Progress 10/01/13 to 09/30/18
Outputs
Target Audience:In the short term, this research will provide accurate and sensitive diagnostics tools for early detection of trunk pathogen. This knowledge can benefit vineyard managers, grapevine nurseries, farm advisors and private vineyard consultants. The developed molecular tools have the potentiality to be implemented in diagnostic labs. In addition the information on mechanisms of disease resistance in grapevine to powdery mildew, Pierce's disease and wood pathogens can benefit public and private grape breeding programs in the long term. Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided?The following people were trained in Dr. Cantu's laboratory as part of this project: Graduate students: Laura Jones (MSc student, Viticulture and Enology, degree awarded in Fall 2014) Abraham Morales-Cruz (PhD student, Horticulture and Agronomy, degree awarded in Winter 2018) Jerry Lin (MSc student Viticulture & Enology - degree awarded in Fall 2018; currently PhD student, Horticulture & Agronomy) Postdoctoral researcher: Dr. Barbara Blanco-Ulate Dr. Katherine Amrine Dr. Melanie Massonnet Dr. Andrea Minio Dr. Amanda Vondras Dr. Shahin Ali Undergraduate students: Gabrielle Allenbeck (honors student major: Viticulture and Enology) Zirou Ye (major: Viticulture and Enology) Yang He (major: Statistics) Dingren Liang (major: Global Disease) Lucero Espinoza (major: Plant Biotechnology) Aarush Gopalakrishnan (major: Computer Science) Visiting scholars: Alexandre Carriot (MSc student, Univ. of Bordeaux), Aurelie Sastre (MSc student, Univ. of Bordeaux), Chiara Broccanello (PhD student, Univ. of Padoa), Daniele Buonassisi (PhD student, Univ. Udine), Maggie Levy (Professor, Hebrew Univ.), Shiho Miki (MSc student, Shimane Univ.). How have the results been disseminated to communities of interest?I interacted regularly with members of the local grape industry groups by way of seminars (e.g.: Napa Valley Grapegrowers, Vintage report, Current Wine & Winegrape Research, Current Issues of Vineyard Health) and UC Davis outreach events (e.g.: "UC Davis on the road" events). What do you plan to do during the next reporting period to accomplish the goals?
Nothing Reported
Impacts
What was accomplished under these goals?
In the five years of this project, we have successfully applied systems biology (i.e., the computational integration of genomics, transcriptomics, and metabolomics data) to a variety of grape traits, with a focus on grape responses to microbial activities. We have sequenced and analyzed transcriptomes for several grape pathosystems that provide not only a novel and comprehensive view of the activities of grape genes associated with biotic stress, but also the information needed to construct gene networks and identify critical-regulatory hubs of grapevine immune responses (Amrine et al., 2015a). We completed the sequencing and analysis of the powdery mildew responsive transcriptomes of seven V. vinifera accessions from Central Asia that display varying levels of genetic resistance to powdery mildew (Amrine et al., 2015b). Transcriptomes of individuals segregating for the V. piasezkii resistance loci Ren6 and Ren7 (Pap et al., 2016) were sequenced in Winter 2015 and are being analyzed using a novel associative transcriptomics approach, where we use transcriptome sequencing to identify and score molecular markers representing variation in both gene sequences and gene expression, which are then correlated with variation in powdery mildew resistance. Biological material for transcriptional responses of V. cinerea (Ren2), V. romanetii (Ren4), and Muscadinia rotundifolia (Run1 & 2) was collected in Summer 2016. We have used similar approaches to study grapevine responses to Xylella fastidiosa (Rapicavoli et al., 2018) and to the fungal agents of esca, eutypa dieback, and botryosphaeria dieback (Morales-Cruz et al., 2017; Massonnet et al., 2017). As a result of these projects, we have developed one of the most extensive dataset of plant transcriptional responses to pathogens. This dataset has given us the opportunity to start developing novel network analysis and machine learning techniques to build computer models of the grape transcriptional dynamics, and discover core regulators and other novel genetic loci that can be manipulated through marker assisted breeding for trait improvement. In Blanco-Ulate et al. (2015), we integrated transcriptomics, metabolomics, and enzyme activity assays to characterize the impact of noble rot on the development and metabolism of white-skinned grape berries under field conditions. We also extended the phenotypical observations to the metabolites of commercial botrytized wines produced from the same vineyard where the berries were collected, and corroborated that key flavor compounds that result from noble rot are carried over to the wines. This approach allowed us to demonstrate that noble rot acts as a developmental trigger in white-skinned berries to promote developmental and metabolic events associated with healthy ripening of red-skinned berries, including the expression of the important developmental regulators R2R3-MYBs and the biosynthesis of anthocyanins. We applied the same approach to study the impact of red blotch on berry development and metabolism. In Blanco-Ulate et al. (2017) we describe how red blotch disrupts normal berry development with consequent induction of primary metabolic pathways normally associated with early berry development, while inhibiting ripening-associated secondary metabolic pathways involved in the generation of color, flavor and aroma compounds. These studies demonstrate the effectiveness of integrating transcriptomics with chemical and enzymatic analyses to understand the regulation of berry metabolism in the vineyard. As a result, we now can monitor at great detail the genetic and biochemical activities responsible for the biosynthesis of flavor compounds in function of the grape genotype or cultural, pathological or environmental conditions. During the duration of this project, our research on grapevine pathogen biology has focused mostly on the fungi that cause trunk diseases. Grapevines, like other perennial crops, are affected by so-called 'trunk diseases', which damage the trunk and other woody tissues. Mature grapevines typically contract more than one trunk disease and often multiple grapevine trunk pathogens (GTPs) are recovered from infected tissues. The co-existence of different GTP species in complex and dynamic microbial communities complicates the study of the molecular mechanisms underlying disease development especially under vineyard conditions. As a consequence, most studies on host-plant interactions in the trunk-disease complex rely on inoculations with a single pathogen. In Morales-Cruz (2017), we described the development of a novel community-level transcriptomics (i.e., closed-reference metatranscriptomics) approach that can monitor simultaneously the virulence activities of multiple GTPs in planta. This novel approach is based on the extensive genomic resources that we have developed in the past four years to study grapevine trunk pathogens. The approach was tested using both controlled inoculations and samples from mature grapevines displaying a variety of disease symptoms collected from commercial vineyards. We also show that this approach provides a more effective way to study activities of fungal communities than the commonly applied metatranscriptomics based on de novo assembly of RNAseq reads. This approach will facilitate the study of grapevine trunk disease complex, we also expect that will be applied to other pathosystems where the activities of multiple organisms determine the disease outcome. The highly specific and quantitative nature of the mapping approach can find useful application for disease diagnostics both in production vineyards and nurseries, particularly. In Massonnet et al (2018), we described a comprehensive analysis of the patterns of gene expression of virulence functions of Neofusicoccum parvum, primarily involved in cell wall degradation and secondary metabolism. Neofusicoccum parvum is a cosmopolitan fungal pathogen that causes Botryosphaeria dieback of grapevine. It is an aggressive pathogen that causes important economic losses in all major grape-growing regions of the world. From a scientific perspective, it has become for an increasing number of laboratories in the US and Europe a model fungus to study the grapevine trunk-disease complex. We integrated cutting-edge genome sequencing and assembly methods with RNA sequencing analyses to profile genome-wide virulence factor expression as the fungus feeds on different growth substrates, including wood from different grape varieties, and during an extensive time course of interaction with the woody stems of grape plants. Using a combination of univariate and multivariate statistical testing, and co-expression network analysis, we demonstrated that co-regulated and physically clustered genes coding for virulence factors are induced when N. parvum feeds on a woody substrate or at specific stages of infection. Based on results of the analyses of promoter motifs and co-expression network topology we discuss the role of a multi-layered regulatory system of chromatin and transcriptional regulators in controlling the activity of what now appear to be genomic clusters of virulence factors. With collaborator Caroline Roper (UC Riverside), we were invited to write a critical review on research related to diseases caused by Xylella fastidiosa, including Pierce's diseases of grapevines (Rapicavoli et al., 2017).
