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Chapter 38 : Genetics and Pathogenicity

Authors: John F. Leslie1, Jin-Rong Xu2
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Affiliations: 1: Department of Plant Pathology, Throckmorton Plant Sciences Center, Kansas State University, Manhattan, KS 66506-5502; 2: Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN 47907-2054
Content Type: Monograph
Publication Year: 2010

Category: Microbial Genetics and Molecular Biology; Fungi and Fungal Pathogenesis

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Abstract:

Various members of the genus are associated with plant diseases and the production of various classes of mycotoxins, with many secondary metabolites still only poorly characterized. The conditionally dispensable chromosome of appears to contain many pea pathogenicity genes that are important for host range determinants but are dispensable for normal growth in culture. Several well-conserved signal transduction pathways have been studied in some species. Mitogen-activated protein kinase (MAPK) genes homologous to the PMK1 have been characterized in (FMK1) and (GPMK1/MAK1). All of the sequenced genomes contain multiple copies of genes encoding cutinases, xylanases, polygalacturonases (PG), and other cell wall-degrading enzyme (CWDE) genes, indicating the importance of these hydrolytic enzymes. head scab has been linked to deoxynivalenol (DON) in two ways. First there were mechanistic studies conducted by researchers showing that strains that produced more DON were more aggressive than strains that produced nivalenol as an alternative to DON or that produced no trichothecenes whatsoever. Second, in a quantitative trait locus analysis, another group of researchers showed that the cluster of genes responsible for trichothecene biosynthesis was at the heart of the only major quantitative trait locus in a cross between fungal strains that differed in their ability to cause fusarium head scab. Genetics- and genomics-based approaches will certainly further improve our understanding of molecular mechanisms and evolution of pathogenesis.

Citation: Leslie J, Xu J. 2010. Genetics and Pathogenicity, p 607-621. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch38
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Fusarium Genetics and Pathogenicity
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Citation: Leslie J, Xu J. 2010. Genetics and Pathogenicity, p 607-621. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch38
/content/10.1128/9781555816636.ch38.ch38fig01
FIGURE 1
Spore morphology characters used in the identification of species. Drawings are idealized and not necessarily to scale. (A through D) Macroconidial shapes. (A) Typical macroconidium; the apical cell is on the left, and the basal cell is on the right; (B) slender, straight, almost needle-like macroconidium, e.g., ; (C) macroconidium with dorsoventral curvature, e.g., ; (D) macroconidium with the dorsal side more curved than the ventral, e.g., . (E through H) Macroconidial apical cell shapes; (E) blunt, e.g., ; (F) papillate, e.g., ; (G) hooked, e.g., ; (H) tapering, e.g., . (I through L) Macroconidial basal cell shapes; (I) Foot shaped, e.g., ; (J) elongated foot shape, e.g., ; (K) distinctly notched, e.g., ; (L) barely notched, e.g., . (M through T) Microconidial spore shapes; (M) oval; (N) two-celled oval; (O) three-celled oval; (P) reniform; (Q) obovoid with a truncate base; (R) pyriform; (S) napiform; (T) globose. (U through X) Phialide morphology; (U) monophialides, e.g., (V) monophialides, e.g., ; (W) Polyphialides, e.g., ; (X) polyphialides, e.g., . (Y and Z) Microconidial chains; (Y) short chains, e.g., ; (Z) long chains, e.g., . (After .)
10.1128/9781555816636/f0608-01_thmb.gif
10.1128/9781555816636/f0608-01.gif
Image of FIGURE 1
FIGURE 1

Spore morphology characters used in the identification of species. Drawings are idealized and not necessarily to scale. (A through D) Macroconidial shapes. (A) Typical macroconidium; the apical cell is on the left, and the basal cell is on the right; (B) slender, straight, almost needle-like macroconidium, e.g., ; (C) macroconidium with dorsoventral curvature, e.g., ; (D) macroconidium with the dorsal side more curved than the ventral, e.g., . (E through H) Macroconidial apical cell shapes; (E) blunt, e.g., ; (F) papillate, e.g., ; (G) hooked, e.g., ; (H) tapering, e.g., . (I through L) Macroconidial basal cell shapes; (I) Foot shaped, e.g., ; (J) elongated foot shape, e.g., ; (K) distinctly notched, e.g., ; (L) barely notched, e.g., . (M through T) Microconidial spore shapes; (M) oval; (N) two-celled oval; (O) three-celled oval; (P) reniform; (Q) obovoid with a truncate base; (R) pyriform; (S) napiform; (T) globose. (U through X) Phialide morphology; (U) monophialides, e.g., (V) monophialides, e.g., ; (W) Polyphialides, e.g., ; (X) polyphialides, e.g., . (Y and Z) Microconidial chains; (Y) short chains, e.g., ; (Z) long chains, e.g., . (After .)

Citation: Leslie J, Xu J. 2010. Genetics and Pathogenicity, p 607-621. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch38
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FIGURE 2
Perithecia, asci, and ascospores of , and . (A) Cluster of perithecia of on wheat straw; bar = 200 μm. (B) Perithecia of on carnation leaf pieces from CLA; bar = 200 μm. (C) Perithecium of oozing ascospores in a cirrhus; bar = 200 μm. (D) Perithecium of oozing ascospores in a cirrhus; bar = 200 μm. (E) Asci and ascospores of , note three-septate ascospores; bar = 25 μm. (F) Asci and ascospores of ; bar = 25 μm. (G) Ascospores of , note one-septate ascospores; bar = 10 μm. (H) Ascospores of ; bar = 10 μm. (After .)
10.1128/9781555816636/f0610-01_thmb.gif
10.1128/9781555816636/f0610-01.gif
Image of FIGURE 2
FIGURE 2

Perithecia, asci, and ascospores of , and . (A) Cluster of perithecia of on wheat straw; bar = 200 μm. (B) Perithecia of on carnation leaf pieces from CLA; bar = 200 μm. (C) Perithecium of oozing ascospores in a cirrhus; bar = 200 μm. (D) Perithecium of oozing ascospores in a cirrhus; bar = 200 μm. (E) Asci and ascospores of , note three-septate ascospores; bar = 25 μm. (F) Asci and ascospores of ; bar = 25 μm. (G) Ascospores of , note one-septate ascospores; bar = 10 μm. (H) Ascospores of ; bar = 10 μm. (After .)

