Domestication of maize, sorghum, and sugarcane did not drive the divergence of their smut pathogens

Evolution

Volumn 61, Issue 2, 2007, Pages 388-403

  Munkacsi, Andrew B ^a,b   Stoxen, Sam ^a   May, Georgiana ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b NewYork Presbyterian Hospital   (United States)

Author keywords

Crop domestication; Crop pathogen; Divergence times; Origin of disease; Plant pathology; Smut fungi; Symbiosis

Indexed keywords

AGRICULTURAL PRACTICE; COEVOLUTION; DIVERGENCE; DOMESTICATION; FUNGUS; MAIZE; PATHOGEN; PATHOLOGY; PHYLOGENY; SORGHUM; SUGAR CANE; SYMBIOSIS;

AGRICULTURE; ARTICLE; FUNGAL GENE; FUNGUS; GENETIC RECOMBINATION; GENETIC VARIABILITY; GENETICS; MAIZE; MICROBIOLOGY; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY; PLANT DISEASE; SORGHUM; SUGARCANE;

AGRICULTURE; BASE SEQUENCE; FUNGI; GENES, FUNGAL; PHYLOGENY; PLANT DISEASES; RECOMBINATION, GENETIC; SACCHARUM; SORGHUM; VARIATION (GENETICS); ZEA MAYS;

EUKARYOTA; FUNGI; SPORISORIUM REILIANUM; USTILAGO MAYDIS; ZEA MAYS;

EID: 33947148526     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2007.00036.x     Document Type: Article

References (73)