Publications
- Type:
Journal Articles
Status:
Published
Year Published:
2018
Citation:
Massonnet M., Morales-Cruz A., Minio A., Figueroa-Balderas R., Lawrence
D. P., Travadon R., Rolshausen P. E., Baumgartner K., and D. Cantu. Whole genome resequencing and pan-transcriptome reconstruction highlight the impact of genomic structural variation on secondary metabolism gen clusters in the grapevine Esca pathogen Phaeoacremonium minimum. Frontiers in Microbiology 9,1784
- Type:
Journal Articles
Status:
Published
Year Published:
2018
Citation:
Zaini P.A., Nascimento R., Gouran H., Cantu D., Chakraborty S., Phu M.,
Goulart L.R., and A.M. Dandekar. Molecular Profiling of Pierces Disease Outlines the Response Circuitry of Vitis vinifera to Xylella fastidiosa Infection. Frontiers in Plant Science 9,771
- Type:
Journal Articles
Status:
Published
Year Published:
2018
Citation:
Koyama R., Ruffo R., De Souza R.T., Borges W.F.S., Anderson M., Waterhouse A.L., Cantu D., Fidelibus M.W., and B. Blanco-Ulate. Exogenous abscisic acid promotes anthocyanin biosynthesis and increased expression of flavonoid biosynthesis genes in Vitis vinifera x Vitis labrusca table grapes in a subtropical region. Frontiers in Plant Science 9,323
- Type:
Journal Articles
Status:
Published
Year Published:
2017
Citation:
Buonassisi D., Perazzoli M., Peressotti E., Tadiello A., Musetti R., Velasco R., Cantu D. and S. Vezzulli. Grapevine downy mildew dual epidemics: a leaf and in florescence transcriptomics study. Acta Horticulturae 265 - 270
- Type:
Journal Articles
Status:
Published
Year Published:
2018
Citation:
Rapicavoli J., Blanco-Ulate B., Muszynski A., Figueroa-Balderas R., Morales-Cruz A., Azadi P., Dobruchowska J., Castro C., Cantu D. and C. Roper. Lipopolysaccharide O-antigen delays plant innate immune recognition of Xylella fastidiosa. Nature Communications 9,390
|
Progress 10/01/16 to 09/30/17
Outputs
Target Audience:In the short term, this research will provide accurate and sensitive diagnostics tools for early detection of trunk pathogen. This knowledge can benefit vineyard managers, grapevine nurseries, farm advisors and private vineyard consultants. The developed molecular tools have the potentiality to be implemented in diagnostic labs. In addition the information on mechanisms of disease resistance in grapevine to powdery mildew, Pierce's disease and wood pathogens can benefit public and private grape breeding programs. Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided?Graduate students: Abraham Morales-Cruz (PhD student Horticulture & Agronomy) Jerry Lin (MSc student Viticulture & Enology & since Fall 2017 PhD student Horticulture & Agronomy) Brianna Fochs (MSc student Plant Biology) Visiting students: Shiho Miki (MSc student, Shimane University, Japan) Postdoctoral researcher: Dr. Melanie Massonnet Dr. Andrea Minio Dr. Amanda Vondras Undergraduate students: Aarush Gopalakrishnan (major: Computer Science) Yang He (major: Statistics) How have the results been disseminated to communities of interest?I interacted regularly with members of the local grape industry groups by way of seminars (e.g.: Napa Valley Grapegrowers, Vintage report, Current Wine & Winegrape Research) and UC Davis outreach events (e.g.: "UC Davis on the road" events). What do you plan to do during the next reporting period to accomplish the goals?Work in progress for objective 1 - Characterize the grapevine disease responsive genes, pathways, and regulatory networks We are dissecting the regulatory gene networks associated with early immune responses of grapevines to specific molecular patterns of Xylella fastidiosa (Xf). The goal of this project is to investigate the role of lipopolysaccharide (LPS), an abundant bacterial cell surface polysaccharide, as pathogen associated molecular pattern of Xf responsible of triggering localized and systemic immunity in grapevines. Dr. Roper's group generated a Xf mutant (designated wzy) that produces an altered lipopolysaccharide (LPS). We observed that the altered Xf cells lose virulence and rapidly activate aspects of a grapevine's basal immune response. Wzy mutants provide a unique and powerful experimental tool to study the molecular basis of basal immunity in grapevines. We completed a transcriptome profiling experiment at four time points within the first 24 hours post inoculation and the manuscript describing the specific patterns of transcriptional regulation responsive to the wzy mutant is currently under review. Work in progress for objective 2 - Identify the major regulatory functions of the grapevine disease response by integrating transcriptomics and genetic mapping In the previous review period, we completed the sequencing and analysis of the powdery mildew responsive transcriptomes of seven V. vinifera accessions from Central Asia that display varying levels of genetic resistance to powdery mildew. Transcriptomes of individuals segregating for the V. piasezkii resistance loci Ren6 and Ren7 were sequenced in Winter 2015 and are being analyzed using a novel associative transcriptomics approach, where we use transcriptome sequencing to identify and score molecular markers representing variation in both gene sequences and gene expression, which are then correlated with variation in powdery mildew resistance. Biological material for transcriptional responses of V. cinerea (Ren2), V. romanetii (Ren4), and Muscadinia rotundifolia (Run1 & 2) was collected in Summer 2016. We have used similar approaches to study grapevine responses to Xylella fastidiosa and to the fungal agents of esca, eutypa dieback, and botryosphaeria dieback (as described above). As a result of these projects, my laboratory is developing one of the most extensive dataset of plant transcriptional responses to pathogens. We are now implementing and adapting network analysis and machine learning techniques to build computer models of the grape immune system, and discover core regulators and other novel genetic loci that can be manipulated through marker assisted breeding. Work in progress for objective 3 - Characterize the mechanisms of fungal pathogenesis in grapevine We have completed the sequencing of multiple isolates of the trunk pathogens E. lata and Pm. minimum. We are analyzing the intraspecific genetic diversity to explore the genetic bases of the broad variability in virulence observed in populations of these pathogens.