Citation: Leslie J, Xu J. 2010. Genetics and Pathogenicity, p 607-621. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch38
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FIGURE 3
Chlamydospores of species. (A and B) Single, verrucose chlamydospores of ; (C and D) clustered chlamydospores of ; (E) chain of verrucose chlamydospores of ; (F) paired, smooth-walled chlamydospores of ; (G) single, verrucose chlamydospore of . ; (H) paired, verrucose chlamydospores of ; (I) clustered, smooth-walled chlamydospores of ; (J and L) chains of verrucose chlamydospores of ; (K) chain of verrucose chlamydospores of . Scale bars: panels A through E, 50 μm; panels F through L, 25 μm. (After .)
10.1128/9781555816636/f0610-02_thmb.gif
10.1128/9781555816636/f0610-02.gif
Image of FIGURE 3
FIGURE 3

Chlamydospores of species. (A and B) Single, verrucose chlamydospores of ; (C and D) clustered chlamydospores of ; (E) chain of verrucose chlamydospores of ; (F) paired, smooth-walled chlamydospores of ; (G) single, verrucose chlamydospore of . ; (H) paired, verrucose chlamydospores of ; (I) clustered, smooth-walled chlamydospores of ; (J and L) chains of verrucose chlamydospores of ; (K) chain of verrucose chlamydospores of . Scale bars: panels A through E, 50 μm; panels F through L, 25 μm. (After .)

Citation: Leslie J, Xu J. 2010. Genetics and Pathogenicity, p 607-621. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch38
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References

