Natural selection on coding and noncoding DNA sequences is associated with virulence genes in a plant pathogenic fungus

Genome Biology and Evolution

Volumn 6, Issue 9, 2014, Pages 2368-2379

  Rech, Gabriel E ^a   Sanz Martín, Jose M ^a   Anisimova, Maria ^b,c   Sukno, Serenella A ^a   Thon, Michael R ^a  

^a UNIVERSITY OF SALAMANCA   (Spain)

^b ETH ZURICH   (Switzerland)

^c ZURICH UNIVERSITY OF APPLIED SCIENCES   (Switzerland)

Author keywords

Arms race hypothesis; Colletotrichum graminicola; PAML; Pathogenicity; Positive selection

Indexed keywords

5' UNTRANSLATED REGION; CODON; VIRULENCE FACTOR;

5' UNTRANSLATED REGION; CODON; COLLETOTRICHUM; FUNGUS; GENETIC SELECTION; GENETICS; MICROBIOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PLANT DISEASE; VIRULENCE;

5' UNTRANSLATED REGIONS; BASE SEQUENCE; CODON; COLLETOTRICHUM; EVOLUTION, MOLECULAR; FUNGI; MOLECULAR SEQUENCE DATA; PLANT DISEASES; SELECTION, GENETIC; VIRULENCE; VIRULENCE FACTORS;

EID: 84926486730     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evu192     Document Type: Article

References (84)