1. Alvarez, N., D. McKey, M. Hossaert-McKey, C. Born, L. Mercier, and B. Benrey. 2005. Ancient and recent evolutionary history of the bruchid beetle, Acanthoscelides obtectus Say, a cosmopolitan pest of beans. Mol. Ecol. 14:1015-1024.
2. Anderson, R. M., and R. M. May. 1991. Infectious Diseases of Humans: Dynamics and Control. Oxford Univ. Press, Oxford.
3. Bakkeren, G., and J. W. Kronstad. 1996. The pheromone cell signaling components of the Ustilago a mating-type loci determine intercompatibility between species. Genetics 143:1601-1613.
4. Bakkeren, G., J. W. Kronstad, and C. A. Levesque. 2000. Comparison of AFLP fingerprints and ITS sequences as phylogenetic markers in Ustilaginomycetes. Mycologia 92:510-521.
5. Banke, S., and B. A. McDonald. 2005. Migration patterns among global populations of Mycosphaerella graminicola. Mol. Ecol. 14:1881-1896.
6. Bauer, R., D. Begerow, F. Oberwinkler, M. Piepenbring, and M. L. Berbee. 2001. Ustilaginomycetes. Pp. 57-84 in D. J. McLaughlin, E. McLaughlin, M. Lemke, eds. The Mycota VII Part B: Systematics and Evolution. Springer, Berlin.
7. Beach, D., M. Piper, and P. Nurse. 1982. Construction of a Schizosaccharomyces pombe gene bank in a yeast bacterial shuttle vector and its use to isolate genes by complementation. Mol. Gen. Genet. 187:326-329.
8. Begerow, D., R. Bauer, and T. Boekhout. 2000. Phylogenetic placements of ustilaginomycetous anamorphs as deduced from nuclear LSU rDNA sequences. Mycol. Res. 104:53-60.
9. Berbee, M. L., M. Pirseyedi, and S. Hubbard. 1999. Cochliobolus phylogenetics and the origin of known, highly virulent pathogens, inferred from ITS and glyceraldehyde-3-phosphate dehydrogenase sequences. Mycologia 91:964-977.
10. Boekhout, T., and J. W. Fell. 1998. Pseudozyma Bandoni emend. Boekhout and a comparison with the yeast state of Ustilago maydis (De Candolle) Corda. in C. P. Kurtzman, J. W. Fell, eds. The Yeasts: A taxonomic study. Elsevier, New York.
11. Boekhout, T., J. W. Fell, and K. O'Donnell. 1995. Molecular systematics of some yeast-like anamorphs belonging to the Ustilaginales and Tilletiales. Stud. Mycol. 38:175-183.
12. Borlaug, N. E. 1972. A cereal breeder and ex-forester's evaluation of the progress and problems involved in breeding for rust resistant forest trees: moderator's summary. US Dep. Agric. Misc. Publ. 1221:615-642. Washington D.C., U.S.A.
13. Burdon, J. J., P. H. Thrall, and L. Ericson. 2006. The current and future dynamics of disease in plant communities. Annu. Rev. Phyopathol. 44:19-39.
14. Cannon, S. B., H. Zu, A. M. Baumgarten, R. Spangler, G. May, and D. Cook. 2002. Diversity, distribution, and ancient taxonomic relationships within the TIR and non-TIR NBS-LRR resistance gene subfamilies. J. Mol. Evol. 54:548-562.
15. Carbone, I., and L. M. Kohn. 2001. A microbial population-species interface: nested cladistic and coalescent inference with multilocus data. Mol. Ecol. 10:947-964.
16. Couch, B. C., I. Fudal, M.-H. Lebrun, D. Tharreau, B. Valent, P. van Kim, J.-L. Nottéghem, and L. M. Kohn. 2005. Origins of host-specific populations of the blast pathogen Magnaporthe oryzae in crop domestication with subsequent expansion of pandemic clones on rice and weeds of rice. Genetics 170:613-630.
17. Felsenstein, J. 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol. 17:368-376.
18. _. 2005. PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle.
19. Fischer, G. W., and C. S. Holton. 1957. Biology and control of the smut fungi. The Ronald Press, New York.
20. Gaut, B. S., and J. F. Doebley. 1997. DNA sequence evidence for the segmental allotetraploid origin of maize. Proc. Natl. Acad. Sci. USA 94:6809-6814.
21. Gilbert. 2002. Evolutionary ecology of plant diseases in natural ecosystems. Annu. Rev. Phytopathol. 40:13-43.
22. Graur, D., and W. H. Li. 2000. Rates and patterns of nucleotide substitution. Pp. 99-164 in Fundamental of molecular evolution (2nd. ed.). Sinauer Associates, Sunderland.
23. Grenfell, B. T., O. G. Pybus, J. R. Gog, J. L. N. Wood, J. M. Daly, J. A. Murnford, and E. C. Holmes. 2004. Unifying the epidemiological and evolutionary dynamics of pathogens. Science 303:327-332.
