Ignazio Carbone

Associate Professor
ignazio_carbone@ncsu.edu
Center for Integrated Fungal Research
Department of Plant Pathology
Campus Box 7244 – Partners III Building Raleigh, NC 27695-7244
Phone: (919) 513-4866 Fax: (919) 513-0024

Biography

University of Toronto, Ph.D, 2000

Research

Dr. Carbone’s Lab

My research interests are in evolutionary biology, molecular population genetics and genomics. Research in my laboratory is interdisciplinary and combines sampling of genetic and phenotypic variation in natural fungal populations, in silico comparative analyses of fungal genomes, and the development of integrative evolutionary analysis tools. An important aspect of our work is developing new methodologies and tools to examine the influence of mutation, recombination, gene flow, selection and demography on the evolution of fungal genomes, populations and species. Our computational goal is to effectively manage and integrate the plethora of new approaches for making inferences on population processes from DNA sequence variation, bringing together simple summary-statistics, nonparametric methods and complex parameter-rich models. We have been developing new methodologies and tools for integrating genetic and phenotypic data within an evolutionary framework.  Recently we released a flexible and scalable workbench tool that manages a series of population genetic programs.

A major focus is examining the evolution of fungal secondary metabolism, specifically the sterigmatocystin (ST), O-methylsterigmatocystin (OMST) and aflatoxin (AF) biosynthetic pathway in Aspergillus. The genes for ST, OMST, and AF are clustered and these compounds are synthesized as end products by numerous ascomycetes. Although all three metabolites (ST, OMST, and AF) are potent carcinogens in animals, the biological and evolutionary significance of these bioreactive compounds in fungi is unknown. We are combining inferences from macro- and micro-evolutionary analyses to understand the conservation of these metabolites among Aspergillus species and how diversity is generated and maintained within species over long periods of time.  Recent work examines genetic variation in experimental populations and in field studies using biological control strains.

Teaching

PP 707 Plant-Microbe Interactions is a required course in the Plant Pathology core curriculum that is offered every Spring and is co-taught with Dr. Gary Payne. My section of the course covers the following topics: 1) introduction to population genetics concepts; 2) phylodynamics of pathogen evolution; 3) population biology and disease management; 4) inoculum source and evolutionary potential; 5) durable resistance; 6) host-pathogen coevolution; and 7) quorum-sensing systems in bacteria.

PP 715 Applied Evolutionary and Population Genetic Data Analysis is an advanced graduate course taught in the Fall of alternate years. This course introduces students to nonparametric and model-based methods for inferences on population processes (mutation, migration, drift, recombination, and selection). The goal is to provide a theoretical and conceptual overview of these methods as well as hands-on training on implementation and biological interpretation of results. Sample data sets in computer laboratories will integrate summary statistic, cladistic, coalescent, and Bayesian approaches to examine population processes in different pathosystems with specific emphasis on eukaryotic microbes, viruses and bacteria.

