Progress 01/01/13 to 09/30/17
Outputs
Target Audience:Our target audience included scientists working in the fields of plant pathology, plant sciences, and plant breeding, the general public, as well as various stakeholders in California's agriculture. The results described in this HATCH project have been published in prestigious international peer-reviewed journal, including PloS Genetics, FEBS Journal and FEBS Letters, and they have been broadly communicated through conferences, symposia, sponsored events, and other type of meetings to the rest of the scientific community as well as to the agbiotech industry through Seed Central in Davis, and students from the UC Davis graduate groups of Plant Pathology and Plant Sciences. Some of our results have also been communicated to the general public through articles appearing in popular science magazines as well as in numerous science news blogs and public domain news-media. I also gave several interviews to national and international TV and radio stations, newspapers, and online news media and magazines. Of notable reference is an interview that I did on August 24 2016 with Mark Niu, the San Francisco correspondent for CCTV-America, China's largest broadcaster whose shows are seen around the world in more than 100 countries, including nationwide in the U.S. on Dish TV, and Comcast. The theme of the interview was again about fungal diseases of bananas and the importance of our research on the three Sigatoka pathogens (https://www.youtube.com/watch?v=8MeAa-gK6dg). I also did four short 10 min interviews with two radio stations in the US and two radio stations in Australia. In addition, I gave an interview to Globe and Mail, Canada's National Newspaper, as well as to News-O-Matic, an online daily news app with articles written specifically for kids aged 7-11. In relation to the results from our Hatch project, I also wrote an online article for "The Conversation US" (https://theconversation.com/with-the-familiar-cavendish-banana-in-danger-can-science-help-itsurvive-64206), a news/analysis website with content written by academics and aimed at the general public. The article was published on Oct. 23rd as an "Editor's Pick" and it was republished in numerous other news sites around the world, including CNN, The Guardian, The Australian Broadcasting Cooperation, Business Insider, Digg, Associated Press, Houston Chronicle, SF Gates, and several others. The article has received over 693,000 reads since its publication. Selected oral presentations at conferences, symposia, sponsored events, and other type of meetings: · "Comparative genomics of the sigatoka disease complex on banana Indicates a direct link between pathogen emergence and nutritional virulence". Hellenic Bioinformatics Conference, September 9, 2017 · "Comparative analysis of three newly sequenced species of Dothideomycetes". Dothideomycetes Comparative Genomics workshop, 29th Fungal Genetics Conference at Asilomar, March 14, 2017 · "Molecular mechanisms of fungal pathogenesis on plants: from systems biology to translational Research". Invited Seminar, Seed Central Discover Series, Davis, April 14, 2016. · "Fungal core effector proteins: evolutionary dynamics, biochemistry, and functional significance for organismal biology and disease". Seminar, Host-Microbe Interactions Seminar Series, UC Davis. February 11, 2016 · "Comparative genomics of the Sigatoka disease complex in banana offers new insights into the host-driven adaptation of fungi". Seminar, PLP290 Plant Pathology Graduate Seminar Series, UC Davis. February 1, 2016 · "Letters from the hidden kingdom: Dothideomycetous fungi as model organisms to study host-driven speciation and the molecular mechanisms of fungal pathogenesis on plants". Invited Seminar, Plant Sciences Seminar Series, UC Davis. November 27, 2015 · "Dothideomycetous fungi as model organisms to study host-driven speciation and the molecular mechanisms of fungal pathogenesis on plants". Invited Seminar, Mediterranean Agronomic Institute of Chania (MACH), Greece. September 22, 2015. · "Mechanisms of pathogenesis and the evolution of virulence in Mycosphaerella fungal plant pathogens: New models for fungal host-microbe interactions?" Plenary Talk, 3rd International Conference on Model Hosts, Chania, Greece, September 19, 2015 · "Letters from the hidden kingdom: Dothideomycetous fungi as model organisms to study host-driven speciation and the molecular mechanisms of fungal pathogenesis on plants". Invited Seminar, Institute of Molecular Biology and Biotechnology (IMBB), University of Crete, Greece. September 16, 2015 · "Structure-function analysis of the fungal Avr4 core effector family". Poster Presentation, The 4th International Conference on Biotic Plant Interactions (ICBPI), Nanjing, Jiangsu, China, August 1-3, 2015 · "Comparative genomics of the Sigatoka disease complex on banana". Dothideomycetes Comparative Genomics workshop, 28th Fungal Genetics Conference at Asilomar March 17, 2015 · "Structure-function analysis of the fungal Avr4 core effector family". Poster Presentation, 28th Fungal Genetics Conference March 17-22, 2015 · "Comparative genomics of the Sigatoka disease complex on banana". Poster Presentation, 28th Fungal Genetics Conference at Asilomar March 17-22, 2015 · Biochemical and functional characterization of the AVR4 core fungal effector family. Plenary Talk, XVI International Congress on Molecular Plant-Microbe Interactions, Rhodes, Greece, July 9 2014 · Going bananas on the 5th floor: The population genomics of Black Sigatoka effectors. UC Davis department of Plant Pathology Faculty Seminar Series, June 14. Selected media coverage: • Can science stop the looming banana extinction? (CNN: http://www.cnn.com/2016/10/25/health/bananaextinction/) • The banana as we know it is in imminent danger (The Guardian: https://www.theguardian.com/ commentisfree/2016/oct/25/banana-farming-danger-cavendish-crop-genetics ) • One of the most popular fruit crops in the world could be decimated by disease (Business Insider: http://www. businessinsider.com/banana-disease-pandemic-fruit-preservation2016-10) • With the familiar Cavendish banana in danger, can science help it survive? (Associated Press: http://bigstory.ap. org/article/e4b2694a48ca4690ad6a471219e1b994/familiar-cavendish-banana-danger-can-science-help-it) • Genome sequencing may help avert banana armageddon (University of California: https://www. universityofcalifornia.edu/news/genome-sequencing-may-help-avert-banana-armageddon) • UC Davis study finds genome sequencing could avert banana armageddon (Daily Democrat: http://www. dailydemocrat.com/article/NI/20160811/NEWS/160819979) • Sequencing of fungal disease genomes may help prevent banana armageddon (ScienceDialy: https://www. sciencedaily.com/releases/2016/08/160811143530.htm) • Sequencing of fungal disease genomes may help prevent banana armageddon (EurekAlert: https://www. eurekalert.org/pub_releases/2016-08/p-sof081016.php) • Genomic Studies Tackle Banana Plant Pathogens (Genome web) • One super-susceptible clone, a versatile fungus and failing fungicides - black Sigatoka and banana (PLoS Blogs: http://blogs.plos.org/biologue/2016/08/12/one-super-susceptible-clone-a-versatile-fungus-and-failing-fungicides-blacksigatoka- and-banana/ ) • Genome Sequencing May Help Avert Banana Armageddon (Technology Org: http://www.technology. org/2016/08/12/genome-sequencing-may-help-avert-banana-armageddon/) Changes/Problems:We initially planned to sequence the genomes of at least 13 Dothideomycete plant pathogens. However, due to lack of funding, we have sequenced