Impacts
What was accomplished under these goals?
Objective 1 - Characterize the grapevine disease responsive genes, pathways, and regulatory networks. In the 2016-2017 period we have completed and published (Massonnet et al., 2017) the study of grapevine responses to the ascomycete pathogen Neofusicoccum parvum. Neofusicoccum parvum is a cosmopolitan fungal pathogen that causes Botryosphaeria dieback of grapevine. It is an aggressive pathogen that causes important economic losses in all major grape-growing regions of the world. From a scientific perspective, it has become for an increasing number of laboratories in the US and Europe a model fungus to study the grapevine trunk-disease complex, which includes (in addition to Botryosphaeria dieback) Eutypa dieback, Phomopsis dieback, and Esca. We used RNAseq to profile grapevine responses to N. parvum infection. We studied both local (wood) and distal (leaf) responses. The grape transcriptome was sequenced at seven time points (0, 3, and 24 hours; 2, 6, 8, and 12 weeks) to cover both early and late responses to the infection. While most intense transcriptional responses were detected in the stems at 24 hours, strong responses were not detected in the leaves until the next sampling point at 2 weeks post-inoculation. Network co-expression analysis identified modules of co-expressed genes common to both organs and showed most of these genes were asynchronously modulated. The temporal shift between stem vs. leaf responses affected transcriptional modulation of genes involved in both signal perception and transduction, as well as downstream biological processes, including oxidative stress, cell wall rearrangement and cell death. Promoter analysis of the genes asynchronously modulated in stem and leaves during N. parvum colonization suggests that the temporal shift of transcriptional reprogramming between the two organs might be due to asynchronous co-regulation by common transcriptional regulators. Topology analysis of stem and leaf co-expression networks pointed to specific transcription factor-encoding genes, including WRKY and MYB, which may be associated with the observed transcriptional responses in the two organs. Understanding the signals that are responsible for the communication between different grapevine organs during infection will help shed light into the systemic signaling mechanisms in woody plants. The identification of molecular patterns that accumulate in leaves specifically in presence of trunk infection will enable early detection of trunk diseases and the timely removal of infected parts. As described below in the work in progress section we are completing the analysis of transcriptional responses to powdery mildew and Pierce's disease. Objective 2 - Identify the major regulatory functions of the grapevine disease response by integrating transcriptomics and genetic mapping. Transcriptomes of individuals segregating for the V. piasezkii resistance loci Ren6 and Ren7 were sequenced in Winter 2015 and are being analyzed using a novel associative transcriptomics approach, where we use transcriptome sequencing to identify and score molecular markers representing variation in both gene sequences and gene expression, which are then correlated with variation in powdery mildew resistance. Biological material for transcriptional responses of V. cinerea (Ren2), V. romanetii (Ren4), and Muscadinia rotundifolia (Run1 & 2) was collected in Summer 2016. Analyses are ongoing. Objective 3 - Characterize the mechanisms of fungal pathogenesis in grapevine. Mature grapevines typically contract more than one trunk disease and often multiple grapevine trunk pathogens (GTPs) are recovered from infected tissues. The co-existence of different GTP species in complex and dynamic microbial communities complicates the study of the molecular mechanisms underlying disease development especially under vineyard conditions. As a consequence, most studies on host-plant interactions in the trunk-disease complex rely on inoculations with a single pathogen. In the publication by Morales-Cruz et al. (2017), we described the development of a novel community-level transcriptomics (i.e., closed-reference metatranscriptomics) approach that can monitor simultaneously the virulence activities of multiple GTPs in planta. This novel approach is based on the extensive genomic resources that we have developed in the past four years to study grapevine trunk pathogens. The approach was tested using both controlled inoculations and samples from mature grapevines displaying a variety of disease symptoms collected from commercial vineyards. We also show that this approach provides a more effective way to study activities of fungal communities than the commonly applied metatranscriptomics based on de novo assembly of RNAseq reads. This approach will facilitate the study of grapevine trunk disease complex, we also expect that will be applied to other pathosystems where the activities of multiple organisms determine the disease outcome. The highly specific and quantitative nature of the mapping approach can find useful application for disease diagnostics both in production vineyards and nurseries, particularly.
