https://orcid.org/0000-0002-0547-1093
ABSTRACT
Grapevine trunk diseases (GTDs), caused by a complex of fungi, are a global threat to vineyard longevity. Identifying the fungi in each growing region is crucial for interpreting symptoms and understanding disease progression. Despite considerable research, the spectrum of fungi involved in GTDs in New Zealand remains uncertain and species identities within key taxonomic groups require validation with molecular sequences. We provide a synopsis of fungi from known pathogenic GTD taxa that have been identified in culture-dependent studies in New Zealand, especially those accessible through culture collections such as the International Collection of Microorganisms from Plants (ICMP). Results from a 2007–2010 countrywide vineyard survey for GTD fungi are presented, plus new isolates and associated DNA sequences from a 2017 survey of Marlborough and Hawke’s Bay vineyards and from institutional microbial collections. These new records clarify that authentic Eutypa lata and Phaeomoniella chlamydospora fungi, which are widely studied GTD pathogens, are present and probably common in New Zealand. First records of Inonotus, Diatrype, Sporocadus and Phaeoacremonium species are presented from New Zealand vineyards. The DNA sequences presented from GTD pathogens will facilitate the use of molecular detection technologies for measuring pathogen distributions in New Zealand vineyards and for biosecurity detections.
Introduction
Grapevine trunk diseases (GTDs) attack the woody tissues of grapevines (Vitis spp.) resulting in trunk rots, which usually develop over several years. These diseases produce a range of plant-wide symptoms such as shoot stunting, foliar chlorosis, and reduced berry yield (Bertsch et al. Citation2013). GTDs are increasing in incidence and threaten the productivity of vineyards worldwide; approximately 13% of French vineyards are unproductive as a consequence (Gramaje et al. Citation2017). GTDs are important in New Zealand, despite the younger average age of vineyards (17 years; W. Kerner pers. comm. 2019), with approximately 9% of vines having external symptoms of disease in Marlborough and Hawke’s Bay (Sosnowski and Mundy Citation2014). The predominance of the susceptible Sauvignon blanc wine-grape variety raises the possibility that New Zealand vineyards are predisposed to future GTD problems (Mundy and Manning Citation2010). Chemical treatment options for GTD are limited (Mondello et al. Citation2018), with registered products in New Zealand all being sprays or paints for post-pruning protection. Disease remediation may consist of re-grafting, vine surgery or complete vine removal.
Although there is a high degree of culturability among fungi from grapevine trunk tissues (Kraus et al. Citation2019), precise diagnoses of the pathogens contributing to GTDs has been confounded by the long-term nature of the disease and involvement of multiple fungal species. International research has focused on three important GTDs of mature grapevines and associated fungi. Eutypa dieback, which occurs in most grape-growing regions of the world (Munkvold Citation2001), is associated with Diatrypaceae fungi, especially Eutypa lata (Rolshausen et al. Citation2006). At least 17 other Diatrypaceae are also associated with the disease, including Cryptovalsa, Eutypella, Diatrype and Diatrypella species (Trouillas et al. Citation2010, Citation2011; Moyo et al. Citation2018). In regions such as the Hunter Valley of Australia (Trouillas et al. Citation2011), E. lata is less common than other Diatrypaceae. Esca is associated with a complex of fungi especially Phaeoacremonium species, Phaeomoniella chlamydospora and a range of basidiomycete species (Mugnai et al. Citation1999; Bertsch et al. Citation2013). Phaeomoniella chlamydospora has been detected worldwide (Gramaje et al. Citation2009; Bertsch et al. Citation2013), including in a substantial proportion of Australian esca samples (Edwards and Pascoe Citation2004). Botryosphaeria dieback is caused by fungi in the Botryosphaeriaceae, a large and species-rich group of woody-plant infecting fungi. Compared with other New Zealand trunk pathogens, those associated with botryosphaeria dieback are well characterised (Baskarathevan et al. Citation2012; Billones-Baaijens et al. Citation2013; Shafi et al. Citation2017).