the genomes of only five species. We have submitted proposals to federal (i.e. NSF and USDA-NIFA) and other funding agencies, seeking for funds to complete the sequencing of the other genomes as well, but these so far have not been successful. We keep applying though for additional funds. What opportunities for training and professional development has the project provided?A post-doctoral fellow from the field of computational biology has worked on this project from October 2013 till July 2015. Due to the high impact of his work that resulted in three publications, the post-doctoral fellow has managed to get a permanent position as an independent Researcher and Bioinformatics Scientist at St. Jude Children's Research Hospital, Memphis, TN). A second post-doctoral fellow also from the field of bioinformatics has been employed in this project from July 2016 till July 2017 to work on the comparative analysis of the fungal genomes that we have sequenced. Part of the analysis was initiated but was not completed by the first post-doctoral fellow that was employed in this project. How have the results been disseminated to communities of interest?es, extensively. The results described in this HATCH project have been published in prestigious international peer-reviewed journal, including PloS Genetics, FEBS Journal and FEBS Letters, and they have been broadly communicated through conferences, symposia, sponsored events, and other type of meetings to the rest of the scientific community as well as to the agbiotech industry through Seed Central in Davis, and students from the UC Davis graduate groups of Plant Pathology and Plant Sciences. Some of our results have also been communicated to the general public through articles appearing in popular science magazines as well as in numerous science news blogs and public domain news-media. I also gave several interviews to national and international TV and radio stations, newspapers, and online news media and magazines. Refer to the section on "Target Audience" for more details. What do you plan to do during the next reporting period to accomplish the goals?
Nothing Reported
Impacts
What was accomplished under these goals?
Dothideomycetes constitute the largest and phylogenetically most diverse class of Ascomycetes that includes notorious pathogens that cause destructive diseases on major agronomic and staple food crops. Many Dothideomycetes are known to be host-specific or to have a narrow host-range, but the identity of the host can differ dramatically even among closely-related species. Thus, the ability of these fungi to jump between hosts and become rapidly adapted on their new hosts, makes these pathogens excellent model organisms for studies on host-shift speciation in fungi. The research objectives in this HATCH project were to determine the genomic changes associated with speciation and shifts in virulence spectra of 13 evolutionary closely-related (hemi)biotrophic plant pathogenic Dothideomycete fungi. The main focus was on secretomes and effector proteins in more specific, as pathoadaptive gains and losses in these proteins can contribute to the underlying differences in virulence spectra among evolutionary closely related species. The research questions posed addressed the origin, distribution and evolution of effector proteins in the selected Dothideomycete plant pathogens, their role in virulence and their ability to determine host-specificity. Overall, our studies provided a deeper understanding of fungal pathogenesis on plants and shed light on the genomic changes associated with adaptation of plant pathogens to different hosts. As afore mentioned, 13 species of Dothideomycete were selected for genome sequencing. These species were the banana pathogens Pseudocercospora musae, Pseudocercospora emusae, Pseudocercospora longispora, Passalora loranthicola, and Mycosphaerella mozambica, the Solanae pathogens Pseudocercospora fuligena, Pseudocercospora atromarginalis and Paracercospora egenula, the eucalyptus pathogens Pseudocercospora paraguayensis, Pseudocercospora pseudoecalyptorum, Mycosphaerella aurantia and Mycosphaerella africana, and finally the citrus pathogen Pseudocercospora angolensis. The rationale for selecting these species was based on their very close evolutionary relationships to each other and to species that we have studied in the past (i.e. the tomato pathogen Cladosporium fulvum and the banana pathogen Pseudocercospora fijiensis), their host-specificity, common hemi-biotrophic lifestyle on the host, and importance as plant pathogens. From the 13 selected species we have sequenced the genomes of five species, i.e. of the banana pathogens P. musae, P. emusae and M. mozambica, the tomato pathogen P. fuligena, and the eggpant pathogen P. egenula. Lack of sufficient funds was the main reason why we did not sequence the genomes of all 13 species as originally planned. In the subsequent comparative genomic analyses we have also included the genomes of the banana pathogen P. fijiensis and of the tomato C. fulvum that we have sequenced in the past. We initially focused on the comparative genome analysis of the Sigatoka disease complex in banana, which is caused by the closely-related species P. musae (yellow sigatoka), P. eumusae (eumusae leaf spot), and P. fijiensis (black sigatoka). The disease is currently the most destructive disease in banana, reducing yields by more than 40%. Despite their common ancestry, very close-phylogenetic relationship and shared host-specificity, the three species show clear differences in virulence with P. fijiensis and P. eumusae being the most aggressive. This feature provided us with the opportunity to understand the genomic modifications associated with shifts in virulence spectra after speciation. Our comparative genomic analysis revealed that changes in gene family sizes among the three species are not selectively neutral but more respectful of the species virulence profiles rather than their evolutionary relationships. Specifically, P. eumusae and P. fijiensis share convergent patterns of expansions and contractions in core gene families related to metabolism and degradation of plant cell walls, suggesting that virulence-jumps and speciation in these fungi are to a certain extent linked to recurrent genomic changes in molecular pathways associated with nutrient acquisition and assimilation. This is an important and novel finding because the concept of metabolic fitness on the host has not been properly explored in studies of plant pathogenic fungi. To further investigate whether similar trends could be identified in cases of host-jumps as well, we expanded the above comparative genome analysis to include the genomes of the tomato pathogens C. fulvum and P. fuligena, the eggplant pathogen P. egenula and the banana pathogen M. mozambica. Genome-based phylogenetic analysis of the seven Dothideomycetes indicated that there are two major clades; one that contains P. fuligena, P. eumusae, P. fijiensis and P. musae, and one that contains C. fulvum, P. egenula and M. mozambica. As the Musa (P. eumusae, P. fijiensis, P. musae and M. mozambica) and Solanum pathogens (P. fuligena, P. egenula and C. fulvum) were intermingled within the two clades, it suggests that host-specificity developed after speciation events. Functional annotation and comparison of the species' gene complements identified 70 gene families, including 9 gene families of secreted proteins and one effector that are present only in the three Solanum pathogens but absent in the banana ones. In an analogous way, 6 gene families, including 