and nuclear ribosomal internal transcribed spacer (ITS) region sequences, suggested that subclades including (i) Neon. radicicola, which consisted of numerous phylogenetically distinct units, (ii) Neon. macroconidialis (Samuels & Brayford) Seifert, and (iii) a subclade comprising two distinct isolates, one from V. vinifera in Ontario, Canada and the other from Picea sp. in Quebec, Canada, were monophyletic. Other “Cylindrocarpon” species appeared to be excluded from this monophyletic group (Halleen et al., 2006a). Significant variation in cultural and morphological characters was observed among “Cylindrocarpon” strain isolates from grapevines in nurseries and vineyards of South Africa, New Zealand, Australia and France, which were morphologically and phylogenetically characterized by Halleen et al., (2004). Thus, these authors described a novel species, “C.” macrodidymum Schroers, Halleen & Crous, also associated with black-foot disease of grapevines. Since then, this species has been reported in California (Petit and Gubler, 2005), Portugal (Rego et al., 2005), Chile (Auger et al., 2007), Spain (Alaniz et al., 2007), Uruguay (Abreo et al., 2010), northeastern United States and southeastern Canada (Petit et al., 2011) and Turkey (Özben et al., 2012). “Cylindrocarpon” obtusisporum and “C.” macrodidymum had been considered as two different species associated with black-foot disease of grapevines. Nevertheless, Halleen et al. (2004) suggested the possibility that Grasso and Magnano di San Lio (1975) and Scheck et al. (1998a) misidentified “C.” obtusisporum and that it was in fact “C.” macrodidymum. In this sense, Halleen et al. (2004) indicated that macroconidia of “C.” macrodidymum measure [(26–)34– 36–38(–45)×(4–)5.5–6–6.5(–8) μm], whereas those of Phytopathologia Mediterranea 248 C. Agustí-Brisach and J. Armengol the type of “C.” obtusisporum measure (30–35×4–5 μm) (Cooke, 1884). However, the shape of the macroconidia distinguishes “C.” macrodidymum from the type of “C.” obtusisporum, which Cooke (1884) described as having conidia with obtuse ends. Booth (1966) described macroconidia of similar shape in “C.” obtusisporum. According to Booth, however, 2–3-septate macroconidia of “C.” obtusisporum measure (34–50×6–7.5 μm). “Cylindrocarpon” obtusisporum isolates obtained from California formed perithecia when cross-inoculated with “C.” macrodidymum, giving further evidence to support the misidentification theory. This was also confirmed by sequence comparisons (Halleen et al., 2006a). In 2005, Petit and Gubler confirmed the presence of “C.” macrodidymum in the USA, and concluded that black-foot disease in California is caused by “C.” macrodidymum and “C.” destructans (Petit and Gubler, 2005). Moreover, Halleen et al., (2004) established a new genus, Campylocarpon Halleen, Schroers & Crous, which is “Cylindrocarpon”-like in morphology, associated with black-foot disease of grapevines. Species of this genus and members of the former “Nectria” mammoidea group, are excluded from Neonectria/“Cylindrocarpon”, because phylogenetic analyses revealed that these species are phylogenetically not closely related to Neonectria/“Cylindrocarpon” genera (Halleen et al., 2004; Schroers et al., 2008). From this genus, two species were included as the causal agents of black-foot disease: Campylocarpon fasciculare Schroers, Halleen & Crous, which has been reported in South Africa (Halleen et al., 2004), Brazil (Correia et al., 2012), and Spain (Alaniz et al., 2011b) and Campyl. pseudofasciculare Halleen, Schroers & Crous, which has been reported in South Africa (Halleen et al., 2004), Uruguay (Abreo et al., 2010), Brazil (Correia et al., 2012) and Perú (Álvarez et al., 2012). As highlighted before, “C.” destructans was originally identified as the causal agent of black-foot disease (Maluta and Larignon, 1991), but the status of “C.” destructans as the causal agent of the disease was since then questioned. In fact, Halleen et al. (2006b), compared “C.” destructans strains isolated from diseased grapevines in France, New Zealand, Portugal and South Africa with “C.” destructans-like anamorphs obtained from various herbaceous or woody hosts. DNA analyses of their ITS and TUB showed that these isolates were genetically