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Identification and Pathogenicity of Lignicolous Fungi Associated with Grapevine Trunk Diseases Citation: M.L

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Identification and Pathogenicity of Lignicolous Fungi Associated with Grapevine Trunk Diseases Citation: M.L Phytopathologia Mediterranea Firenze University Press The international journal of the www.fupress.com/pm Mediterranean Phytopathological Union Research Paper Identification and pathogenicity of lignicolous fungi associated with grapevine trunk diseases Citation: M.L. Raimondo, A. Carlucci, C. Ciccarone, A. Sadallah, F. Lops in southern Italy (2019) Identification and pathogenic- ity of lignicolous fungi associated with grapevine trunk diseases in southern Italy. Phytopathologia Mediterranea Maria Luisa RAIMONDO1, Antonia CARLUCCI1,*, Claudio CICCA- 58(3): 639-662. doi: 10.14601/Phy- RONE1, Abderraouf SADALLAH1,2,3, Francesco LOPS1 to-10742 1 Department of Science of Agriculture, Food and Environment, University of Foggia, Via Accepted: December 22, 2019 Napoli, 25, 71122 Foggia, Italy 2 CIHEAM- Mediterranean Agronomic Institute of Bari, Via Ceglie, 9, 70010 Valenzano Published: December 30, 2019 (Ba), Italy Copyright: © 2019 M.L. Raimondo, A. 3 Department of Soil, Plant and Food Sciences, University of Bari Aldo Moro, Via Amen- Carlucci, C. Ciccarone, A. Sadallah, F. dola 165/A, 70126, Bari, Italy Lops. This is an open access, peer- *Corresponding author: [email protected] reviewed article published by Firenze University Press (http://www.fupress. com/pm) and distributed under the Summary. Over the last 10 years, several fungi were isolated from grapevines with terms of the Creative Commons Attri- grapevine trunk disease (GTD) symptoms, in the Apulia and Molise regions of Italy. bution License, which permits unre- Morphological and molecular analyses allowed the identification of species belonging to stricted use, distribution, and reproduc- Botryosphaeriaceae, Phaeoacremonium species, Phaeomoniella chlamydospora, Pleuros- tion in any medium, provided the origi- toma richardsiae and less-common fungi associated with grapevine trunk diseases, such nal author and source are credited. as Cadophora, Colletotrichum, Seimatosporium and Truncatella. These last genera were Data Availability Statement: All rel- isolated at significant frequencies, so they were investigated for possible involvement evant data are within the paper and its in GTDs. To screen the large numbers of isolates collected, microsatellite-PCR analysis Supporting Information files. was carried out with the M13 primer, and 29 strains were further studied by amplifica- tion of different genes, for multi-locus analyses. Phylogenies and morphological analy- Competing Interests: The Author(s) ses allowed identification, for first time in Italy, of fungi associated with GTDs, includ- declare(s) no conflict of interest. ing Cadophora luteo-olivacaea, Colletotrichum fioriniae, Seimatosporium vitis-vinifera and Editor: Lizel Mostert. Truncatella angustata. Pathogenicity assays with these fungi and other fungi known to be pathogens for grapevines (Lasiodiplodia citricola, Phaeoacremonium italicum, Pleurostoma richardsiae) showed that they caused disease symptoms on two Italian grapevine cultivars (‘Bombino bianco’, ‘Nero di Troia’), although with different degrees of severity. Among the fungi isolated for the first time in Italy, Sei. vitis-vinifera was the most aggressive, while C. fioriniae the least pathogenic. All of these fungi were re-isolated from grapevine, and thus fulfilled Koch’s postulates, confirming their pathogenicity on grapevine. Keywords. Cadophora luteo-olivacea, Colletotrichum fioriniae, Seimatosporium vitis- vinifera, Truncatella angustata, phylogenies, artificial inoculation. INTRODUCTION Several diseases caused by fungi that have been associated with grape- vines over the last 20 years have caused severe yield losses in other grape producing countries (Gramaje et al., 2018; Guerin-Dubrana et al., 2019). Grapevine trunk diseases (GTDs) are considered to be the most destruc- Phytopathologia Mediterranea 58(3): 639-662, 2019 ISSN 0031-9465 (print) | ISSN 1593-2095 (online) | DOI: 10.14601/Phyto-10742 640 Maria Luisa Raimondo et alii tive and severe diseases of grapevine in Mediterranean (Rego et al., 2000; Agusti-Brisach and Armengol, 2013; countries, including Spain, France, Portugal and Italy, Carlucci et al., 2017). Conversely, apoplexy, Esca and and also in the United States of America, Australia, and grapevine leaf symptoms, and Phomopsis, Eutypa and Asia (Gubler et al., 2005; Gramaje et al., 2018; Guerin- Botryosphaeria diebacks are most frequently observed Dubrana et al., 2019). The main fungi that cause GTDs on mature grapevines (Guerin-Dubrana et al., 2019). are species involved in different diseases, which include To date, up to 138 fungal species belonging to 35 Esca and Petri disease (Larignon