Despite ongoing studies of these most well-known GTD pathogens, attempts to focus on a small number of pathogenic fungi have been confounded by linkages drawn between an ever-expanding group of up to 133 fungal taxa associated with GTDs, albeit often without confirmation of pathogenicity (Gramaje et al. Citation2017). Species of Cadophora (Gramaje et al. Citation2011; Úrbez-Torres, Haag, et al. Citation2013; Travadon et al. Citation2015), Cytospora (Arzanlou and Narmani Citation2015; Lawrence, Travadon, Pouzoulet, et al. Citation2017), and pestalotioid fungi in the Sporocadaceae (Lawrence, Travadon, Baumgartner Citation2017; Maharachchikumbura et al. Citation2017), have all been isolated from diseased grapevine trunks and linked with GTDs. Once thought to cause grapevine dead-arm disease, Diaporthe (=Phomopsis) spp. are now primarily associated with cane and leaf spot and possibly are weak GTD pathogens (Úrbez-Torres, Peduto, et al. Citation2013).
Fungal species composition associated with GTDs is known to differ with the geographical region (Gramaje et al. Citation2017), further complicating disease diagnosis. Although DNA sequence analyses have substantially improved the identification of fungi from GTD, this approach has not been applied systematically across New Zealand studies. There have been few submissions of DNA sequences from New Zealand GTD isolates to GenBank, and most are limited to the ribosomal internal transcribed spacer (ITS), which is frequently insufficient to distinguish closely related fungi (Mostert et al. Citation2005; Rolshausen et al. Citation2006). DNA sequences from multiple loci are recommended to distinguish species within GTD-associated taxa, including the Botryosphaeriaceae (Slippers et al. Citation2004), Phaeoacremonium (Gramaje et al. Citation2015), Cadophora (Travadon et al. Citation2015) and Diaporthe (Úrbez-Torres, Peduto, et al. Citation2013).
An understanding of plant disease cannot be built when the identities of the fungi present in the ecosystem are unresolved. In this review, we summarise information on fungi isolated in association with GTDs from New Zealand. We identify fungal voucher specimens that have been placed in New Zealand culture collections for contemporary investigations, and collate existing molecular information from these isolates. We generate a significant number of new sequences, including from genetic loci other than the ribosomal ITS.
Materials and methods
2007–2010 survey. A survey was conducted progressively across 41 vineyard blocks in the North Island and the South Island of New Zealand. Vineyard blocks were selected in-part based on information from vineyard managers who reported symptoms of trunk diseases. Five vines from each block, including at least three symptomatic vines with cankers, leaf symptoms or poor growth, were sampled. Five-mm diameter trunk cores, approximately 80 cm above the ground, were taken from each vine, using a No 4333 forestry corer (Mattson). The corer was cleaned between samples with 70% ethanol to prevent cross-contamination.
2017 survey. Five vineyards each in Marlborough and Hawke’s Bay were surveyed for GTD symptoms, especially for basidiomycete infection i.e. resupinate or effused reflexed fruiting bodies, or large cankers with possible wood rot. Bark and decayed wood were removed, and the tissue surface sterilised with 75% ETOH prior to sampling of the discoloured margin of lesions.
Fungal isolations
2007–2010 survey. Cores was surface sterilised for 30 s in 70% ethanol, 2 min in 3.5% w/v sodium hypochlorite and 30 s in 70% ethanol. Then 5- to 10-mm tissue pieces were placed on potato dextrose agar (PDA) amended with 100 µg/mL each of streptomycin and penicillin G potassium salts, and incubated at 20°C with lights (12 h photoperiod).
2017 survey. Five 2 mm3 wood chips from each lesion were surface sterilised for 15–20 s in 75% ethanol, rinsed twice with sterile distilled water, and dried. Wood chips were placed on 0.5× malt extract agar (MEA), containing 1% streptomycin, and incubated in darkness at room temperature. After 1–2 weeks, hyphal tips from suspected basidiomycetes were transferred to MEA supplemented with 0.01% streptomycin and benomyl (4 µg/mL) or to PDA plates with 0.01% streptomycin for other fungi. If the hyphae were particularly dense, a portion was transferred to water agar to encourage greater dispersal of growth, before continuing with subculture. Of the >400 initial isolates, cultures with similar growth form were grouped and representatives from each selected for sequencing.
