The increasing demand for food coupled to various environmental pressures, is increasing the importance of sustainable agricultural practices.
BackgroundTrunk diseases threaten the longevity and productivity of grapevines in all viticulture production systems. They are caused by distantly-related fungi that form chronic wood infections. Variation in wood-decay abilities and production of phytotoxic compounds are thought to contribute to their unique disease symptoms. We recently released the draft sequences of Eutypa lata, Neofusicoccum parvum and Togninia minima, causal agents of Eutypa dieback, Botryosphaeria dieback and Esca, respectively. In this work, we first expanded genomic resources to three important trunk pathogens, Diaporthe ampelina, Diplodia seriata, and Phaeomoniella chlamydospora, causal agents of Phomopsis dieback, Botryosphaeria dieback, and Esca, respectively. Then we integrated all currently-available information into a genome-wide comparative study to identify gene families potentially associated with host colonization and disease development.ResultsThe integration of RNA-seq, comparative and ab initio approaches improved the protein-coding gene prediction in T. minima, whereas shotgun sequencing yielded nearly complete genome drafts of Dia. ampelina, Dip. seriata, and P. chlamydospora. The predicted proteomes of all sequenced trunk pathogens were annotated with a focus on functions likely associated with pathogenesis and virulence, namely (i) wood degradation, (ii) nutrient uptake, and (iii) toxin production. Specific patterns of gene family expansion were described using Computational Analysis of gene Family Evolution, which revealed lineage-specific evolution of distinct mechanisms of virulence, such as specific cell wall oxidative functions and secondary metabolic pathways in N. parvum, Dia. ampelina, and E. lata. Phylogenetically-informed principal component analysis revealed more similar repertoires of expanded functions among species that cause similar symptoms, which in some cases did not reflect phylogenetic relationships, thereby suggesting patterns of convergent evolution.ConclusionsThis study describes the repertoires of putative virulence functions in the genomes of ubiquitous grapevine trunk pathogens. Gene families with significantly faster rates of gene gain can now provide a basis for further studies of in planta gene expression, diversity by genome re-sequencing, and targeted reverse genetic approaches. The functional validation of potential virulence factors will lead to a more comprehensive understanding of the mechanisms of pathogenesis and virulence, which ultimately will enable the development of accurate diagnostic tools and effective disease management.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1624-z) contains supplementary material, which is available to authorized users.
This review illuminates key findings in our understanding of grapevine xylem resistance to fungal vascular wilt diseases. Grapevine (Vitis spp.) vascular diseases such as esca, botryosphaeria dieback, and eutypa dieback, are caused by a set of taxonomically unrelated ascomycete fungi. Fungal colonization of the vascular system leads to a decline of the plant host because of a loss of the xylem function and subsequent decrease in hydraulic conductivity. Fungal vascular pathogens use different colonization strategies to invade and kill their host. Vitis vinifera cultivars display different levels of tolerance toward vascular diseases caused by fungi, but the plant defense mechanisms underlying those observations have not been completely elucidated. In this review, we establish a parallel between two vascular diseases, grapevine esca disease and Dutch elm disease, and argue that the former should be viewed as a vascular wilt disease. Plant genotypes exhibit differences in xylem morphology and resistance to fungal pathogens causing vascular wilt diseases. We provide evidence that the susceptibility of three commercial V. vinifera cultivars to esca disease is correlated to large vessel diameter. Additionally, we explore how xylem morphological traits related to water transport are influenced by abiotic factors, and how these might impact host tolerance of vascular wilt fungi. Finally, we explore the utility of this concept for predicting which V. vinifera cultivars are most vulnerable of fungal vascular wilt diseases and propose new strategies for disease management.
Fungal wilt diseases are a threat to global food safety. Previous studies in perennial crops showed that xylem vessel diameter affects disease susceptibility. We tested the hypothesis that xylem vessel diameter impacts occlusion processes and pathogen compartmentalization in Vitis vinifera L. We studied the interaction between four grape commercial cultivars with the vascular wilt pathogen Phaeomoniella chlamydospora. We used qPCR and wood necrotic lesion length to measure fungal colonization coupled with histological studies to assess differences in xylem morphology, pathogen compartmentalization, and fungal colonization strategy. We provided evidence that grape cultivar with wide xylem vessel diameter showed increased susceptibility to P. chlamydospora. The host response to pathogen included vessel occlusion with tyloses and gels, deposition of non-structural phenolic compounds and suberin in vessel walls and depletion of starch in parenchyma cells. Pathogen compartmentalization was less efficient in wide xylem vessels than in narrow diameter vessels. Large vessels displayed higher number of tyloses and gel pockets, which provided substrate for P. chlamydospora growth and routes to escape occluded vessels. We discuss in which capacity xylem vessel diameter is a key determinant of the compartmentalization process and in turn grape cultivar resistance to disease caused by P. chlamydospora.
