Whole-Genome Resequencing and Pan-Transcriptome Reconstruction Highlight the Impact of Genomic Structural Variation on Secondary Metabolite Gene Clusters in the Grapevine Esca Pathogen Phaeoacremonium minimum

Massonnet, Mélanie; Morales‐Cruz, Abraham; Minio, Andrea; Figueroa‐Balderas, Rosa; Lawrence, Daniel P.; Travadon, Renaud; Rolshausen, Philippe E.; Baumgartner, Kendra

doi:10.3389/fmicb.2018.01784

Cited by 35 publications

(30 citation statements)

References 130 publications

(166 reference statements)

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“…Interestingly, differences in virulence of P. minimum and P. chlamydospora isolates were reported by several authors (Santos et al ., ; Massonnet et al ., ). Massonnet et al .…”

Section: Resultsmentioning

confidence: 97%

“…Massonnet et al . (), analysed the genomic structure (linked to secondary metabolism clusters) of distinct P. minimum isolates which displayed different virulence level, linking their pathogenic behaviour to those genomic differences. Noteworthy, no data about the virological state of such isolates were taken into account, leading to an incomplete analysis of the possible causes influencing their virulence on grapevine plants.…”

Section: Resultsmentioning

confidence: 99%

“…Interestingly, differences in virulence of P. minimum and P. chlamydospora isolates were reported by several authors (Santos et al, 2006;Massonnet et al, 2018). Massonnet et al (2018), analysed the genomic structure (linked to secondary metabolism clusters) of distinct P. minimum isolates which displayed different virulence level, linking their pathogenic behaviour to Fig.…”

Section: Ecological Implicationsmentioning

confidence: 95%

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Isolation, molecular characterization and virome analysis of culturable wood fungal endophytes in esca symptomatic and asymptomatic grapevine plants

Nerva

Turina

Zanzotto

et al. 2019

Environmental Microbiology

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Summary Europe is the world largest grape producer, but in recent years, the report of diseases due to infection by grapevine trunk pathogens (GTPs) is becoming one of the main constraints for viticulture. Among grapevine trunk diseases (GTDs), esca syndrome is one of the most complex, characterized by simultaneous infection of several fungi, which leads to important reduction in yield and quality. Previous characterization of fungal isolates associated with esca syndrome leads to the recognition of at least three important players: Phaeocremonium minimum, Phaemoniella chlamydospora and Fomitiporia mediterranea. Here we isolated and characterized molecularly fungal endophytes directly from field wood tissues of plants showing or not esca symptoms. In addition, to better characterize such collection, a deep RNA sequencing (100 M reads in paired‐end) to screen for mycovirus presence was performed. Thirty‐nine viral genomes were detected, 38 of which were putative new viral species; some of these viruses infected GTPs, including P. minimum and F. mediterranea. In this work, we reported for the first time a curated collection of grapevine fungal endophytes identifying the associated mycoviruses some of which could be employed in future biotechnological exploitation as biological control agents for sustainable plant protection.

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“…Interestingly, differences in virulence of P. minimum and P. chlamydospora isolates were reported by several authors (Santos et al ., ; Massonnet et al ., ). Massonnet et al .…”

Section: Resultsmentioning

confidence: 97%

Section: Resultsmentioning

confidence: 99%

Section: Ecological Implicationsmentioning

confidence: 95%

See 1 more Smart Citation

Isolation, molecular characterization and virome analysis of culturable wood fungal endophytes in esca symptomatic and asymptomatic grapevine plants

Nerva

Turina

Zanzotto

et al. 2019

Environmental Microbiology

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“…The fungi most strongly associated with esca wood necrosis in the trunk have been identified (Larignon and Dubos, 1997;Mugnai et al, 1999;Fischer 2006;White et al, 2011;Bruez et al, 2014;Morales-Cruz et al, 2018). While the disease was formerly associated with the presence of soft rot (caused by basidiomycetes such as Fomitiporia mediterranea), studies have identified two vascular pathogens, Phaeomoniella chlamydospora and Phaeoacremonium minimum, which are detected in trunk necrotic tissues of esca symptomatic vines (Feliciano et al, 2004;Massonnet et al, 2018;Morales-Cruz et al, 2018). Esca leaf symptoms are only observed on mature vines (more than 7 years old) in the field (Mondello et al, 2018) and cannot be reliably reproduced by inoculating vines with the causal fungi (Surico et al, 2006;Bruno et al, 2007), despite testing various methodologies (Reis et al, 2019).…”

