Phytotoxic metabolites from Neofusicoccum parvum, a pathogen of Botryosphaeria dieback of grapevine

Cultivar Contributes to the Beneficial Effects of Bacillus subtilis PTA-271 and Trichoderma atroviride SC1 to Protect Grapevine Against Neofusicoccum parvum

Frontiers in Microbiology ◽

10.3389/fmicb.2021.726132 ◽

2021 ◽

Vol 12 ◽

Author(s):

Catarina Leal ◽

Nicolas Richet ◽

Jean-François Guise ◽

David Gramaje ◽

Josep Armengol ◽

...

Keyword(s):

Bacillus Subtilis ◽

Trichoderma Atroviride ◽

In Planta ◽

Neofusicoccum Parvum ◽

Beneficial Effects ◽

Grapevine Trunk Diseases ◽

Mutual Antagonism ◽

Direct Benefits ◽

Botryosphaeria Dieback

Grapevine trunk diseases (GTDs) are a big threat for global viticulture. Without effective chemicals, biocontrol strategies are developed as alternatives to better cope with environmental concerns. A combination of biological control agents (BCAs) could even improve sustainable disease management through complementary ways of protection. In this study, we evaluated the combination of Bacillus subtilis (Bs) PTA-271 and Trichoderma atroviride (Ta) SC1 for the protection of Chardonnay and Tempranillo rootlings against Neofusicoccum parvum Bt67, an aggressive pathogen associated to Botryosphaeria dieback (BD). Indirect benefits offered by each BCA and their combination were then characterized in planta, as well as their direct benefits in vitro. Results provide evidence that (1) the cultivar contributes to the beneficial effects of Bs PTA-271 and Ta SC1 against N. parvum, and that (2) the in vitro BCA mutual antagonism switches to the strongest fungistatic effect toward Np-Bt67 in a three-way confrontation test. We also report for the first time the beneficial potential of a combination of BCA against Np-Bt67 especially in Tempranillo. Our findings highlight a common feature for both cultivars: salicylic acid (SA)-dependent defenses were strongly decreased in plants protected by the BCA, in contrast with symptomatic ones. We thus suggest that (1) the high basal expression of SA-dependent defenses in Tempranillo explains its highest susceptibility to N. parvum, and that (2) the cultivar-specific responses to the beneficial Bs PTA-271 and Ta SC1 remain to be further investigated.

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Flowering as the Most Highly Sensitive Period of Grapevine (Vitis vinifera L. cv Mourvèdre) to the Botryosphaeria Dieback Agents Neofusicoccum parvum and Diplodia seriata Infection

International Journal of Molecular Sciences ◽

10.3390/ijms15069644 ◽

2014 ◽

Vol 15 (6) ◽

pp. 9644-9669 ◽

Cited By ~ 13

Author(s):

Alessandro Spagnolo ◽

Philippe Larignon ◽

Maryline Magnin-Robert ◽

Agnès Hovasse ◽

Clara Cilindre ◽

...

Keyword(s):

Vitis Vinifera ◽

Sensitive Period ◽

Vitis Vinifera L ◽

Diplodia Seriata ◽

Neofusicoccum Parvum ◽

Highly Sensitive ◽

Botryosphaeria Dieback

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Defense Responses in Grapevine (cv. Mourvèdre) after Inoculation with the Botryosphaeria Dieback Pathogens Neofusicoccum parvum and Diplodia seriata and Their Relationship with Flowering

International Journal of Molecular Sciences ◽

10.3390/ijms18020393 ◽

2017 ◽

Vol 18 (2) ◽

pp. 393 ◽

Cited By ~ 11

Author(s):

Alessandro Spagnolo ◽

Vincenzo Mondello ◽

Philippe Larignon ◽

Sandra Villaume ◽

Fanja Rabenoelina ◽

...

Keyword(s):

Defense Responses ◽

Diplodia Seriata ◽

Neofusicoccum Parvum ◽

Botryosphaeria Dieback

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Wood Metabolomic Responses of Wild and Cultivated Grapevine to Infection with Neofusicoccum parvum, a Trunk Disease Pathogen

Metabolites ◽

10.3390/metabo10060232 ◽

2020 ◽

Vol 10 (6) ◽

pp. 232 ◽

Cited By ~ 2

Author(s):

Clément Labois ◽

Kim Wilhelm ◽

Hélène Laloue ◽

Céline Tarnus ◽

Christophe Bertsch ◽

...