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1. Bacon, C. W.,, J. K. Porter,, W. P. Norred, and, J. F. Leslie. 1996. Production of fusaric acid by Fusarium species. Appl. Environ. Microbiol. 62: 4039– 4043.
2. Bae, H.,, M. S. Kim,, R. C. Sicher,, H. J. Bae, and, B. A. Bailey. 2006. Necrosis- and ethylene-inducing peptide from Fusarium oxysporum induces a complex cascade of transcripts associated with signal transduction and cell death in Arabidopsis. Plant Physiol. 141: 1056– 1067.
3. Bagga, S., and, D. Straney. 2000. Modulation of cAMP and phosphodiesterase activity by flavonoids which induce spore germination of Nectria haematococca MP VI ( Fusarium solani). Physiol. Mol. Plant Pathol. 56: 51– 61.
4. Bai, G. H.,, A. E. Desjardins, and, R. D. Plattner. 2002. Deoxynivalenol-nonproducing Fusarium graminearum causes initial infection, but does not cause disease spread in wheat spikes. Mycopathologia 153: 91– 98.
5. Bailey, B. A. 1995. Purification of a protein from culture filtrates of Fusarium oxysporum that induces ethylene and necrosis in leaves of Erythroxylum coca. Phytopathology 85: 1250– 1255.
6. Bluhm, B. H.,, X. Zhao,, J. E., Flaherty,, J.-R. Xu, and, L. D. Dunkle. 2007. RAS2 regulates growth and pathogenesis in Fusarium graminearum. Mol. Plant-Microbe Interact. 20: 627– 636.
7. Boehm, E. W. A.,, R. C. Ploetz, and, H. C. Kistler. 1994. Statistical analysis of electrophoretic karyotype variation among vegetative compatibility groups of Fusarium oxysporum f. sp. cubense. Mol. Plant-Microbe Interact. 7: 196– 207.
8. Bowden, R. L.,, I. Fuentes-Bueno,, J. F. Leslie,, J. Lee, and, Y.-W. Lee. 2008. Methods for detecting chromosomal rearrangements in Gibberella zeae. Cereal Res. Commun. 36(Suppl. B): 603– 608.
9. Calero-Nieto, F.,, A. di Pietro,, M. I. G. Roncero, and, C. Hera. 2007. Role of the transcriptional activator XlnR of Fusarium oxysporum in regulation of xylanase genes and virulence. Mol. Plant-Microbe Interact. 20: 977– 985.
10. Canero, D. C., and, M. I. G. Roncero. 2008. Influence of the chloride channel of Fusarium oxysporum on extracellular lac-case activity and virulence on tomato plants. Microbiology 154: 1474– 1481.
11. Caracuel, Z.,, C. Casanova,, M. I. G. Roncero,, A. di Pietro, and, J. Ramos. 2003a. pH response transcription factor PacC controls salt stress tolerance and expression of the P-type Na +-ATPase Ena1 in Fusarium oxysporum. Eukaryot. Cell 2: 1246– 1252.
12. Caracuel, Z.,, M. I. G. Roncero,, E. A. Espeso,, C. I. Gonzalez-Verdejo,, F. I. Garcia-Maceira, and, A. di Pietro. 2003b. The pH signaling transcription factor PacC controls virulence in the plant pathogen Fusarium oxysporum. Mol. Microbiol. 48: 765– 779.
13. Caracuel, Z.,, A. L. Martinez-Rocha,, A. di Pietro,, M. P. Madrid, and, M. I. G. Roncero. 2005. Fusarium oxysporum gas1 encodes a putative β-1,3-glucanosyltransferase required for virulence on tomato plants. Mol. Plant-Microbe Interact. 18: 1140– 1147.
14. Cechin, A. L.,, M. Sinigaglia,, N. Lemke,, S. Echeverrigaray,, O. G. Cabrera,, G. A. G. Pereira, and, J. C. M. Mombach. 2008. Cupin: a candidate molecular structure for the Nep1- like protein family. BMC Plant Biol. 8: 50.
15. Chulze, S. N.,, A. Torres,, M. L. Ramirez, and, J. F. Leslie. 2000. Genetic variation in Fusarium section Liseola from no-till maize in Argentina. Appl. Environ. Microbiol. 66: 5312– 5315.
16. Correll, J. C.,, C. J. R. Klittich, and, J. F. Leslie. 1987. Nitrate non-utilizing mutants of Fusarium oxysporum and their use in vegetative compatibility tests. Phytopathology 77: 1640– 1646.
17. Cumagun, C. J. R.,, R. L. Bowden,, J. E. Jurgenson,, J. F. Leslie, and, T. Miedaner. 2004. Genetic mapping of pathogenicity and aggressiveness of Gibberella zeae ( Fusarium graminearum) towards wheat. Phytopathology 94: 520– 526.
18. Cuomo, C. A.,, U. Gueldener,, J.-R. Xu,, F. Trail,, B. G. Turgeon,, A. di Pietro,, J. D. Walton,, L.-J. Ma,, S. E. Baker,, M. Rep,, G. Adam,, J. Antoniw,, T. Baldwin,, S. Calvo,, Y. L. Chang,, D. de Caprio,, L. R. Gale,, S. Gnerre,, R. S. Goswami,, K. Hammond-Kosack,, L. J. Harris,, K. Hilburn,, J. C. Kennell,, S. Kroken,, J. K. Magnuson,, G. Mannhaupt,, E. Mauceli,, H. W. Mewes,, R. Mitterbauer,, G. Muehlbauer,, M. Munsterkotter,, D. Nelson,, K. O’Donnell,, T. Ouellet,, W. H. Qi,, H. Quesneville,, M. I. G. Roncero,, K. Y. Seong,, I. V. Tetko,, M. Urban,, C. Waalwijk,, T. J. Ward,, J. Q. Yao,, B. W. Birren, and, H. C. Kistler. 2007. The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 317: 1400– 1402.
19. Delgado-Jarana, J. S.,, A. L. Martinez-Rocha,, R. Roldan-Rodriguez,, M. I. G. Roncero, and, A. di Pietro. 2005. Fusarium oxysporum G-protein β subunit Fgb1 regulates hyphal growth, development, and virulence through multiple signaling pathways. Fungal Genet. Biol. 42: 61– 72.
20. Desjardins, A. E. 2006. Fusarium Mycotoxins: Chemistry, Genetics and Biology. APS Press, St. Paul, MN.
21. Desjardins, A. E.,, M. Busman,, M. Muhitch, and, R. H. Proctor. 2007. Complementary host-pathogen genetic analyses of the role of fumonisins in the Zea mays-Gibberella moniliformis interaction. Physiol. Mol. Plant Pathol. 70: 149– 160.