identical with “C.” liriodendri J.D. MacDon. & E.E. Butler, which was first associated with root rot of tulip poplar (Liriodendron tulipifera L.) in California by MacDonald and Butler (1981). Thus, because these species had identical sequences, “C.” destructans isolates collected from asymptomatic or diseased grapevines affected by black-foot disease were renamed as “C.” liriodendri, associating “C.” destructans only with root rot on other herbaceous or woody hosts (Halleen et al., 2006b). In addition, in order to clarify the taxonomy of “C.” destructans causing black-foot in California, Petit and Gubler (2007) also compared “C.” destructans isolates obtained from grapevines in California with “C.” liriodendri isolates from South Africa. All of them were identical, and consequently “C.” destructans isolates were also renamed as “C.” liriodendri. This species has been later reported as a black-foot pathogen of grapevine in Australia (Whitelaw-Weckert et al., 2007), Spain (Alaniz et al., 2007), Brazil (Russi et al., 2010), Iran (Mohammadi et al., 2009), Switzerland (Casieri et al., 2009), Uruguay (Abreo et al., 2010) and northeastern United States and southeastern Canada (Petit et al., 2011). The teleomorphs of “C.” liriodendri and “C.” macrodidymum were described as Neonectria liriodendri Halleen, Rego & Crous and N. macrodidyma Halleen, Schroers & Crous (Halleen et al., 2004, 2006b). In 2008, a new species associated with black-foot disease of grapevines, “C.” pauciseptatum Schroers & Crous, was described in New Zealand and Slovenia (Schroers et al., 2008). To date, this species has been isolated from affected grapevines in Uruguay (Abreo et al., 2010), Canada (O’Gorman and Haag, 2011), Spain (Martin et al., 2011) and Portugal (Cabral et al., 2012a). Phylogenetic studies carried out in New Zealand and Slovenia by Schroers et al. (2008), indicated that “C.” pauciseptatum is the closest phylogenetic sister-taxon of “C.” macrodidymum and both species are closely related to the “C.” destructans-complex, which also includes “C.” liriodendri. Thus, at this moment, “C.” destructans, “C.” liriodendri, “C.” macrodidymum, “C.” obtusisporum, “C.” pauciseptatum, Campyl. fasciculare and Campyl. pseudofasciculare were considered as the main species associated with young vines showing symptoms of black-foot disease in most of grapevine producing areas worldwide. In addition, other “Cylindrocarpon” species have been associated occasionally with blackfoot disease of grapevine: “Cylindrocarpon” didymum (Harting) Wollenw. in Canada (Petit et al., 2011), “C.” olidum (Wollenw.) Wollenw. in Spain (De Francisco 249 Vol. 52, No. 2, August, 2013 An update of black-foot disease of grapevine et al., 2009) and “C.” olidum var. crassum Gerlach in Uruguay (Abreo et al., 2010). Chaverri et al. (2011) performed a phylogenetic study of Neonectria, “Cylindrocarpon” and related genera with “Cylindrocarpon”-like anamorphs. Morphological and molecular phylogenetic analyses data accumulated over several years have indicated that Neonectria sensu stricto and “Cylindrocarpon” sensu stricto are phylogenetically congeneric, while Neonectria sensu lato and “Cylindrocarpon” sensu lato do not form a monophyletic group, suggesting that Neonectria/“Cylindrocarpon” represents more than one genus. Thus, based on results of the phylogenetic study, these authors divided Neonectria into five genera based on a combination of characters linked to perithecial anatomy and conidial septation: Neonectria/“Cylindrocarpon” sensu stricto (Booth’s groups 1 and 4), Rugonectria, Thelonectria (group 2), Ilyonectria (group 3) and anamorph genus Campylocarpon. According to this, only Neonectria has “Cylindrocarpon” anamorphs, while the remaining genera have “Cylindrocarpon”-like anamorphs, and since then are referred to as “Cylindrocarpon”. Consequently, “C.” liriodendri and “C.” macrodidymum were included into Ilyonectria genus, with I. radicicola as the type species, and re-identified as Ilyonectria liriodendri (Halleen, Rego & Crous) Chaverri & Salgado and I. macrodidyma (Halleen, Schroers & Crous) P. Chaverri & Salgado, respectively (Chaverri et al., 2011). Moreover, Cabral et al. (2012a) were able to delineate 12 new taxa in the I. radicicola-complex, previously