3 gene families of secreted proteins and one effector were identified in all four Musa pathogens but were absent in the Solanaceae ones. Such gene families may represent genes associated with adaptation of the pathogens on these two hosts, respectively. In contrast to what was observed with the Sigatoka disease complex species, PCA analysis and Hierarchical Clustering based on copy number variation in the species entire proteomes showed partial only clustering according to host adaptation. Clustering of the species based on variation in their repertoires of small secreted effector proteins and CAzymes, showed that clustering was again mostly according to their phylogeny rather than their host. Thus, adaptation of different pathogens on a specific host seems to follow multiple evolutionary routes and not to be dictated by pathoadaptive gains and losses in specific gene families. In this HATCH project we have also performed a molecular evolutionary analysis of the Avr4 core effector family. Avr4 is a 135-residue effector protein from the tomato pathogen C. fulvum with homologues in many other fungi, which utilizes a carbohydrate-binding module of family 14 (CBM14) to bind chitin present in fungal cell walls and protect it from hydrolysis by plant-derived chitinases during infection. CBM14s are short modules of approximately 70 residues that bind to chitin, a key structural polysaccharide found in diverse organisms, including crustaceans, cephalopods, insects, and fungi. Our genome-wide searches recovered an impressive number of CBM14s and putative Avr4 homologues from diverse lineages across nearly all domains of life. However, their highly disseminated distribution in various taxa across the tree of life reveal a dynamic mode of birth-and-death evolution, whereas positive selection acting on paralogous CBM14-containing proteins suggest changes in substrate specificity of this ancient family. Using the Avr4 effector family as a basis, we have also performed a rigorous molecular evolutionary analysis of modularity in CBM14s. Specifically, we have investigated the global diversity of domain types present in modular CBM14 proteins and further characterized the complexity, evolution, and taxonomic distribution of their modular domain rearrangements. These studies allowed us to depict a robust picture on how promiscuous CBMs, such as the CBM14 have been exploited several times in nature in a variety of different protein architectures, as a means to facilitate functional complexity and innovation in higher eukaryotes.
Publications
- Type:
Journal Articles
Status:
Submitted
Year Published:
2018
Citation:
Structure of the Cladosporium fulvum Avr4 effector in complex with chitin uncouples the ligand-binding function from Cf-4 recognition
- Type:
Conference Papers and Presentations
Status:
Other
Year Published:
2017
Citation:
Comparative genomics of the sigatoka disease complex on banana Indicates a direct link between pathogen emergence and nutritional virulence
- Type:
Conference Papers and Presentations
Status:
Other
Year Published:
2017
Citation:
Comparative analysis of three newly sequenced species of Dothideomycetes
|
Progress 10/01/15 to 09/30/16
Outputs
Target Audience:The results from our comparative genomic studies on the sigatoka disease complex, have been published in the prestigious international peer-reviewed journal PloS Genetics (http://journals.plos.org/plosgenetics/article?id=10.1371/journal. pgen.1005904) and have been subsequently reported in numerous science news blogs and public domain news-media. I also gave several interviews to National and International TV and Radio stations, Newspapers, and Online News Media and Magazines. Almost all interviews regarded our work on the Sigatoka pathogens of banana and the current state of this crop. Of notable reference is an interview that I did on August 24 2016 with with Mark Niu, the San Francisco correspondent for CCTV-America, China's largest broadcaster whose shows are seen around the world in more than 100 countries, including nationwide in the U.S. on Dish TV, and Comcast. The theme of the interview was again about fungal diseases of bananas and the importance of our research on the three Sigatoka pathogens (https://www.youtube.com/watch?v=8MeAa-gK6dg). I also did four short 10min interviews with two radio stations in the US and two radio stations in Australia. In addition, I gave an interview to Globe and Mail, Canada's National Newspaper, as well as to News-O-Matic, an online daily news app with articles written specifically for kids aged 7-11. In relation to the results from our Hatch project, I also wrote an online article for "The Conversation US" (https://theconversation.com/with-the-familiar-cavendish-banana-in-danger-can-science-help-itsurvive- 64206), a news/analysis website with content written by academics and aimed at the general public. The article was published on Oct. 23rd as an "Editor's Pick" and it was republished in numerous other news sites around the world, including CNN, The Guardian, The Australian Broadcasting Cooperation, Business Insider, Digg, Associated Press, Houston Chronicle, SF Gates, and several others. The article had over 655,000 reads in less than a month. Selected Media Coverage: • Can science stop the looming banana extinction? (CNN: http://www.cnn.com/2016/10/25/health/bananaextinction/) • The banana as we know it is in imminent danger (The Guardian: https://www.theguardian.com/ commentisfree/2016/oct/25/banana-farming-danger-cavendish-crop-genetics ) • One of the most popular fruit crops in the world could be decimated by disease (Business Insider: http://www. businessinsider.com/banana-disease-pandemic-fruit-preservation2016-10) • With the familiar Cavendish banana in danger, can science help it survive? (Associated Press: http://bigstory.ap. org/article/e4b2694a48ca4690ad6a471219e1b994/familiar-cavendish-banana-danger-can-science-help-it) • Genome sequencing may help avert banana armageddon (University of California: https://www. universityofcalifornia.edu/news/genome-sequencing-may-help-avert-banana-armageddon) • UC Davis study finds genome sequencing could avert banana armageddon (Daily Democrat: http://www. dailydemocrat.com/article/NI/20160811/NEWS/160819979) • Sequencing of fungal disease genomes may help prevent banana armageddon (ScienceDialy: https://www. sciencedaily.com/releases/2016/08/160811143530.htm) • Sequencing of fungal disease genomes may help prevent banana armageddon (EurekAlert: https://www. eurekalert.org/pub_releases/2016-08/p-sof081016.php) • Genomic Studies Tackle Banana Plant Pathogens (Genome web) • One super-susceptible clone, a versatile fungus and failing fungicides - black Sigatoka and banana (PLoS Blogs: http://blogs.plos.org/biologue/2016/08/12/one-super-susceptible-clone-a-versatile-fungus-and-failing-fungicides-blacksigatoka- and-banana/ ) • Genome Sequencing May Help Avert Banana Armageddon (Technology Org: http://www.technology. org/2016/08/12/genome-sequencing-may-help-avert-banana-armageddon/) Finally Results related to this Hatch Project were also presented during four invited seminars at UC Davis that reached out to two graduate groups (Plant Pathology and Plant sciences) and agrobiotech industry. Results were also presented in the form of a poster presentation during the XVII International Congress on Molecular Plant-Microbe Interactions, the major scientific event in the field of plant-microbe interactions that is held every two years. 