24. Guernier, V., M. E. Hochberg, and J.-F. Guégan. 2004. Ecology drives the worldwide distribution of human diseases. PLoS Biology 2:740-746.
25. Hanada, K., Y. Suzuki, and T. Gojobori. 2004. A large variation in the rates of synonymous substitution for RNA viruses and its relationship to a diversity of viral infections transmission modes. Mol. Biol. Evol. 21:1074-1080.
26. Hansen, E. M. 1987. Speciation in plant pathogenic fungi. The influence of agricultural practice. Can. J. Plant Pathol. 9:403-410.
27. Hiura, U. 1978. Genetic basis of formae speciales in Erysiphe graminis. Pp. 101-128 in D. M. Spencer, ed. The powdery mildews. Academic Press, London.
28. Hoberg, E. P., N. L. Alkire, A. de Queiroz, and A. Jones. 2001. Out of Africa: origins of the Taenia tapeworms in humans. Proc. Roy. Soc. Lond. B 268:781-787.
29. Holliday, R. 1974. Ustilago maydis. Pp. 575-595 in R. C. King, ed. Handbook of Genetics, Vol. 1. Plenum Press, New York.
30. James, G. 2004. An introduction to sugarcane (2nd ed.). Pp. 1-7 in G. James, ed. Sugarcane. Blackwell Publishing, Oxford.
31. Johnson, T. 1961. Man-guided evolution in plant rusts. Science 133:357-362.
32. Jukes, T. H., and C. R. Cantor. 1969. Evolution of protein molecules. Pp. 21-132 in H. N. Munro, ed. Mammalian Protein Metabolism. Academic Press, New York.
33. Kasuga, T., T. J. White, and J. W. Taylor. 2002. Estimation of nucleotide substitution rates in eurotiomycete fungi. Mol. Biol. Evol. 19:2318-2324.
34. Kellogg, E. A. 2001. Evolutionary history of the grasses. Plant Physiol. 125:1198-1205.
35. Kimber, C. T. 2000. Origins of domesticated sorghum and its early diffusion to India and China. Pp. 3-99 in C. W. Smith and R. A. Frederiksen, eds. Sorghum: origin, history, technology, and production. Wiley and Sons, New York.
36. Kimura, M. 1981. Estimation of evolutionary distances between homologous nucleotide sequences. Proc. Natl. Acad. Sci. USA. 78:454-458.
37. Kosakovsky Pond, S. L., S. D. W. Frost, and S. V. Muse. 2005. HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676-679.
38. Kretzer, A. M., and T. D. Bruns. 1999. Use of atp6 in fungal phylogenetics: an example from the Boletales. Mol. Phylogen. Evol. 13:483-492.
39. Kumar, S., K. A. Balczarek, and Z.-C. Lai. 1996. Evolution of the hedgehog gene family. Genetics 142:965-972.
40. Maddison, D. R., and W. P. Maddison. 2000. MacClade 4.0: Analysis of Phylogeny and Character Evolution. Sinauer Associates, Sunderland.
41. Matheny, P. B., Y. J. Liu, J. F. Ammirati, and B. D. Hall. 2002. Using RPB1 sequences to improve phylogenetic inference among mushrooms (Inocybe, Agaricales). Amer. J. Bot. 89:688-698.
42. Matsuoka, Y., Y. Vigouroux, M. M. Goodman, J. Sanchez, E. Buckler, and J. Doebley. 2002. A single domestication for maize shown by multilocus microsatellite genotyping. Proc. Natl. Acad. Sci. USA 99:6080-6084.
43. Ming, R., S.-C. Liu, Y.-R. Lin, J. da Silva, W. Wilson, D. Braga, A. van Deynze, T. F. Wenslaff, K. K. Wu, P. H. Moore, W. Burnquist, M. E. Sorrells, J. E. Irvine, and A. H. Paterson. 1998. Detailed alignment of Saccharum and Sorghum chromosomes: comparative organization of closely related diploid and polyploidy genomes. Genetics 150:1663-1682.
44. Muse, S. V., and B. S. Gaut. 1994. A likelihood approach for comparing synonymous and nonsynonymous nucleotide substitution rates with application to the chloroplast genome. Mol. Biol. Evol. 11:715-724.
45. Palumbi, S. R. 2001a. The Evolution Explosion: How Humans Cause Rapid Evolutionary Change. W. W. Norton and Co., New York.
46. _. 2001b. Humans as the world's greatest evolutionary force. Science 293:1786-1790.
47. Parker, I. M., and G. S. Gilbert. 2004. The evolutionary ecology of novel plant-pathogen interactions. Annu. Rev. Ecol. Evol. Syst. 35:675-700.
48. Percy, D. M., R. D. M. Page, and Q. C. B. Cronk. 2004. Plant-insect interactions: double-dating associated insect and plant lineages reveals asynchronous radiations. Syst. Biol. 53:120-127.
