High genome heterozygosity and endemic genetic recombination in the wheat stripe rust fungus

Nature Communications

Volumn 4, Issue , 2013, Pages

  Zheng, Wenming ^a,b   Huang, Lili ^a   Huang, Jinqun ^c   Wang, Xiaojie ^a   Chen, Xianming ^d   Zhao, Jie ^a   Guo, Jun ^a   Zhuang, Hua ^a   Qiu, Chuangzhao ^c   Liu, Jie ^a   Liu, Huiquan ^a   Huang, Xueling ^a   Pei, Guoliang ^a   Zhan, Gangming ^a   Tang, Chunlei ^a   Cheng, Yulin ^a   Liu, Minjie ^a   Zhang, Jinshan ^a   Zhao, Zhongtao ^a   Zhang, Shijie ^a   Han, Qingmei ^a   Han, Dejun ^a   Zhang, Hongchang ^a   Zhao, Jing ^a   Gao, Xiaoning ^a   Wang, Jianfeng ^a   Ni, Peixiang ^c   Dong, Wei ^c   Yang, Linfeng ^c   Yang, Huanming ^c   Xu, Jin Rong ^e   Zhang, Gengyun ^c   Kang, Zhensheng ^a   more..

^a NORTHWEST A F UNIVERSITY   (China)

^b HENAN AGRICULTURAL UNIVERSITY   (China)

^c State Key Laboratory of Agricultural Genomics   (China)

^d WASHINGTON STATE UNIVERSITY   (United States)

^e PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DISEASE INCIDENCE; GENETIC ANALYSIS; GENETIC VARIATION; GENOME; HETEROZYGOSITY; PATHOGENICITY; PROTEIN; RECOMBINATION; RUST DISEASE; SEXUAL REPRODUCTION; WHEAT;

ARTICLE; DNA ISOLATION; EXON; EXPRESSED SEQUENCE TAG; FUNGAL GENOME; FUNGUS; FUSARIUM GRAMINEARUM; GENE EXPRESSION; GENETIC RECOMBINATION; GENETIC VARIABILITY; GENOME ANALYSIS; GENOME SIZE; HETEROZYGOSITY; INTRON; MAGNAPORTHE ORYZAE; NONHUMAN; PUCCINIA STRIIFORMIS; REPRODUCTION; RETROPOSON; SINGLE NUCLEOTIDE POLYMORPHISM; STRIPE RUST; UREDINIOSPORE; USTILAGO MAYDIS; VIRULENCE; WHEAT;

PUCCINIA STRIIFORMIS F. SP. TRITICI; TRITICUM AESTIVUM; UREDINALES;

BASIDIOMYCOTA; BIOLOGICAL EVOLUTION; GENOME, FUNGAL; HETEROZYGOTE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MOLECULAR SEQUENCE ANNOTATION; OPEN READING FRAMES; PHYLOGENY; PLANT DISEASES; POLYMORPHISM, SINGLE NUCLEOTIDE; RECOMBINATION, GENETIC; TRITICUM; VIRULENCE;

EID: 84889261375     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms3673     Document Type: Article

References (54)

