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5. Sequential breakdown of the Cf‐9 leaf mould resistance locus in tomato by Fulvia fulva.

Author

de la Rosa, Silvia, Schol, Christiaan R., Ramos Peregrina, Ángeles, Winter, David J., Hilgers, Anne M., Maeda, Kazuya, Iida, Yuichiro, Tarallo, Mariana, Jia, Ruifang, Beenen, Henriek G., Rocafort, Mercedes, de Wit, Pierre J. G. M., Bowen, Joanna K., Bradshaw, Rosie E., Joosten, Matthieu H. A. J., Bai, Yuling, and Mesarich, Carl H.

Subjects
PLANT diseases, DELETION mutation, GENE expression, GENOMICS, CULTIVARS
Abstract

Summary: Leaf mould, caused by Fulvia fulva, is a devastating disease of tomato plants. In many commercial tomato cultivars, resistance to this disease is governed by the Cf‐9 locus, which encodes five paralogous receptor‐like proteins. Two of these proteins confer resistance: Cf‐9C recognises the previously identified F. fulva effector Avr9 and provides resistance during all plant growth stages, while Cf‐9B recognises the yet‐unidentified F. fulva effector Avr9B and provides mature plant resistance only. In recent years, F. fulva strains have emerged that can overcome the Cf‐9 locus, with Cf‐9C circumvented through Avr9 deletion. To understand how Cf‐9B is circumvented, we set out to identify Avr9B.Comparative genomics, transient expression assays and gene complementation experiments were used to identify Avr9B, while gene sequencing was used to assess Avr9B allelic variation across a world‐wide strain collection.A strict correlation between Avr9 deletion and resistance‐breaking mutations in Avr9B was observed in strains recently collected from Cf‐9 cultivars, whereas Avr9 deletion but no mutations in Avr9B were observed in older strains.This research showcases how F. fulva has evolved to sequentially break down the Cf‐9 locus and stresses the urgent need for commercial tomato cultivars that carry novel, stacked resistance genes active against this pathogen. [ABSTRACT FROM AUTHOR]

Published
2024
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6. Cell Wall Carbohydrate Dynamics during the Differentiation of Infection Structures by the Apple Scab Fungus, Venturia inaequalis

Author

Rocafort, Mercedes, primary, Srivastava, Vaibhav, additional, Bowen, Joanna K., additional, Díaz-Moreno, Sara M., additional, Guo, Yanan, additional, Bulone, Vincent, additional, Plummer, Kim M., additional, Sutherland, Paul W., additional, Anderson, Marilyn A., additional, Bradshaw, Rosie E., additional, and Mesarich, Carl H., additional

Published
2023
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7. Cell Wall Carbohydrate Dynamics during the Differentiation of Infection Structures by the Apple Scab Fungus, Venturia inaequalis

Author

Rocafort, Mercedes, Srivastava, Vaibhav, Bowen, Joanna K., Diaz-Moreno, Sara M, Guo, Yanan, Bulone, Vincent, Plummer, Kim M., Sutherland, Paul W., Anderson, Marilyn A., Bradshaw, Rosie E., Mesarich, Carl H., Rocafort, Mercedes, Srivastava, Vaibhav, Bowen, Joanna K., Diaz-Moreno, Sara M, Guo, Yanan, Bulone, Vincent, Plummer, Kim M., Sutherland, Paul W., Anderson, Marilyn A., Bradshaw, Rosie E., and Mesarich, Carl H.