22. di Pietro, A.,, F. I. Garcia-Maceira,, E. Meglecz, and, M. I. G. Roncero. 2001. A MAP kinase of the vascular wilt fungus Fusarium oxysporum is essential for root penetration and pathogenesis. Mol. Microbiol. 39: 1140– 1152.
23. Duvick, J. 2001. Prospects for reducing fumonisin contamination of maize through genetic modification. Environ. Health Perspect. 109(Suppl. 2): 337– 342.
24. Duyvesteijn, R. G. E.,, R. van Wijk,, Y. Boer,, M. Rep,, B. J. C. Cornelissen, and, M. A. Haring. 2005. Frp1 is a Fusarium oxysporum F-box protein required for pathogenicity on tomato. Mol. Microbiol. 57: 1051– 1063.
25. Eljaschewitsch, J.,, J. Sandfort,, K. Tintelnot,, I. Horbach, and, B. Ruf. 1996. Port-a-cath-related Fusarium oxysporum infection in an HIV-infected patient: treatment with liposomal amphotericin B. Mycoses 39: 115– 119.
26. Enkerli, J.,, G. Bhatt, and, S. F. Covert. 1998. Maackiain detoxification contributes to the virulence of Nectria haematococca MP VI on chickpea. Mol. Plant-Microbe Interact. 11: 317– 326.
27. Flaherty, J. E.,, A. M. Pirttila,, B. H. Bluhm, and, C. P. Woloshuk. 2003. PAC1, a pH-regulatory gene from Fusarium verticillioides. Appl. Environ. Microbiol. 69: 5222– 5227.
28. Fleiϐner, A.,, C. Sopalla, and, K. M. Weltring. 2002. An ATP-binding cassette multidrug-resistance transporter is necessary for tolerance of Gibberella pulicaris to phytoalexins and virulence on potato tubers. Mol. Plant-Microbe Interact. 15: 102– 108.
29. Foroozan, R.,, R. C. Eagle,, Jr., and, E. J. Cohen. 2000. Fungal keratitis in a soft contact lens wearer. CLAO J. 26: 166– 168.
30. Gajdusek, D. C. 1953. Acute infectious hemorrhagic fevers and mycotoxicosis in the Union of Soviet Socialist Republics, p. 82–106. In Medical Science Publication no. 2. Walter Reed Army Medical Center, Washington, DC.
31. Gale, L. R.,, J. D. Bryant,, S. Calvo,, H. Giese,, T. Katan,, K. O’Donnell,, H. Suga,, M. Taga,, T. R. Usgaard,, T. J. Ward, and, H. C. Kistler. 2005. Chromosome complement of the fungal plant pathogen Fusarium graminearum based on genetic and physical mapping and cytological observations. Genetics 171: 985– 1001.
32. Garcia-Maceira, F. I.,, A. di Pietro,, M. D. Huertas-Gonzalez,, M. C. Ruiz-Roldan, and, M. I. G. Roncero. 2001. Molecular characterization of an endopolygalacturonase from Fusarium oxysporum expressed during early stages of infection. Appl. Environ. Microbiol. 67: 2191– 2196.
33. Garvey, G. C.,, S. P. McCormick, and, I. Rayment. 2008. Structural and functional characterization of the TRI101 trichothecene 3-O-acetyltransferase from Fusarium sporotrichioides and Fusarium graminearum: kinetic insights to combating Fusarium head blight. J. Biol. Chem. 283: 1660– 1669.
34. Glenn, A. E.,, N. C. Zitomer,, A. M. Zimeri,, L. D. Williams,, R. T. Riley, and, R. H. Proctor. 2008. Transformation-mediated complementation of a FUM gene cluster deletion in Fusarium verticillioides restores both fumonisin production and pathogenicity on maize seedlings. Mol. Plant-Microbe Interact. 21: 87– 97.
35. Gomez-Gomez, E.,, M. C. Ruiz-Roldan,, A. di Pietro,, M. I. G. Roncero, and, C. Hera. 2002. Role in pathogenesis of two endo-β-1,4-xylanase genes from the vascular wilt fungus Fusarium oxysporum. Fungal Genet. Biol. 35: 213– 222.
36. Graebe, J. E. 1987. Gibberellin biosynthesis and control. Annu. Rev. Plant Physiol. 38: 419– 465.
37. Greenshields, D. L.,, G. S. Liu,, J. Feng,, G. Selvaraj, and, Y. D. Wei. 2007. The siderophore biosynthetic gene SID1, but not the ferroxidase gene FET3, is required for full Fusarium graminearum virulence. Mol. Plant Pathol. 8: 411– 421.
38. Guarro, J.,, M. Nucci,, T. Akiti, and, J. Gene. 2000. Mixed infection caused by two species of Fusarium in a human immunodeficiency virus-positive patient. J. Clin. Microbiol. 38: 3460– 3462.
39. Han, Y.,, X. Liu,, U. Benny,, H. C. Kistler, and, H. D. VanEtten. 2001. Genes determining pathogenicity to pea are clustered on a supernumerary chromosome in the fungal plant pathogen Nectria haematococca. Plant J. 25: 305– 314.
40. Han, Y. K.,, M. D. Kim,, S.-H. Lee,, S.-H. Yun, and, Y.-W. Lee. 2007. A novel F-box protein involved in sexual development and pathogenesis in Gibberella zeae. Mol. Microbiol. 63: 768– 779.
41. Harris, L. J.,, A. E. Desjardins,, R. D. Plattner,, P. Nicholson,, G. Butler,, J. C. Young,, G. Weston,, R. H. Proctor, and, T. M. Hohn. 1999. Possible role of trichothecene mycotoxins in virulence of Fusarium graminearum on maize. Plant Dis. 83: 954– 960.
42. Hemo, I.,, J. Pe’Er, and, I. Polacheck. 1989. Fusarium oxysporum keratitis. Ophthalmologica 198: 3– 7.
43. Herrmann, M.,, R. Zocher, and, A. Haese. 1996. Effect of disruption of the enniatin synthetase gene on the virulence of Fusarium avenaceum. Mol. Plant-Microbe Interact. 9: 226– 232.
44. Hornok, L.,, C. Waalwijk, and, J. F. Leslie. 2007. Genetic factors affecting sexual reproduction in toxigenic Fusarium species. Int. J. Food Microbiol. 119: 54– 58.