1. Brown, J. K. M. & Hovmøller, M. S. Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297, 537-541 (2002). (Pubitemid 34815327)
2. Fisher, M. C. et al. Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186-194 (2012).
3. Kolmer, J. A. Tracking wheat rust on a continental scale. Curr. Opin. Plant Biol. 8, 441-449 (2005). (Pubitemid 40817389)
4. Milus, E. A., Kristensen, K. & Hovmøller, M. S. Evidence for increased aggressiveness in a recent widespread strain of Puccinia striiformis f. sp. tritici causing stripe rust of wheat. Phytopathology 99, 6 (2009).
5. Hovmøller, M. S., Walter, S. & Justesen, A. F. Escalating threat of wheat rusts. Science 329, 369 (2010).
6. Shan, W., Chen, S., Kang, Z., Wu, L. & Li, Z. Genetic diversity in Puccinia striiformis Westend. f.sp. tritici revealed by pathogen genome-specific repetitive sequence. Can. J. Bot. 76, 587-595 (1998). (Pubitemid 28428579)
7. Hovmøller, M. S., Sørensen, C. K., Walter, S. & Justesen, A. F. Diversity of Puccinia striiformis on cereals and grasses. Annu. Rev. Phytopathol. 49, 197-217 (2011).
8. Jin, Y., Szabo, L. J. & Carson, M. Century-old mystery of Puccinia striiformis life history solved with the identification of Berberis as an alternate host. Phytopathology 100, 432-435 (2010).
9. Zhao, J., Zhang, H.-C., Yao, J.-N., Huang, L.-L. & Kang, Z.-S. Confirmation of Berberis spp. as alternate hosts of Puccinia striiformis f. sp. tritici on wheat in China. Mycosystema 30, 895-900 (2011).
10. Webb, C. A. & Fellers, J. P. Cereal rust fungi genomics and the pursuit of virulence and avirulence factors. FEMS Microbiol. Lett. 264, 1-7 (2006). (Pubitemid 44511047)
11. Line, R. F. Stripe rust of wheat and barley in North America: a retrospective historical review 1. Annu. Rev. Phytopathol. 40, 75-118 (2002). (Pubitemid 35235576)
12. Duplessis, S. et al. Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc. Natl Acad. Sci. 108, 9166-9171 (2011).
13. Spanu, P. D. et al. Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330, 1543-1546 (2010).
14. Cantu, D. et al. Next generation sequencing provides rapid access to the genome of Puccinia striiformis f. sp. tritici, the causal agent of wheat stripe rust. PLoS One 6, e24230 (2011).
15. Wan, A., Liren, W., Jin, S & Wang, B. Wang Baotong Discovery and studies on CY32, a new race of Puccinia striiformis f. sp. tritici in China. Acta Phytophylacica Sinica 30, 6 (2003).
16. Li, R., Li, Y., Kristiansen, K. & Wang, J. SOAP: short oligonucleotide alignment program. Bioinformatics 24, 713-714 (2008). (Pubitemid 351321217)
17. Li, R. et al. De novo assembly of human genomes with massively parallel short read sequencing. Genome Res. 20, 265-272.
18. Denisov, G. et al. Consensus generation and variant detection by Celera Assembler. Bioinformatics 24, 1035-1040 (2008). (Pubitemid 351514052)
19. Harris, R. S. Improved Pairwise Alignment of Genomic DNA. PhD thesis, Pennsylvania State Univ (2007).
20. Li, R. et al. The sequence and de novo assembly of the giant panda genome. Nature 463, 311-317 (2010).
21. Parra, G., Bradnam, K. & Korf, I. CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23, 1061-1067 (2007). (Pubitemid 47050556)
22. Wang, J. et al. The diploid genome sequence of an Asian individual. Nature 456, 60-65 (2008).
23. Li, R. et al. SNP detection for massively parallel whole-genome resequencing. Genome Res. 19, 1124-1132 (2009).
24. Kamper, J. et al. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444, 97-101 (2006). (Pubitemid 44684763)
25. Alexeyenko, A., Tamas, I., Liu, G. & Sonnhammer, E. L. Automatic clustering of orthologs and inparalogs shared bymultiple proteomes. Bioinformatics 22, e9-e15 (2006).
26. Dyrløv, J. D., Nielsen, H., von Heijne, G. & Brunak, S. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340, 783-795 (2004). (Pubitemid 38829638)
27. Emanuelsson, O., Brunak, S., von Heijne, G. & Nielsen, H. Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2, 953-971 (2007). (Pubitemid 46745592)
28. Saunders, D. G. O. et al. Using hierarchical clustering of secreted protein families to classify and rank candidate effectors of rust fungi. PLoS One 7, e29847 (2012).
29. Dean, R. A. et al. The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434, 980-986 (2005). (Pubitemid 40586040)