Selected Publications
  1. Call, A., Sun, Y-X., Yu, Y., Pearman, P. B., Thomas, D. T., Trigiano, R., Carbone, I. and J. Xiang 2015.  Genetic structure and post-glacial expansion of Cornus florida L. (Cornaceae): Integrative evidence from phylogeography, population demographic history, and species distribution modeling.  Journal of Systematics and Evolution DOI: 10.1111/jse.12171.
  2. Putman, A. I., Tredway, L. P. and I. Carbone. 2015.  Characterization and distribution of mating-type genes of the turfgrass pathogen Sclerotinia homoeocarpa on a global scale. Fungal Genetics and Biology 81: 25-40.
  3. Lassiter, E. S., Russ, C., Nusbaum, C., Zeng, Q., Saville, A., Olarte, R., Carbone, I., Hu, C-H, Thorne, J. L. and J. B. Ristaino.  2015. Mitochondrial genome sequences and evolutionary relationships of the Phytophthora Ic clade species. Current Genetics DOI: 10.1007/s00294-015-0480-3.
  4. Meyers, M., R. Heiniger, L. Boerema, I. Carbone. 2015. The Use of Management Practices to Reduce Mycotoxin Contamination in Corn. AG-807. Raleigh, NC: North Carolina Cooperative Extension Service. http://content.ces.ncsu.edu/the-use-of-management-practices-to-reduce-mycotoxin-contamination-in-corn/.
  5. Olarte, R. A., Worthington, C.J., Horn, B.W., Moore, G.G., Singh, R., Monacell, J.W., Dorner, J.T., Stone, E.A., Xie, D-Y. and I. Carbone.  2015. Enhanced diversity and aflatoxigenicity in interspecific hybrids of Aspergillus flavus and Aspergillus parasiticus. Molecular Ecology 24: 1889-1909.
  6. Olarte, R. A., Horn, B., Singh, R., and I. Carbone. 2015. Sexual recombination in Aspergillus tubingensis. Mycologia DOI:10.3852/14-233.
  7. Putman, A.I. and I. Carbone. 2014. Challenges in analysis and interpretation of microsatellite data for population genetic studies.  Ecology and Evolution 4: 4399–4428.  PMID: 25540699
  8. Barnes, I., Wingfield, M. J., Carbone, I., Kirisits, T. and B. D. Wingfield. 2014.  Population structure and diversity of an invasive pine needle pathogen reflects anthropogenic activity.  Ecology and Evolution 4: 3642–3661. PMID: 25478155.
  9. Oono, R., Lutzoni, F., Arnold, A.E., Kaye, L., U’Ren, J. M., May, G. and I. Carbone. 2014.  Genetic variation in horizontally transmitted fungal endophytes of pine needles reveals population structure in cryptic species. American Journal of Botany 101:1362-1374.  PMID: 25156984.
  10. U’Ren, J. M., Riddle, J.M., Monacell, J.T., Carbone, I., Miadlikowska, J. and A. E. Arnold.  2014.  Tissue storage and primer selection influence pyrosequencing-based inferences of diversity and community composition of endolichenic and endophytic fungi. Molecular Ecology Resources 14: 1032–1048. PMID: 24628864.
  11. Monacell, J. T. and I. Carbone. 2014.  Mobyle SNAP Workbench: A web-based analysis portal for population genetics and evolutionary genomics. Bioinformatics 30: 1488-90. doi: 10.1093/bioinformatics/btu055
  12. Miller, J. D., Schaafsma, A. W., Bhatnagar, D., Bondy, G., Carbone, I., Harris, L., Harrison, G., Munkvold, G., Oswald, I., Pestka, J., Sharpe, L., Sumarah, M., Tittlemier, S. and T. Zhou.  2014.  Mycotoxins that affect the North American Agri-Food sector: state of the art and directions for the future. World Mycotoxin Journal 7 (1): 63-82
