Host-induced aneuploidy and phenotypic diversification in the Sudden Oak Death pathogen Phytophthora ramorum

BMC Genomics

Volumn 17, Issue 1, 2016, Pages

  Kasuga, Takao ^a   Bui, Mai ^a   Bernhardt, Elizabeth ^b   Swiecki, Tedmund ^b   Aram, Kamyar ^c   Cano, Liliana M ^d   Webber, Joan ^e   Brasier, Clive ^e   Press, Caroline ^f   Grünwald, Niklaus J ^f   Rizzo, David M ^c   Garbelotto, Matteo ^g  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b Phytosphere Research   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF FLORIDA   (United States)

^e FOREST RESEARCH   (United Kingdom)

^f HORTICULTURAL CROPS RESEARCH LABORATORY   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Aneuploidy; Invasive pathogens; Loss of heterozygosity; Transposable elements

Indexed keywords

MESSENGER RNA; TRANSCRIPTOME; TRANSPOSON;

ANEUPLOIDY; ARTICLE; CHAMAECYPARIS; CHAMAECYPARIS LAWSONIANA; CHROMOSOME BREAKAGE; CHROMOSOME REARRANGEMENT; CONTROLLED STUDY; COPY NUMBER VARIATION; FUNGAL GENOME; FUNGAL PLANT DISEASE; GROWTH ACCELERATION; GROWTH RATE; HETEROZYGOSITY LOSS; HIGH THROUGHPUT SEQUENCING; HOST INDUCED PHENOTYPIC DIVERSIFICATION; NONHUMAN; OAK; OOMYCETES; PHENOTYPIC VARIATION; PHYTOPHTHORA RAMORUM; PLANT FUNGUS INTERACTION; QUERCUS CHRYSOLEPIS; SUDDEN OAK DEATH; TRANSPOSON; UMBELLULARIA CALIFORNICA; CALIFORNIA; GENE DUPLICATION; GENE EXPRESSION PROFILING; GENETIC LINKAGE; GENETICS; GENOTYPE; MICROBIOLOGY; PHENOTYPE; PHYTOPHTHORA; PLANT DISEASE; SINGLE NUCLEOTIDE POLYMORPHISM;

ANEUPLOIDY; CALIFORNIA; DNA COPY NUMBER VARIATIONS; DNA TRANSPOSABLE ELEMENTS; GENE DUPLICATION; GENE EXPRESSION PROFILING; GENETIC LINKAGE; GENOTYPE; LOSS OF HETEROZYGOSITY; PHENOTYPE; PHYTOPHTHORA; PLANT DISEASES; POLYMORPHISM, SINGLE NUCLEOTIDE; QUERCUS; TRANSCRIPTOME;

EID: 84974633040     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-016-2717-z     Document Type: Article

References (82)