Publications
- Type:
Journal Articles
Status:
Published
Year Published:
2017
Citation:
Blanco-Ulate B, Hopfer H, Figueroa-balderas R, Ye Z, Rivero RM, Albacete A, P�rez-alfocea F, Koyama R, Anderson MM, Smith RJ, Ebeler SE, and D Cantu (2017) Red blotch disease alters grape berry development and metabolism by interfering with the transcriptional and hormonal regulation of ripening. Journal of Experimental Botany. doi: 10.1093/cercor/bhw393
- Type:
Journal Articles
Status:
Awaiting Publication
Year Published:
2017
Citation:
Morales-cruz A, Allenbeck G, Figueroa-balderas R, Ashworth VE, Lawrence DP, Travadon R, Smith RJ, Baumgartner K, Philippe E, and D Cantu (2017) Closed-reference metatranscriptomics enables in planta profiling of putative virulence activities in the grapevine trunk-disease complex. Molecular Plant Pathology 99275: 114
- Type:
Journal Articles
Status:
Published
Year Published:
2017
Citation:
Massonnet M, Figueroa Balderas R, Galarneau E, Miki S, Lawrence D, Sun Q, Wallis CM, Baumgartner K, and D Cantu (2017) Neofusicoccum parvum colonization of the grapevine woody stem triggers asynchronous host responses at the site of infection and in the leaves. Front Plant Sciences 8: 1117
- Type:
Journal Articles
Status:
Awaiting Publication
Year Published:
2017
Citation:
Rapicavoli J, Ingel B, Blanco-Ulate B., D Cantu, and Roper C. Xylella fastidiosa: An examination of a re-emerging plant pathogen. Molecular Plant Pathology. doi: 10.1111/mpp.12585
|
Progress 10/01/15 to 09/30/16
Outputs
Target Audience:In the short term, this research will provide accurate and sensitive diagnostics tools for early detection of trunk pathogen. This knowledge can benefit vineyard managers, grapevine nurseries, farm advisors and private vineyard consultants. The developed molecular tools have the potentiality to be implemented in diagnostic labs. In addition the information on mechanisms of disease resistance in grapevine to powdery mildew can benefit public and private grape breeding programs. Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided?The following people were trained in Dr. Cantu's laboratory as part of this project in the period of this progress report: Graduate students: Abraham Morales-Cruz (PhD student Horticulture & Agronomy) Jerry Lin (MSc student Viticulture & Enology) Visiting students: Jadran Garcia Navarrete (MSc student, Costa Rica Institute of Technology, Costa Rica) Shiho Miki (MSc student, Shimane University, Japan) Postdoctoral researcher: Dr. Melanie Massonnet Dr. Barbara Blanco-Ulate (now Assistant Professor at UC Davis) Undergraduate students: Ye Zirou (major: Viticulture and Enology) Jade Hendry (major: Viticulture and Enology) Gabrielle Allenbeck (UCD Honors Student; major: Viticulture and Enology) How have the results been disseminated to communities of interest?I interacted regularly with members of the local grape industry groups by way of seminars (e.g.: Napa Valley Grapegrowers, Vintage report, Current Wine & Winegrape Research) and UC Davis outreach events (e.g.: "UC Davis on the road" events). What do you plan to do during the next reporting period to accomplish the goals?Work in progress for objective 1 - Characterize the grapevine disease responsive genes, pathways, and regulatory networks We are dissecting the regulatory gene networks associated with early immune responses of grapevines to specific molecular patterns of Xylella fastidiosa (Xf). The goal of this project is to investigate the role of lipopolysaccharide (LPS), an abundant bacterial cell surface polysaccharide, as pathogen associated molecular pattern of Xf responsible of triggering localized and systemic immunity in grapevines. Dr. Roper's group generated a Xf mutant (designated wzy) that produces an altered lipopolysaccharide (LPS). We observed that the altered Xf cells lose virulence and rapidly activate aspects of a grapevine's basal immune response. Wzy mutants provide a unique and powerful experimental tool to study the molecular basis of basal immunity in grapevines. We completed a transcriptome profiling experiment at four time points within the first 24 hours post inoculation and the manuscript describing the specific patterns of transcriptional regulation responsive to the wzy mutant is currently under preparation. Work in progress for objective 2 - Identify the major regulatory functions of the grapevine disease response by integrating transcriptomics and genetic mapping Biological material for transcriptional responses to powdery mildew of V. cinerea (Ren2), V. romanetii (Ren4), and Muscadinia rotundifolia (Run1 & 2) was collected in Summer 2016. We are using similar approaches to study grapevine responses to the fungal agents of esca, eutypa dieback, and botryosphaeria dieback. As a result of these projects, my laboratory is developing one of the most extensive dataset of plant transcriptional responses to pathogens. We are now implementing and adapting network analysis and machine learning techniques to build computer models of the grape immune system, and discover core regulators and other novel genetic loci that can be manipulated through marker assisted breeding. Work in progress for objective 3 - Characterize the mechanisms of fungal pathogenesis in grapevine We are currently annotating the complete and highly-contiguous genomes of the causal agents of Esca and Eutypa dieback as well as completing the assemblies of 15 Botryosphaeria pathogens. These genomes, in combination with transcriptional data and information on genetic diversity within species, will be used to study the molecular mechanisms of pathogenesis and virulence on grapevines. We are also taking advantage of this unprecedentedly extensive genomic information to develop precise metatranscriptomic methods to characterize the in planta activities of microbial populations associated with trunk diseases.
Impacts
What was accomplished under these goals?