30. Cuomo, C. A. et al. The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 317, 1400-1402 (2007). (Pubitemid 47417482)
31. Catanzariti, A. M., Dodds, P. N., Lawrence, G. J., Ayliffe, M. A. & Ellis, G. J. Haustorially-expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell 18, 243-256 (2006). (Pubitemid 43951327)
32. Kemen, E. et al. Identification of a protein from rust fungi transferred from haustoria into infected plant cells. Mol. Plant-Microbe Interact 18, 1130-1139 (2005). (Pubitemid 41484236)
33. Godfrey, D. et al. Powdery mildew fungal effector candidates share N-terminal Y/F/WxC-motif. BMC Genomics 11, 317 (2010).
34. Morgan, W. & Kamoun, S. RXLR effectors of plant pathogenic oomycetes. Curr. Opin. Microbiol. 10, 332-338 (2007). (Pubitemid 47404953)
35. Martin, F. et al. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452, 88-92 (2008). (Pubitemid 351355085)
36. Amselem, J. et al. Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet. 7, e1002230 (2011).
37. Kemen, E. & Jones, J. D. G. Obligate biotroph parasitism: can we link genomes to lifestyles? Trends Plant Sci. 17, 448-457 (2012).
38. Voegele, R. T., Struck, C., Hahn, M. & Mendgen, K. The role of haustoria in sugar supply during infection of broad bean by the rust fungus Uromyces fabae. Proc. Natl Acad. Sci. 98, 8133-8138 (2001). (Pubitemid 32642699)
39. Wahl, R., Wippel, K., Goos, S., Ka?mper, J. & Sauer, N. A novel high-affinity sucrose transporter is required for virulence of the plant pathogen Ustilago maydis. PLoS Biol. 8, e1000303 (2010).
40. Spanu, P. D. The genomics of obligate (and nonobligate) biotrophs. Annu. Rev. Phytopathol. 50, 91-109 (2012).
41. Struck, C., Ernst, M. & Hahn, M. Characterization of a developmentally regulated amino acid transporter (AAT1p) of the rust fungus Uromyces fabae. Mol. Plant Pathol. 3, 23-30 (2002). (Pubitemid 34161583)
42. Struck, C., Mueller, E., Martin, H. & Lohaus, G. The Uromyces fabae UfAAT3 gene encodes a general amino acid permease that prefers uptake of in planta scarce amino acids. Mol. Plant Pathol. 5, 183-189 (2004). (Pubitemid 38693396)
43. Hahn, M., Neef, U., Struck, C., Go?ttfert, M. & Mendgen, K. A putative amino acid transporter is specifically expressed in haustoria of the rust fungus Uromyces fabae. Mol. Plant Microbe Interact. 10, 438-445 (1997). (Pubitemid 27204366)
44. Chen, X., Penman, L., Wan, A. & Cheng, P. Virulence races of Puccinia striiformis f. sp. tritici in 2006 and 2007 and development of wheat stripe rust and distributions, dynamics, and evolutionary relationships of races from 2000 to 2007 in the United States. Can. J. Plant Pathol. 32, 315-333 (2010).
45. Wellings, C. R. Puccinia striiformis in Australia: a review of the incursion, evolution, and adaptation of stripe rust in the period 1979-2006. Aust. J. Agric. Res. 58, 567-575 (2007). (Pubitemid 47012076)
46. Ali, S., Leconte, M., Walker, A.-S., Enjalbert, J. & de Vallavieille-Pope, C. Reduction in the sex ability of worldwide clonal populations of Puccinia striiformis f.sp. tritici. Fungal Genet. Biol. 47, 828-838 (2010).
47. Chen, X. M. & Line, R.F. Inheritance of stripe rust resistance in wheat cultivars used to differentiate races of Puccinia striiformis in North America. Phytopathology 82, 633-637 (1992).
48. Kim, U.-J., Shizuya, H., de Jong, P. J., Birren, B. & Simon, M. I. Stable propagation of cosmid sized human DNA inserts in an F factor based vector. Nucleic Acids Res. 20, 1083-1085 (1992).
49. Varshney, R. K. et al. Draft genome sequence of pigeonpea (Cajanus cajan), an orphan legume crop of resource-poor farmers. Nat. Biotech. 30, 83-89 (2012).
50. Elsik, C. G. et al. Creating a honey bee consensus gene set. Genome Biol. 8, R13 (2007).
51. Li, H. et al. TreeFam: a curated database of phylogenetic trees of animal gene families. Nucleic Acids Res. 34, D572-D580.
52. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004). (Pubitemid 38832724)
53. Flutre, T., Duprat, E., Feuillet, C. & Quesneville, H. Considering transposable element diversification in de novo annotation approaches. PLoS One 6, e16526 (2011).
54. Qiu, Q. et al. The yak genome and adaptation to life at high altitude. Nat. Genet. 44, 946-949 (2012).