1. Davis M. Invasion biology. New York: Oxford University Press; 2009.
2. Brasier CM. Episodic selection as a force in fungal microevolution, with special reference to clonal speciation and hybrid introgression. Can J Bot. 1995;73:S1213-21.
3. Rando OJ, Verstrepen KJ. Timescales of genetic and epigenetic inheritance. Cell. 2007;128(4):655-68.
4. Goodwin SB, Sujkowski LS, Fry WE. Rapid evolution of pathogenicity within clonal lineages of the potato late blight disease fungus. Phytopathology. 1995;85(6):669-76.
5. Hüberli D, Tommerup IC, Dobrowolski MP, Calver MC, Hardy GESJ. Phenotypic variation in a clonal lineage of two Phytophthora cinnamomi populations from Western Australia. Mycol Res. 2001;105:1053-64.
6. Farrer RA, Henk DA, Garner TW, Balloux F, Woodhams DC, Fisher MC. Chromosomal copy number variation, selection and uneven rates of recombination reveal cryptic genome diversity linked to pathogenicity. PLoS Genet. 2013;9(8):e1003703.
7. Selmecki A, Forche A, Berman J. Aneuploidy and isochromosome formation in drug-resistant Candida albicans. Science. 2006;313(5785):367-70.
8. Rancati G, Pavelka N, Fleharty B, Noll A, Trimble R, Walton K, Perera A, Staehling-Hampton K, Seidel CW, Li R. Aneuploidy underlies rapid adaptive evolution of yeast cells deprived of a conserved cytokinesis motor. Cell. 2008;135(5):879-93.
9. Kwon-Chung KJ, Chang YC. Aneuploidy and drug resistance in pathogenic fungi. PLoS Pathog. 2012;8(11):e1003022.
10. Rizzo DM, Garbelotto M, Davidson JM, Slaughter GW, Koike ST. Phytophthora ramorum as the cause of extensive mortality of Quercus spp. and Lithocarpus densiflorus in California. Plant Dis. 2002;86(3):205-14.
11. Brasier C, Webber J. Plant pathology sudden larch death. Nature. 2010;466(7308):824-5.
12. Werres S, Marwitz R, Veld WAMI, De Cock AWAM, Bonants PJM, De Weerdt M, Themann K, Ilieva E, Baayen RP. Phytophthora ramorum sp nov., a new pathogen on Rhododendron and Viburnum. Mycol Res. 2001;105:1155-65.
13. Parke JL, Linderman RG, Osterbauer NK, Griesbach JA. Detection of Phytophthora ramorum blight in Oregon nurseries and completion of Koch's postulates on Pieris, Rhododendron, Viburnum and Camellia. Plant Dis. 2004;88(1):87.
14. Goss EM, Carbone I, Grünwald NJ. Ancient isolation and independent evolution of the three clonal lineages of the exotic sudden oak death pathogen Phytophthora ramorum. Mol Ecol. 2009;18(6):1161-74.
15. Ivors K, Garbelotto M, Vries IDE, Ruyter-Spira C, Hekkert BT, Rosenzweig N, Bonants P. Microsatellite markers identify three lineages of Phytophthora ramorum in US nurseries, yet single lineages in US forest and European nursery populations. Mol Ecol. 2006;15(6):1493-505.
16. Grünwald NJ, Goss EM, Press CM. Phytophthora ramorum: a pathogen with a remarkably wide host range causing sudden oak death on oaks and ramorum blight on woody ornamentals. Mol Plant Pathol. 2008;9(6):729-40.
17. Van Poucke K, Franceschini S, Webber JF, Vercauteren A, Turner JA, Mccracken AR, Heungens K, Brasier CM. Discovery of a fourth evolutionary lineage of Phytophthora ramorum: EU2. Fungal Biol. 2012;116(11):1178-91.
18. Grünwald NJ, Goss EM, Ivors K, Garbelotto M, Martin FN, Prospero S, Hansen E, Bonants PJM, Hamelin RC, Chastagner G et al: Standardizing the nomenclature for clonal lineages of the sudden oak death pathogen, Phytophthora ramorum. Phytopathology. 2009;99(7):792-5.
19. Brasier C, Kirk S, Rose J. Differences in phenotypic stability and adaptive variation between the main European and American lineages of Phytophthora ramorum. In: 3rd Int IUFRO Work: 2006; Friesing, Germany. Farnham: Forest Research; 2006. p. 166-73.