Objective 1 - Characterize the grapevine disease responsive genes, pathways, and regulatory networks In the 2015-2016 period we have completed and published the study of the impact of Botrytis cinerea during noble rot on berry development and metabolism (see Blanco-Ulate et al., 2015). Noble rot results from exceptional infections of ripe grape (Vitis vinifera) berries by Botrytis cinerea. Unlike bunch rot, noble rot promotes favorable changes in grape berries and the accumulation of secondary metabolites that enhance wine grape composition. Noble rot-infected berries of cv Sémillon, a white-skinned variety, were collected over 3 years from a commercial vineyard at the same time that fruit were harvested for botrytized wine production. Using an integrated transcriptomics and metabolomics approach, we demonstrated that noble rot alters the metabolism of cv Sémillon berries by inducing biotic and abiotic stress responses as well as ripening processes. During noble rot, B. cinerea induced the expression of key regulators of ripening-associated pathways, some of which are distinctive to the normal ripening of red-skinned cultivars. Enhancement of phenylpropanoid metabolism, characterized by a restricted flux in white-skinned berries, was a common outcome of noble rot and red-skinned berry ripening. Transcript and metabolite analyses together with enzymatic assays determined that the biosynthesis of anthocyanins is a consistent hallmark of noble rot in cv Sémillon berries. The biosynthesis of terpenes and fatty acid aroma precursors also increased during noble rot. We finally characterized the impact of noble rot in botrytized wines. Altogether, the results of this work demonstrated that noble rot causes a major reprogramming of berry development and metabolism. This desirable interaction between a fruit and a fungus stimulates pathways otherwise inactive in white-skinned berries, leading to a greater accumulation of compounds involved in the unique flavor and aroma of botrytized wines. We have applied a similar experimental approach to study the molecular and biochemical mechanisms underlying the altered synthesis of critical aroma and flavor compounds in red blotch-infected berries. Grapevine Red Blotch associated Virus (GRBaV) is a major threat to the wine industry in the United States. GRBaV infections (aka red blotch disease) compromise crop yield and berry chemical composition, affecting the flavor and aroma properties of must and wine. In this first study, we combined genome-wide transcriptional profiling with targeted metabolite analyses and biochemical assays to characterize the impact of the disease on red-skinned berry ripening and metabolism. Using naturally infected berries collected from two vineyards, we were able to identify consistent berry responses to GRBaV across different environmental and cultural conditions. Extensive alteration of both primary and secondary metabolism occurred in GRBaV-infected berries during ripening. Notably, GRBaV infections of post-véraison berries resulted in the induction of primary metabolic pathways normally associated with early berry development (e.g., thylakoid electron transfer and Calvin cycle), while inhibiting ripening-associated pathways, such as a reduced metabolic flux in the central and peripheral phenylpropanoid pathways. Metabolic reprogramming correlated with perturbations at multiple regulatory levels of berry development. Red blotch caused the abnormal expression of transcription factors (e.g., NACs, MYBs and AP2-ERFs) and elements of the post-transcriptional machinery that function during red-skinned berry ripening. Abscisic acid, ethylene and auxin pathways, which control both the initiation of ripening and stress responses, were also compromised. Based on these results we concluded that GRBaV infections disrupt normal berry development and stress responses by altering transcription factors and hormone networks, which result in the inhibition of ripening pathways involved in the generation of color, flavor, and aroma compounds. As described below in the "work in progress" section we started expanding the transcriptome sequencing to grape responses to powdery mildew, Pierce's disease and trunk pathogens. Objective 2 - Identify the major regulatory functions of the grapevine disease response by integrating transcriptomics and genetic mapping Transcriptomes of individuals segregating for the V. piasezkii resistance loci Ren6 and Ren7 were sequenced in Winter 2015 and are being analyzed using a novel associative transcriptomics approach, where we use transcriptome sequencing to identify and score molecular markers representing variation in both gene sequences and gene expression, which are then correlated with variation in powdery mildew resistance. Objective 3 - Characterize the mechanisms of fungal pathogenesis in grapevine In the review period we have completed the re-sequencing of over 30 genomes from isolates of Neofusicoccum parvum, Eutypa lata, and Togninia minima and other trunk pathogens with distinct geographical origins, hosts, and aggressiveness and are now analyzing their genetic diversity in relation to virulence profiles, cell wall degrading capabilities, and toxin biosynthesis. Using single molecule sequencing technology we have reconstructed (telomere-to-telomere) the complete DNA sequences of all chromosomes of E. lata and N. parvum (see Massonnet et al., 2016). The ascomycete N. parvum, one of the causal agents of Botryosphaeria dieback, is a destructive wood-infecting fungus and a serious threat to grape production worldwide. The capability of colonizing woody tissue combined with the secretion of phytotoxic compounds is thought to underlie its pathogenicity and virulence. We have characterized the repertoire of virulence factors and their transcriptional dynamics as the fungus feeds on different substrates and colonizes the woody stem. We annotated the highly contiguous genome constructed using single molecule real-time DNA sequencing. Transcriptome profiling by RNA-sequencing determined the genome-wide patterns of expression of virulence factors both in vitro (potato dextrose agar or medium amended with grape wood as substrate) and in planta. Pairwise statistical testing of differential expression followed by co-expression network analysis revealed that physically clustered genes coding for putative virulence functions were induced depending on substrate or stage of plant infection. Co-expressed gene clusters were significantly enriched not only in genes associated with secondary metabolism, but also with cell wall degradation, suggesting that dynamic co-regulation of transcriptional networks contribute to multiple aspects of N. parvum virulence. In most of the co-expressed clusters, all genes shared at least a common motif in their promoter region indicative of co-regulation by the same transcription factor. Co-expression analysis also identified chromatin regulators with correlated expression with inducible clusters of virulence factors, suggesting a complex, multi-layered regulation of the virulence repertoire of N. parvum.