Abstract

Scab, caused by the biotrophic fungal pathogen Venturia inaequalis, is the most economically important disease of apples. During infection, V. inaequalis colonizes the subcuticular host environment, where it develops specialized infection structures called runner hyphae and stromata. These structures are thought to be involved in nutrient acquisition and effector (virulence factor) delivery, but also give rise to conidia that further the infection cycle. Despite their importance, very little is known about how these structures are differentiated. Likewise, nothing is known about how these structures are protected from host defenses or recognition by the host immune system. To better understand these processes, we first performed a glycosidic linkage analysis of sporulating tubular hyphae from V. inaequalis developed in culture. This analysis revealed that the V. inaequalis cell wall is mostly composed of glucans (44%) and mannans (37%), whereas chitin represents a much smaller proportion (4%). Next, we used transcriptomics and confocal laser scanning microscopy to provide insights into the cell wall carbohydrate composition of runner hyphae and stromata. These analyses revealed that, during subcuticular host colonization, genes of V. inaequalis putatively associated with the biosynthesis of immunogenic carbohydrates, such as chitin and b-1,6-glucan, are downregulated relative to growth in culture, while on the surface of runner hyphae and stromata, chitin is deacetylated to the less-immunogenic carbohydrate chitosan. These changes are anticipated to enable the subcuticular differentiation of runner hyphae and stromata by V. inaequalis, as well as to protect these structures from host defenses and recognition by the host immune system. IMPORTANCE Plant-pathogenic fungi are a major threat to food security. Among these are subcuticular pathogens, which often cause latent asymptomatic infections, making them difficult to control. A key feature of these pathogens is thei, QC 20230823

Published
2023
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11. Cell wall carbohydrate dynamics during the differentiation of infection structures by the apple scab fungus, Venturia inaequalis

Author

Rocafort, Mercedes, primary, Srivastava, Vaibhav, additional, Bowen, Joanna K., additional, Díaz-Moreno, Sara M., additional, Bulone, Vincent, additional, Plummer, Kim M., additional, Sutherland, Paul W., additional, Anderson, Marilyn A., additional, Bradshaw, Rosie E., additional, and Mesarich, Carl H., additional

Published
2022
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13. Search for host defense markers uncovers an apple agglutination factor corresponding with fire blight resistance

Author

Chavonet, Erwan, Gaucher, Matthieu, Warneys, Romain, Bodelot, Antoine, Heintz, Christelle, Juillard, Anthony, Cournol, Raphaël, Widmalm, Göran, Bowen, Joanna K., Hamiaux, Cyril, Brisset, Marie-Noëlle, Degrave, Alexandre, Chavonet, Erwan, Gaucher, Matthieu, Warneys, Romain, Bodelot, Antoine, Heintz, Christelle, Juillard, Anthony, Cournol, Raphaël, Widmalm, Göran, Bowen, Joanna K., Hamiaux, Cyril, Brisset, Marie-Noëlle, and Degrave, Alexandre

Abstract

Pathenogenesis-related (PR) proteins are extensively used as molecular markers to dissect the signaling cascades leading to plant defense responses. However, studies focusing on the biochemical or biological properties of these proteins remain rare. Here, we identify and characterize a class of apple (Malus domestica) PR proteins, named M. domestica AGGLUTININS (MdAGGs), belonging to the amaranthin-like lectin family. By combining molecular and biochemical approaches, we show that abundant production of MdAGGs in leaf tissues corresponds with enhanced resistance to the bacterium Erwinia amylovora, the causal agent of the disease fire blight. We also show that E. amylovora represses the expression of MdAGG genes by injecting the type 3 effector DspA/E into host cells and by secreting bacterial exopolysaccharides. Using a purified recombinant MdAGG, we show that the protein agglutinates E. amylovora cells in vitro and binds bacterial lipopolysaccharides at low pH, conditions reminiscent of the intercellular pH occurring in planta upon E. amylovora infection. We finally provide evidence that negatively charged polysaccharides, such as the free exopolysaccharide amylovoran progressively released by the bacteria, act as decoys relying on charge–charge interaction with the MdAGG to inhibit agglutination. Overall, our results suggest that the production of this particular class of PR proteins may contribute to apple innate immunity mechanisms active against E. amylovora.