20. Elliott M, Sumampong G, Varga A, Shamoun SF, James D, Masri S, Grünwald NJ: Phenotypic differences among three clonal lineages of Phytophthora ramorum. For Pathol. 2011;41(1):7-14.
21. Kasuga T, Kozanitas M, Bui M, Hüberli D, Rizzo DM, Garbelotto M. Phenotypic diversification is associated with host-induced transposon derepression in the Sudden Oak Death pathogen Phytophthora ramorum. PLoS One. 2012;7(4):e34728.
22. Davidson JM, Wickland AC, Patterson HA, Falk KR, Rizzo DM. Transmission of Phytophthora ramorum in mixed-evergreen forest in California. Phytopathology. 2005;95(5):587-96.
23. Swiecki TJ, Bernhardt E. Evaluation of stem water potential and other tree and stand variables as risk factors for Phytophthora ramorum canker development in coast live oak. In: Proceedings in 5th Oak Symposium: Oaks in California's Changing Landscape: 2001. San Diego: USDA Forest Service; 2001. p. 787-9.
24. Callahan ME, Switzer WM, Matthews AL, Roberts BD, Heneine W, Folks TM, Sandstrom PA: Persistent zoonotic infection of a human with simian foamy virus in the absence of an intact orf-2 accessory gene. J Virol. 1999;73(11):9619-24.
25. O'Fallon B. Population structure, levels of selection, and the evolution of intracellular symbionts. Evolution. 2008;62(2):361-73.
26. Swiecki TJ, Bernhardt E, Aram K, Rizzo MD, Kasuga T, Bui M. Phytophthora ramorum causes cryptic bole cankers in canyon live oak. Plant Health Prog. 2016;17(1):20-6.
27. Sionov E, Lee H, Chang YC, Kwon-Chung KJ. Cryptococcus neoformans overcomes stress of azole drugs by formation of disomy in specific multiple chromosomes. PLoS Pathog. 2010;6(4):e1000848.
28. Xi R, Hadjipanayis AG, Luquette LJ, Kim TM, Lee E, Zhang J, Johnson MD, Muzny DM, Wheeler DA, Gibbs RA et al: Copy number variation detection in whole-genome sequencing data using the Bayesian information criterion. Proc Natl Acad Sci U S A. 2011;108(46):E1128-36.
29. Tyler BM, Tripathy S, Zhang XM, Dehal P, Jiang RHY, Aerts A, Arredondo FD, Baxter L, Bensasson D, Beynon JL et al: Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science. 2006;313(5791):1261-6.
30. Sansome E, Brasier CM, Griffin MJ. Chromosome size differences in Phytophthora palmivora, a pathogen of cocoa. Nature. 1975;255(5511):704-5.
31. Sansome S, Brasier CM. Diploidy and chromosomal structural hybridity in Phytophthora infestans. Nature. 1973;241:344-5.
32. Brasier CM, Sansome E. Diploidy and gametangial meiosis in Phytophthora cinnamomi, Phytophthora infestans and Phytophthora drechsleri. T Brit Mycol Soc. 1975;65:49-65.
33. Mannaert A, Downing T, Imamura H, Dujardin JC. Adaptive mechanisms in pathogens: universal aneuploidy in Leishmania. Trends Parasitol. 2012;28(9):370-6.
34. Brasier C, Webber JF. Natural stem infection of Lawson cypress (Chamaecyparis lawsoniana) caused by Phytophthora ramorum. New Dis Report. 2012;25:26.
35. Bartz SR, Rogel ME, Emerman M. Human immunodeficiency virus type 1 cell cycle control: Vpr is cytostatic and mediates G2 accumulation by a mechanism which differs from DNA damage checkpoint control. J Virol. 1996;70(4):2324-31.
36. Ben-Abdallah M, Sturny-Leclere A, Ave P, Louise A, Moyrand F, Weih F, Janbon G, Memet S: Fungal-induced cell cycle impairment, chromosome instability and apoptosis via differential activation of NF-kappaB. PLoS Pathog. 2012;8(3):e1002555.
37. Umeda M, Murata-Kamiya N, Saito Y, Ohba Y, Takahashi M, Hatakeyama M. Helicobacter pylori CagA causes mitotic impairment and induces chromosomal instability. J Biol Chem. 2009;284(33):22166-72.
38. Goodwin SB, Schneider RE, Fry WE. Use of Cellulose-Acetate Electrophoresis for Rapid Identification of Allozyme Genotypes of Phytophthora-Infestans. Plant Dis. 1995;79(11):1181-5.