45. Hou, Z.,, C. Xue,, Y. Peng,, T. Katan,, H. C. Kistler, and, J.-R. Xu. 2002. A mitogen-activated protein kinase gene ( MGV1) in Fusarium graminearum is required for female fertility, heterokaryon formation, and plant infection. Mol. Plant-Microbe Interact. 15: 1119– 1127.
46. Houterman, P. M.,, B. J. C. Cornelissen, and, M. Rep. 2008. Suppression of plant resistance gene-based immunity by a fungal effector. PLoS Pathog. 4(5): e1000061.
47. Hsieh, W. H.,, S. N. Smith, and, W. C. Snyder. 1977. Mating groups in Fusarium moniliforme. Phytopathology 67: 1041– 1043.
48. Imazaki, I.,, M. Kurahashi,, Y. Iida, and, T. Tsuge. 2007. Fow2, a Zn(II) 2Cys 6-type transcription regulator, controls plant infection of the vascular wilt fungus Fusarium oxysporum. Mol. Microbiol. 63: 737– 753.
49. Inoue, I.,, F. Namiki, and, T. Tsuge. 2002. Plant colonization by the vascular wilt fungus Fusarium oxysporum requires FOW1, a gene encoding a mitochondrial protein. Plant Cell 14: 1869– 1883.
50. Jain, S.,, K. Akiyama,, K. Mae,, T. Ohguchi, and, R. Takata. 2002. Targeted disruption of a G protein α subunit gene results in reduced pathogenicity in Fusarium oxysporum. Curr. Genet. 41: 407– 413.
51. Jain, S.,, K. Akiyama,, T. Kan,, T. Ohguchi, and, R. Takata. 2003. The G protein β subunit FGB1 regulates development and pathogenicity in Fusarium oxysporum. Curr. Genet. 43: 79– 86.
52. Jain, S.,, K. Akiyama,, R. Takata, and, T. Ohguchi. 2005. Signaling via the G protein α-subunit FGA2 is necessary for pathogenesis in Fusarium oxysporum. FEMS Microbiol. Lett. 243: 165– 172.
53. Jenczmionka, N. J.,, F. J. Maier.,, A. P. Losch, and, W. Schafer. 2003. Mating, conidiation and pathogenicity of Fusarium graminearum, the main causal agent of the head-blight disease of wheat, are regulated by the MAP kinase gpmk1. Curr. Genet. 43: 87– 95.
54. Jennings, J. C.,, P. C. Apel-Birkhold,, N. M. Mock,, C. J. Baker,, J. D. Anderson, and, B. A. Bailey. 2001. Induction of defense responses in tobacco by the protein Nep1 from Fusarium oxysporum. Plant Sci. 161: 891– 899.
55. Joffe, A. Z. 1983. Environmental conditions conducive to Fusarium toxin formation causing serious outbreaks in animals and man. Vet. Res. Commun. 7: 187– 193.
56. Jurgenson, J. E.,, K. A. Zeller, and, J. F. Leslie. 2002a. An expanded genetic map of Gibberella moniliformis ( Fusarium verticillioides). Appl. Environ. Microbiol. 68: 1972– 1979.
57. Jurgenson, J. E.,, R. L. Bowden,, K. A. Zeller,, J. F. Leslie,, N. J. Alexander, and, R. D. Plattner. 2002b. A genetic map of Gibberella zeae ( Fusarium graminearum). Genetics 160: 1452– 1460.
58. Kathariou, S., and, P. T. Spieth. 1982. Spore killer polymorphism in Fusarium moniliforme. Genetics 102: 19– 24.
59. Kawabe, M.,, K. Mizutani,, T. Yoshida,, T. Teraoka,, K. Yoneyama,, I. Yamaguchi, and, T. Arie. 2004. Cloning of the pathogenicity-related gene FPD1 in Fusarium oxysporum f. sp. lycopersici. J. Gen. Plant Pathol. 70: 16– 20.
60. Kim, J.-E.,, K. Myong,, W.-B. Shim,, S.-H. Yun, and, Y.-W. Lee. 2007. Functional characterization of acetylglutamate synthase and phosphoribosylamine-glycine ligase genes in Gibberella zeae. Curr. Genet. 51: 99– 108.
61. Kistler, H. C. 2001. Evolution of host specificity in Fusarium oxysporum, p. 70–96. In B. A. Summerell,, J. F. Leslie,, D. Back-house,, W. L. Bryden, and, L. W. Burgess (ed.), Fusarium: Paul E. Nelson Memorial Symposium. APS Press, St. Paul, MN.
62. Klittich, C. J. R., and, J. F. Leslie. 1988. Nitrate reduction mutants of Fusarium moniliforme ( Gibberella fujikuroi). Genetics 118: 417– 423.
63. Lee, J.,, T. Lee,, Y.-W. Lee,, S.-H. Yun, and, B. G. Turgeon. 2003. Shifting fungal reproductive mode by manipulation of mating type genes: obligatory heterothallism of Gibberella zeae. Mol. Microbiol. 50: 145– 152.
64. Lee, J.,, J. E. Jurgenson,, J. F. Leslie, and, R. L. Bowden. 2008. Alignment of genetic and physical maps of Gibberella zeae. Appl. Environ. Microbiol. 74: 2349– 2359.
65. Leslie, J. F. 1991. Mating populations in Gibberella fujikuroi ( Fusarium section Liseola). Phytopathology 81: 1058– 1060.
66. Leslie, J. F. 1993. Fungal vegetative compatibility. Annu. Rev. Phytopathol. 31: 127– 151.
67. Leslie, J. F., and, R. L. Bowden. 2008. Fusarium graminearum: when species concepts collide. Cereal Res. Commun. 36(Suppl. B): 609– 615.
68. Leslie, J. F., and, K. K. Klein. 1996. Female fertility and mating-type effects on effective population size and evolution in filamentous fungi. Genetics 144: 557– 567.
69. Leslie, J. F., and, B. A. Summerell. 2006. The Fusarium Laboratory Manual. Blackwell Professional, Ames, IA.
70. Leslie, J. F.,, K. A. Zeller,, M. Wohler, and, B. A. Summerell. 2004. Interfertility of two mating populations in the Gibberella fujikuroi species complex. Eur. J. Plant Pathol. 110: 610– 618.
71. Leu, H. S.,, A. Y. S. Lee, and, T. T. Kuo. 1995. Recurrence of Fusarium solani abscess formation in an otherwise healthy patient. Infection 23: 303– 305.
72. Link, H. F. 1809. Observationes in ordines plantarum naturales, Dissertatio I. Mag. Ges. Naturf. Freunde Berlin 3: 3– 42.