Travadon, R., Rolshausen, P. E., Gubler, W. D., Cadle-Davidson, L., and Baumgartner, K. 2013. Susceptibility of cultivated and wild Vitis spp. to wood infection by fungal trunk pathogens. Plant Dis. 97:1529-1536. Cultivars of European grapevine, Vitis vinifera, show varying levels of susceptibility to Eutypa dieback and Esca, in terms of foliar symptoms. However, little is known regarding cultivar susceptibility of their woody tissues to canker formation. Accordingly, we evaluated the relative susceptibility of V. vinifera cultivars ('Cabernet Franc", 'Cabernet Sauvignon', 'Chardonnay', 'Merlot', 'Riesling', 'Petite Syrah', and 'Thompson Seedless') and species or interspecific hybrids of North American Vitis (Vitis hybrid 'Concord', V. arizonica 'b42-26', V. rupestris x V. cinérea '111547-1', and Fennell 6 [V. aestivalis] x Malaga [V; vinifera] 'DVIT0166') to canker formation by seven trunk pathogens (Neofiisicoccum parvum, Lasiodipiodia theobromae, Phaeomonieila chiamydospora, Togninia minima, Phomopsis viticoia, Eutypa lata, and an undescribed Eutypa sp.). Susceptibility was based on the length of wood discoloration (LWD) in the woody stems of rooted plants in duplicate greenhouse experiments. Cultivars of V. vinifera andConcord did not vai^ significantly in susceptibility to N. pan'um or L theobromae (LWD of 21 to 88 mm at 14 weeks post inoculation; P > 0.16), suggesting that they are similarly susceptible to Botryosphaeria dieback. The table-grape Thompson Seedless was most susceptible to P. viticoia (mean LWD of 61 mm at 11 months post inoculation; P < 0.0001). V. vinifera cultivars and Concord showed similar susceptibility to the Esca pathogens, Phaeomoniella chiamydospora and T. minima. Susceptibility to E. lata was greatest in V. arizonica b42-26 (mean LWD of 96 mm at 11 months post inoculation; P < 0.03). In fact, all four American Vitis spp. were more susceptible to Eutypa dieback than the V. vinifera cultivars. Our findings suggest that no one cultivar is likely to provide resistance to the range of tmnk pathogens but that certain cultivars may be promising candidates for commercially relevant host resistance in grape-production systems where the dominant cultivars are very susceptible.Mention of trade names or commercial products is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA. USDA is an equal opportunity provider and employer.
Eutypa lata is a vascular pathogen of woody plants. In the present study we (i) determined which component(s) of the cell wall polymers were degraded in naturally infected grapevines and in artificially inoculated grape wood blocks; (ii) compared the pattern of wood decay in the tolerant grape cv. Merlot versus the susceptible cv. Cabernet Sauvignon; and (iii) identified secondary metabolites and hydrolytic enzymes expressed by E. lata during wood degradation. Biochemical analyses and a cytochemical study indicated that glucose-rich polymers were primary targets of E. lata. Structural glucose and xylose of the hemicellulose fraction of the plant cell wall and starch were depleted in infected woods identically in both cultivars. Moreover, the more tolerant cv. Merlot always had more lignin in the wood than the susceptible cv. Cabernet Sauvignon, indicating that this polymer may play a role in disease resistance. In vitro assays demonstrated the production by E. lata of oxidases, glycosidases and starch degrading enzymes. Phytotoxic secondary metabolites were also produced but our data suggest that they may bind to the wood. Finally, we demonstrated that free glucose in liquid cultures repressed primary but not secondary metabolism.
The plant vascular system has remained an underexplored niche despite its potential for hosting beneficial microbes. The aim of this work was to determine the origin of the microbial endophytes inhabiting grapevine. We focused on a single commercial vineyard in California over a two-year period and used an amplicon metagenomics approach to profile the bacterial (16S–V4) and fungal (ITS) communities of the microbiome across a continuum of six grapevine compartments: bulk soil, rhizosphere, root, cordon, cane and sap. Our data supported that roots are a bottleneck to microbial richness and that they are mostly colonized with soilborne microbes, including plant growth-promoting bacteria recruited by the host, but also saprophytic and pathogenic fungal invaders. A core group of taxa was identified throughout the vine; however, there was clear partitioning of the microbiome with niche adaptation of distinct taxonomic groups. Above- and belowground plant tissues displayed distinct microbial fingerprints and were intermixed in a limited capacity mostly by way of the plant sap. We discuss how cultural practices and human contact may shape the endosphere microbiome and identify potential channels for transmission of its residents.
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