Fungal identification
2007–2010 survey. Pathogenic fungi (associated with GTD disease in published literature) were identified to genus-level by morphological features (non-pathogens are not included in the results). Selected isolates from this collection have been identified by DNA sequencing at Landcare Research, and sequences made publicly accessible through the ICMP.
2017 survey. DNA was extracted from mycelia of all isolates using the Extract-N-Amp PCR Kit (Sigma Aldrich). The nuclear rDNA internal transcribed spacer region (ITS) of all isolates was amplified by PCR with the universal primers ITS1 and ITS4 (White et al. Citation1990). PCR products were directly Sanger sequenced (Lincoln University) using the PCR primers. For extra taxonomic resolution, amplification and sequencing of a β-tubulin gene fragment from selected isolates were performed with the Bt2a/Bt2b primer pair (Glass and Donaldson Citation1995), and for the partial elongation factor 1α gene with the primers EF1-728F and EF1-986R (Carbone and Kohn Citation1999). Ribosomal large subunit (LSU) fragments were amplified and sequenced with the LROR/LR5 primer pair (Vilgalys and Hester Citation1990).
The most likely taxonomic identity of fungi was assessed by comparing BLASTN alignments to GenBank DNA sequences.
Isolate collections
In addition to isolates gathered in this work, records of microbial collections at Plant & Food Research (PFR), Lincoln University and the ICMP were manually searched for accessions from known GTD pathogen taxa. For a large proportion of the ICMP accessions, associated DNA sequences have been made publicly accessible by Landcare Research. For selected isolates in the PFR collections, new marker DNA sequences were generated in this study as described for the 2017 survey above.
Results
From 41 vineyards sampled in the 2007–2010 survey, the most commonly isolated fungi were Botryosphaeriaceae (70 isolates), Eutypa (58 isolates) and Phaeomoniella (65 isolates), with some cores providing multiple genera (). Less common were Phaeoacremonium spp. (9 isolates) and Cadophora (6 isolates). Other potential GTD fungi isolated during the survey included species of Cylindrocarpon spp. (12 isolates), Diaporthe (21 isolates) and Verticillium (2 isolates). Genus Cylindrocarpon has since been subject to taxonomic revision; without DNA sequences, these isolates cannot be more accurately placed in a current taxon. Nine isolates were deposited into the ICMP collection and the identity of six has since been confirmed with DNA sequence analyses ().
Table 1. Pathogenic fungi isolated from the 2007–2010 grapevine trunk disease survey.
Table 2. Summary of New Zealand grapevine trunk disease (GTD) fungi.
From 2017, 113 cultures were retained based on colony morphology. After ITS DNA sequencing, 23 taxa were identified from the survey (Supplementary Table 1). Multiple cultures with identical DNA sequences collected from a single vine (notably an Inonotus sp. and Phaeoacremonium viticola) were treated as single isolates. Ten 2017 isolates from GTD pathogenic taxa were subject to additional β-tubulin, EF1α or ribosomal LSU sequencing ().
In total, 68 fungal isolates from grapevine pathogen taxa were identified in the ICMP and a further 135 accessions are listed from the PFR and Lincoln University collections ().
Diatrypaceae
Morphologically identified accessions of E. lata were collected from Vitis as early as the 1970s (records in New Zealand Fungi and Bacteria collection; nzfungi2), and from 58% of North Island and 53% of South Island sites in the 2007–2010 survey ().
ITS sequences generated from 16 Marlborough Eutypa isolates (), closely matched authentic GenBank E. lata accessions (e.g. CBS208.87, DQ006925 (Rolshausen et al. Citation2014)). Three ITS sequences, which differed from each other at two nucleotide positions, were identified among the E. lata isolates.
Diatrypaceae taxa from New Zealand vineyards present in ICMP are identified as Eutypella citricola, a Diatrypella sp., and a Diatrype sp. (). New isolates of the Diatrypella sp. were obtained from the PFR collection and isolates of a second Diatrype sp. in 2017 ().