73. Lu, S. W.,, B. G. Turgeon, and, O. C. Yoder. 2001. Cochliobolus heterostrophus and Fusarium graminearum: evidence for a common virulence factor. Phytopathology 91: S56.
74. Madrid, M. P.,, A. di Pietro, and, M. I. G. Roncero. 2003. Class V chitin synthase determines pathogenesis in the vascular wilt fungus Fusarium oxysporum and mediates resistance to plant defence compounds. Mol. Microbiol. 47: 257– 266.
75. Maier, F. J.,, T. Miedaner,, B. Hadeler,, A. Felk,, S. Salomon,, M. Lemmens,, H. Kassner, and, W. Schafer. 2006. Involvement of trichothecenes in fusarioses of wheat, barley and maize evaluated by gene disruption of the trichodiene synthase ( Tri5) gene in three field isolates of different chemo-type and virulence. Mol. Plant Pathol. 7: 449– 461.
76. Martinez-Rocha, A. L.,, M. I. G. Roncero,, A. Lopez-Ramirez,, M. Marine,, J. Guarro,, G. Martinez-Cadena, and, A. di Pietro. 2008. Rho1 has distinct functions in morphogenesis, cell wall biosynthesis and virulence of Fusarium oxysporum. Cell. Microbiol. 10: 1339– 1351.
77. Martín-Udíroz, M.,, M. P. Madrid, and, M. I. G. Roncero. 2004. Role of chitin synthase genes in Fusarium oxysporum. Microbiology 150: 3175– 3187.
78. Martín-Urdíroz, M.,, M. I. G. Roncero,, J. A. Gonzalez-Reyes, and, C. Ruiz-Roldan. 2008. ChsVb, a class VII chitin synthase involved in septation, is critical for pathogenicity in Fusarium oxysporum. Eukaryot. Cell 7: 112– 121.
79. Matuo, T., and, W. C. Snyder. 1973. Use of morphology and mating populations in the identification of special forms in Fusarium solani. Phytopathology 63: 562– 565.
80. Miao, V. P.,, S. F. Covert, and, H. D. VanEtten. 1991. A fungal gene for antibiotic resistance in a dispensable (“B”) chromosome. Science 254: 1773– 1776.
81. Mselle, J. 1999. Fungal keratitis as an indicator of HIV infection in Africa. Trop. Doctor 29: 133– 135.
82. Munkvold, G. P. 2003. Cultural and genetic approaches to managing mycotoxins in maize. Annu. Rev. Phytopathol. 41: 99– 116.
83. Munkvold, G. P.,, R. L. Hellmich, and, L. G. Rice. 1999. Comparison of fumonisin concentrations in kernels of transgenic Bt maize hybrids and nontransgenic hybrids. Plant Dis. 83: 130– 138.
84. Namiki, F.,, M. Matsunaga,, M. Okuda,, I. Inoue.,, K. Nishi,, Y. Fujita, and, T. Tsuge. 2001. Mutation of an arginine biosynthesis gene causes reduced pathogenicity in Fusarium oxysporum f. sp. melonis. Mol. Plant-Microbe Interact. 14: 580– 584.
85. Nirenberg, H. I., and, K. O’Donnell. 1998. New Fusarium species and combinations within the Gibberella fujikuroi species complex. Mycologia 90: 434– 458.
86. Ochiai, N.,, T. Tokai,, T. Nishiuchi,, N. Takahashi-Ando,, M. Fujimura, and, M. Kimura. 2007. Involvement of the osmosensor histidine kinase and osmotic stress-activated protein kinases in the regulation of secondary metabolism in Fusarium graminearum. Biochem. Biophys. Res. Comm. 363: 639– 644.
87. O’Donnell, K.,, T. J. Ward,, D. M. Geiser,, H. C. Kistler, and, T. Aoki. 2004. Genealogical concordance between the mating type locus and seven other nuclear genes supports formal recognition of nine phylogenetically distinct species within the Fusarium graminearum clade. Fungal Genet. Biol. 41: 600– 623.
88. Oide, S.,, W. Moeder,, S. Krasnoff,, D. Gibson,, H. Haas,, K. Yoshioka, and, B. G. Turgeon. 2006. NPS6, encoding a nonribosomal peptide synthetase involved in siderophore-mediated iron metabolism, is a conserved virulence determinant of plant pathogenic ascomycetes. Plant Cell 18: 2836– 2853.
89. Okubara, P. A.,, A. E. Blechl,, S. P. McCormick,, N. J. Alexander,, R. Dill-Macky, and, T. M. Hohn. 2002. Engineering deoxynivalenol metabolism in wheat through the expression of a fungal trichothecene acetyltransferase gene. Theor. Appl. Genet. 106: 74– 83.
90. Ospina-Giraldo, M. D.,, E. Mullins, and, S. Kang. 2003. Loss of function of the Fusarium oxysporum SNF1 gene reduces virulence on cabbage and Arabidopsis. Curr. Genet. 44: 49– 57.
91. Pagliarusco, A.,, L. Tomazzoli,, G. Amalfitano,, L. Polonelli, and, L. Bonomi. 1995. Mycotic keratitis by Fusarium moniliforme. Acta Ophthalmol. Scand. 73: 560– 562.
92. Pareja-Jaime, Y.,, M. I. G. Roncero, and, M. C. Ruiz-Roldan. 2008. Tomatinase from Fusarium oxysporum f. sp. lycopersici is required for full virulence on tomato plants. Mol. Plant-Microbe Interact. 21: 728– 736.
93. Poppenberger, B.,, F. Berthiller,, H. Bachmann,, D. Lucyshyn,, C. Peterbauer,, R. Mitterbauer,, R. Schuhmacher,, R. Krska,, J. Glössl, and, G. Adam. 2006. Heterologous expression of Arabidopsis UDP-glucosyltransferases in Saccharomyces cerevisiae for production of zearalenone-4- O-glucoside. Appl. Environ. Microbiol. 72: 4404– 4410.
94. Prados-Rosales, R. C.,, C. Serena,, J. Delgado-Jarana,, J. Guarro, and, A. di Pietro. 2006. Distinct signaling pathways coordinately contribute to virulence of Fusarium oxysporum on mammalian hosts. Microbes Infect. 8: 2825– 2831.
95. Proctor, R. H.,, T. M. Hohn, and, S. P. McCormick. 1995. Reduced virulence of Gibberella zeae caused by disruption of a trichothecene toxin biosynthetic gene. Mol. Plant-Microbe Interact. 8: 593– 601.