Publications
- Type:
Journal Articles
Status:
Published
Year Published:
2016
Citation:
Massonnet M, Morales-cruz A, Figueroa-balderas R, Lawrence DP, Baumgartner K, Cantu D (2016) Condition-dependent co-regulation of genomic clusters of virulence factors in the grapevine trunk pathogen Neofusicoccum parvum. Mol Plant Pathol. doi: 10.1111/mpp.12491
- Type:
Journal Articles
Status:
Published
Year Published:
2015
Citation:
Blanco-Ulate B, Amrine KC, Collins TS, Rivero RM, Vicente AR, Morales-Cruz A, Doyle CL, Ye Z, Allen G, Heymann H, et al (2015) Developmental and metabolic plasticity of white-skinned grape berries in response to Botrytis cinerea during noble rot. Plant Physiol 169: pp.00852.2015
- Type:
Journal Articles
Status:
Published
Year Published:
2016
Citation:
Pap D, Riaz S, Dry IB, Jermakow A, Tenscher AC, Cantu D, Ol�h R, Walker MA (2016) Identification of two novel powdery mildew resistance loci, Ren6 and Ren7, from the wild Chinese grape species Vitis piasezkii. BMC Plant Biol 16: 170
|
Progress 10/01/14 to 09/30/15
Outputs
Target Audience:In the short term, this research will provide accurate and sensitive diagnostics tools for early detection of trunk pathogen. This knowledge can benefit vineyard managers, grapevine nurseries, farm advisors and private vineyard consultants. The developed molecular tools have the potentiality to be implemented in diagnostic labs. In addition the information on mechanisms of disease resistance in grapevine to powdery mildew can benefit public and private grape breeding programs. Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided?The following people were trained in Dr. Cantu's laboratory as part of this project in the period of this progress report: Graduate students: Abraham Morales-Cruz (PhD student Horticulture & Agronomy) Jerry Lin (MSc student Viticulture & Enology) Visiting students: Daniele Buonassisi (Foundation Edmund Mach, Italy) Renata Koyama (Londrina State University, Brazil) Postdoctoral researcher: Dr. Katherine C.H. Amrine Dr. Barbara Blanco-Ulate Undergraduate students: Ye Zirou (major: Viticulture and Enology) Jade Hendry (major: Viticulture and Enology) Gabrielle Allenbeck (UCD Honors Student; major: Viticulture and Enology) How have the results been disseminated to communities of interest?I interacted regularly with members of the local grape industry groups by way of seminars (e.g.: Napa Valley Grapegrowers, Vintage report, Current Wine & Winegrape Research) and UC Davis outreach events (e.g.: "UC Davis on the road" events). What do you plan to do during the next reporting period to accomplish the goals?Work in progress for objective 1 - Characterize the grapevine disease responsive genes, pathways, and regulatory networks We started dissecting the regulatory gene networks associated with early immune responses of grapevines to specific molecular patterns of Xylella fastidiosa (Xf). The goal of this project is to investigate the role of lipopolysaccharide (LPS), an abundant bacterial cell surface polysaccharide, as pathogen associated molecular pattern of Xf responsible of triggering localized and systemic immunity in grapevines. Dr. Roper's group generated a Xf mutant (designated wzy) that produces an altered lipopolysaccharide (LPS). We observed that the altered Xf cells lose virulence and rapidly activate aspects of a grapevine's basal immune response. We completed a transcriptome profiling experiment at four time points within the first 24 hours post inoculation and the manuscript describing the specific patterns of transcriptional regulation responsive to the wzy mutant is currently under preparation. The objectives for the 2015-2017 phase of the project are to apply transcriptomics to characterize the systemic response to Xf, and test if LPS-induced resistance to Pierce's disease persists after winter dormancy and is transmissible through the graft unions. Work in progress for objective 2 - Identify the major regulatory functions of the grapevine disease response by integrating transcriptomics and genetic mapping In Winter 2015 we produced replicated powdery mildew infections in control environment for individual genotypes segregating for Ren6, Ren7, or both Ren6/Ren7. As for the Ren1 project, PM-infected leaves were collected one day and five days after inoculation with E. necator c-strain conidia. In total, 96 libraries were produced and sequenced. The genomes of the two parents of the F1 population were shotgun sequenced at 50X coverage using Illumina technology. Genomic DNA sequences were aligned to the reference PN40024 and sequence variants were used to develop a synthetic diploid reference for mapping the F1 RNAseq data. An average of 14.5 million high-quality RNAseq reads were generated and aligned to the reconstructed diploid reference. Statistical testing was carried out to identify genes and alleles induced by PM. We are currently comparing powdery mildew responses across the F1 individuals to identify Ren6 and Ren7 specific responses. Dormant cuttings for the remaining genotypes carrying Run1, Run2 or Ren4 were collected and are being rooted. We expect to be able to complete the powdery mildew infections and start the RNA sequencing in Spring 2016. Work in progress for objective 3 - Characterize the mechanisms of fungal pathogenesis in grapevine We have re-sequenced over 30 genomes from isolates of N. parvum, E. lata, and T. minima with distinct geographical origins, hosts, and aggressiveness and are now analyzing their genetic diversity in relation to virulence profiles, cell wall degrading capabilities, and toxin biosynthesis.
Impacts
What was accomplished under these goals?
Objective 1 - Characterize the grapevine disease responsive genes, pathways, and regulatory networks. The interaction between grape berries and B. cinerea during the development of noble rot provides a valuable experimental system to study how plant metabolism is modulated in response to biotic stress under field conditions. We previously demonstrated that B. cinerea promotes susceptibility by inducing ripening/senescence in unripe fruit and, during this review period, used transcriptomics and fruit mutant analysis to develop a model describing how ethylene, salicylic acid, jasmonic acid and abscisic acid influence the susceptibility of fruit to B. cinerea. Results from a study led by my research group demonstrate for the first time that B. cinerea infections, as noble rot, act as a developmental trigger in white-skinned berries to promote ripening-associated secondary metabolism. Using state-of-the-art transcriptomics and metabolomics approaches as well as enzymatic assays on field samples from multiple years of collection, we determined that noble rot: (i) triggers major regulatory switches known to control the activation of ripening associated pathways; (ii) activates metabolic pathways in white-skinned berries that are generally associated with ripening of red-skinned berries; (iii) differs from bunch rot as it induces ripening-associated pathways involved in the accumulation of key aroma and flavor compounds of wine grapes. The results of this work not only demonstrate the effectiveness of integrating multiple -omics approaches to understand the impact of plant-microbe interactions on plant metabolism under field conditions, but also provide valuable information that may lead to the development of novel agronomical and/or biotechnological approaches to improve fruit quality traits. Objective 2 - Identify the major regulatory functions of the grapevine disease response by integrating transcriptomics and genetic mapping. Grape powdery mildew, caused by the biotrophic ascomycete Erysiphe necator, is a devastating fungal disease that affects most Vitis vinifera cultivars. We have previously identified a panel of V. vinifera accessions from Central Asia with partial resistance toPM that possess a Ren1-like local haplotype. In this study, we show that in addition to the typical Ren1-associated late post-penetration resistance, these accessions display a range of different levels of disease development suggesting that alternative alleles or additional genes contribute to determining the outcome of the interaction with the pathogen. To identify potential Ren1-dependent transcriptional responses and functions associated with the different levels of resistance, we sequenced and analyzed the transcriptomes of these Central Asian accessions at two time points of powdery mildew infection. Transcriptomes were compared to identify constitutive differences and PM-inducible responses that may underlie their disease resistant phenotype. Responses to E. necator in all resistant accessions were characterized by an early up-regulation of 13 genes, most encoding putative defense functions, and a late down-regulation of 32 genes, enriched in transcriptional regulators and protein kinases. Potential Ren1-dependent responses included a hotspot of co-regulated genes on chromosome 18. We also identified 81 genes whose expression levels and dynamics correlated with the phenotypic differences between the most resistant accessions 'Karadzhandahal', DVIT3351.27, and O34-16 and the other genotypes. This study provides a first exploration of the functions associated with varying levels of partial resistance to powdery mildew in V. vinifera accessions that can be exploited as sources of genetic resistance in grape breeding programs. Objective 3 - Characterize the mechanisms of fungal pathogenesis in grapevine. Trunk 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. The 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. This 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 ultimately 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. In the 2015 - 2016 grant cycle, we have also tested different NGS-based methods for the detection of trunk pathogen in symptomatic infected field material and compared the results with traditional diagnostic approaches. All methods we tested were in agreement with traditional diagnostic methods. NGS-based methods also detected simultaneously multiple pathogen species with no need of tedious and hands-on sample culturing and colony purification. Additionally, unlike traditional qualitative diagnostics, deep sequencing also allowed to determine the relative abundance of the different species.