Phaeomonielles
Of five P. chlamydospora isolates present in ICMP, only one is identified by DNA sequence information. P. chlamydospora isolates were abundant in both the 2007–2010 survey () and a PFR collection (24 isolates). Phaeomoniella chlamydospora isolates were morphologically identified from 74% of samples from Clearwater et al. (Citation2000). Alignment of eight new P. chlamydospora ITS sequences with the single ICMP sequence () showed differences at two nucleotide positions. The ITS sequences from these New Zealand isolates are identical to authentic GenBank P. chlamydospora accessions such as CBS 229.95 (Vu et al. Citation2019).
Phaeoacremonium
In 2007-2010, Phaeoacremonium spp. were isolated from fewer New Zealand vineyards than other GTD pathogens (). In 2017, an isolate from Marlborough was identified for the first time as Phaeoacremonium viticola, while another was identified as P. fraxinopennsylvanicum (=P. mortoniae), a species previously recorded in New Zealand (). Based on ITS, actin and β-tubulin DNA sequences, Phaeoacremonium from grapevine rootstocks or scions were identified as P. armeniacum, P. globosum and P. occidentale (Graham et al. Citation2009) (). Another New Zealand Phaeoacremonium accession is identified as P. paululum.
Botryosphaeraciae
The ten Botryosphaeraciae species reported from New Zealand grapevines are represented in the ICMP or in other New Zealand collections: Neofusicoccum luteum, Neofusicoccum parvum, Neofusicoccum australe, Diplodia mutila, Botryosphaeria dothidea, Neofusicoccum ribis, Diplodia seriata, Neofusicoccum macroclavatum, Dothiorella iberica and Dothiorella sarmentorum (). For the bulk of these isolates, ITS sequences have been generated, with a smaller number of β-tubulin and EF1α sequences. From 2017, and in the PFR collection, six D. seriata isolates were collected and identified ().
Hymenochaetales/wood rotting basidiomycetes
The 2017 survey yielded a single Hymenochaetales species (). Sequence heterogeneity allowed the acquisition of only a short ITS sequences from this species, but suggested that it was most closely related to an uncharacterised Inonotus species collected from Australian grapevines (Fischer et al. Citation2005). Ribosomal LSU sequences were also collected from the isolate but did not further clarify its relationship to known fungal species.
Twenty-four cultures of Trametes versicolor, a white-rotting basidiomycete which may saprophytically colonise already dead wood (Fischer and Kassemeyer Citation2003), were collected from three vineyards in Marlborough and Hawke’s Bay in 2017 (Supplementary Table 1).
Cadophora
Seven ICMP isolates from Vitis are identified as Cadophora luteo-olivacea, of which three have ITS sequences available () (Johnston et al. Citation2010). Three further ICMP Cadophora isolates are of uncertain taxonomic identity based on ITS sequence comparisons ().
Diaporthales
In 2017, 10 Diaporthe ampelina (=Phomopsis viticola) cultures with identical ITS sequences were obtained from two Marlborough vineyards (). Other Diaporthe spp. in the PFR collection () corresponded to taxa previously collected from New Zealand: D. foeniculina, D. rudis, D. cotoneastri and two unnamed species defined by phylogenetics (Johnston P, unpublished). Sequence data from further genes are required to confirm species identities among New Zealand Diaporthe.
A single Marlborough isolate from the Plant & Food Research collection was found to be Cytospora chrysosperma by ITS sequencing ().
Pestalotioid fungi
Single isolates of a Pestalotiopsis sp. and Truncatella angustata (morphologically identified) from New Zealand grapevines are present in ICMP (). Seven Sporocadaceae collected in 2018 from Marlborough () had β-tubulin sequences suggesting a close relationship to Sporocadus rosigena. This is the first record of S. rosigena in New Zealand (New Zealand Organism Register; NZOR). Classification within Sporocadaceae is undergoing revision (Liu et al. Citation2019).
