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The Status of Botryosphaeriaceae Species Infecting Grapevines

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The Status of Botryosphaeriaceae Species Infecting Grapevines Phytopathol. Mediterr. (2011) 50 (Supplement), S5−S45 REVIEW The status of Botryosphaeriaceae species infecting grapevines JOSÉ RAMóN ÚRBEZ-TORRES Agriculture and Agri-Food Canada, Pacific Agri-Food Research Centre, Summerland, BC V0H 1Z0, Canada Summary. Species in the Botryosphaeriaceae have a cosmopolitan distribution, and occur on a wide range of annual and perennial hosts including grapevines. To date, morphological and taxonomic studies, as well as analyses of nucleotide sequences of multiple genes, have allowed the identification of at least 21 different species in the Botryosphaeriaceae occurring in grapevines worldwide. Grapevine disease symptoms caused by members of this family include leaf spots, fruit rots, shoot dieback, bud necrosis, vascular discoloration of the wood, and perennial cankers, and their current status as pathogens is reviewed. Additionally, the disease name Botryosphaeria dieback is proposed here to describe the different grapevine trunk disease symptoms caused by species of Botryosphaeriaceae. Much has been written during the last decade about the associa- tion between species in the Botryosphaeriaceae and grapevine trunk diseases, which has contributed to a better understanding of the role that these fungal taxa play in grapevine diseases. Although virulence has been shown to vary between species and isolates of the same species in different countries, these fungi have become well-recognized as important grapevine pathogens worldwide. Latest and novel findings from studies conducted in different countries, on disease etiology and species distribution, epidemiology and biology are discussed. Much progress has been achieved in the development and implementation of novel diagnostic and detection techniques.Vineyard sanitation techniques, as well as chemical, biological, and cultural control strategies available at the present time to reduce the infection caused by botryosphaeriaceous fungi, are presented in this review. Key words: black dead arm, black rot, Botryosphaeria canker, Botryosphaeria dieback, excoriose, Macrophoma rot. Introduction and eventual death in economically important woody perennial crops and ornamental plants as Species in the Botryosphaeriaceae Theiss. & P. well as both in native and introduced forest tree Syd. 1918 occur in most parts of the world under species (Farr and Rossman, 2011). Additionally, various ecological niches, and are found as endo- some species in the Botryosphaeriaceae have phytes, parasites and saprophytes on a vast num- been recognized as opportunistic human patho- ber of both annual and perennial plants (Barr, gens causing subcutaneous, ocular and/or inter- 1972; Punithalingam, 1980; von Arx, 1987; Slip- nal organ infections (Rebell and Forster, 1976; pers and Wingfield, 2007). Several species of this Maslen et al., 1996; Summerbell et al., 2004; Tan family are significant plant pathogens causing et al., 2008; Woo et al., 2008). leaf spots, fruit rots, dieback, perennial cankers, Although it is currently well-accepted that Bo- tryosphaeria Cesari & De Notaris. is a member of the Botryosphaeriales in the family Botryospha- Corresponding author: J.R. Úrbez-Torres Fax: +1 250 494 0755 eriaceae (Hawksworth et al., 1995; Crous et al., E-mail: [email protected] 2006; Cannon and Kirk, 2007), the taxonomic his- S5 J.R. Úrbez-Torres tory of Botryosphaeria is complex, and the genus ic conflicts previously existing in Botryosphaeria has been subjected to numerous taxonomic rear- (Jacobs and Rehner, 1998; Denman et al., 2000; rangements in the systematic position of both the Smith and Stanosz, 2001; Zhou and Stanosz, family and the genera included (Denman et al., 2001). As consequence of some of these studies, 2000). Since the introduction of Botryosphaeria Botryosphaeria was suggested to be monophyletic for nine species, over 250 different Botryospha- and the different taxa identified within this teleo- eria spp. have now been recorded including vari- morphic genus were placed under the well-differ- eties and formae specialies (Robert et al., 2005). entiated anamorphic genera Fusicoccum Corda Although many of these species have been either (hyaline and thin-walled conidia) or Diplodia Fr. transferred to other genera or considered syno- (pigmented and thick-walled conidia). However, nyms over the years, there were still 143 differ- these studies could not resolve the taxonomic ent species comprised in the genus Botryospha- status of Lasiodiplodia Ellis & Everh., another eria by 2000 (Denman et al., 2000). However, anamorphic genus with grapevine pathogens de- species identification in Botryosphaeria has been scribed, and suggested that it should be included