1. Aguileta G, et al. 2010. Finding candidate genes under positive selection in non-model species: examples of genes involved in host specialization in pathogens. Mol Ecol. 19:292-306.
2. Aguileta G, et al. 2012. Genes under positive selection in a model plant pathogenic fungus, Botrytis. Infect Genet Evol. 12:987-996.
3. Albert PR. 2011. What is a functional genetic polymorphism? Defining classes of functionality. J Psychiatry Neurosci. 36:363-365.
4. Andolfatto P. 2005. Adaptive evolution of non-coding DNA in Drosophila. Nature 437:1149-1152.
5. Andolfatto P. 2007. Hitchhiking effects of recurrent beneficial amino acid substitutions in the Drosophila melanogaster genome. Genome Res. 17:1755-1762.
6. Anisimova M, Bielawski JP, Yang Z. 2001. Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution. Mol Biol Evol. 18:1585-1592.
7. Anisimova M, Liberles D. 2012. Detecting and understanding natural selection. In: Cannarozzi GM, Schneider A, editors. Codon evolution: mechanisms and models. Oxford (United Kingdom): Oxford University Press. p. 73-96.
8. Baek J-M, Kenerley CM. 1998. The arg2 gene of Trichoderma virens: cloning and development of a homologous transformation system. Fungal Genet Biol. 23:34-44.
9. Bergstrom GC, Nicholson RL. 1999. The biology of corn anthracnose: knowledge to exploit for improved management. Plant Dis. 83:596-608.
10. Bickel RD, Dunham JP, Brisson JA. 2013. Widespread selection across coding and noncoding DNA in the Pea aphid genome. G3 3:993-1001.
11. Bishop JG, Dean AM, Mitchell-Olds T. 2000. Rapid evolution in plant chitinases: molecular targets of selection in plant-pathogen coevolution. Proc Natl Acad Sci USA. 97:5322-5327.
12. Borneman AR, et al. 2007. Divergence of transcription factor binding sites across related yeast species. Science 317:815-819.
13. Bustamante CD, et al. 2005. Natural selection on protein-coding genes in the human genome. Nature 437:1153-1157.
14. Cannon PF, Damm U, Johnston PR, Weir BS. 2012. Colletotrichum-current status and future directions. Stud Mycol. 73:181-213.
15. Dean R, et al. 2012. The top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol. 13:414-430.
16. Dodds PN, et al. 2006. Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc Natl Acad Sci USA. 103:8888-8893.
17. Doehlemann G, Hemetsberger C. 2013. Apoplastic immunity and its suppression by filamentous plant pathogens. New Phytol. 198:1001-1016.
18. Doniger SW, et al. 2008. A catalog of neutral and deleterious polymorphism in yeast. PLoS Genet. 4:e1000183.
19. Ellwood SR, Syme RA, Moffat CS, Oliver RP. 2012. Evolution of three Pyrenophora cereal pathogens: recent divergence, speciation and evolution of non-coding DNA. Fungal Genet Biol. 49:825-829.
20. Emerson JJ, et al. 2010. Natural selection on cis and trans regulation in yeasts. Genome Res. 20:826-836.
21. Emes RD, Yang Z. 2008. Duplicated paralogous genes subject to positive selection in the genome of Trypanosoma brucei. PLoS One 3:e2295.
22. ENCODE Project Consortium. 2012. An integrated encyclopedia of DNA elements in the human genome. Nature 489:57-74.
23. Fay JC, Benavides JA. 2005. Hypervariable noncoding sequences in Saccharomyces cerevisiae. Genetics 170:1575-1587.
24. Fitch WM, Leiter JM, Li XQ, Palese P. 1991. Positive Darwinian evolution in human influenza A viruses. Proc Natl Acad Sci USA. 88:4270-4274.
25. Fraser H. 2013. Gene expression drives local adaptation in humans. Genome Res. 23:1089-1096.
26. Frey TJ, Weldekidan T, Colbert T, Wolters PJCC, Hawk JA. 2011. Fitness evaluation of Rcg1, a locus that confers resistance to Colletotrichum graminicola (Ces.) G. W. Wils. Using near-isogenic maize hybrids. Crop Sci. 51:1551.
27. Gaffney DJ, Keightley PD. 2006. Genomic selective constraints in Murid noncoding DNA. PLoS Genet. 2:e204.
28. Gasch AP, et al. 2004. Conservation and evolution of cis-regulatory systems in Ascomycete fungi. PLoS Biol. 2:e398.
29. Gazave E, Marqués-Bonet T, Fernando O, Charlesworth B, Navarro A. 2007. Patterns and rates of intron divergence between humans and chimpanzees. Genome Biol. 8:R21.
30. Gibbons JG, et al. 2012. The evolutionary imprint of domestication on genome variation and function of the filamentous fungus Aspergillus oryzae. Curr Biol. 22:1403-1409.
31. Gil M, Zanetti MS, Zoller S, Anisimova M. 2013. CodonPhyML: Fast Maximum Likelihood Phylogeny Estimation under Codon Substitution Models. Mol Biol Evol. 30:1270-1280.
32. Greenwood TA, Kelsoe JR. 2003. Promoter and intronic variants affect the transcriptional regulation of the human dopamine transporter gene. Genomics 82:511-520.
33. Haddrill PR, Bachtrog D, Andolfatto P. 2008. Positive and negative selection on noncoding DNA in Drosophila simulans. Mol Biol Evol. 25:1825-1834.
34. Haygood R, Babbitt CC, Fedrigo O, Wray GA. 2010. Contrasts between adaptive coding and noncoding changes during human evolution. Proc Natl Acad Sci USA. 107:7853-7857.
35. Haygood R, Fedrigo O, Hanson B, Yokoyama K-D, Wray GA. 2007. Promoter regions of many neural- and nutrition-related genes have experienced positive selection during human evolution. Nat Genet. 39:1140-1144.
36. Hranilovic D, et al. 2004. Serotonin transporter promoter and intron 2 polymorphisms: relationship between allelic variants and gene expression. Biol Psychiatry. 55:1090-1094.
37. Hughes AL. 2012. Evolution of adaptive phenotypic traits without positive Darwinian selection. Heredity 108:347-353.
38. Jamil FF, Nicholson RL. 1991. Response of sorghum lines of different ages to Colletotrichum graminicola isolates from shattercane, sorghum and corn. Pak J Phytopathol. 3:12-18.
39. Kamenidou S, Jain R, Hari K, Robertson JM, Fletcher J. 2013. The microbial rosetta stone central agricultural database: an information resource on high-consequence plant pathogens. Plant Dis. 97:1097-1102.
40. Keightley PD, Lercher MJ, Eyre-Walker A. 2005. Evidence for widespread degradation of gene control regions in hominid genomes. PLoS Biol. 3:e42.