Published
2022
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15. The Venturia inaequalis effector repertoire is expressed in waves and is dominated by expanded families with predicted structural similarity to avirulence proteins from other plant-pathogenic fungi

Author

Rocafort, Mercedes, primary, Bowen, Joanna K., additional, Hassing, Berit, additional, Cox, Murray P., additional, McGreal, Brogan, additional, de la Rosa, Silvia, additional, Plummer, Kim M., additional, Bradshaw, Rosie E., additional, and Mesarich, Carl H., additional

Published
2022
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16. Additional file 1 of The Venturia inaequalis effector repertoire is dominated by expanded families with predicted structural similarity, but unrelated sequence, to avirulence proteins from other plant-pathogenic fungi

Author

Rocafort, Mercedes, Bowen, Joanna K., Hassing, Berit, Cox, Murray P., McGreal, Brogan, de la Rosa, Silvia, Plummer, Kim M., Bradshaw, Rosie E., and Mesarich, Carl H.

Abstract

Additional file 1: Table S1. RNA-seq transcriptome sequencing read statistics from this study. Samples used for the RNA-seq transcriptome sequencing experiment were derived from an infection time course of Venturia inaequalis on detached leaves from susceptible apple cultivar ‘Royal Gala’ at 12 and 24 hours post-inoculation (hpi), as well as 2, 3, 5 and 7 days post-inoculation (dpi), and during growth. Table S2. Effector candidate (EC) protein families or singletons from Venturia inaequalis that have sequence similarity to EC or avirulence (Avr) effector proteins from other plant-pathogenic fungi. Table S3. Effector candidates (ECs) of Venturia inaequalis (Vi) with predicted structural similarity to EC or avirulence (Avr) effector proteins from other plant-pathogenic fungi that have a characterized tertiary structure present in the RCSB PDB.

Published
2022
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17. Additional file 8 of The Venturia inaequalis effector repertoire is dominated by expanded families with predicted structural similarity, but unrelated sequence, to avirulence proteins from other plant-pathogenic fungi

Author

Rocafort, Mercedes, Bowen, Joanna K., Hassing, Berit, Cox, Murray P., McGreal, Brogan, de la Rosa, Silvia, Plummer, Kim M., Bradshaw, Rosie E., and Mesarich, Carl H.

Abstract

Additional file 8: S1 Text. Supplementary methods for the identification of dikaritin RiPP gene clusters in Venturia inaequalis.

Published
2022
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18. Additional file 2 of The Venturia inaequalis effector repertoire is dominated by expanded families with predicted structural similarity, but unrelated sequence, to avirulence proteins from other plant-pathogenic fungi

Author

Rocafort, Mercedes, Bowen, Joanna K., Hassing, Berit, Cox, Murray P., McGreal, Brogan, de la Rosa, Silvia, Plummer, Kim M., Bradshaw, Rosie E., and Mesarich, Carl H.