Keyword(s):

Vitis Vinifera ◽

Strong Increase ◽

Primary Metabolism ◽

Alcohol Content ◽

Neofusicoccum Parvum ◽

Specialized Metabolites ◽

Grapevine Trunk Diseases ◽

Botryosphaeria Dieback ◽

Trunk Diseases ◽

Resveratrol Oligomer

Grapevine trunk diseases (GTDs), which are associated with complex of xylem-inhabiting fungi, represent one of the major threats to vineyard sustainability currently. Botryosphaeria dieback, one of the major GTDs, is associated with wood colonization by Botryosphaeriaceae fungi, especially Neofusicoccum parvum. We used GC-MS and HPLC-MS to compare the wood metabolomic responses of the susceptible Vitis vinifera subsp. vinifera (V. v. subsp. vinifera) and the tolerant Vitis vinifera subsp. sylvestris (V. v. subsp. sylvestris) after artificial inoculation with Neofusicoccum parvum (N. parvum). N. parvum inoculation triggered major changes in both primary and specialized metabolites in the wood. In both subspecies, infection resulted in a strong decrease in sugars (fructose, glucose, sucrose), whereas sugar alcohol content (mannitol and arabitol) was enhanced. Concerning amino acids, N. parvum early infection triggered a decrease in aspartic acid, serine, and asparagine, and a strong increase in alanine and β-alanine. A trend for more intense primary metabolism alteration was observed in V. v. subsp. sylvestris compared to V. v. subsp. vinifera. N. parvum infection also triggered major changes in stilbene and flavonoid compounds. The content in resveratrol and several resveratrol oligomers increased in the wood of both subspecies after infection. Interestingly, we found a higher induction of resveratrol oligomer (putative E-miyabenol C, vitisin C, hopeaphenol, ampelopsin C) contents after wood inoculation in V. v. subsp. sylvestris.

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Toxicity of extracellular proteins from Diplodia seriata and Neofusicoccum parvum involved in grapevine Botryosphaeria dieback

PROTOPLASMA ◽

10.1007/s00709-014-0716-y ◽

2014 ◽

Vol 252 (2) ◽

pp. 679-687 ◽

Cited By ~ 19

Author(s):

M. Bénard-Gellon ◽

S. Farine ◽

M. L. Goddard ◽

M. Schmitt ◽

E. Stempien ◽

...

Keyword(s):

Extracellular Proteins ◽

Diplodia Seriata ◽

Neofusicoccum Parvum ◽

Botryosphaeria Dieback

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Characterization of the Mycovirome of the Phytopathogenic Fungus, Neofusicoccum parvum

Viruses ◽

10.3390/v13030375 ◽

2021 ◽

Vol 13 (3) ◽

pp. 375

Author(s):

Armelle Marais ◽

Chantal Faure ◽

Gwenaëlle Comont ◽

Thierry Candresse ◽

Elodie Stempien ◽

...

Keyword(s):

High Throughput Sequencing ◽

Phylogenetic Analyses ◽

Phytopathogenic Fungus ◽

Sequencing Analysis ◽

Single Strain ◽

Neofusicoccum Parvum ◽

The Family ◽

Pcr Products ◽

Botryosphaeria Dieback

Neofusicoccum parvum is a fungal plant-pathogen belonging to the family Botryosphaeriaceae, and is considered one of the most aggressive causal agents of the grapevine trunk disease (GTD) Botryosphaeria dieback. In this study, the mycovirome of a single strain of N. parvum (COLB) was characterized by high throughput sequencing analysis of total RNA and subsequent bioinformatic analyses. Contig annotations, genome completions, and phylogenetic analyses allowed us to describe six novel mycoviruses belonging to four different viral families. The virome is composed of two victoriviruses in the family Totiviridae, one alphaendornavirus in the family Endornaviridae, two mitoviruses in the family Mitoviridae, and one narnavirus belonging to the family Narnaviridae. The presence of the co-infecting viruses was confirmed by sequencing the RT-PCR products generated from total nucleic acids extracted from COLB. This study shows that the mycovirome of a single N. parvum strain is highly diverse and distinct from that previously described in N. parvum strains isolated from grapevines.