1. "Comparative genomics of the Sigatoka disease complex on banana indicates a direct link between pathogen emergence and nutritional virulence". Poster Presentation, XVII International Congress on Molecular Plant-Microbe Interactions, Portland, Oregon, USA, July 17-21, 2016. 2. "Molecular Mechanisms of Fungal Pathogenesis on Plants: From Systems Biology to Translational Research". Invited Seminar, Seed Central Discover Series, Davis, April 14, 2016. 3. "Fungal core effector proteins: evolutionary dynamics, biochemistry, and functional significance for organismal biology and disease". Invited Seminar, Host-Microbe Interactions Seminar Series, UC Davis. February 11, 2016 4. "Comparative genomics of the Sigatoka disease complex in banana offers new insights into the host-driven adaptation of fungi". Seminar, PLP290 Plant Pathology Graduate Seminar Series, UC Davis. February 1, 2016 5. "Letters from the hidden kingdom: Dothideomycetous fungi as model organisms to study host-driven speciation and the molecular mechanisms of fungal pathogenesis on plants". Invited Seminar, Plant Sciences Seminar Series, UC Davis. November 27, 2015 Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided?A post-doctoral fellow from the field of bioinformatics has been employed in this project since July 2016 to work on the comparative analysis of the fungal genomes that we have sequenced. Part of the analysis was initiated but was not completed by the first post-doctoral fellow that was employed in this project from October 2013 till July 2015. How have the results been disseminated to communities of interest?Results from this Hatch project have appeared in the form of popular science articles in several Newspapers, Online News Media and Magazines. In addition, results were presented to the agbiotech industry through Seed Central in Davis, and students from the UC Davis graduate groups of Plant Pathology and Plant Sciences. Finally, results were communicated in a form of a poster to an international conference on Molecular Plant-Microbe interactions. What do you plan to do during the next reporting period to accomplish the goals?We will continue and finalize the analysis of the additional three genomes that we have sequenced. Depending on availability of funds, we will sequence six additional genomes from species of Dothideomycete.
Impacts
What was accomplished under these goals?
Dothideomycetes constitute the largest and phylogenetically most diverse class of Ascomycetes that includes notorious pathogens that cause destructive diseases on major agronomic, biofuel, and staple food crops such as wheat, banana, barley, corn, sugar beet, canola, and others. Species of Mycosphaerella, Pseudocercospora, Cercospora and Cochliobolus are all prominent examples of Dothideomycete fungi that set-off disease epidemics on various filed crops almost yearly. Many Dothideomycetes are also known to be host-specific or to have a narrow host-range, but the identity of the host can differ dramatically even among closely-related species. Thus, the tendency of these fungi to jump between hosts and become rapidly adapted and specialized on their new hosts, makes these pathogens a major source of emerging diseases and excellent model organisms for studies on host-shift speciation in fungi. We have previously reported on the genome sequencing and comparative genome analysis of the banana pathogens that constitute the notorious Sigatoka disease complex, i.e. Pseudocercospora eumusae (syn. Mycosphaerella eumusae), Pseudocercospora musae (syn. Mycosphaerella musicola), and Pseudocercospora fijiensis (syn. Mycosphaerella fijiensis). Despite their common ancestry, very close-phylogenetic relationship and shared host-specificity, the three species show clear differences in virulence with P. fijiensis and P. eumusae being the most aggressive. This feature provided us with the opportunity to understand the genomic modifications associated with shifts in the species virulence spectra (virulence jumps) after speciation. Our comparative genomic and evolutionary analyses revealed that changes in gene family sizes among the three species are not selectively neutral but more respectful of the species virulence profiles rather than their evolutionary relationships. Specifically, P. eumusae and P. fijiensis share convergent patterns of expansions and contractions in core gene families related to metabolism and degradation of plant cell walls, suggesting that virulence-jumps and speciation in these fungi are to a certain extent linked to recurrent genomic changes in molecular pathways associated with nutrient acquisition and assimilation. This is an important and novel finding because the concept of metabolic fitness on the host has not been properly explored so far in studies of plant pathogenic fungi. To further investigate whether similar trends could be identified in cases of host-jumps as well, we are exploring the genome organization, evolution, and content among close-related species of Dothideomycetes that are pathogenic to Musa and Solanum species. To this end, we report the genome sequences of an additional three Dothideomycete fungi, i.e. of the tomato pathogen Pseudocercospora fuligena, of the eggplant pathogen Pseudocercospora egenula and of the banana pathogen Mycosphaerella mozambica. All three pathogens are phylogenetically very closely related to the three species that constitute the Sigatoka disease complex of banana as well as to the tomato pathogen Cladosporium fulvum, the genome of which has also been recently reported. We estimated the genome size of M. mozambica, P. fuligena, and P. egenula to be 39.33 Mb, 53.51 Mb, and 64.76 Mb, respectively. The differences in genome size among the seven species is largely due to differential lineage-specific amplification of repeat content, particularly the LTR elements. The newly sequenced Musa pathogen M. mozambica is fundamentally different from the three species that constitute the Sigatoka disease complex (i.e. P. eumusae, P. musae and P. fijiensis) in terms of its repeat content. Genome based phylogenetic tree of the seven Dothideomycetes computed using the concatenated sequences of single-copy genes indicated that there were two major clades; one that contains P. fuligena together with P. eumusae, P. fijiensis and P. musae, and one that contains C. fulvum together with P. egenula and M. mozambica. As the Musa (P. eumusae, P. fijiensis, P. musae and M. mozambica) and Solanum pathogens (P. fuligena, P. egenula and C. fulvum) were intermingled within both clades, it suggests that host-specificity developed after speciation events. Orthology-based comparative analysis of the species' gene and proteome complements indicated that a total of 4,802 protein-coding gene families contain at least one gene copy in each of the seven species that represent their core proteome complement. Functional annotation and characterization of the species' extensive catalogue of genes indicate abundant species- and lineage-specific adaptations. Clustering of the species based on variation in their repertoires of proteins known to be involved in host specialization such as small secreted proteins and CAzymes, showed that clustering was mostly according to their phylogeny rather than their host. In order to analyze the effect of proximity of a gene to a repeat region, the RIP index of the genes was calculated as a function of distance to the repeat sequences. Finally, putative virulence associated genes were studied to identify key effectors in each species that could be regarded as species-specific in addition to those ones that might play an essential role specifically in the Musa or Solanum complex.