Discussion
Identifying pathogens is crucial to understanding the development of GTDs, and for interpreting geographical differences in disease symptomology. In New Zealand, the much-studied GTD pathogen Eutypa lata (Diatrypaceae) is traditionally assumed to cause eutypa dieback (Mundy and Manning Citation2010), but E. lata identification has remained without support from publicly available DNA sequence data. We show here that there are at least five Diatrypaceae spp. on New Zealand grapevines, some of which have been isolated on multiple occasions. Nevertheless, this work tentatively supports the contention that E. lata is the most common species in Marlborough grapevines. Similarly, our data suggest that a second globally important GTD pathogen, Phaeomoniella chlamydospora, is common in New Zealand vineyards. P. chlamydospora is associated with esca disease in the northern hemisphere, and yet the classical symptoms of esca – foliar interveinal red or white ‘tiger’ stripes, and superficial black fruit spots – have not been observed in New Zealand vineyards (Mundy and Manning Citation2010). Phaeoacremonium minimum, which is also thought to play a role in causing esca (Mostert et al. Citation2006; Gramaje et al. Citation2015), has not been detected in New Zealand, while other Phaeoacremonium species are rarely detected. The lack of esca symptoms may relate to fungal community composition or to agronomic features such as the wider availability of irrigation in New Zealand. Esca disease often features wood rotting by the basidiomycete Fomitiporia mediterranea (Fischer Citation2002) which is absent from New Zealand. Outside Europe, this niche may be occupied by other wood-degrading Hymenochaetales (Cloete et al. Citation2015), such as Fomitiporia australiensis in Australia (Fischer et al. Citation2005). The Inonotus-like species reported here is the first recorded wood rot Hymenochaetales in New Zealand grapevines. Further studies will investigate the distribution of this species across the wider New Zealand national vineyard, and whether it acts as a primary pathogen of live wood tissue.
Pathology assays are required to establish if the Cadophora, Diaporthales, and pestalotioid fungi described here are associated with disease or are primarily endophytic. International evidence for the involvement fungi from these taxa in initiation of GTD (Gramaje et al. Citation2011; Úrbez-Torres, Haag, et al. Citation2013; Úrbez-Torres, Peduto, et al. Citation2013; Travadon et al. Citation2015; Lawrence, Travadon, Baumgartner Citation2017; Maharachchikumbura et al. Citation2017) comes from a smaller number of studies than for other prominent pathogens.
The DNA sequences reported here demonstrate that many published quantitative molecular assays (Pouzoulet et al. Citation2013, Citation2017) can be used to detect GTD fungi with confidence in New Zealand. This sequence collection also provides a baseline of knowledge for applying new sequencing-based technologies for identifying multiple GTD pathogens simultaneously (Bulman et al. Citation2018; Morales-Cruz et al. Citation2018; Mundy et al. Citation2018). Ultimately, these techniques will accelerate our understanding of pathogen distribution and ecology in New Zealand vineyards.
Supplementary Material
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We would like to thank all industry representatives who allowed us to sample vines.
Disclosure statement
No potential conflict of interest was reported by the author(s).