Abstract

Additional file 2: Fig. S1. Bioinformatic pipeline used for transcriptome analysis and genome annotation. Total RNA was extracted from apple leaves infected with Venturia inaequalis at 12 and 24 hours post-inoculation (hpi), as well as 2, 3, 5 and 7 days post-inoculation (dpi). As a reference for growth in culture, total RNA was also extracted from V. inaequalis grown on the surface of cellophane membranes overlaying potato dextrose agar at 7 dpi. Four biological replicates were included per sample. PE: paired-end; CDS: coding sequence; CAZyme: carbohydrate-active enzyme; EC: effector candidate. Fig. S2. Plant cell wall-degrading enzyme (PCWDE)-encoding genes of Venturia inaequalis upregulated during infection of susceptible apple cultivar ‘Royal Gala’, relative to growth of the fungus in culture on the surface of cellophane membranes overlying potato dextrose agar. A. Proportion of in planta upregulated PCWDE-encoding genes in each host infection-specific temporal expression wave. B. Heatmap of PCWDE-encoding genes upregulated in planta that demonstrate a peak level of expression during waves 1 and 2 of the early infection stage at 12 and 24 hours post-inoculation (hpi). C. Heatmap of PCWDE-encoding genes upregulated in planta that demonstrate a peak level of expression during wave 3 of the mid infection stage at 2 and 3 days post-inoculation (dpi) and waves 4 and 5 of the mid-late infection stage at 5 and 7 dpi. Block labels on the left indicate gene expression wave. Numbers in brackets indicate number of genes per wave. Gene expression data are scaled rlog-normalized counts across all samples (Z-score), averaged from four biological replicates. Labels on the right indicate carbohydrate-active enzyme (CAZyme) classification. Bar plots depict the maximum log2 DESeq2-normalized count value across all in planta time points. AA: auxiliary activity; GH: glycoside hydrolase; CE: carbohydrate esterase; PL: polysaccharide lyase; CBM: carbohydrate-binding module. Fig. S3. Prediction of effectors from Venturia inaequalis. A. Pipeline for the identification of effector candidates (ECs) from V. inaequalis. B. Comparison of the number of ECs predicted from V. inaequalis isolate MNH120 in this study and a previous study [19]. The comparison is based on an exact protein sequence match. The previous study by Deng et al. [19] defined ECs as small proteins of

Published
2022
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19. Search for host defense markers uncovers an apple agglutination factor corresponding with fire blight resistance

Author

Chavonet, Erwan, primary, Gaucher, Matthieu, additional, Warneys, Romain, additional, Bodelot, Antoine, additional, Heintz, Christelle, additional, Juillard, Anthony, additional, Cournol, Raphaël, additional, Widmalm, Göran, additional, Bowen, Joanna K, additional, Hamiaux, Cyril, additional, Brisset, Marie-Noëlle, additional, and Degrave, Alexandre, additional

Published
2021
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20. CRISPR-Cas9 gene editing and rapid detection of gene-edited mutants using high-resolution melting in the apple scab fungus,Venturia inaequalis

Author

Rocafort, Mercedes, primary, Arshed, Saadiah, additional, Hudson, Debbie, additional, Singh, Jaspreet, additional, Bowen, Joanna K., additional, Plummer, Kim M., additional, Bradshaw, Rosie E., additional, Johnson, Richard D., additional, Johnson, Linda J., additional, and Mesarich, Carl H., additional

Published
2021
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22. Ten-Year Results of FAST: A Randomized Controlled Trial of 5-Fraction Whole-Breast Radiotherapy for Early Breast Cancer

Author

Brunt, Adrian Murray, primary, Haviland, Joanne S., additional, Sydenham, Mark, additional, Agrawal, Rajiv K., additional, Algurafi, Hafiz, additional, Alhasso, Abdulla, additional, Barrett-Lee, Peter, additional, Bliss, Peter, additional, Bloomfield, David, additional, Bowen, Joanna, additional, Donovan, Ellen, additional, Goodman, Andy, additional, Harnett, Adrian, additional, Hogg, Martin, additional, Kumar, Sri, additional, Passant, Helen, additional, Quigley, Mary, additional, Sherwin, Liz, additional, Stewart, Alan, additional, Syndikus, Isabel, additional, Tremlett, Jean, additional, Tsang, Yat, additional, Venables, Karen, additional, Wheatley, Duncan, additional, Bliss, Judith M., additional, and Yarnold, John R., additional

Published
2020
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27. Genetic control of α‐farnesene production in apple fruit and its role in fungal pathogenesis

Author

Souleyre, Edwige J. F., primary, Bowen, Joanna K., additional, Matich, Adam J., additional, Tomes, Sumathi, additional, Chen, Xiuyin, additional, Hunt, Martin B., additional, Wang, Mindy Y., additional, Ileperuma, Nadeesha R., additional, Richards, Kate, additional, Rowan, Daryl D., additional, Chagné, David, additional, and Atkinson, Ross G., additional