known as the “C.” destructans-complex, by using a multi-gene DNA analysis supported by morphological characters. Other Ilyonectria species within I. radicicola-complex have been also found associated with black-foot disease of grapevine: Ilyonectria europaea A. Cabral, Rego & Crous, I. lusitanica A. Cabral, Rego & Crous, I. pseudodestructans A. Cabral, Rego & Crous and I. robusta (A.A. Hildebr.) A. Cabral, Rego & Crous, reported in Portugal (Cabral et al., 2012a, 2012c). Another Ilyonectria spp., I. vitis has also been described in Portugal (Cabral et al., 2012a), and isolates belonging to Neonectria mammoidea group have also been associated with the disease in Canada (Petit et al., 2011). Soon thereafter, following this study, Cabral et al. (2012c), demonstrated the existence of polymorphism into I. macrodidyma-complex. This hypothesis was in agreement with the results obtained by Alaniz et al. (2009), who already detected relevant genetic diversity in “C.” macrodidymum by using inter-simple sequence repeat (ISSR) technique. However, previous phylogenetic analysis showed low variation in the large subunit (LSU) ribosomal DNA (rDNA), TUB and ITS sequences of “C.” macrodidymum isolates obtained from grapevine in different countries (Halleen et al, 2004; Petit and Gubler, 2005; Alaniz et al., 2007). Thus, in order to clarify this hypothesis, Cabral et al. (2012c) performed a phylogenetic study of I. macrodidyma-complex by using ITS, TUB, histone H3 gene (HIS) and translation elongation factor 1-α (TEF) sequence analysis. Consequently, six new species of Ilyonectria (I. alcacerensis A. Cabral, Oliveira & Crous, I. estremocensis A. Cabral, Nascimento & Crous, I. novozelandica A. Cabral & Crous, I. torresensis A. Cabral, Rego & Crous, and Ilyonectria sp. 1, I. sp. 2,) and I. macrodidyma, which are morphologically rather similar, were recognised into the I. macrodidyma-complex. All these species have been reported in Portugal, with the exception of I. novozelandica which has been reported in South Africa, USA, New Zealand (Cabral et al., 2012a, 2012c). Recently, I. alcacerensis, I. macrodidyma, I. novozelandica, and I. torresensis have also been found on grapevines in Spain (Agustí-Brisach et al., 2013a, 2013b). Regarding, “C.” pauciseptatum, it is not clear in which genera it has to be included, although it is very similar in morphology to I. anthuriicola A. Cabral & Crous (Cabral et al., 2012a). Finally, another genus, Cylindrocladiella Boesew., which is also Cylindrocarpon-like in morphology, has recently been associated with black-foot disease of grapevines (Van Coller et al., 2005; Agustí-Brisach et al., 2012; Jones et al., 2012). This genus was established by Boesewinkel (1982) to accommodate five Cylindrocladium-like species producing small and cylindrical conidia. This decision was based on the fact that species of Cylindrocladiella had different conidiophores branching patterns, conidial shapes, dimensions, cultural characteristics and teleomorphs from those of Cylindrocladium (Van Coller et al., 2005; Lombard et al. 2012). Since then, several taxonomic studies of these fungi have relied on morphologically and to lesser extent on DNA sequence comparisons of the ITS and TUB gene regions, recognizing nine species of Cylindrocladiella (Crous and Wingfield, 1993; Victor et al., 1998; Van Coller et al., 2005). Lombard et al. (2012), have just described 18 new Cylindrocladiella species based on morphological and phylogenetic Phytopathologia Mediterranea 250 C. Agustí-Brisach and J. Armengol studies employing ITS, TUB, HIS and TEF gene regions. Nevertheless, only two species into this genus have been found associated with black-foot disease on grapevines: Cylindrocladiella parva (P.J. Anderson) Boesew., which has been reported in South Africa (Van Coller et al., 2005), New Zealand (Jones et al., 2012) and Spain (Agustí-Brisach et al., 2012) and Cyl. peruviana (Bat., J.L. Bezerra & M.P. Herrera) Boesew., which has been reported in South Africa (Van Coller et al., 2005), Perú (Álvarez et al., 2012) and Spain (Agustí-Brisach et al., 2012). A list of all “Cylindrocarpon”/Ilyonectria, Campylocarpon and Cylindrocladiella species, which have been reported associated with black-foot disease of