  13. Moore, G. G., Elliott, J. L., Singh, R., Horn, B.W., Dorner, J. W., Stone, E. A., Chulze, S. N., Barros, G. G., Naik, M. K., Wright, G. C., Hell, K. and I. Carbone. 2013.  Sexuality generates diversity in the aflatoxin gene cluster: evidence on a global scale. PLoS Pathogens 9(8): e1003574. doi:10.1371/journal.ppat.1003574
  14. Horn, B. W., Sorensen, R. B., Lamb, M. C., Sobolev, V. S., Olarte, R. A., Worthington C. J. and I. Carbone. 2013.  Sexual reproduction in Aspergillus flavus sclerotia naturally produced in corn.  Phytopathology 104:75-85. (cover page)
  15. Horn, B. W., Olarte, R. A., Peterson, S. W. and I. Carbone. 2013. Sexual reproduction in Aspergillus tubingensis from section Nigri. Mycologia 105: 1153–1163. DOI: 10.3852/13-101.
  16. Bradshaw, R. E., Slot, J. C., Moore, G. G., Chettri, P., de Wit, P. J.G.M., Ehrlich, K. C., Ganley, A. R. D., Olson, M. A., Rokas, A., Carbone, I. and M. P. Cox.  2013.  Fragmentation of an aflatoxin-like gene cluster in a forest pathogen New Phytologist 198: 525–535.
  17. Putman, A. I., Carbone, I., and L. P. Tredway.  2013.  Development and characterization of 14 microsatellite loci for the plant pathogenic fungus Sclerotinia homoeocarpa Molecular Ecology Resources 13:966–968.
  18. Wei, W., Ayub, Q., Chen, Y., McCarthy, S., Hou, Y., Carbone, I., Xue, Y., and C. Tyler-Smith.  2013.  A calibrated human Y-chromosomal phylogeny based on resequencing.  Genome Research, DOI:10.1101/gr.143198.112.
  19. Olarte, R. A., Horn, B. W., Dorner, J. W., Monacell, J. T., Singh, R., Stone, E. A. and I. Carbone.  2012.  Effect of sexual recombination on population diversity in alfatoxin production by Aspergillus flavus and evidence for cryptic heterokaryosis. Molecular Ecology 21: 1453–1476. DOI: 10.1111/j.1365-294X.2011.05398.x.  *Paper is the topic of a News and Views Perspective article: Fisher, M. C. and D. A. Henk. 2012.  Sex, drugs and recombination: the wild life of Aspergillus. Molecular Ecology 21: 1305–1306.
  20. Abbas, H. K., Weaver, M. A., Horn, B. W., Carbone, I., Monacell, J. T. and W. T. Shier.  2011. Selection of Aspergillus flavus isolates for biological control of aflatoxins in corn.  Toxin Reviews 30: 59-70.
  21. Olson, H., Carbone, I. and M. Benson. 2011.  Phylogenetic history of Phytophthora cryptogea and P. drechsleri isolates from floriculture crops in North Carolina greenhouses.  Phytopathology  101:1373-1384.
  22. Litvintseva, A. P., Carbone, I., Rossouw, J., Thakur, R., Govender, N. P., and T. G. Mitchell. 2011. Evidence that the human pathogenic fungus Cryptococcus neoformans var. grubii may have evolved in Africa. PLoS One 6(5): e19688. doi:10.1371/journal.pone.0019688.
  23. Wu, F., Bhatnagar, D., T. Bui-Klimke, I. Carbone, R. Hellmich, G. Munkvold, P. Paul, G. Payne, E. Takle. 2011. Climate Change Impacts on Mycotoxin Risks in US Maize. World Mycotoxin Journal 4: 79-93.
  24. Kaye, A.C., J.W. Moyer, E.J. Parks, I. Carbone, and M.A. Cubeta. 2011. Population genetic analysis of tomato spotted wilt virus on peanut in North Carolina and Virginia. Phytopathology 101:147-153.
  25. Horn, B. W., Moore, G. G. and I. Carbone. 2011. Sexual reproduction in aflatoxin-producing Aspergillus nomius.  Mycologia 103: 174–183. DOI: 10.3852/10-115.
  26. Arnold, A. E., Carbone, I., Lutzoni, F. and G. May.  2011. A multidimensional study of endophytic fungal diversity.  IMA Fungus 2: 2-4.
  27. Moore, G. G., Singh, R., Horn, B. W., and I. Carbone. 2009. Recombination and lineage-specific gene loss in the aflatoxin gene cluster of Aspergillus flavus. Molecular Ecology 18: 4870-4887.