Published
2019
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29. Additional file 6: of Comparative analysis of the predicted secretomes of Rosaceae scab pathogens Venturia inaequalis and V. pirina reveals expanded effector families and putative determinants of host range

Author

Deng, Cecilia, Plummer, Kim, Jones, Darcy, Mesarich, Carl, Shiller, Jason, Taranto, Adam, Robinson, Andrew, Kastner, Patrick, Hall, Nathan, Templeton, Matthew, and Bowen, Joanna

Abstract

Pipeline of programmes used to identify the in silico-predicted secretome of each isolate. (DOCX 147 kb)

Published
2017
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30. Additional file 8: of Comparative analysis of the predicted secretomes of Rosaceae scab pathogens Venturia inaequalis and V. pirina reveals expanded effector families and putative determinants of host range

Author

Deng, Cecilia, Plummer, Kim, Jones, Darcy, Mesarich, Carl, Shiller, Jason, Taranto, Adam, Robinson, Andrew, Kastner, Patrick, Hall, Nathan, Templeton, Matthew, and Bowen, Joanna

Abstract

The predicted proteins belonging to OrthoMCL clusters present in the secretomes of five Venturia isolates. The coloured horizontal bars represent proportions of predicted proteins (scale at bottom of figure) that have been annotated according to the key at the top of the figure, that are present in the secretomes indicated by grey boxes to the left of the figure (white boxes indicate lack of similar proteins). S: indicates singleton proteins. Numbers in the boxes are numbers of proteins. The order of the categories in the key is the same as that in the horizontal bars. For example: the core secretome is represented by the top-most horizontal bar; there are similar proteins present in each of the secretomes (5 grey boxes), of which 15% (77 proteins) are classified as SSPs between 200 and 500 amino acids in length with 2 or more cysteines. (PPTX 56 kb)

Published
2017
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31. Additional file 13: of Comparative analysis of the predicted secretomes of Rosaceae scab pathogens Venturia inaequalis and V. pirina reveals expanded effector families and putative determinants of host range

Author

Deng, Cecilia, Plummer, Kim, Jones, Darcy, Mesarich, Carl, Shiller, Jason, Taranto, Adam, Robinson, Andrew, Kastner, Patrick, Hall, Nathan, Templeton, Matthew, and Bowen, Joanna

Subjects
food and beverages
Abstract

Small, secreted protein (SSP) family 07 members. Sequence logo of members of A. family 07 from Vi1 and B. family 07 from all isolates. (DOCX 221 kb)

Published
2017
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34. Comparative analysis of the predicted secretomes of Rosaceae scab pathogens Venturia inaequalis and V. pirina reveals expanded effector families and putative determinants of host range

Author

Deng, Cecilia H., primary, Plummer, Kim M., additional, Jones, Darcy A. B., additional, Mesarich, Carl H., additional, Shiller, Jason, additional, Taranto, Adam P., additional, Robinson, Andrew J., additional, Kastner, Patrick, additional, Hall, Nathan E., additional, Templeton, Matthew D., additional, and Bowen, Joanna K., additional

Published
2017
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35. Variation in host and pathogen in the Neonectria/Malus interaction; toward an understanding of the genetic basis of resistance to European canker

Author

Gómez-Cortecero, Antonio, Saville, Robert J., Scheper, Reiny W.A., Bowen, Joanna K., Agripino De Medeiros, Hugo, Kingsnorth, Jennifer, Xu, Xiangming, Harrison, Richard J., Gómez-Cortecero, Antonio, Saville, Robert J., Scheper, Reiny W.A., Bowen, Joanna K., Agripino De Medeiros, Hugo, Kingsnorth, Jennifer, Xu, Xiangming, and Harrison, Richard J.