grapevine and their geographical distribution, is presented in Table 1. Morphological and cultural characterization “Cylindrocarpon”/Ilyonectria, Campylocarpon and Cylindrocladiella species have characteristic distinctive morphological and cultural patterns (Figures 2 and 3; Table 2). The anamorphs of “Cylindrocarpon”/ Ilyonectria produce abundant microconidia and chlamydospores. Macroand microconidia apparently are produced from the same conidiophores which are 40–160 μm long, generally simple, unbranched or sparsely branched, irregularly or verticillately branched, rarely densely branched, and with cylindrical phialides. Macroconidia are straight or curved, hyaline, 1–3-septate, rarely > 3-septate [25– 50(–55)×5–7.5 μm], generally with a prominent basal or lateral abscission scar or hilum. Microconidia are ellipsoidal to ovoid, hyaline, 0–1-septate, with a lateral or basal hilum [3–15×2.5–5(–6) μm] (Figures 2A, 2B). Chlamydospores are abundant, generally intercalary, globose, single or in chains, becoming brownish. In addition, colony morphology on PDA is very heterogeneous (Figure 2C). Aerial mycelium is floccose to felted, and the colour varies from white to yellow or light to dark brown. The margin of the colony can be entire, slightly lobulated, or lobulated (Figures 3A–3H) (Booth, 1966; Samuels and Brayford, 1990; Chaverri et al., 2011). Table 1. Fungal species which have been reported associated with black-foot disease of grapevines and their geographical distribution. Species Distribution Campylocarpon fasciculare Schroers, Halleen & Crous South Africa (Halleen et al., 2004), Spain (Alaniz et al., 2011b) and Brazil (Correia et al., 2012). Campylocarpon pseudofasciculare Halleen, Schroers & Crous South Africa (Halleen et al., 2004), Uruguay (Abreo et al., 2010), Brazil (Correia et al., 2012) and Perú (Álvarez et al., 2012) “Cylindrocarpon” destructans (Zinssm.) Scholten France (Maluta and Larignon, 1991), Italy (Grasso, 1984), Argentina (Gatica et al., 2001), Germany (Fischer and Kassemeyer, 2003), Pennsylvania (Gugino and Travis, 2003), Brazil (Garrido et al., 2004) and Canada (Petit et al., 2011) “Cylindrocarpon” didymum (Harting) Wollenw. Canada (Petit et al., 2011) “Cylindrocarpon” obtusisporum (Cooke & Harkn.) Wollenw. Sicily (Grasso and Magnano di San Lio, 1975) and California (Scheck et al., 1998a) “Cylindrocarpon” olidum (Wollenw.) Wollenw. Spain (De Francisco et al., 2009) “Cylindrocarpon” olidum var. crassum Gerlach Uruguay (Abreo et al., 2010) “Cylindrocarpon” pauciseptatum Schroers & Crous New Zealand and Slovenia (Schroers et al., 2008), Uruguay (Abreo et al., 2010) Canada (O’Gorman and Haag, 2011), Spain (Martin et al., 2011) and Portugal (Cabral et al., 2012a) Cylindrocladiella parva (P.J. Anderson) Boesew. South Africa (Van Coller et al., 2005), New Zealand (Jones et al., 2012) and Spain (Agustí-Brisach et al., 2012) (Continued) 251 Vol. 52, No. 2, August, 2013 An update of black-foot disease of grapevine Campylocarpon is similar to “Cylindrocarpon”/Ilyonectria, although Campylocarpon spp. produce macroconidia mostly curved, while microconidia are absent and chlamydospores are rare or also absent. Conidiophores appear arising laterally from single or fasciculate aerial hyphae or from creeping substrate hyphae, singly or in loose or dense aggregates (Figure 2D). Conidial heads form pionnotes-like aggregates. Conidiophore show a stipe base to 16 μm wide, which bear several phialides or a penicillus of irregular branches with terminal branches bearing 1 or several phialides. Macroconidia are as in Ilyonectria, but typically curved, and with up to 6 septa, [(24–)35–60(–62)×6.5–9 μm], apical cell obtuse, basal cell obtuse or with inconspicuous hilum (Figure 2E). Regarding colony morphology on PDA, aerial mycelium is abundant, covering the whole or sectors of the colony, white to off-white or slightly brownish, thickly cottony to felty, intermingled with or giving rise to erect white or brown hyphal strands. This strands sometimes are partly covered by off-white slime (Figures 3I, 3J) (Halleen et al., 2004; Chaverri et al., 2011). Cylindrocladiella species produce hyaline, single, subverticillate, as well as penicilliate conidiophores, Species Distribution Cylindrocladiella