  28. Parks, R., Carbone, I., Murphy, P and C. Cowger.  2009. Population genetic analysis of an eastern U.S. wheat powdery mildew population reveals geographic subdivision and recent common ancestry with U.K. and Israeli populations.  Phytopathology 99: 840-849.
  29. Lourenço Jr., V., Moya, A., González-Candelas, F., Carbone, I., Maffia, L. A. and E. S. G. Mizubuti.  2009. Molecular diversity and evolutionary processes of Alternaria solani in Brazil inferred using genealogical and coalescent approaches. Phytopathology 99: 765-774.
  30. Horn, B. W., Moore, G. G. and I. Carbone. 2009. Sexual reproduction in Aspergillus flavus.  Mycologia 101: 423-429.
  31. Goss, E. M., Carbone, I., and N. J. Grünwald. 2009. Ancient isolation and independent evolution of the three clonal lineages of the exotic sudden oak death pathogen Phytophthora ramorum. Molecular Ecology 18: 1161-1174.
  32. Horn, B. W., Ramirez-Prado, J. H. and I. Carbone. 2009. The sexual state of Aspergillus parasiticusMycologia 101: 275-280.
  33. Horn, B. W., Ramirez-Prado, J. H. and I. Carbone. 2009. Sexual reproduction and recombination in the aflatoxin-producing fungus Aspergillus parasiticusFungal Genetics and Biology 46: 169-175. (cover page) (recommended by Faculty of 1000 Biology)
  34. Ramirez-Prado, J. H., Moore, G. G., Horn, B. W. and I. Carbone. 2008. Characterization and population analysis of the mating-type genes in Aspergillus flavus and Aspergillus parasiticusFungal Genetics and Biology 45: 1292-1299.
  35. Brown DE, Powell A. J., Carbone I. and R. A Dean. 2008. GT-Miner: a graph-theoretic data miner, viewer and model processor. Bioinformation 3(5): 235-237.
  36. Charlton, N. D., Carbone, I., Tavantzis, S. M., and M. A. Cubeta. 2008. Phylogenetic relatedness of the M2 double-stranded RNA in Rhizoctonia fungi. Mycologia 100: 555-564.
  37. Parks, R., Carbone, I. Murphy, J. P., Marshall, D. S. and C. Cowger. 2008. Virulence structure of the Eastern U.S. wheat powdery mildew population.  Plant Disease 92: 1074-1082.
  38. Powell, A. J. Conant, G. C., Brown, D. E. Carbone, I. and R. A. Dean. 2008. Altered patterns of gene duplication and differential gene gain and loss in fungal pathogens.  BMC Genomics 9: 147.
  39. Clark, C. M. and I. Carbone. 2008. Chloroplast DNA phylogeography in long lived Huon Pine (Lagarostrobos franklinii), a Tasmanian rainforest conifer. Canadian Journal of Forest Research 38: 1576-1589.
  40. Carbone, I., Jakobek, J. L., Ramirez-Prado, J. H. and B. W. Horn. 2007. Recombination, balancing selection and adaptive evolution in the aflatoxin gene cluster of Aspergillus parasiticus.  Molecular Ecology 16: 4401-4417. (recommended by Faculty of 1000 Biology)
  41. Carbone, I., Ramirez-Prado, J. H., Jakobek, J. L., and B. W. Horn. 2007. Gene duplication, modularity and adaptation in the evolution of the aflatoxin gene cluster. BMC Evolutionary Biology 7:111.
  42. Moser, J. M., Carbone, I., Arasu, P. and G. Gibson. 2007. Impact of population structure on genetic diversity of a potential vaccine target in the canine hookworm (Ancyclostoma caninum).  Journal of Parasitology 93: 796-805.
  43. Deng, J., Carbone, I. and R. A Dean. 2007. The evolutionary history of cytochrome P450 genes in four filamentous ascomycetes. BMC Evolutionary Biology 7: 30.