ORCID
Joy Tyson http://orcid.org/0000-0002-0547-1093
Peter Johnston http://orcid.org/0000-0003-0761-9116
Simon Bulman http://orcid.org/0000-0003-2320-5511
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Funding
References
- Arzanlou M, Narmani A. 2015. ITS sequence data and morphology differentiate Cytospora chrysosperma associated with trunk disease of grapevine in northern Iran. Journal of Plant Protection Research. 55:117–125. doi: 10.1515/jppr-2015-0015
- Baskarathevan J, Jaspers MV, Jones EE, Ridgway HJ. 2012. Incidence and distribution of botryosphaeriaceous species in New Zealand vineyards. European Journal of Plant Pathology. 132:549–560. doi: 10.1007/s10658-011-9900-5
- Bertsch C, Ramirez-Suero M, Magnin-Robert M, Larignon P, Chong J, Abou-Mansour E, Spagnolo A, Clement C, Fontaine F. 2013. Grapevine trunk diseases: complex and still poorly understood. Plant Pathology. 62:243–265. doi: 10.1111/j.1365-3059.2012.02674.x
- Billones-Baaijens R, Ridgway HJ, Jones EE, Jaspers MV. 2013. Inoculum sources of Botryosphaeriaceae species in New Zealand grapevine nurseries. European Journal of Plant Pathology. 135:159–174. doi: 10.1007/s10658-012-0075-5
- Bulman S, McDougal R, Hill K, Lear G. 2018. Opportunities and limitations for DNA metabarcoding in Australasian plant-pathogen biosecurity. Australasian Plant Pathology. 47:467–474. doi: 10.1007/s13313-018-0579-3
- Carbone I, Kohn LM. 1999. A method for designing primer sets for speciation studies in filamentous Ascomycetes. Mycologia. 91:553–556. doi: 10.1080/00275514.1999.12061051
- Clearwater LM, Stewart A, Jaspers MV. 2000. Incidence of the ‘black goo’ fungus, Phaeoacremonium chlamydosporum, in declining grapevines in New Zealand. New Zealand Plant Protection. 53:448. doi: 10.30843/nzpp.2000.53.3676
- Cloete M, Mostert L, Fischer M, Halleen F. 2015. Pathogenicity of South African Hymenochaetales taxa isolated from esca-infected grapevines. Phytopathologia Mediterranea. 54:368–379.
- Edwards J, Pascoe IG. 2004. Occurrence of Phaeomoniella chlamydospora and Phaeoacremonium aleophilum associated with Petri disease and esca in Australian grapevines. Australasian Plant Pathology. 33:273–279. doi: 10.1071/AP04016
- Fischer M. 2002. A new wood-decaying basidiomycete species associated with esca of grapevine: Fomitiporia mediterranea (Hymenochaetales). Mycological Progress. 1:315–324. doi: 10.1007/s11557-006-0029-4
- Fischer M, Edwards J, Cunnington JH, Pascoe IG. 2005. Basidiomycetous pathogens on grapevine: a new species from Australia-Fomitiporia australiensis. Mycotaxon. 92:85–96.
- Fischer M, Kassemeyer H-H. 2003. Fungi associated with esca disease of grapevine in Germany. Vitis-Geilweilerhof. 42:109–116.
- Glass NL, Donaldson GC. 1995. Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Applied and Environmental Microbiology. 61:1323–1330. doi: 10.1128/AEM.61.4.1323-1330.1995
- Graham A, Johnston P, Weir B. 2009. Three new Phaeoacremonium species on grapevines in New Zealand. Australasian Plant Pathology. 38:505–513. doi: 10.1071/AP09035
- Gramaje D, Mostert L, Armengol J. 2011. Characterization of Cadophora luteo-olivacea and C. melinii isolates obtained from grapevines and environmental samples from grapevine nurseries in Spain. Phytopathologia Mediterranea. 50:112–126.
- Gramaje D, Mostert L, Groenewald JZ, Crous PW. 2015. Phaeoacremonium: from esca disease to phaeohyphomycosis. Fungal Biology. 119:759–783. doi: 10.1016/j.funbio.2015.06.004
- Gramaje D, Munoz RM, Lerma ML, Garcia-Jimenez J, Armengol J. 2009. Fungal grapevine trunk pathogens associated with Syrah decline in Spain. Phytopathologia Mediterranea. 48:396–402.