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confidence: 99%

Exploring the Hydraulic Failure Hypothesis of Esca Leaf Symptom Formation

et al. 2019

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Vascular pathogens cause disease in a large spectrum of perennial plants, with leaf scorch being one of the most conspicuous symptoms. Esca in grapevine (Vitis vinifera) is a vascular disease with huge negative effects on grape yield and the wine industry. One prominent hypothesis suggests that vascular disease leaf scorch is caused by fungal pathogen-derived elicitors and toxins. Another hypothesis suggests that leaf scorch is caused by hydraulic failure due to air embolism, the pathogen itself, and/or plant-derived tyloses and gels. In this study, we transplanted mature, naturally infected esca symptomatic vines from the field into pots, allowing us to explore xylem integrity in leaves (i.e. leaf midveins and petioles) using synchrotron-based in vivo x-ray microcomputed tomography and light microscopy. Our results demonstrated that symptomatic leaves are not associated with air embolism. In contrast, symptomatic leaves presented significantly more nonfunctional vessels resulting from the presence of nongaseous embolisms (i.e. tyloses and gels) than control leaves, but there was no significant correlation with disease severity. Using quantitative PCR, we determined that two vascular pathogen species associated with esca necrosis in the trunk were not found in leaves where occlusions were observed. Together, these results demonstrate that symptom development is associated with the disruption of vessel integrity and suggest that symptoms are elicited at a distance from the trunk where fungal infections occur. These findings open new perspectives on esca symptom expression where the hydraulic failure and elicitor/toxin hypotheses are not necessarily mutually exclusive.

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“…For the former, grape and fungal DNA were combined as follows: 90% grape with 10% E. lata isolate Napa209 [69], Phaeoa. minimum isolate 1119 [70], or Phaeom. chlamydospora isolate C42 [71]; 80% grape with 10% of each of two fungal isolates (in all three pair-wise combinations of the three isolates); and 70% grape DNA with 10% of each of the three fungal isolates.…”

Section: Methodsmentioning

confidence: 99%

Profiling grapevine trunk pathogensin planta: A case for community-targeted DNA metabarcoding

Morales‐Cruz

Figueroa‐Balderas

García

et al. 2018

Preprint

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21DNA metabarcoding, commonly used in exploratory microbial ecology studies, is a promising 22 method for the simultaneous in planta-detection of multiple pathogens associated with disease 23 complexes, such as the grapevine trunk diseases. Their detection is particularly challenging, due 24 to the presence within an individual wood lesion of multiple co-infecting trunk pathogens and 25 other wood-colonizing fungi, which span a broad range of taxa in the Fungal Kingdom. As such, 26 we designed metabarcoding primers, using as template the ribosomal internal transcribed spacer 27 of grapevine trunk-associated Ascomycete fungi (GTAA) and compared them to two universal 28 primer widely used in microbial ecology. We first performed in silico simulations and then tested 29 the primers by high-throughput amplicon sequencing of (i) multiple combinations of mock 30 communities, (ii) time-course experiments with controlled inoculations, and (iii) diseased field 31 samples from vineyards under natural levels of infection. All analyses showed that GTAA had 32 greater affinity and sensitivity, compared to those of the universal primers. Importantly, with 33 GTAA, profiling of mock communities and comparisons with shotgun-sequencing metagenomics 34 of field samples gave an accurate representation of genera of important trunk pathogens, namely 35Phaeomoniella, Phaeoacremonium, and Eutypa, the abundances of which were greatly over-or 36 under-estimated with universal primers. Overall, our findings not only demonstrate that DNA 37 metabarcoding gives qualitatively and quantitatively accurate results when applied to grapevine 38 trunk diseases, but also that primer customization and testing are crucial to ensure the validity of 39 DNA metabarcoding results. 40 41 42 identification and, thus, require skilled expertise in mycology [20]. However, these approaches 66 still require an initial culturing step, which may limit the detection of slow-growing fungi. 67 Alternatively, with species or genus-specific markers, PCR could be used to determine in planta 68 the presence of certain species, thereby skipping the culturing step [21, 22]. One limitation of this 69 approach, however, is that it may not detect all trunk pathogens in a given sample [23, 24]. Indeed, 70 certain combinations of fungi may be important in the severity of symptom expression [25]. 71Because trunk pathogens cause mixed infections, attempts have been made to characterize the 72 composition of the trunk-pathogen community. For example, finger-printing techniques like 73 Automated Ribosomal Intergenic Spacer Analysis (ARISA) [26] and Single-Strand Conformation 74Polymorphism (SSCP) [27, 28] have been used to compare fungal communities among different 75 samples of grapevine wood, although these do not identify trunk pathogens to the species level. A 76 DNA macroarray system, based on reverse dot-blot hybridization containing oligonucleotides 77 complementary to portions of the -tubulin locus, was developed for species-level identification, 78 specifically for dete...

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Whole-Genome Resequencing and Pan-Transcriptome Reconstruction Highlight the Impact of Genomic Structural Variation on Secondary Metabolite Gene Clusters in the Grapevine Esca Pathogen Phaeoacremonium minimum

Cited by 35 publications

References 130 publications

Isolation, molecular characterization and virome analysis of culturable wood fungal endophytes in esca symptomatic and asymptomatic grapevine plants

Isolation, molecular characterization and virome analysis of culturable wood fungal endophytes in esca symptomatic and asymptomatic grapevine plants

Exploring the Hydraulic Failure Hypothesis of Esca Leaf Symptom Formation

Profiling grapevine trunk pathogensin planta: A case for community-targeted DNA metabarcoding

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