Publications
- Type:
Other
Status:
Published
Year Published:
2016
Citation:
Stergiopoulos I, Drenth A, Kema GHJ (2016): With the familiar Cavendish banana in danger, can science help
it survive? The Conversation (US Edition)
- Type:
Other
Status:
Published
Year Published:
2016
Citation:
Stergiopoulos I, Drenth A, Kema GHJ (2016): Les bananes vont-elles dispara�tre ? The Conversation (French
Edition)
- Type:
Other
Status:
Published
Year Published:
2016
Citation:
Stergiopoulos I (2016): Genome Sequencing May Help Avert Banana Armageddon. Food and Agriculture
News, University of California Davis.
- Type:
Journal Articles
Status:
Published
Year Published:
2016
Citation:
Chang TC, Salvucci A, Crous PW and Stergiopoulos I* (2016). Comparative genomics of the Sigatoka
disease complex on banana suggests a link between parallel evolutionary changes in Pseudocercospora
fijiensis and Pseudocercospora eumusae and increased virulence on the banana host. PLoS Genetics, 12(8):
e1005904
- Type:
Journal Articles
Status:
Published
Year Published:
2016
Citation:
Arango Isaza RE, Diaz-Trujillo C, Dhillon B, Aerts A, Carlier J, Crane CF, de Jong TV, de Vries I, Dietrich R,
Farmer AD, Fereira GF, Garcia S, Guzm�n M, Hamelin RC, Lindquist EA, Mehrabi R, Quir�s O, Schmutz J,
Shapiro H, Reynolds E, Scalliet G, Souza Jr M, Stergiopoulos I, Van der Lee TAJ, De Wit PJGM, Zapater MF,
Zwiers L-H, Grigoriev IV, Goodwin SB, & Kema GHJ* (2016); Combating a global threat to a clonal crop:
banana black Sigatoka pathogen Pseudocercospora fijiensis (synonym Mycosphaerella fijiensis) genomes
reveal clues for disease control. PLoS Genetics, 12(8):e1005876
- Type:
Conference Papers and Presentations
Status:
Published
Year Published:
2016
Citation:
Stergiopoulos I, Chang TC, Salvucci A, and Crous P; Comparative genomics of the Sigatoka disease
complex on banana indicates a direct link between pathogen emergence and nutritional virulence. In Book of
Abstracts XVII International Congress on Molecular Plant-Microbe Interactions, Portland, Oregon, USA, July
17-21, 2016. P12-401
|
Progress 10/01/14 to 09/30/15
Outputs
Target Audience:Results related to this project were presented in several international conferences and workshops in the form of Invited Talks (x2) or Poster Presentations (x1) as well as at several Academic Institutes in the form of Invited Seminars (x3) 1. "Letters from the hidden kingdom: Dothideomycetous fungi as model organisms to study host-driven speciation and the molecular mechanisms of fungal pathogenesis on plants". Invited Seminar, Plant Sciences Seminar Series, UC Davis. November 27, 2015 2. "Dothideomycetous fungi as model organisms to study host-driven speciation and the molecular mechanisms of fungal pathogenesis on plants". Invited Seminar, Mediterranean Agronomic Institute of Chania (MACH), Greece. September 22, 2015. 3. "Mechanisms of pathogenesis and the evolution of virulence in Mycosphaerella fungal plant pathogens: New models for fungal host-microbe interactions?" Plenary Talk, 3rd International Conference on Model Hosts, Chania, Greece, September 19, 2015 4. "Letters from the hidden kingdom: Dothideomycetous fungi as model organisms to study host-driven speciation and the molecular mechanisms of fungal pathogenesis on plants". Invited Seminar, Institute of Molecular Biology and Biotechnology (IMBB), University of Crete, Greece. September 16, 2015 5. "Comparative genomics of the Sigatoka disease complex on banana". Invited Talk, Dothideomycetes Comparative Genomics workshop, 28th Fungal Genetics Conference at Asilomar March 17, 2015 7. "Comparative genomics of the Sigatoka disease complex on banana". Poster Presentation, 28th Fungal Genetics Conference at Asilomar March 17-22, 2015 Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided?A post-doctoral fellow from the field of computational biology has worked on this project from October 2013 till July 2015. Due to the high impact of his work that resulted in already three publications, the post-doctoral fellow has managed to get a permanent position as an independent Researcher and Bioinformatics Scientist at St. Jude Children's Research Hospital, Memphis, TN). How have the results been disseminated to communities of interest?As exemplified earlier, results related to this project were presented in several international conferences and workshops in the form of Invited Talks (x2) or Poster Presentations (x1) as well as at several Academic Institutes in the form of Invited Seminars (x3). In particular, results from these studies were presented at (i) the Dothideomycetes Comparative Genomics workshop, in Asilomar, California, (ii) the 28th Fungal Genetics Conference at Asilomar, California, (iii) the 3rd International Conference on Model Hosts, at Chania, Greece, (iv) the Institute of Molecular Biology and Biotechnology (IMBB), University of Crete, Greece, (iv) at the Mediterranean Agronomic Institute of Chania (MACH), Greece, and (v-vi) the departments of Plant Sciences and Plant Pathology at UC Davis. What do you plan to do during the next reporting period to accomplish the goals?We will continue and finalize the genomic analysis of the tomato pathogen Pseudocercospora fuligena and the banana pathogen Mycosphaerella mozambica. We are also planning to sequence this year the genomes of four more genomes from species of Dothideomycete.
Impacts
What was accomplished under these goals?