49. Piepenbring, M., M. Stoll, and F. Oberwinkler. 2002. The generic position of Ustilago maydis, Ustilago scitamineum, and Ustilago esculenta (Ustilaginales). Mycol. Prog. 1:71-80.
50. Posada, D., and K. A. Crandall. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817-818.
51. Rachowicz, L. J., J.-M. Hero, R. A. Alford, J. W. Taylor, J. A. T. Morgan, V. T. Vredenburg, J. P. Collins, and C. J. Briggs. 2005. The novel and endemic pathogen hypotheses: Competing explanations for the origin of emerging infectious diseases of wildlife. Cons. Biol. 19:1441-1448.
52. Rehner, S. A., and E. Buckley. 2005. A Beauveria phylogeny inferred from nuclear ITS and EF1-α sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia 97:84-98.
53. Roux, C., T. Almaraz, and G. Durrieu. 1998. Phylogeny of some smut fungi based on ITS sequence analysis. CR. Acad. Sci. Ser. III 321:603-609.
54. Rozas, J., J. C. Sánchez-Delbarrio, X. Messeguer, and R. Rozas. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496-2497.
55. Saenz, G. S., and J. W. Taylor. 1999. Phylogeny of the Erysiphales (powdery mildews) inferred from internal transcribed spacer ribosomal DNA sequences. Can. J. Bot. 77:150-168.
56. Sanderson, M. J. 2002. Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol. Biol. Evol. 19:101-109.
57. _. 2003. r8s; inferring absolute rates of evolution and divergence times in the absence of a molecular clock. Bioinformatics 19:301-302.
58. Sawyer, S. A. 2000. GENECONV: A Computer Package for the Statistical Detection of Gene Conversion. Distributed by the author, Department of Mathematics, Washington University in St. Louis, available at http://www.wustl.edu/~sawyer.
59. Smith, T. L., and S. A. Leong. 1990. Isolation and characterization of a Ustilago maydis glyceraldehyde-3-phosphate dehydrogenase-encoding gene. Gene 93:111-117.
60. Stoll, M., M. Piepenbring, D. Begerow, and F. Oberwinkler. 2003. Molecular phylogeny of Ustilago and Sporisorium species (Basidiomycota, Ustilaginales) based on internal transcribed spacer (ITS) sequences. Can. J. Bot. 81:976-984.
61. Stoll, M., D. Begerow, and F. Oberwinkler. 2005. Molecular phylogeny of Ustilago, Sporisorium, and related taxa based on combined analyses of rDNA sequences. Mycol. Res. 109:342-356.
62. Sugita, T., M. Takashima, N. Poonwan, N. Mekha, K. Malaithao, B. Thungmuthasawat, S. Prasarn, P. Luangsook, and T. Kudo. 2003. The first isolation of Ustilaginomycetous anamorphic yeasts, Pseudozyma species, from patients' blood and a description of two new species: P. parantarctica and P. thailandica. Microbiol. Immunol 47:183-190.
63. Swigonova, Z., J. Lai, J. Ma, W. Ramakrishna, V. Llaca, J. Bennetzen, and J. Messing. 2004. Close split of sorghum and maize genome progenitors. Genome Res. 14:1916-1923.
64. Swofford, D. L. 2002. PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4.0b10. Sinauer Associates, Sunderland.
65. Tamura, K., and M. Nei. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10:512-526.
66. Taylor, J. W., D. J. Jacobson, and M. C. Fisher. 1999. The evolution of asexual fungi: reproduction, speciation and classification. Ann. Rev. Phytopathol. 37:197-246.
67. Taylor, J. W., D. J. Jacobson, S. Kroken, T. Kasuga, D. M. Geiser, D. S. Hibbett, and M. C. Fisher. 2000. Phylogenetic species recognition and species concepts in fungi. Fung. Genet. Biol. 31:21-32.
68. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 24:4876-4882.
69. Thrall, P. H., and J. J. Burdon. 2003. Evolution of virulence in a plant host-pathogen metapopulation. Science 299:1735-1737.
70. Tyler, L. J., and C. P. Shumway. 1935. Hybridization between Sphacelotheca sorghi and Sorosporium reilianum. Phytopathol. 25:375-376.
71. Vaheeduddin, S. 1942. The pathogenicity and genetics of some sorghum smuts. Minn. Agric. Expt. Sta. Tech. Bull. 154.
72. Wolfe, K. H., P. M. Sharp, and W. H. Li. 1989. Rates of synonymous substitution in plant nuclear genes. J. Mol. Evol. 29:208-211.
73. Zambino, P. J., and L. J. Szabo. 1993. Phylogenetic relationships of selected cereal and grass rusts based on rDNA sequence analysis. Mycologia 85:401-414.