Publications
- Type:
Journal Articles
Status:
Published
Year Published:
2015
Citation:
Morales-Cruz A., Amrine K.C.H., Blanco-Ulate B.; Lawrence D.P., Travadon R., Rolshausen P., Baumgartner K., and D. Cantu. Distinctive expansion of gene families associated with plant cell wall degradation, secondary metabolism, and nutrient uptake in the genomes of grapevine trunk pathogens. BMC Genomics 16:469
- Type:
Journal Articles
Status:
Published
Year Published:
2015
Citation:
Amrine K.C.H., Blanco-Ulate B., Riaz S., Pap D., Jones L., Figueroa-Balderas R., Walker M.A., and D. Cantu. Comparative transcriptomics of Central Asian Vitis vinifera accessions reveals distinct defense strategies against powdery mildew. Horticulture Research 2
- Type:
Journal Articles
Status:
Published
Year Published:
2015
Citation:
Burns K.N., Kluepfel D.A., Strauss S.L., Bokulich N.A., Cantu D., and K.L. Steenwerth. Vineyard soil bacterial diversity and composition revealed by 16S rRNA genes: differentiation by geographic features. Soil Biology and Biochemistry 91:232-247
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Progress 10/01/13 to 09/30/14
Outputs
Target Audience: This research will provide more accurate and sensitive diagnostics tools for early detection of trunk pathogen and monitoring of development of fungicide resistance in fungal population to guide chemical management of diseases. This knowledge can benefit vineyard managers, grapevine nurseries, farm advisors and private vineyard consultants. The developed molecular tools have the potentiality to be easily applied by diagnostic labs. In addition the information on mechanisms of disease resistance in grapevine in combination with the understanding on how pathogen populations respond to the deployment of resistance genes can benefit public and private grape breeding programs. Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided? The following people were trained in Dr. Cantu’s laboratory as part of this project in the period of this progress report: Graduate students: Laura Jones (graduated Summer 2014 MSc Viticulture and Enology; current title: enologist at Cliff Lede Vineyards, Yountville, CA) Abraham Morales-Cruz (PhD student Horticulture & Agronomy) Visiting students: Aurelie Sastre (MSc student, University of Bordeaux, France) Alexandre Carriot (MSc student, University of Bordeaux, France) Chiara Broccanello (PhD student, University of Padua, Italy) Postdoctoral researcher: - Dr. Katherine C.H. Amrine (Fall 2013 - present) - Dr. Barbara Blanco-Ulate (Spring 2014 - present) - Dr. Eduardo Gutierrez-Rodriguez (Fall 2012 - Summer 2013 - current title: Assistant Professor, North Caroline State) Undergraduate students: Ye Zirou (major: Viticulture and Enology; minor: Economics) Jade Hendry (major: Viticulture and Enology) How have the results been disseminated to communities of interest? Dr. Cantu regularly interacts with members of the local grape industry groups by way of seminars (e.g.: Association of Napa Valley Vintners meetings; EJ Gallo technical seminar) and UC Davis outreach events (e.g.: Recent Advancement of Viticulture and Enology meetings, Current Wine & Winegrape Research meetings, “UC Davis on the road” events). What do you plan to do during the next reporting period to accomplish the goals? Work in progress for objective 1 - Characterize the grapevine disease responsive genes, pathways, and regulatory networks We are currently analyzing RNA-seq data obtained from seven Vitis vinifera accessions collected from central Asia, which display partial resistance to powdery mildew. Plants were challenged with E. necator conidia and leaf tissue was collected 1 and 5 days after inoculation. Ninety six libraries were successfully sequenced and are currently processed to identify a core of genes commonly activated in presence of a resistant phenotype despite the differences in the genetic background of the accessions used. We are currently also generating sequencing libraries of RNA extracted from grapevine leaf petioles challenged by Xylella fastidiosa (agent of Pierce’s Disease) wild-type cell (virulent) and wzy mutants (avirulent). Work in progress for objective 2 - Identify the major regulatory functions of the grapevine disease response by integrating transcriptomics and genetic mapping Transcriptomic data are being generated from a population generated from a cross of V. piazeskii (resistant to powdery mildew) and V. vinifera (susceptible to powdery mildew) segregating for two major powdery mildew resistance genes, named by our group in collaboration with Dr. Walker (UC Davis), Ren6 and Ren7. Transcriptomic data will be integrated with genetic mapping to identify regulatory genomic hotspots. Work in progress for objective 3 - Characterize the mechanisms of fungal pathogenesis in grapevine The whole genomes of additional isolates of E. lata, N. parvum, and T. minima were sequenced and are being analyzed to identify polymorphic regions and determine hypothetical associations with patterns of host specialization and virulence. RNA-seq is also being applied to profile the expression of all potential virulence factors to determine their timing and level of expression.
Impacts
What was accomplished under these goals?