and Dubos, 1997; genera have been reported as responsible for GTDs. Mugnai et al., 1999; Gramaje et al., 2011; Navarrete However, pathogenicity towards grapevine wood has et al., 2011; Bertsch et al., 2013; Carlucci et al., 2015a; not been tested and/or confirmed for all of these fungi Travadon et al., 2015), Botryosphaeria dieback (Urbez- (Gramaje et al., 2018; Berlanas et al., 2020; Brown et al., Torres, 2011), Diaporthe and Eutypa diebacks (Larignon 2020). For instance, ‘Pestalotioides fungi’ have been fre- and Dubos, 1997; Fourie and Halleen, 2004; Urbez-Tor- quently associated with symptomatic and asymptomatic res et al., 2013), and black foot disease (Halleen et al., vineyards (Farr and Rossman, 2018; Liu et al., 2019), 2004; Agusti-Brisach and Armengol, 2013; Carlucci et although no detailed information is available about their al., 2017). involvement in GTD symptoms. In Italy, incidence of The main external symptom of GTDs is general Esca, grapevine leaf symptoms and apoplexy is signifi- decline of affected plants. The specific external symp- cant and increasing in all grapevine production regions toms consist of tiger-stripe leaves, stunted shoots and (Guerin-Dubrana et al., 2019). In Apulia, Molise and Sic- chlorotic leaves which are sometimes cupped and with ily, Botryosphaeria dieback has also been reported (Cris- necrotic margins, flattened areas of the wood without tinzio, 1978; Burruano et al., 2008; Carlucci et al., 2009; bark, cankered wood and wedge-shaped perennial can- 2015b). Eutypa and Phomopsis diebacks are known to kers, black and sunken necrotic lesions on roots, and occur, if not frequently, in Italian vineyards (Guerin- reddish brown discolouration at the bases of trunks Dubrana et al., 2019). Pleurostoma richardsiae, Dacty- (Gramaje et al., 2018). Internal symptoms include dark- lonectria torresensis, Ilyonectria liriodendri and The- coloured xylem vessels of the grapevine trunks, with lonectria blackeriella were reported for the first time in exudate from the vessels when the trunks are cut in Italy by Carlucci et al. (2015a; 2017). cross-section, and dark streaks in longitudinal sec- A collection of fungi from a decennial survey carried tions (Phaeomoniella chlamydospora, Phaeoacremonium out in symptomatic vineyards in the Apulia and Molise spp., Cadophora spp.). There can also be black subcor- regions of Italy was subjected to identification and char- acterisation by morphological and molecular approach- tical streaking (Pleurostoma richardsiae) and necrosis es, and pathogenicity testing of representative isolates of the wood tissues. Other symptoms are of rootstock was carried out to determine their putative involvement browning in young grapevines (due to black foot fungi). in GTDs. The present paper describes results from this Cordon dieback can also occur, with loss of spurs and research. internal necrotic wedge-shaped staining in stem cross- sections (Eutypa lata, Botryosphaeria spp.), and wood white rot (caused by Basidiomycete fungi) (Gramaje et MATERIALS AND METHODS al., 2018). Grapevines can be affected by one or more GTDs Fungal isolates at the same time, as individual plants can be infected by different pathogens, due to co-occurrence of multi- Symptomatic grapevine samples were collected and ple infections throughout a season, and over years. This analysed during the years 2009 to 2018. The samples produces overlapping of the symptoms described above, were from many vineyards in the Foggia, Barletta-Trani- which makes their association with the specific responsi- Andria and Campobasso provinces in Italy, and were ble fungi particularly difficult to define, and detection of taken from different grapevine cultivars, including ‘San- causal pathogens challenging (Gramaje et al., 2018). giovese’, ‘Montepulciano’, ‘Nero di Troia’, ‘Pinot grigio’, High isolation frequency of particular fungal spe- ‘Trebbiano toscano’, ‘Moscato bianco’ and ‘Chardonnay’ cies involved in GTDs from mature, young and nursery (Table 1). grapevines in different countries can be different, due to External symptoms observed on affected grapevine climatic and geographic conditions, to specific pathogen plants included stunting, reduced grapevine vigour, aggressiveness, and to host cultivar susceptibility (Guer- shoot dieback, and leaf discolouration with intervein- in-Dubrana et al., 2019). Petri and black-foot diseases are al chlorosis and necrosis. Internal symptoms included mostly detected on planting material and young vines black discolouration of wood under the bark, and necro- Lignicolous fungi associated with GTDs 641 Table 1. Information on vineyards surveyed and sampled in the Apulia and Molise regions (southern Italy). Vineyard Survey Year Location Cultivar Age (year) N. samples GTD Incidence* (%) 2009 Cerignola (FG) ‘Sangiovese’ 27 8 13.4 Lucera (FG) ‘Nero di Troia’ 15 3 11.5 Lucera (FG) ‘Moscato bianco’ 10 3 9.8 2011
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