The aim of the Hatch project is to identify and functionally characterize the effector repertoire of 13 Dothideomycete species that although they are evolutionary relatives they differ in their host-range. These studies will provide a deeper understanding of fungal pathogenesis on plants and will shed further light on the genomic and evolutionary changes associated with adaptation of plant pathogens to different hosts and life-styles. During the 3nd year of this hatch project we have finalized the comparative genome analysis of the Sigatoka disease complex in banana, which is caused by the closely-related Dothideomycete fungi Pseudocercospora musae (syn. Mycosphaerella musicola; yellow sigatoka), Pseudocercospora eumusae (syn. Mycosphaerella eumusae; eumusae leaf spot), and Pseudocercospora fijiensis (syn. Mycosphaerella fijiensis; black sigatoka). The disease is currently the most destructive disease in banana, reducing yields by more than 40%. The socio-economic impact of the disease caused by these pathogens is particularly high in developing countries and communities in sub-Saharan Africa and Southeast Asia that almost exclusively depend on the banana crop for their survival. Therefore, managing and understanding the pathobiology of this disease is of urgent importance and is currently under critical public review for humanitarian, biosafety, and environmental reasons. The three species have surfaced as major pathogens of bananas during the last century and although they have evolved from a recent common ancestor, clear differences in virulence exist amongst them, with P. fijiensis and P. eumusae being the most aggressive. Our comparative genome analysis has shown that speciation has largely altered the genome architecture and composition of the three species, suggesting that the evolution of virulence in these pathogens has, to an extent, been facilitated by a number of species-specific adaptations. Still, gene counts remained relatively equal and in the range of other Dothideomycetes. Phylogenetic reconstruction based on a set of 46 conserved single-copy genes strongly supported an earlier evolutionary radiation of P. fijiensis from P. musae and P. eumusae. However, pairwise analyses of gene content indicated that the more virulent P. eumusae and P. fijiensis share complementary patterns of expansions and contractions in core gene families related to metabolism and enzymatic degradation of plant cell walls, suggesting that the evolution of virulence in these two pathogens has, to some extent, been facilitated by convergent changes in metabolic pathways associated with nutrient acquisition and assimilation. In spite of their common ancestry and shared host-specificity, the three species retain fairly dissimilar repertoires of effector proteins, suggesting that they likely evolved different strategies for manipulating the host immune system. Finally, 234 gene families, including seven putative effectors, were exclusively present in the three Sigatoka species, and could thus be related to adaptation to the banana host. Overall, the results from our study enable a deeper understanding of the Sigatoka disease complex and the evolution of virulence in these pathogens that can be further exploited in genetic engineering or breeding programs for banana improvement. In addition, it offers vital fundamental knowledge on the evolution of virulence and the genetics of host-adaptation in plant pathogens. The results of this study have been recently accepted for publication by PLoS Genetics (Chang TC, Salvucci A, Crous PW and Stergiopoulos I* (2016). Comparative genomics of the Sigatoka disease complex on banana suggests a link between parallel evolutionary changes in Pseudocercospora fijiensis and Pseudocercospora eumusae and increased virulence on the banana host. PLoS Genetics, Accepted). In addition, we have also participated in the initial analysis of the P. fijiensis genome and a manuscript describing the major findings form this research ahs also been accepted by PLoS Genetics (Arango Isaza RE, Diaz-Trujillo C, Dhillon B, Aerts A, Carlier J, Crane CF, de Jong TV, de Vries I, Dietrich R, Farmer AD, Fereira GF, Garcia S, Guzmán M, Hamelin RC, Lindquist EA, Mehrabi R, Quirós O, Schmutz J, Shapiro H, Reynolds E, Scalliet G, Souza Jr M, Stergiopoulos I, Van der Lee TAJ, De Wit PJGM, Zapater M-F, Zwiers L-H, Grigoriev IV, Goodwin SB, & Kema GHJ* (2016); Combating a global threat to a clonal crop: banana black Sigatoka pathogen Pseudocercospora fijiensis (synonym Mycosphaerella fijiensis) genomes reveal clues for disease control. PLoS Genetics, Accepted) Next to P. musae and P. eumusae, we are also continuing to analyze the genomes of the tomato pathogen Pseudocercospora fuligena and of another banana pathogen Mycosphaerella mozambica. Both pathogens are closely related to the three species that constitute the Sigatoka complex and thus analyzing the genomes of these pathogens will offer unique insight into host-shift speciation in Dothideomycete fungi and the role of effectors in such processes. In 2015, we have also finalized the molecular evolutionary analysis of the Avr4 chitin-binding core effector family, a member of the the Carbohydrate-Binding Module Family 14 (CBM14), shedding light in its origin, taxonomic distribution across the entire tree of life, and history of diversification as a result of gene duplication, rapid sequence diversification imposed by positive selection and recombination with novel protein domains. The results from this research have been published in the FEBS Journal (Chang TC and Stergiopoulos I. Inter- and intra-domain horizontal gene transfer, gain-loss asymmetry, and positive selection mark the evolutionary history of the CBM14 family. FEBS Journal 2015, 282(10):2014-2028). In addition, using the Avr4 chitin-binding core effector family as a basis, we have performed a rigorous molecular evolutionary and phylogenetic analysis of modularity in family 14 carbohydrate-binding modules (CBM14s). Specifically, we have investigated the global diversity of domain types present in modular CBM14-containing proteins and further characterized the complexity, evolution, and taxonomic distribution of their modular domain rearrangements. These studies allowed us to depict a robust picture on how promiscuous CBMs, such as the CBM14 have been exploited several times in nature in a variety of different protein architectures, as a means to facilitate functional complexity and innovation in higher eukaryotes. The results form this analysis have been published in FEBS Letters (Chang TC and Stergiopoulos I. Evolutionary analysis of the global landscape of protein domain types and domain architectures associated with family 14 carbohydrate-binding modules. FEBS Letters 2015, 589 (15), 1813-1818).
Publications
- Type:
Journal Articles
Status:
Published
Year Published:
2015
Citation:
Chang TC and Stergiopoulos I. Evolutionary analysis of the global landscape of protein domain types and domain architectures associated with family 14 carbohydrate-binding modules. FEBS Letters, 589 (15), 1813-1818.
- Type:
Journal Articles
Status:
Accepted
Year Published:
2015
Citation:
Chang TC, Salvucci A, Crous PW and Stergiopoulos I. Comparative genomics of the Sigatoka disease complex on banana suggests a link between parallel evolutionary changes in Pseudocercospora fijiensis and Pseudocercospora eumusae and increased virulence on the banana host. PLoS Genetics, Accepted
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Progress 10/01/13 to 09/30/14
Outputs
Target Audience: Results related to this project were communicated by means of an oral presentation (plenary talk) during the XVI International Congress on Molecular Plant-Microbe Interactions that was held in Rhodes, Greece, July 6-10 2014. This is the major scientific event in the field of plant-microbe interactions that is held every two years and in 2014 attracted more than 1,200 participants from 55 countries around the globe. Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided? A post-doctoral fellow from the field of computational biology has been recruited in October 2013 to work on this project. The post-doctoral fellow is currently working on analyzing the genome sequences of the four Dothideomycete species that were sequenced as part of this hatch project. The post-doctoral fellow also worked with the PI on elucidating the evolutionary history of the Avr4 core effector family. How have the results been disseminated to communities of interest? Results related to this project were communicated by means of an oral presentation (plenary talk) during the XVI International Congress on Molecular Plant-Microbe Interactions that was held in Rhodes, Greece, July 6-10 2014. This is the major scientific event in the field of plant-microbe interactions that is held every two years and in 2014 attracted more than 1,200 participants from 55 countries around the globe. Results will also be communicated by means of a poster presentation during the 28th Fungal Genetics Conference to be held at Pacific Grove, CA, March 17-22 and as an oral presentation during the Dothideomycete satellite meeting. What do you plan to do during the next reporting period to accomplish the goals? We will continue and finalize the analysis of the four genomes that we have already sequenced. Depending on availability of funds (grants are already submitted for this purpose), we are planning to sequence six additional genomes from species of Dothideomycete this year.