- Gramaje D, Úrbez-Torres JR, Sosnowski MR. 2017. Managing grapevine trunk diseases with respect to etiology and epidemiology: current strategies and future prospects. Plant Disease. 102:12–39. doi: 10.1094/PDIS-04-17-0512-FE
- Johnston P, Park D, Manning M. 2010. Neobulgaria alba sp. nov. and its Phialophora-like anamorph in native forests and kiwifruit orchards in New Zealand. Mycotaxon. 113:385–396. doi: 10.5248/113.385
- Kraus C, Voegele RT, Fischer M. 2019. Temporal development of the Culturable, endophytic fungal community in Healthy grapevine Branches and Occurrence of GTD-associated fungi. Microbial Ecology. 77:866–876. doi: 10.1007/s00248-018-1280-3
- Lawrence DP, Travadon R, Baumgartner K. 2017. Novel Seimatosporium species from grapevine in northern California and their interactions with fungal pathogens involved in the trunk-disease complex. Plant Disease. 102:1081–1092. doi: 10.1094/PDIS-08-17-1247-RE
- Lawrence DP, Travadon R, Pouzoulet J, Rolshausen PE, Wilcox WF, Baumgartner K. 2017. Characterization of Cytospora isolates from wood cankers of declining grapevine in North America, with the descriptions of two new Cytospora species. Plant Pathology. 66:713–725. doi: 10.1111/ppa.12621
- Liu F, Bonthond G, Groenewald JZ, Cai L, Crous PW. 2019. Sporocadaceae, a family of coelomycetous fungi with appendage-bearing conidia. Studies in Mycology. 92:287–415. doi: 10.1016/j.simyco.2018.11.001
- Maharachchikumbura SS, Larignon P, Al-Sadi AM, Zuo-Yi L. 2017. Characterization of Neopestalotiopsis, Pestalotiopsis and Truncatella species associated with grapevine trunk diseases in France. Phytopathologia Mediterranea. 55:380–390.
- Mondello V, Songy A, Battiston E, Pinto C, Coppin C, Trotel-Aziz P, Clément C, Mugnai L, Fontaine F. 2018. Grapevine trunk diseases: A review of fifteen years of trials for their control with chemicals and biocontrol agents. Plant Disease. 102:1189–1217. doi: 10.1094/PDIS-08-17-1181-FE
- Morales-Cruz A, Figueroa-Balderas R, García JF, Tran E, Rolshausen PE, Baumgartner K, Cantu D. 2018. Profiling grapevine trunk pathogens in planta: a case for community-targeted DNA metabarcoding. BMC Microbiology. 18:214. doi: 10.1186/s12866-018-1343-0
- Mostert L, Groenewald JZ, Summerbell RC, Gams W, Crous PW. 2006. Taxonomy and pathology of Togninia (Diaporthales) and its Phaeoacremonium anamorphs. Studies in Mycology. 54:1–113. doi: 10.3114/sim.54.1.1
- Mostert L, Groenewald JZ, Summerbell RC, Robert V, Sutton DA, Padhye AA, Crous PW. 2005. Species of Phaeoacremonium associated with infections in humans and environmental reservoirs in infected woody plants. Journal of Clinical Microbiology. 43:1752–1767. doi: 10.1128/JCM.43.4.1752-1767.2005
- Moyo P, Mostert L, Spies CF, Damm U, Halleen F. 2018. Diversity of Diatrypaceae species associated with dieback of grapevines in South Africa, with the Description of Eutypa cremea sp. nov. Plant Disease. 102:220–230. doi: 10.1094/PDIS-05-17-0738-RE
- Mugnai L, Graniti A, Surico G. 1999. Esca (black Measles) and Brown wood-streaking: two old and elusive diseases of grapevines. Plant Disease. 83:404–418. doi: 10.1094/PDIS.1999.83.5.404
- Mundy DC, Manning MA. 2010. Ecology and management of grapevine trunk diseases in New Zealand: a review. New Zealand Plant Protection. 63:160–166. doi: 10.30843/nzpp.2010.63.6558
- Mundy DC, Vanga BR, Thompson S, Bulman S. 2018. Assessment of sampling and DNA extraction methods for identification of grapevine trunk microorganisms using metabarcoding. New Zealand Plant Protection. 71:10–18. doi: 10.30843/nzpp.2018.71.159
- Munkvold GP. 2001. Eutypa dieback of grapevine and apricot. Plant Health Progress. 2:9. doi: 10.1094/PHP-2001-0219-01-DG