  44. Gómez-Alpizar, L., I. Carbone, and J. B. Ristaino. 2007. An Andean origin of Phytophthora infestans inferred from nuclear and mitochondrial gene genealogies. Proc Nat. Acad. Sci. 104: 3306-3311.
  45. Malvárez, G, Carbone, I., Grünwald N. J., Subbarao, K. V., Schafer, M. and L. M. Kohn. 2007. New populations of Sclerotinia sclerotiorum from lettuce in California and peas and lentils in Washington.  Phytopathology 97: 512-525.
  46. Aylor, D. L., Price, E.W. and I. Carbone. 2006. SNAP: Combine and Map modules for multilocus population genetic analysis.  Bioinformatics 22: 1399-1401.
  47. Charles, L., I. Carbone, K. G. Davies, D. Bird, M. Burke, B. R. Kerry, and C. H. Opperman. 2005. Phylogenetic Analysis of Pasteuria penetrans by Use of Multiple Genetic Loci.  Journal of Bacteriology 187: 5700-5708.
  48. Dean, R.A., Talbot, N.J., Ebbole, D.J., Farman, M.L., Mitchell, T., Orbach, M.J., Thon, M., Kulkarni, R., Xu, J-R.,Pan, H., Read, N.D., Lee, Y-H., Carbone, I., Brown, D., Oh, Y.Y., Donofrio, N., Jeong, J.S., Soanes, D.M., Djonovic, S., Kolomiets, E., Rehmeyer, C., Li, W., Harding, M., Kim S., Lebrun M-H., Bohnert, H., Coughlan, S., Butler, J., Calvo, S., Ma, L-J., Nicol, R., Purcell, S., Nusbaum, C., Galagan, J.E., Birren, B.W. 2005. The genome sequence of the rice blast fungus Magnaporthe griseaNature 434: 980-986.
  49. Price, E.W. and I. Carbone. 2005. SNAP: workbench management tool for evolutionary population genetic analysis. Bioinformatics 21: 402-404.
  50. Carbone, I., Y. Liu, B. I. Hillman and M. G. Milgroom. 2004. Recombination and migration of Cryphonectria hypovirus 1 as inferred from gene genealogies and the coalescent. Genetics 166: 1611-1629.
  51. Phillips, D.V., I. Carbone, S. E. Gold, and L. M. Kohn. 2002. Phylogeography and genotype – symptom associations in early and late season infections of canola by Sclerotinia sclerotiorum.  Phytopathology 92: 785-793.
  52. Carbone, I. and L. M. Kohn. 2001. Multilocus nested haplotype networks extended with DNA fingerprints show common origin and fine-scale, ongoing genetic divergence in a wild microbial metapopulation.  Molecular Ecology 10: 2409-2422.
  53. Carbone, I. and L. M. Kohn. 2001. A microbial population-species interface: nested cladistic and coalescent inference with multilocus data. Molecular Ecology 10: 947-964.
  54. Carbone, I., and L. M. Kohn. 1999. A method for designing primer sets for speciation studies in filamentous ascomycetes.  Mycologia 91: 553-556.
  55. Carbone, I., J. B. Anderson, and L. M. Kohn. 1999. Patterns of descent in clonal lineages and their multilocus fingerprints are resolved with combined gene genealogies.  Evolution 53: 11-21.
  56. Carbone, I., J. B. Anderson, and L. M. Kohn. 1995. A group-I intron in the mitochondrial small subunit ribosomal RNA gene of Sclerotinia sclerotiorumCurrent Genetics 27: 166-176.
  57. Carbone, I., and L. M. Kohn. 1993. Ribosomal DNA sequence divergence within internal transcribed spacer 1 of the Sclerotiniaceae.  Mycologia 85:  415-427.
  58. Kohn, L. M., E. Stasovski, I. Carbone, J. Royer, and J. B. Anderson. 1991. Mycelial incompatibility and molecular markers identify genetic variability in field populations of Sclerotinia sclerotiorumPhytopathology 81: 480-485.
  59. Kohn, L. M., I. Carbone, and J. B. Anderson. 1990. Mycelial interactions in Sclerotinia sclerotiorumExperimental Mycology 14: 255-267.