Impacts
What was accomplished under these goals?
The aim of this Hatch project is to identify and functionally characterize the effector repertoire of 13 Dothideomycete species that although they are evolutionary relatives they differ in their host-range. These studies will provide a deeper understanding of fungal pathogenesis on plants and will shed further light on the genomic and evolutionary changes associated with adaptation of plant pathogens to different hosts and life-styles. This is extremely important in today's global ecosystem, not only because infectious diseases caused by fungi are increasingly recognized as a major threat to global food production and security, but also because globalization continuously brings previously isolated hosts and pathogens in contact with each other, thus increasing the risk for the emergence of new diseases. The engineering of durable resistance is one of the main goals of plant pathology and the successful completion of this project will generate novel opportunities for achieving this goal. Effector pathogenomics will facilitate the discovery and functional profiling of microbial effectors and cognate plant resistance genes at a high rate that will accelerate the engineering of resistance in plants through molecular breeding programs. During the 2nd year of this hatch project we have sequenced and are in the process of analyzing the genomes of four Dothideomycete species. Among the sequenced species are Mycosphaerella eumusae and Mycosphaerella musicola, which together with Mycosphaerella fijiensis are the casual agents of the so-called Sigatoka disease complex in banana. This disease complex is currently a serious threat to banana plantations around the world causing extensive damage and having a devastating socioeconomic impact in communities that exclusively depend on this crop for their survival, like in Africa and SE Asia. The three species emerged on bananas during the last century and are assumed to have evolved from a recent common ancestor. Clear differences, however, in virulence exist amongst the three species that correlate with the time of their appearance. In order to understand the evolutionary trends and genomic modifications associated with shifts in their virulence spectra and to identify their pathogenic core (e.g effectors) that can be exploited in disease management programs, we have sequenced and analyzed the genomes of M. eumusae and M. musicola and compared them with the available genome sequence of M. fijiensis. Despite their close phylogenetic relatedness, the three species differ in their genome sizes, mainly due to different rates of LTR retrotransposon proliferation. Still, gene counts have remained relatively the same and in the range of other Dothideomycete species. Analyses of gene content showed that ~13% of the genes in each species are species-specific, suggesting that they participate in species-specific processes. 234 gene families were also identified, including 18 secreted protein families and 8 putative effectors that were shared specifically by the three species and no other fungi, and which could thus be related to adaptation to the banana host. Notably, only 19 effectors (~15%) were shared among the three species, suggesting that altered effector repertoires partially forms the basis of their differential virulence. An excess of positive selection on putative effectors and the secretome in general as compared to non-secreted proteins was also evident, further reinforcing this notion. Currently, a research manuscript is in preparation that describes the comparative genomics of the Sigatoka disease complex and the genomic changes that are involved in the emergence of these pathogens and shifts in their virulence spectra. Next to M. musicola and M. eumusae we have also sequenced and currently analyzing the genomes of the tomato pathogen Pseudocercospora fuligena and of another banana pathogen Mycosphaerella mozambica. P. fuligena is very closely-related to the three species that constitute the Sigatoka complex but has made a host jump to tomato. M. mozambica on the other hand is closely-related to P. fuligena and has jumped back to banana. Analyzing the genomes of these pathogens will offer unique insight into host-shift speciation in Dothideomycete fungi and the role of effectors in such processes. Analysis of these genomes is currently under way and is expected to be completed within 2015. Finally, as part of this hatch project we have performed a molecular evolutionary analysis of the Avr4 chitin-binding core effector family, shedding light in its origin, taxonomic distribution across the entire tree of life, and history of diversification as a result of gene duplication, rapid sequence diversification imposed by positive selection and recombination with novel protein domains. Avr4 is a chitin-binding effector protein that was first identified from the tomato pathogen Cladosporium fulvum (a species of Dothideomycete and close relative of M. fijiensis), which in tomato is perceived by the cognate trans-membrane receptor-like protein Cf4. The cysteine-bond pattern of Avr4 reveals that it is a member of the the Carbohydrate-Binding Module Family 14 (CBM14), a large superfamily of short modules of approximately 70 aa in length that bind specifically to chitin, a β(1→4) linked N-acetyl-D-glucosamine (GlcNAc) polysaccharide and a key structural polysaccharide found in diverse organisms, including crustaceans, cephalopods, insects, and fungi. Based on our findings we strongly argue for a paradigm shift in the scientific community, that the biology and evolution of effector proteins and virulence traits in general should be studied in a broader ecological context that will allow us to fully understand microbial pathogenicity beyond the current perspective of host-microbe interactions. The findings from this work have been submitted for publication in December 2014.
Publications
- Type:
Journal Articles
Status:
Under Review
Year Published:
2015
Citation:
Ti-Cheng Chang and Stergiopoulos Ioannis; Elevated rates of horizontal gene transfer, gain-loss asymmetry, and domain fusions mark the evolutionary history of the carbohydrate-binding module family 14 (CBM14) across the tree of life.