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Drought Exacerbates Botryosphaeria Dieback Symptoms in Grapevines and Confounds Host-based Molecular Markers of Infection by Neofusicoccum parvum

Plant Disease ◽

10.1094/pdis-09-18-1549-re ◽

2019 ◽

Vol 103 (7) ◽

pp. 1738-1745 ◽

Cited By ~ 1

Author(s):

Erin R. A. Galarneau ◽

Daniel P. Lawrence ◽

Renaud Travadon ◽

Kendra Baumgartner

Keyword(s):

Drought Stress ◽

Interactive Effect ◽

Disease Diagnosis ◽

Cross Reactivity ◽

Water Volume ◽

Marker Genes ◽

Lesion Length ◽

Neofusicoccum Parvum ◽

Botryosphaeria Dieback ◽

Putative Marker

Neofusicoccum parvum, causal fungus of the grapevine trunk disease Botryosphaeria dieback, attacks the wood of Vitis vinifera. Because lesions are internal, using putative host-based markers of infection from leaves for diagnosis is a nondestructive option. However, their specificity under drought stress is unknown. Potted ‘Cabernet-Sauvignon’ were inoculated with N. parvum in the greenhouse after wounding (IW), and with wounded and nonwounded noninoculated controls. At 2 weeks postinoculation (WPI), half of the plants were severely stressed (SS), receiving 30% water volume of the well-watered (WW) plants. Larger lesions at 12 WPI among IW-SS plants, compared with all other treatments, revealed an interactive effect of inoculation and drought on lesion length. Expression of eight putative marker genes was analyzed in leaves by qPCR at the onset of drought stress, and at 8 and 12 WPI. One marker showed consistent over-expression at 8 WPI in IW plants, regardless of water treatment, suggesting specificity to infection. By 12 WPI, higher expression of seven genes in all SS plants (across inoculation treatments) revealed specificity to drought. Cross-reactivity of markers to drought, therefore, limits their utility for disease diagnosis in the field, where drought induced by climate and deficit irrigation is common.

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Production of Phytotoxic Metabolites by Botryosphaeriaceae in Naturally Infected and Artificially Inoculated Grapevines

Plants ◽

10.3390/plants10040802 ◽

2021 ◽

Vol 10 (4) ◽

pp. 802

Author(s):

Pierluigi Reveglia ◽

Regina Billones-Baaijens ◽

Jennifer Millera Millera Niem ◽

Marco Masi ◽

Alessio Cimmino ◽

...

Keyword(s):

Fungal Pathogens ◽

Protocatechuic Acid ◽

Physiological Factors ◽

Diplodia Seriata ◽

Grapevine Trunk Diseases ◽

Botryosphaeria Dieback ◽

Trunk Diseases ◽

One Year ◽

Pathogen Dna

Grapevine trunk diseases (GTDs) are considered a serious problem to viticulture worldwide. Several GTD fungal pathogens produce phytotoxic metabolites (PMs) that were hypothesized to migrate to the foliage where they cause distinct symptoms. The role of PMs in the expression of Botryosphaeria dieback (BD) symptoms in naturally infected and artificially inoculated wood using molecular and analytical chemistry techniques was investigated. Wood samples from field vines naturally infected with BD and one-year-old vines inoculated with Diplodia seriata, Spencermartinsia viticola and Dothiorella vidmadera were analysed by cultural isolations, quantitative PCR (qPCR) and targeted LC-MS/MS to detect three PMs: (R)-mellein, protocatechuic acid and spencertoxin. (R)-mellein was detected in symptomatic naturally infected wood and vines artificially inoculated with D. seriata but was absent in all non-symptomatic wood. The amount of (R)-mellein detected was correlated with the amount of pathogen DNA detected by qPCR. Protocatechuic acid and spencertoxin were absent in all inoculated wood samples. (R)-mellein may be produced by the pathogen during infection to break down the wood, however it was not translocated into other parts of the vine. The foliar symptoms previously reported in vineyards may be due to a combination of PMs produced and climatic and physiological factors that require further investigation.

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