96. Proctor, R. H.,, A. E. Desjardins,, S. P. McCormick,, R. D. Plattner,, N. J. Alexander, and, D. W. Brown. 2002. Genetic analysis of the role of trichothecene and fumonisin mycotoxins in the virulence of Fusarium. Eur. J. Plant Pathol. 108: 691– 698.
97. Puhalla, J. E. 1984. A visual indicator of heterokaryosis in Fusarium oxysporum f. sp. apii from celery. Can. J. Bot. 62: 540– 545.
98. Puhalla, J. E. 1985. Classification of Fusarium oxysporum on the basis of vegetative compatibility. Can. J. Bot. 63: 179– 183.
99. Puhalla, J. E., and, P. T. Spieth. 1983. Heterokaryosis in Fusarium moniliforme. Exp. Mycol. 7: 328– 335.
100. Puhalla, J. E., and, P. T. Spieth. 1985. A comparison of heterokaryosis and vegetative incompatibility among varieties of Gibberella fujikuroi ( Fusarium moniliforme). Exp. Mycol. 9: 39– 47.
101. Raju, N. B. 1994. Ascomycete spore killers: chromosomal elements that distort genetic ratios among the products of meiosis. Mycologia 86: 461– 473.
102. Rep, M.,, H. C. van der Does,, M. Meijer,, R. van Wijk,, P. M. Houterman,, H. L. Dekker,, C. G. de Koster, and, B. J. C. Cornelissen. 2004. A small, cysteine-rich protein secreted by Fusarium oxysporum during colonization of xylem vessels is required for I-3-mediated resistance in tomato. Mol. Microbiol. 53: 1373– 1383.
103. Rogers, L. M.,, M. A. Flaishman, and, P. E. Kolattukudy. 1994. Cutinase gene disruption in Fusarium solani f. sp. pisi decreases its virulence on pea. Plant Cell 6: 935– 945.
104. Roncero, M. I. G.,, C. Hera,, M. Ruiz-Rubio,, F. I. G. Maceira,, M. P. Madrid,, Z. Caracuel,, F. Calero,, J. Delgado-Jarana,, R. Roldan-Rodriguez.,, A. L. Martinez-Rocha,, C. Velasco,, J. Roa,, M. Martin-Urdiroz,, D. Cordoba, and, A. di Pietro. 2003. Fusarium as a model for studying virulence in soilborne plant pathogens. Physiol. Mol. Plant Pathol. 62: 87– 98.
105. Rosa, R. H.,, Jr.,, D. Miller, and, E. C. Alfonso. 1994. The changing spectrum of fungal keratitis in South Florida. Ophthalmology 101: 1005– 1013.
106. Sagaram, U. S., and, W.-B. Shim. 2007. Fusarium verticillioides GBB1, a gene encoding heterotrimeric G protein β subunit, is associated with fumonisin B 1 biosynthesis and hyphal development but not with fungal virulence. Mol. Plant Pathol. 8: 375– 384.
107. Schmale, D. G.,, J. F. Leslie,, K. A. Zeller,, A. A. Saleh,, E. J. Shields, and, G. C. Bergstrom. 2006. Genetic structure of atmospheric populations of Gibberella zeae. Phytopathology 96: 1021– 1026.
108. Schoental, R. 1994. Mycotoxins in food and the plague of Athens. J. Nutr. Med. 4: 83– 85.
109. Seo, B. W.,, H. K. Kim,, Y.-W. Lee, and, S.-H. Yun. 2007. Functional analysis of a histidine auxotrophic mutation in Gibberella zeae. Plant Pathol. J. 23: 51– 56.
110. Seong, K.,, Z. M. Hou,, M. Tracy,, H. C. Kistler, and, J.-R. Xu. 2005. Random insertional mutagenesis identifies genes associated with virulence in the wheat scab fungus Fusarium graminearum. Phytopathology 95: 744– 750.
111. Seong, K.,, L. Li,, Z. M. Hou,, M. Tracy,, H. C. Kistler, and, J.-R. Xu. 2006. Cryptic promoter activity in the coding region of the HMG-CoA reductase gene in Fusarium graminearum. Fungal Genet. Biol. 43: 34– 41.
112. Shim, W.-B.,, U. S. Sagaram,, Y.-E. Choi,, J. So,, H. H. Wilkinson, and, Y.-W. Lee. 2006. FSR1 is essential for virulence and female fertility in Fusarium verticillioides and F. graminearum. Mol. Plant-Microbe Interact. 19: 725– 733.
113. Skov, J.,, M. Lemmens, and, H. Giese. 2004. Role of a Fusarium culmorum ABC transporter ( FcABC1) during infection of wheat and barley. Physiol. Mol. Plant Pathol. 64: 245– 254.
114. Snyder, W. C., and, H. N. Hansen. 1940. The species concept in Fusarium. Am. J. Bot. 27: 64– 67.
115. Snyder, W. C., and, H. N. Hansen. 1941. The species concept in Fusarium with reference to section Martiella. Am. J. Bot. 28: 738– 742.
116. Snyder, W. C., and, H. N. Hansen. 1945. The species concept in Fusarium with reference to Discolor and other sections. Am. J. Bot. 32: 657– 666.
117. Snyder, W. C., and, H. N. Hansen. 1954. Variation and speciation in the genus Fusarium. Ann. N. Y. Acad. Sci. 60: 16– 23.
118. Spector, C., and, B. O. Phinney. 1968. Gibberellin biosynthesis genetic studies in Gibberella fujikuroi. Physiol. Plant. 21: 127– 136.
119. Stahl, D. J.,, A. Theuerkauf,, R. Heitefuss, and, W. Schafer. 1994. Cutinase of Nectria haematococca ( Fusarium solani f. sp. pisi) is not required for fungal virulence or organ specificity on pea. Mol. Plant-Microbe Interact. 7: 713– 725.
120. Sulyok, M.,, R. Krska, and, R. Schuhmacher. 2007. Application of liquid chromatography-tandem mass spectrometric method to multi-mycotoxin determination in raw cereals and evaluation of matrix effects. Food Addit. Contam. 24: 1184– 1195.
121. Temporini, E. D., and, H. D. VanEtten. 2004. An analysis of the phylogenetic distribution of the pea pathogenicity genes of Nectria haematococca MP VI supports the hypothesis of their origin by horizontal transfer and uncovers a potentially new pathogen of garden pea: Neocosmospora boniensis. Curr. Genet. 46: 29– 36.