39. Michelmore RW, Sansome ER. Cytological Studies of Heterothallism and Secondary Homothallism in Bremia-Lactucae. T Brit Mycol Soc. 1982;79(Oct):291-7.
40. Tyler BM, Forster H, Coffey MD. Inheritance of avirulence factors and restriction-fragment-length-polymorphism markers in outcrosses of the oomycete Phytophthora sojae. Mol Plant-Microbe Interact. 1995;8(4):515-23.
41. Mortimer AM, Shaw DS, Sansome ER. Genetical studies of secondary homothallism in Phytophthora drechsleri. Arch Microbiol. 1977;111(3):255-9.
42. Carter DA, Buck KW, Archer SA, Van der Lee T, Shattock RC, Shaw DS. The detection of nonhybrid, trisomic, and triploid offspring in sexual progeny of a mating of Phytophthora infestans. Fungal Genet Biol. 1999;26(3):198-208.
43. Vercauteren A, Boutet X, D'hondt L, Van Bockstaele E, Maes M, Leus L, Chandelier A, Heungens K: Aberrant genome size and instability of Phytophthora ramorum progenies. Fungal Genet Biol. 2011;48(5):537-43.
44. Lamour KH, Mudge J, Gobena D, Hurtado-Gonzales OP, Schmutz J, Kuo A, Miller NA, Rice BJ, Raffaele S, Cano LM et al. Genome sequencing and mapping reveal loss of heterozygosity as a mechanism for rapid adaptation in the vegetable pathogen Phytophthora capsici. Mol Plant Microbe Interact. 2012;25(10):1350-60.
45. Mantikou E, Wong KM, Repping S, Mastenbroek S. Molecular origin of mitotic aneuploidies in preimplantation embryos. Bba-Mol Basis Dis. 2012;1822(12):1921-30.
46. Arlt MF, Durkin SG, Ragland RL, Glover TW. Common fragile sites as targets for chromosome rearrangements. DNA Repair. 2006;5(9-10):1126-35.
47. Durkin SG, Glover TW. Chromosome fragile sites. Annu Rev Genet. 2007;41:169-92.
48. Selmecki AM, Maruvka YE, Richmond PA, Guillet M, Shoresh N, Sorenson AL, De S, Kishony R, Michor F, Dowell R et al: Polyploidy can drive rapid adaptation in yeast. Nature. 2015;519(7543):349-52.
49. Doring HP, Nelsen-Salz B, Garber R, Tillmann E. Double Ds elements are involved in specific chromosome breakage. Mol Gen Genet. 1989;219(1-2):299-305.
50. Ralston E, English J, Dooner HK. Chromosome-breaking structure in maize involving a fractured Ac element. Proc Natl Acad Sci U S A. 1989;86(23):9451-5.
51. St Charles J, Petes TD. High-resolution mapping of spontaneous mitotic recombination hotspots on the 1.1 Mb arm of yeast chromosome IV. PLoS Genet. 2013;9(4):e1003434.
52. Sansome E. Polyploidy and induced gametangial formation in British Isolates of Phytophthora infestans. J Gen Microbiol. 1977;99:311-6.
53. Catal M, King L, Tumbalam P, Wiriyajitsomboon P, Kirk WW, Adams GC. Heterokaryotic nuclear conditions and a heterogeneous nuclear population are observed by flow cytometry in Phytophthora infestans. Cytometry A. 2010;77(8):769-75.
54. Thorburn RR, Gonzalez C, Brar GA, Christen S, Carlile TM, Ingolia NT, Sauer U, Weissman JS, Amon A: Aneuploid yeast strains exhibit defects in cell growth and passage through START. Mol Biol Cell. 2013;24(9):1274-89.
55. Torres EM, Williams BR, Amon A. Aneuploidy: cells losing their balance. Genetics. 2008;179(2):737-46.
56. Gerstein AC, Kuzmin A, Otto SP. Loss-of-heterozygosity facilitates passage through Haldane's sieve for Saccharomyces cerevisiae undergoing adaptation. Nat Commun. 2014;5.
57. Sheltzer JM, Amon A. The aneuploidy paradox: costs and benefits of an incorrect karyotype. Trends Genet. 2011;27(11):446-53.
58. Brasier C. The rise of the hybrid fungi. Nature. 2000;405(6783):134-5.
59. Swiecki TJ, Bernhardt E. Long-term trends in coast live oak and tanoak stands affected by Phytophthora ramorum canker (sudden oak death). In: Sudden Oak Death Fourth Science Symposium: 2010. Albany: USDA Forest Service; 2010. p. 207-9.