41. Keller NP, Turner G, Bennett JW. 2005. Fungal secondary metabolism-from biochemistry to genomics. Nat Rev Microbiol. 3:937-947.
42. Kim S, et al. 2007. Recombination and linkage disequilibrium in Arabidopsis thaliana. Nat Genet. 39:1151-1155.
43. King MC, Wilson AC. 1975. Evolution at two levels in humans and chimpanzees. Science 188:107-116.
44. Kojima K-I. 1971. Is there a constant fitness value for a given genotype? NO! Evolution 25:281-285.
45. Kondrashov AS. 2005. Evolutionary biology: fruitfly genome is not junk. Nature 437:1106-1106.
46. Kosakovsky Pond SL, Frost SDW, Muse SV. 2005. HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676-679.
47. Kosiol C, et al. 2008. Patterns of positive selection in six mammalian genomes. PLoS Genet. 4:e1000144.
48. Kousathanas A, Oliver F, Halligan DL, Keightley PD. 2011. Positive and negative selection on noncoding DNA close to protein-coding genes in wild house mice. Mol Biol Evol. 28:1183-1191.
49. Le Beau FJ. 1950. Pathogenicity studies with Colletotrichum from different hosts on sorghum and sugar cane. Phytopathology 40:430-438.
50. Le Hir H, Nott A, Moore MJ. 2003. How introns influence and enhance eukaryotic gene expression. Trends Biochem Sci. 28:215-220.
51. Li H, Ruan J, Durbin R. 2008. Mapping short DNA sequencing reads and calling variants using mapping quality scores. Genome Res. 18:1851-1858.
52. Li Y-D, et al. 2009. Detecting positive selection in the budding yeast genome. J Evol Biol. 22:2430-2437.
53. Lu T, Yao B, Zhang C. 2012. DFVF: database of fungal virulence factors. Database 2012: bas032.
54. MacKenzie A, Quinn J. 1999. A serotonin transporter gene intron 2 polymorphic region, correlated with affective disorders, has alleledependent differential enhancer-like properties in the mouse embryo. Proc Natl Acad Sci USA. 96:15251-15255.
55. Mazumder B, Seshadri V, Fox PL. 2003. Translational control by the 30-UTR: the ends specify the means. Trends Biochem Sci. 28:91-98.
56. McCarthy FM, et al. 2006. AgBase: a functional genomics resource for agriculture. BMC Genomics 7:229.
57. McDonald JH, Kreitman M. 1991. Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652-654.
58. Merritt C, Rasoloson D, Ko D, Seydoux G. 2008. 3' UTRs are the primary regulators of gene expression in the C. Elegans germline. Curr Biol. 18:1476-1482.
59. Neafsey DE, et al. 2010. Population genomic sequencing of Coccidioides fungi reveals recent hybridization and transposon control. Genome Res. 20:938-946.
60. Nei M, Gojobori T. 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol. Evol. 3:418-426.
61. O'Connell RJ, et al. 2012. Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nat Genet. 44:1060-1065.
62. Oleksiak MF, Churchill GA, Crawford DL. 2002. Variation in gene expression within and among natural populations. Nat Genet. 32:261-266.
63. Pedersen C, et al. 2012. Structure and evolution of barley powdery mildew effector candidates. BMC Genomics 13:694.
64. Petersen TN, Brunak S, Von Heijne G, Nielsen H. 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods. 8:785-786.
65. Raffaele S, Kamoun S. 2012. Genome evolution in filamentous plant pathogens: why bigger can be better. Nat Rev Microbiol. 10:417-430.
66. Rech GE, Vargas WA, Sukno SA, Thon MR. 2012. Identification of positive selection in disease response genes within members of the Poaceae. Plant Signal Behav. 7:1667-1675.
67. Ronald J, Akey JM. 2007. The evolution of gene expression QTL in Saccharomyces cerevisiae. PLoS One 2:e678.
68. Spanu P, Kämper J. 2010. Genomics of biotrophy in fungi and oomycetes-emerging patterns. Curr Opin Plant Biol. 13:409-414.
69. Stukenbrock EH, et al. 2010. Whole-genome and chromosome evolution associated with host adaptation and speciation of the wheat pathogen Mycosphaerella graminicola. PLoS Genet. 6:e1001189.
70. Stukenbrock EH, et al. 2011. The making of a new pathogen: insights from comparative population genomics of the domesticated wheat pathogen Mycosphaerella graminicola and its wild sister species. Genome Res. 21:2157-2166.
71. Sukno SA, García VM, Shaw BD, Thon MR. 2008. Root infection and systemic colonization of maize by Colletotrichum graminicola. Appl Environ Microbiol. 74:823-832.
72. Taft RJ, Pheasant M, Mattick JS. 2007. The relationship between nonprotein-coding DNA and eukaryotic complexity. Bioessays 29:288-299.
73. Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595.
74. Thon MR, Nuckles EM, Takach JE, Vaillancourt LJ. 2002. CPR1: a gene encoding a putative signal peptidase that functions in pathogenicity of Colletotrichum graminicola to maize. Mol Plant Microbe Interact. 15:120-128.
75. Vargas WA, et al. 2012. Plant defense mechanisms are activated during biotrophic and necrotrophic development of Colletotricum graminicola in maize. Plant Physiol. 158:1342-1358.
76. Whitehead A, Crawford DL. 2006. Neutral and adaptive variation in gene expression. Proc Natl Acad Sci USA. 103:5425-5430.
77. Win J, et al. 2007. Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic Oomycetes. Plant Cell 19:2349-2369.
78. Winnenburg R, et al. 2006. PHI-base: a new database for pathogen host interactions. Nucleic Acids Res. 34:D459-D464.
79. Wong WSW, Nielsen R. 2004. Detecting selection in noncoding regions of nucleotide sequences. Genetics 167:949-958.
80. Wray GA. 2007. The evolutionary significance of cis-regulatory mutations. Nat Rev Genet. 8:206-216.
81. Xie X, et al. 2005. Systematic discovery of regulatory motifs in human promoters and 30 UTRs by comparison of several mammals. Nature 434:338-345.
82. Yang Z. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 24. 1586.
83. Zhang J, Rosenberg HF, Nei M. 1998. Positive Darwinian selection after gene duplication in primate ribonuclease genes. Proc Natl Acad Sci USA. 95:3708-3713.
84. Zhen Y, Andolfatto P. 2012. Methods to detect selection on noncoding DNA. Methods Mol Biol. 856:141-159.