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Progress 01/01/13 to 09/30/13
Outputs
Target Audience: Initial results from this project were communicated by means of an oral presentation during the Plant and Animal Genome Conference (PAG) Asia 2013, section “Banana Genomics for food security and biofortification”. The conference was held in Singapore on March 17 - 19, 2013 and it was dedicated to the mission of fostering development of genomic analysis of agricultural products to sustain the world. Next to scientists working in the field of Comparative Genomics within the Plant and Animal Sciences fields, the section on banana genomics was also followed by many banana and agrochemicals industry representatives, farm advisors, banana commodity groups, and even individual banana farmers from the Asia-Pacific region. Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided? A post-doctoral fellow from the field of computational biology has been recruited in October 2013 to work on this project. The post-doctoral fellow will work on the bioinformatics analysis of the genomic and RNAseq data that will be generated through this project. The post-doctoral fellow is currently working with the PI on elucidating the evolutionary origins of a fungal effector family. How have the results been disseminated to communities of interest? Initial results from this project were communicated by means of an oral presentation during the Plant and Animal Genome Conference (PAG) Asia 2013, section “Banana Genomics for food security and biofortification”. The conference was held in Singapore on March 17 - 19, 2013 and it was dedicated to the mission of fostering development of genomic analysis of agricultural products to sustain the world. Next to scientists working in the field of Comparative Genomics within the Plant and Animal Sciences fields, the section on banana genomics was also followed by many banana and agrochemicals industry representatives, farm advisors, banana commodity groups, and even individual banana farmers from the Asia-Pacific region. What do you plan to do during the next reporting period to accomplish the goals? The project has been initiated and we expect to make additional progress during the next reporting period. More specifically, given that we should soon have genomic and RNAseq data for five species in our list, our aim will be to perform a rigorous bioinformatics analysis of these species. Time and resources permitted (grants are already submitted for this purpose) we will then continue with sequencing of the rest of the species as well.
Impacts
What was accomplished under these goals?
The aim of this Hatch project is to identify and functionally characterize the effector repertoire of 13 Dothideomycete species that although they are evolutionary relatives they differ in their host-range. These studies will provide a deeper understanding of fungal pathogenesis on plants and will shed further light on the genomic and evolutionary changes associated with adaptation of plant pathogens to different hosts and life-styles. This is extremely important in today's global ecosystem, not only because infectious diseases caused by fungi are increasingly recognized as a major threat to global food production and security, but also because globalization continuously brings previously isolated hosts and pathogens in contact with each other, thus increasing the risk for the emergence of new diseases. The engineering of durable resistance is one of the main goals of plant pathology and the successful completion of this project will generate novel opportunities for achieving this goal. Effector pathogenomics will facilitate the discovery and functional profiling of microbial effectors and cognate plant resistance genes at a high rate that will accelerate the engineering of resistance in plants through molecular breeding programs. During the first year of the Hatch project we have obtained from collaborators in Netherlands and Japan cultures of the 13 Dothieomycete species, the genome's of which we plan sequencing. The species were selected to be evolutionarily closely-related and have a near-optimal degree of evolutionary divergence for Genome-Wide Selection Scan studies, meaning they are related enough for meaningful orthology assignments and gene alignments, but divergent enough to produce a strong phylogenetic signal. All of the species share very close phylogenetic relationships to species that have been sequenced and studied in the past, i.e. the tomato pathogen Cladosporium fulvum, the pine-tree pathogen Dothistroma septosporum, and the banana pathogen Mycosphaerella fijiensis. Among others the list of species includes the banana pathogens Mycosphaerella eumusae and Mycosphaerella musicola, which together with M. fijiensis are the casual agents of the Sigatoka disease complex in banana, currently the most devastating disease on this crop. The list also includes the tomato pathogen Pseudocercospora fuligena, a close relative to the reference tomato pathogen C. fulvm. Based on their phylogenetic placement the two pathogens do not share an immediate common ancestor, and thus have likely independently adapted on the same host. Three-to-five monospore cultures were generated during the last year for each of the 13 Dothideomycete species. Sequencing of monopsore cultures is an essential feature in any genome sequencing project in order to ensure the genomic uniformity of the sample (i.e that there is no mixture of two different genotypes). However, for the slow-growing Dothideomycete fungi, this is a painstaking and time-consuming process that requires several sub-culturing steps and with each step taking approximately three weeks to complete. We have also isolated genomic DNA of sufficient quantity and quality from five species in our collection. Extraction of high quality fungal DNA is often not a trivial task and this has turned out to be the case with our fungi as well. Throughout the summer of 2013, we have tested several DNA extraction protocols and we have finally produced our own by combining several DNA extraction methods. The DNA was subsequently used for the construction of libraries for sequencing on the Illumina Hiseq2500 platform. To minimize costs for this project, Illumina libraries were made “in-house” with protocols and guidance provided by the Michelmore lab here at UC Davis. The libraries are currently awaiting sequencing on the Illumina HiSeq2500 platform (PE150x150 format) at the UC Davis Genome Center. One of the five species will also be sequenced using the PacBio RS platform and library construction has been currently outsourced to the UC Davis Genome Center. Finally we have also initiated RNAseq for each of the five species in order to assist future genome annotations. For this purpose RNA from two in vitro conditions was isolated for each fungus and libraries were made for sequencing on the Illumina Hiseq2500 platform. RNAseq is currently complete and we are awaiting the data to be released from the UC Davis Genome Center. Another dimension that has been added to these studies is that of population genomics, aiming on linking interspecies divergence with intraspecies polymorphism. For this, we are currently building a collection of C. fulvum (5 strains are currently present in the collection), P. fuligena (30 strains are currently present in the collection), and the three pathogens that constitute the Sigatoka disease complex (~10 strains of each species are currently present in the collection). Time and resources permitted (grants are already submitted for this purpose) we are planning of capturing the landscape of intraspecific genetic variation in ~5-10 strains of each aforementioned pathogen. In 2013 we have completed and published a research paper, which examined the intraspecific variation in four selected effector genes of the banana pathogen M. fijiensis. This work was initiated in the Netherlands but the analysis of the sequences was made here.
Publications
- Type:
Journal Articles
Status:
Published
Year Published:
2013
Citation:
Stergiopoulos I, Collemare J, Mehrabi R and De Wit PJGM (2013): Phytotoxic secondary metabolites and peptides produced by plant pathogenic Dothideomnycetes. FEMS Microbiology Reviews 37(1):67-93
- Type:
Journal Articles
Status:
Awaiting Publication
Year Published:
2013
Citation:
Stergiopoulos I, Cordovez V, �kmen B, Beenen H, Kema GHJ and De Wit PJGM: Positive selection and intragenic recombination contribute to high allelic diversity in effector genes of Mycosphaerella fijiensis, causal agent of the black leaf streak disease of banana. Molecular Plant Pathology DOI: 10.1111/mpp.12104
- Type:
Conference Papers and Presentations
Status:
Published
Year Published:
2013
Citation:
Invited Oral presentation: Plant and Animal Genome Conference (PAG) Asia 2013
W016: Intragenic Recombination and Positive Selection Contribute to High Allelic Diversity in Effector Genes of the Banana Pathogen Mycosphaerella fijiensis.
Section: Banana Genomics for food security and biofortification
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