122. Tobiasen, C.,, J. Aahman,, K. S. Ravnholt,, M. J. Bjerrum,, M. N. Grell, and, H. Giese. 2007. Nonribosomal peptide synthetase (NPS) genes in Fusarium graminearum, F. culmorum and F. pseudograminearium and identification of NPS2 as the producer of ferricrocin. Curr. Genet. 51: 43– 58.
123. Tomimori-Yamashita, J.,, M. M. Ogawa,, S. H. Hirata,, O. Fischman,, N. S. Michalany,, H. K. Yamashita, and, M. M. A. Alchorne. 2002. Mycetoma caused by Fusarium solani with osteolytic lesions on the hand: case report. Mycopathologia 153: 11– 14.
124. Urban, M.,, E. Mott,, T. Farley, and, K. Hammond-Kosack. 2003. The Fusarium graminearum MAP1 gene is essential for pathogenicity and development of perithecia. Mol. Plant Pathol. 4: 347– 359.
125. van der Does, H. C.,, B. Lievens,, L. Claes,, P. M. Houterman,, B. J. C. Cornelissen, and, M. Rep. 2008. The presence of a virulence locus discriminates Fusarium oxysporum isolates causing tomato wilt from other isolates. Environ. Microbiol. 10: 1475– 1485.
126. van Dijk, E.,, H. W. van den Berg, and, A. J. Landwehr. 1980. Fusarium solani infection of a hypertensive leg ulcer in a diabetic. Mykosen 23: 603– 606.
127. Voigt, C. A.,, W. Schafer, and, S. Salomon. 2005. A secreted lipase of Fusarium graminearum is a virulence factor required for infection of cereals. Plant J. 42: 364– 375.
128. Waalwijk, C.,, T. van der Lee,, I. de Vries,, T. Hesselink,, J. Arts, and, G. H. J. Kema. 2004. Synteny in toxigenic Fusarium species: the fumonisin gene cluster and the mating type region as examples. Eur. J. Plant Pathol. 110: 533– 544.
129. Wang, H.,, J. Li,, R. M. Bostock, and, D. G. Gilchrist. 1996. Apoptosis: a functional paradigm for programmed plant cell death induced by a host-selective phytotoxin and invoked during development. Plant Cell 8: 375– 391.
130. Wasmann, C. C., and, H. D. Van Etten. 1996. Transformation-mediated chromosome loss and disruption of a gene for pisatin demethylase decrease the virulence of Nectria haematococca on pea. Mol. Plant-Microbe Interact. 9: 793– 803.
131. Windels, C. E.,, P. M. Barnes, and, T. Kommedahl. 1988. Five-year preservation of Fusarium species on silica gel and soil. Phytopathology 78: 107– 109.
132. Windels, C. E.,, P. M. Barnes, and, T. Kommedahl. 1993. Fusarium species stored for silica gel and soil for ten years. Mycologia 85: 21– 23.
133. Wollenweber, H. W., and, O. A. Reinking. 1935. Die Fusarien, ihre Beschreibung, Schadwirkung und Bekampfung. Verlag Paul Parey, Berlin, Germany.
134. Xu, J.-R., and, J. F. Leslie. 1996. A genetic map of Fusarium moniliforme ( Gibberella fujikuroi mating population A). Genetics 143: 175– 189.
135. Xu, J.-R.,, K. Yan,, M. B. Dickman, and, J. F. Leslie. 1995. Electrophoretic karyotypes distinguish the biological species of Gibberella fujikuroi ( Fusarium section Liseola). Mol. Plant-Microbe Interact. 8: 74– 84.
136. Yu, H. Y.,, J. A. Seo,, J. E. Kim,, K. H. Han,, W.-B. Shim,, S.-H. Yun, and, Y.-W. Lee. 2008. Functional analyses of heterotrimeric G protein Gα and Gβ subunits in Gibberella zeae. Microbiology 154: 392– 401.
137. Zeller, K. A.,, R. L. Bowden, and, J. F. Leslie. 2004. Population differentiation and recombination in wheat scab populations of Gibberella zeae in the United States. Mol. Ecol. 13: 563– 571.
138. Zhang, L.,, K. Yan,, Y. Zhang,, R. Huang,, J. Bian,, C. Zheng,, H. Sun,, Z. Chen,, N. Sun,, R. An,, F. Min,, W. Zhao,, Y. Zhuo,, J. You,, Y. Song,, Z. Yu,, Z. Liu,, K. Yang,, H. Gao,, H. Dai,, X. Zhang,, J. Wang,, C. Fu,, G. Pei,, J. Liu,, S. Zhang,, M. Goodfellow,, Y. Jiang,, J. Kuai,, G. Zhou, and, X. Chen. 2007. High-throughput synergy screening identifies microbial metabolites as combination agents for the treatment of fungal infections. Proc. Natl. Acad. Sci. USA 104: 4606– 4611.

Tables

Fusarium Genetics and Pathogenicity
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Citation: Leslie J, Xu J. 2010. Genetics and Pathogenicity, p 607-621. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch38
/content/10.1128/9781555816636.ch38.ch38tab01
TABLE 1
Genome characteristics of four sequenced species
Generic image for table
TABLE 1

Genome characteristics of four sequenced species

Citation: Leslie J, Xu J. 2010. Genetics and Pathogenicity, p 607-621. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch38
/content/10.1128/9781555816636.ch38.ch38tab02
TABLE 2
Some of the best-known secondary metabolites produced by spp.
Generic image for table
TABLE 2

Some of the best-known secondary metabolites produced by spp.

Citation: Leslie J, Xu J. 2010. Genetics and Pathogenicity, p 607-621. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch38
/content/10.1128/9781555816636.ch38.ch38tab03
TABLE 3
Some virulence factors characterized in species
Generic image for table
TABLE 3

Some virulence factors characterized in species

Citation: Leslie J, Xu J. 2010. Genetics and Pathogenicity, p 607-621. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch38

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