complicated due to the lack of sufficient diversity as a synonym of Diplodia (Denman et al., 2000). among teleomorph features of species within this An additional problem arising from these studies genus. Additionally, the difficulty of finding tele- was that the accepted classification was in dis- omorphs in nature or obtaining them under labo- cordance with the logical state that only a single ratory conditions, has forced the identification of anamorph genus can be associated with a single these fungi to be primarily based on anamorphic teleomorph genus (Seifert et al., 2000). This de- characters (Jacobs and Rehner, 1998; Denman bate continued until 2006, when a phylogenetic et al., 2000; Phillips, 2002). Consequently, many study based on 28S rDNA sequences showed Bo- different anamorph genera have been linked to Bo- tryosphaeria to be polyphyletic comprising sev- tryosphaeria. However, because anamorph gen- eral phylogenetic lineages (Crous et al., 2006). era of Botryosphaeria were not well-defined when Since then, Botryosphaeria was restricted to spe- first described, different species names were giv- cies with Fusicoccum anamorphs, which current- en to similar fungi adding more controversy to ly include Botryosphaeria dothidea (Mough. :Fr.) the genus (Crous and Palm, 1999; Phillips, 2002). Ces. & De Not (anamorph: Fusicoccum aesculi Therefore, species differentiation based only on Corda), Botryosphaeria corticis (Demaree & M.S. anamorphic characters has not been simplified Wilcox) Arx & E. Müll. (anamorph: Fusicoccum due to the fact that different species within the sp.), Fusicoccum ramosum (Pavlic, Burgess, M.J. same genera often have overlapping morphologi- Wingfield), and Fusicoccum atrovirens (J.W.M. cal features (Slippers et al., 2004; Pavlic et al., Mehl & B. Slippers). However, the study could 2009). As a consequence, characterization of Bo- not fully resolve the status of the Diplodia/Lasi- tryosphaeria to species level has not always been odiplodia group. Two years later, Phillips et al. accurate, which has, for many years, raised even (2008) partially solved the Diplodia/Lasiodiplo- more confusion regarding their association and dia conflict based on a multigene phylogenetic pathogenicity on many hosts, including grape- analysis, which introduced four genera into this vines. Revising the taxonomy of Botryosphaeria group revising the taxonomic status of numer- and its current status is beyond the scope of this ous dematiaceous Botryosphaeriaceae, including review and thus, it will not be addressed here. some that infect grapevines. As a consequence More detailed overviews on the taxonomic history of this and other studies (Pavlic et al., 2004; of Botryosphaeria have been published by Crous Abdollahzadeh et al., 2010), it is currently well- and Palm (1999), Denman et al. (2000), Phillips accepted that Lasiodiplodia is a distinct lineage (2000a), Phillips (2002), Crous et al. (2006), and in the Botryosphaeriaceae. Based on these recent Phillips et al. (2008). findings and until completion of novel taxonomic During the late 1990s and early 2000s, the im- studies in Botryosphaeriaceae, the nomenclature plementation of DNA-based identification tech- proposed by both Crous et al. (2006) and Phillips niques and phylogenetic analyses of nucleotide et al. (2008) should be followed in order to avoid sequences helped to resolve some of the taxonom- adding more confusion within this family. There- S6 Phytopathologia Mediterranea J.R. Úrbez-Torres Botryosphaeriaceae occurring on grapevines fore, this review has adopted to use the existing isolated from the resulting lesions, for what can anamorph generic names for many of the taxa to be considered the first evidence of a Botryospha- refer to species in the Botryosphaeriaceae infect- eriaceae species as a grapevine trunk pathogen. ing grapevines. Several studies on Botryosphaeriaceae infecting Among all agricultural commodities affected grapevine wood followed from 1970 to 2000. El- by Botryosphaeriaceae, grapevines are current- Goorani and El Meleigi (1972) showed that Lasi- ly of significant relevance. Grapevine disease odiplodia theobromae (Pat.) Griff. & Maubl. (as symptoms caused by botryosphaeriaceous fungi Botryodiplodia theobromae Pat.) was the causal include leaf spots, fruit rots, shoot dieback, bud agent of grapevine dieback in Egypt. Two years necrosis, vascular discoloration of the wood, and later, Lehoczky (1974a, 1974b) associated D. mu- perennial cankers. Whereas grapevine fruit rot tila with a grapevine dieback which he called symptoms caused by species in the Botryospha- black dead arm, observed both in mature vines in eriaceae have been known and studied over the the field and nursery grafts. Cristinzio (1978) re- years (Clayton, 1975; Ferrin and Ramsdell, 1977; ported for the first time the association of Diplo- Milholland,
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