- Pouzoulet J, Mailhac N, Couderc C, Besson X, Daydé J, Lummerzheim M, Jacques A. 2013. A method to detect and quantify Phaeomoniella chlamydospora and Phaeoacremonium aleophilum DNA in grapevine-wood samples. Applied Microbiology and Biotechnology. 97:10163. doi: 10.1007/s00253-013-5299-6
- Pouzoulet J, Rolshausen PE, Schiavon M, Bol S, Travadon R, Lawrence DP, Baumgartner K, Ashworth VE, Comont G, Corio-Costet M-F, et al. 2017. A method to detect and quantify Eutypa lata and Diplodia seriata-complex DNA in grapevine pruning wounds. Plant Disease. 101:1470–1480. doi: 10.1094/PDIS-03-17-0362-RE
- Rolshausen PE, Baumgartner K, Travadon R, Fujiyoshi P, Pouzoulet J, Wilcox WF. 2014. Identification of Eutypa spp. causing Eutypa dieback of grapevine in eastern North America. Plant Disease. 98:483–491. doi: 10.1094/PDIS-08-13-0883-RE
- Rolshausen PE, Mahoney NE, Molyneux RJ, Gubler WD. 2006. A reassessment of the species concept in Eutypa lata, the causal agent of Eutypa dieback of grapevine. Phytopathology. 96:369–377. doi: 10.1094/PHYTO-96-0369
- Shafi A, Ridgway H, Jaspers M, Jones E. 2017. Conidial production by Botryosphaeriaceae species from grapevine shoot lesions in Marlborough vineyards. New Zealand Plant Protection. 70:295–300. doi: 10.30843/nzpp.2017.70.63
- Slippers B, Crous PW, Denman S, Coutinho TA, Wingfield BD, Wingfield MJ. 2004. Combined multiple gene genealogies and phenotypic characters differentiate several species previously identified as Botryosphaeria dothidea. Mycologia. 96:83–101. doi: 10.1080/15572536.2005.11833000
- Sosnowski M, Mundy D. 2014. Prevalance of grapevine trunk disease in New Zealand vineyards. New Zealand WineGrower, p. 133–138.
- Travadon R, Lawrence DP, Rooney-Latham S, Gubler WD, Wilcox WF, Rolshausen PE, Baumgartner K. 2015. Cadophora species associated with wood-decay of grapevine in North America. Fungal Biol. 119:53–66. doi: 10.1016/j.funbio.2014.11.002
- Trouillas FP, Pitt WM, Sosnowski MR, Huang R, Peduto F, Loschiavo A, Savocchia S, Scott ES, Gubler WD. 2011. Taxonomy and DNA phylogeny of Diatrypaceae associated with Vitis vinifera and other woody plants in Australia. Fungal Diversity. 49:203–223. doi: 10.1007/s13225-011-0094-0
- Trouillas FP, Urbez-Torres JR, Gubler WD. 2010. Diversity of diatrypaceous fungi associated with grapevine canker diseases in California. Mycologia. 102:319–336. doi: 10.3852/08-185
- Úrbez-Torres JR, Haag P, Bowen P, O'Gorman DT. 2013. Grapevine trunk diseases in British Columbia: incidence and characterization of the fungal pathogens associated with esca and Petri diseases of grapevine. Plant Disease. 98:469–482. doi: 10.1094/PDIS-05-13-0523-RE
- Úrbez-Torres JR, Peduto F, Smith R, Gubler W. 2013. Phomopsis dieback: a grapevine trunk disease caused by Phomopsis viticola in California. Plant Disease. 97:1571–1579. doi: 10.1094/PDIS-11-12-1072-RE
- Vilgalys R, Hester M. 1990. Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology. 172:4238–4246. doi: 10.1128/JB.172.8.4238-4246.1990
- Vu D, Groenewald M, de Vries M, Gehrmann T, Stielow B, Eberhardt U, Al-Hatmi A, Groenewald JZ, Cardinali G, Houbraken J, et al. 2019. Large-scale generation and analysis of filamentous fungal DNA barcodes boosts coverage for kingdom fungi and reveals thresholds for fungal species and higher taxon delimitation. Studies in Mycology. 92:135–154. doi: 10.1016/j.simyco.2018.05.001
- White TJ, Burns TD, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innes MA, Gelfard DH, Sninsky JJ, White TJ, editor. PCR protocols. a guide to methods and applications. San Diego, CA: Academic Press; p. 315–322.