peruviana (Bat., J.L. Bezerra & M.P. Herrera) Boesew. South Africa (Van Coller et al., 2005), Spain (Agustí-Brisach et al., 2012) and Perú (Álvarez et al., 2012) Ilyonectria alcacerensis A. Cabral, Oliveira & Crous Portugal (Cabral et al., 2012c) and Spain (Agustí-Brisach et al., 2013b) Ilyonectria estremocensis A. Cabral & Crous Portugal (Cabral et al., 2012c) Ilyonectria europaea A. Cabral, Rego & Crous Portugal (Cabral et al., 2012a) Ilyonectria liriodendri (Halleen, Rego & Crous) Chaverri & Salgado France, New Zealand, Portugal and South Africa (Halleen et al., 2006b), Australia (Whitelaw-Weckert et al., 2007), California (Petit and Gubler, 2007), Spain (Alaniz et al., 2007), Iran (Mohammadi et al., 2009), Switzerland (Casieri et al., 2009), Brazil (Russi et al., 2010), Uruguay (Abreo et al., 2010), northeastern United States and southeastern Canada (Petit et al., 2011), Ilyonectria lusitanica A. Cabral, Rego & Crous Portugal (Cabral et al., 2012a) Ilyonectria macrodidyma (Halleen, Schroers & Crous) P. Chaverri & C. Salgado Australia, France, New Zealand and South Africa (Halleen et al., 2004), California (Petit and Gubler, 2005), Chile (Auger et al., 2007), Uruguay (Abreo et al., 2010), northeastern United States and southeastern Canada (Petit et al., 2011), Portugal (Cabral et al., 2012c), Turkey (Özben et al., 2012) and Spain (Agustí-Brisach et al., 2013b). Ilyonectria novozelandica A. Cabral, Nascimento & Crous South Africa, USA and New Zealand (Cabral et al., 2012c) and Spain (Agustí-Brisach et al., 2013a, b) Ilyonectria pseudodestructans A. Cabral, Rego & Crous Portugal (Cabral et al., 2012a) Ilyonectria robusta (A.A. Hildebr.) A. Cabral, Rego & Crous Portugal (Cabral et al., 2012a) Ilyonectria torresensis A. Cabral, Rego & Crous Australia, Canada, New Zealand, Portugal, South Africa, Spain and USA (Cabral et al., 2012c; Agustí-Brisach et al., 2013a, b) Ilyonectria vitis A. Cabral, Rego & Crous Portugal (Cabral et al., 2012a) Ilyonectria sp. 2 (Cabral et al., 2012c) Portugal (Cabral et al., 2012c) Isolates belonging to Neonectria mammoidea group Canada (Petit et al., 2011) Table 1. Continues. Phytopathologia Mediterranea 252 C. Agustí-Brisach and J. Armengol with primary and secondary branches. The phialides are terminal, hyaline, in whorls of 2–4, with or without obvious collarets. In general, stipe is centrally arranged on conidiophores, with a single basal septum, terminating in a thin-walled, hyaline vesicle of characteristic shape (Figures 2F, 2G). Conidia are cylindrical, rounded at both ends, straight, hyaline, (0)–1-septate, [(9–)11–13(–15)×2–4 μm], sometimes         H I F G A B C E D Figure 2. A, Conidiophores of I. liriodendri; B, Macroand microconidia of Ilyonectria liriodendri; C, Chlamydospores in chains of “Cylindrocarpon” pauciseptatum; D, Conidiophores of Campyl. fasciculare; E, Macroconidia of Campylocarpon fasciculare; F, Penicillate conidiophores of Cylindrocladiella parva; G, Terminal vesicles of Cyl. parva; H, Conidia of Cyl. parva; H, Chlamydospores in chains of Cyl. parva. Scale bars: a‒c, f‒i = 10 μm; d‒e = 25 μm. 253 Vol. 52, No. 2, August, 2013 An update of black-foot disease of grapevine becoming swollen at one end with age (Figure 2H). Chlamydospores are abundant or moderate, more frequently arranged in chains than clusters (Figure 2I). Aerial mycelium ranges from dark to light brown (Figures 3K, 3L) (Crous and Wingfield, 1993; Lombard et al., 2012). Epidemiology Campylocarpon, “Cylindrocarpon”, Cylindrocladiella and Ilyonectria species are generally regarded as pathogens and/or saprobes of a wide range of angiosperm and gymnosperm hosts and substrates in temperate, sub-tropical and tropical regions worldwide (Victor et al., 1998; Chaverri et al., 2011; Lombard et al., 2012). In addition to grapevine, they have also been associated with root rot diseases of other economically important hosts (Chaverri et al., 2011; Lombard et al., 2012), such as: Actinidia chinensis Planch. (Erper et al., 2011), Liriodendron tulipifera L. (MacDonald and Butler, 1981), Olea europaea L. (Úrbez-Torres et al., 2012), Panax quinquefolius L. (Rahman and Punja, 2005), Persea americana Mill. (Vitale et al., 2012), Pinus radiata D. 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