Abstract

Apple canker caused by the phytopathogenic fungus Neonectria ditissima is an economically important disease, which has spread in recent years to almost all pome-producing regions of the world. N. ditissima is able to cross-infect a wide range of apple varieties and causes branch and trunk lesions, known as cankers. Most modern apple varieties are susceptible and in extreme cases suffer from high mortality (up to 50%) in the early phase of orchard establishment. There is no known race structure of the pathogen and the global level of genetic diversity of the pathogen population is unknown. Resistance breeding is underway in many global breeding programmes, but nevertheless, a total resistance to canker has not yet been demonstrated. Here we present preliminary data from a survey of the phylogenetic relationships between global isolates of N. ditissima which reveals only slight evidence for population structure. In addition we report the results of four rapid screening tests to assess the response to N. ditissima in different apple scion and rootstock varieties, which reveals abundant variation in resistance responses in both cultivar and rootstock material. Further seedling tests show that the segregation patterns of resistance and susceptibility vary widely between crosses. We discuss inconsistencies in test performance with field observations and discuss future research opportunities in this area.

Published
2016

50. Venturia inaequalis: the causal agent of apple scab.

Author

BOWEN, JOANNA K., MESARICH, CARL H., BUS, VINCENT G. M., BERESFORD, ROBERT M., PLUMMER, KIM M., and TEMPLETON, MATTHEW D.

Subjects
*VENTURIA inaequalis, *APPLE scab, *PLANT-fungus relationships, *PLANT defenses, *NUCLEOTIDE sequence, *PLANT genomes, *PLANT enzymes, *PLANT gene silencing
Abstract

The fungus Venturia inaequalis infects members of the Maloideae, and causes the disease apple scab, the most important disease of apple worldwide. The early elucidation of the gene-for-gene relationship between V. inaequalis and its host Malus has intrigued plant pathologists ever since, with the identification of 17 resistance ( R)-avirulence ( Avr) gene pairings. The Avr gene products are presumably a subset of the total effector arsenal of V. inaequalis (predominantly proteins secreted in planta assumed to facilitate infection). The supposition that effectors from V. inaequalis act as suppressors of plant defence is supported by the ability of the pathogen to penetrate the cuticle and differentiate into large pseudoparenchymatous structures, termed stromata, in the subcuticular space, without the initiation of an effective plant defence response. If effectors can be identified that are essential for pathogenicity, the corresponding R genes will be durable and would add significant value to breeding programmes. An R gene cluster in Malus has been cloned, but no V. inaequalis effectors have been characterized at the molecular level. However, the identification of effectors is likely to be facilitated by the resolution of the whole genome sequence of V. inaequalis. Teleomorph: Venturia inaequalis Cooke (Wint.); Kingdom Fungi; Phylum Ascomycota; Subphylum Euascomycota; Class Dothideomycetes; Family Venturiaceae; genus Venturia; species inaequalis. Anamorph: Fusicladium pomi (Fr.) Lind or Spilocaea pomi (Fr.). V. inaequalis is a hemibiotroph and overwinters as pseudothecia (sexual fruiting bodies) following a phase of saprobic growth in fallen leaf tissues. The primary inoculum consists of ascospores, which germinate and penetrate the cuticle. Stromata are formed above the epidermal cells but do not penetrate them. Cell wall-degrading enzymes are only produced late in the infection cycle, raising the as yet unanswered question as to how V. inaequalis gains nutrients from the host. Conidia (secondary inoculum) arise from the upper surface of the stromata, and are produced throughout the growing season, initiating multiple rounds of infection. V. inaequalis can be cultured and is amenable to crossing in vitro, enabling map-based cloning strategies. It can be transformed readily, and functional analyses can be conducted by gene silencing. Expressed sequence tag collections are available to aid in gene identification. These will be complemented by the whole genome sequence, which, in turn, will contribute to the comparative analysis of different races of V. inaequalis and plant pathogens within the Dothideomycetes. [ABSTRACT FROM AUTHOR]

Published
2011
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