Accomplishments for objective 1 - Characterize the grapevine disease responsive genes, pathways, and regulatory networks. The transcriptome data being generated and analyzed in the lab (see below in the research plan for next review period) will provide the necessary information to understand regulatory networks controlling disease resistance in grapevine. To optimize the computational tools required for such an analysis we carried out a gene co-expression analysis of all currently publicly available microarray data, which were generated in experiments that studied the interaction of the model plant Arabidopsis thaliana with microbial pathogens (manuscript describing this study is under review in PLoS ONE, revised version submitted on 12/15). This work was conducted specifically to identify (i) modules of functionally related co-expressed genes that are differentially expressed in response to multiple biotic stresses, and (ii) hub genes that may function as core regulators of disease responses. Using Weighted Gene Co-expression Network Analysis (WGCNA) we constructed an undirected network leveraging a rich curated expression dataset comprising 272 microarrays that involved microbial infections of Arabidopsis plants with a wide array of fungal and bacterial pathogens with biotrophic, hemibiotrophic, and necrotrophic lifestyles. WGCNA produced a network with scale-free and small-world properties composed of 205 distinct clusters of co-expressed genes. Modules of functionally related co-expressed genes that are differentially regulated in response to multiple pathogens were identified by integrating differential gene expression testing with functional enrichment analyses of gene ontology terms, known disease associated genes, transcriptional regulators, and cis-regulatory elements. The significance of functional enrichments was validated by comparisons with randomly generated networks. Network topology was then analyzed to identify intra- and inter-modular gene hubs. Based on high connectivity, and centrality in meta-modules that are clearly enriched in defense responses, we propose a list of 66 target genes for reverse genetic experiments to further dissect the Arabidopsis immune system. Our results show that statistical-based data trimming prior to network analysis allows the integration of expression datasets generated by different groups, under different experimental conditions and biological systems, into a functionally meaningful co-expression network. This approach is being applied to the transcriptome datasets currently developed in the lab. Accomplishments for objective 2 - Identify the major regulatory functions of the grapevine disease response by integrating transcriptomics and genetic mapping. Experiments and analyses are in progress. Accomplishments for objective 3 - Characterize the mechanisms of fungal pathogenesis in grapevine. We have recently released the draft sequences of Eutypa lata, Neofusicoccum parvum and Togninia minima, causal agents of Eutypa dieback, Botryosphoeria dieback and Esca, respectively. During the current review period we expanded the available genomic resources to additional important grapevine trunk pathogens and integrated all the currently available information in a genome-wide comparative study to identify gene families potentially associated with host colonization and disease development. The integration of RNA-seq, comparative genomics and ab initio approaches improved the protein-coding gene prediction in T. minima, while shotgun sequencing yielded nearly complete genome drafts of Diaporthe ampelina, Diplodia seriata, and Phaeomoniella chlamydospora, causal agents of Phomopsis dieback, Botryosphoeria dieback, and Esca, respectively. The predicted proteomes of all sequenced ascomycete and basidiomycete grapevine trunk pathogens were annotated focusing 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 and indicated lineage specific evolution of distinct mechanisms of virulence, such as specific cell wall oxidative functions and secondary metabolic pathways in N. parvum, D. ampelina, and E. lata. Phylogenetically informed principal component analysis revealed more similar repertoires of expanded functions in species associated with similar diseases, which in some cases did not reflect phylogenetic relationships suggesting patterns of convergent evolution. A shotgun approach was applied to sequence and assemble the genome of five E. necator isolates, and RNA-seq and comparative genomics were used to predict and annotate protein-coding genes. Our results show that the E. necator genome is exceptionally large and repetitive and suggest that transposable elements are responsible for genome expansion. Frequent structural variations were found between isolates and included copy number variation in EnCYP51, the target of the commonly used sterol demethylase inhibitor (DMI) fungicides. A panel of 89 additional E. necator isolates collected from diverse vineyard sites was screened for copy number variation in the EnCYP51 gene and for presence/absence of a point mutation (Y136F) known to result in higher fungicide tolerance. We show that an increase in EnCYP51 copy number is significantly more likely to be detected in isolates collected from fungicide-treated vineyards. Increased EnCYP51 copy numbers were detected with the Y136F allele, suggesting that an increase in copy number becomes advantageous only after the fungicide-tolerant allele is acquired. We also show that EnCYP51 copy number influences expression in a gene-dose dependent manner and correlates with fungal growth in the presence of a DMI fungicide. This study was published in BMC Genomics – Jones et al., 2014; see publication list for complete reference.
Publications
- Type:
Journal Articles
Status:
Published
Year Published:
2013
Citation:
Block K. L., Rolshausen P., and Cantu D., 2013. In search of solutions to grapevine trunk diseases through crowd-sourced science. Frontiers in Plant Science. 4: 394
- Type:
Journal Articles
Status:
Published
Year Published:
2014
Citation:
Blanco-Ulate B., Morales-Cruz A., Amrine K. C. H., Labavitch J. M., Powell A., and Cantu D., 2014 Genome-wide transcriptional profiling of Botrytis cinerea genes targeting plant cell walls during infections of different hosts. Frontiers in Plant Science. 5, 435
- Type:
Journal Articles
Status:
Published
Year Published:
2014
Citation:
Jones L., Riaz S., Morales-Cruz A., Amrine K. C. H., McGuire B., Douglas W. G., Walker A. M., and Cantu D., 2014. Adaptive Genomic Structural Variation in the Grape Powdery Mildew Pathogen, Erysiphe necator. BMC Genomics 15:1081
- Type:
Journal Articles
Status:
Published
Year Published:
2014
Citation:
Grimplet J., Adam-Blondon A.-F., Bert P.-F., Bitz O., Cantu D., Davies C., Delrot S., Pezzotti M., Rombauts S., Cramer G., 2014. The grapevine gene nomenclature system. BMC Genomics 15: 1077
- Type:
Book Chapters
Status:
Accepted
Year Published:
2015
Citation:
Blanco-Ulate B., Labavitch J. M., Vincenti E., Powell A. L. T., and Cantu D. Chapter 18 - Hitting the wall: Plant cell wall architecture and defenses against Botrytis. Botrytis - the Fungus, the Pathogen and its Management in Agricultural Systems. In press
- Type:
Book Chapters
Status:
Under Review
Year Published:
2015
Citation:
Blanco-Ulate B., Vincenti E., Cantu D., and Powell A. L. T. Chapter 19 - Ripening of tomato fruit and susceptibility to Botrytis cinerea. Botrytis - the Fungus, the Pathogen and its Management in Agricultural Systems.
- Type:
Book Chapters
Status:
Under Review
Year Published:
2015
Citation:
Cantu D., Roper, M. C., Powell, A. L. T., and Labavitch J. M. Chapter 13 - To long life and good health: untangling the complexity of grape diseases to develop pathogen resistant varieties. Biotechnology for Plant Disease Control.
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