60. Nagle AM, McPherson BA, Wood DL, Bonello P, Garbelotto M. Does phloem phenolic chemistry contribute to coast live oak resistance to Phytophthora ramorum? Phytopathology. 2009;99(6):S92.
61. Nagle AM, McPherson BA, Wood DL, Garbelotto M, Bonello P. Relationship between field resistance to Phytophthora ramorum and constitutive phenolic chemistry of coast live oak. For Pathol 2011. 10.1111/j.1439-0329.2010.00703.x.
62. Du TC, Shupe TF, Hse CY. Antifungal activities of three supercritical fluid extracted cedar oils. Holzforschung. 2011;65(2):277-84.
63. Pala-Paul J, Usano-Alemany J, Granda E, Soria AC. Antifungal and antibacterial activity of the essential oil of Chamaecyparis lawsoniana from Spain. Nat Prod Commun. 2012;7(10):1383-6.
64. Sansome E, Harris BJ. Use of camphor-induced polyploidy to determine place of meiosis in fungi. Nature. 1962;196(4851):291-2.
65. English AC, Richards S, Han Y, Wang M, Vee V, Qu J, Qin X, Muzny DM, Reid JG, Worley KC et al: Mind the gap: upgrading genomes with Pacific Biosciences RS long-read sequencing technology. PLoS One. 2012;7(11):e47768.
66. Kim J, Larkin DM, Cai Q, Asan, Zhang Y, Ge RL, Auvil L, Capitanu B, Zhang G, Lewin HA et al: Reference-assisted chromosome assembly. Proc Natl Acad Sci U S A. 2013;110(5):1785-90.
67. Englander L, Roth LF. Interaction of light and sterol on sporangium and chlamydospore production by Phytophthora lateralis. Phytopathology. 1980;70(7):650-4.
68. Tsao PH, Ocana G. Selective isolation of species of Phytophthora from natural soils on an improved antibiotic medium. Nature. 1969;223(5206):636-8.
69. McCluskey K, Wiest A, Plamann M. The Fungal Genetics Stock Center: a repository for 50 years of fungal genetics research. J Biosci. 2010;35(1):119-26.
70. Kasuga T, Bui M. Evaluation of automated cell disruptor methods for oomycetous and ascomycetous model organisms. Fungal Genet Report. 2011;58:4-13.
71. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP: Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003;4(2):249-64.
72. Brazma A, Hingamp P, Quackenbush J, Sherlock G, Spellman P, Stoeckert C, Aach J, Ansorge W, Ball CA, Causton HC et al: Minimum information about a microarray experiment (MIAME) - toward standards for microarray data. Nat Genet. 2001;29(4):365-71.
73. Isolation of genomic DNA from plants and filamentous fungi using the QIAGEN® Genomic-tip. [ http://www.qiagen.com/resources/resourcedetail?id=cb2ac658-8d66-43f0-968e-7bb0ea2c402a&lang=en ]
74. Champouret N, Kamoun S. An improved protocol for the protoplast method of stable DNA transformation of Phytophthora infestans. 2004.
75. Judelson HS, Tyler BM, Michelmore RW. Transformation of the oomycete pathogen, Phytophthora infestans. Mol Plant Microbe Interact. 1991;4(6):602-7.
76. Buffalo V. Scythe - A Bayesian adapter trimmer In: version 0.993 BETA edn. 2011.
77. Joshi NA, Fass JN. Sickle: A sliding-window, adaptive, quality-based trimming tool for FastQ files In: Version 1.29 edn. 2011.
78. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25(14):1754-60.
79. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R: The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25(16):2078-9.
80. Li H. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics. 2011;27(21):2987-93.
81. Thorvaldsdottir H, Robinson JT, Mesirov JP. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform. 2013;14(2):178-92.
82. Tripathy S, Deo T, Tyler BM. Oomycete Transcriptomics Database: a resource for oomycete transcriptomes. BMC Genomics. 2012;13:303.