Analyses of expressed sequence tags in Neurospora reveal rapid evolution of genes associated with the early stages of sexual reproduction in fungi

BMC Evolutionary Biology

Volumn 12, Issue 1, 2012, Pages

  Nygren, Kristiina ^a,e   Wallberg, Andreas ^b   Samils, Nicklas ^a   Stajich, Jason E ^c   Townsend, Jeffrey P ^d   Karlsson, Magnus ^a   Johannesson, Hanna ^e  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d YALE UNIVERSITY   (United States)

^e UPPSALA UNIVERSITY   (Sweden)

Author keywords

dN dS; Microarray; Neurospora; Reproductive genes; Speciation

Indexed keywords

DATA SET; EVOLUTIONARY BIOLOGY; FUNGUS; GENE EXPRESSION; GENOME; HYBRIDIZATION; REPRODUCTIVE ISOLATION; SEXUAL REPRODUCTION;

ANIMALIA; ASCOMYCOTA; FUNGI; NEUROSPORA; NEUROSPORA CRASSA; NEUROSPORA DISCRETA; NEUROSPORA INTERMEDIA; NEUROSPORA TETRASPERMA;

ARTICLE; CLASSIFICATION; EXPRESSED SEQUENCE TAG; FUNGAL GENE; GENETIC ASSOCIATION; GENETICS; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NEUROSPORA; PHYLOGENY; PHYSIOLOGY; REPRODUCTIVE ISOLATION; STATISTICAL MODEL;

EVOLUTION, MOLECULAR; EXPRESSED SEQUENCE TAGS; GENES, FUNGAL; GENES, MATING TYPE, FUNGAL; GENOME-WIDE ASSOCIATION STUDY; LIKELIHOOD FUNCTIONS; MOLECULAR SEQUENCE ANNOTATION; NEUROSPORA; PHYLOGENY; REPRODUCTIVE ISOLATION;

MLCS; MLOWN;

EID: 84869869378     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-12-229     Document Type: Article

References (90)

1. Evolution of reproductive proteins from animals and plants. Clark NL, Aagaard JE, Swanson WJ, Reproduction 2006 131 11 22 10.1530/rep.1.00357 16388004 (Pubitemid 43230698)
2. Sex gene pool evolution and speciation: A new paradigm. Singh RS, Kulathinal RJ, Genes Genet Syst 2000 75 119 130 10.1266/ggs.75.119 10984836
3. The rapid evolution of reproductive proteins. Swanson WJ, Vacquier VD, Nat Rev Genet 2002 3 137 144 11836507 (Pubitemid 34506597)
4. Evolution in the fast lane: rapidly evolving sex-related genes in Drosophila. Haerty W, Jagadeeshan S, Kulathinal RJ, Wong A, Ravi Ram K, Sirot LK, Levesque L, Artieri CG, Wolfner MF, Civetta A, Singh RS, Genetics 2007 177 1321 1335 10.1534/genetics.107.078865 18039869 (Pubitemid 350277035)
5. A scan for positively selected genes in the genomes of humans and chimpanzees. Nielsen R, Bustamante C, Clark AG, Glanowski S, Sackton TB, Hubisz MJ, Fledel-Alon A, Tanenbaum DM, Civello D, White TJ, et al. PLoS Biol 2005 3 976 985
6. Evolutionary expressed sequence tag analysis of Drosophila female reproductive tracts identifies genes subjected to positive selection. Swanson WJ, Wong A, Wolfner MF, Aquadro CF, Genetics 2004 168 1457 1465 10.1534/genetics.104.030478 15579698 (Pubitemid 40007360)
7. Combined EST and proteomic analysis identifies rapidly evolving seminal fluid proteins in Heliconius butterflies. Walters JR, Harrison RG, Mol Biol Evol 2010 27 2000 2013 10.1093/molbev/msq092 20375075
8. Comparisons of pollen coat genes across Brassicaceae species reveal rapid evolution by repeat expansion and diversification. Fiebig A, Kimport R, Preuss D, Proc Natl Acad Sci USA 2004 101 3286 3291 10.1073/pnas.0305448101 14970339 (Pubitemid 38327773)
9. Primary structural features of the S haplotype-specific F-box protein, SFB, in Prunus. Ikeda K, Igic B, Ushijima K, Yamane H, Hauck NR, Nakano R, Sassa H, Iezzoni AF, Kohn JR, Tao R, Sex Plant Reprod 2004 16 235 243 10.1007/s00497-003-0200-x (Pubitemid 38162006)
10. Rapid evolution of a sexual reproduction gene in centric diatoms of the genus Thalassiosira. Armbrust EV, Galindo HM, Appl Environ Microb 2001 67 3501 3513 10.1128/AEM.67.8.3501-3513.2001 (Pubitemid 33641221)
11. Rapid evolution of sex-related genes in Chlamydomonas. Ferris PJ, Pavlovic C, Fabry S, Goodenough UW, Proc Natl Acad Sci USA 1997 94 8634 8639 10.1073/pnas.94.16.8634 9238029 (Pubitemid 27335091)
12. Phylogenetic relationships between mating-type sequences from homothallic and heterothallic ascomycetes. Pöggeler S, Curr Genet 1999 36 222 231 10.1007/s002940050494 10541860 (Pubitemid 29488216)
13. Pervasive adaptive evolution in primate seminal proteins. Clark NL, Swanson WJ, PLoS Genet 2005 1 35 10.1371/journal.pgen.0010035 16170411
14. Sexual selection and the molecular evolution of ADAM proteins. Finn S, Civetta A, J Mol Evol 2010 71 231 240 10.1007/s00239-010-9382-7 20730583
15. The evolution of the pheromonal signal system and its potential role for reproductive isolation in heterothallic Neurospora. Karlsson M, Nygren K, Johannesson H, Mol Biol Evol 2008 25 168 178 18024989
16. Pervasive adaptive evolution in mammalian fertilization proteins. Swanson WJ, Nielsen R, Yang Q, Mol Biol Evol 2003 20 18 20 10.1093/oxfordjournals. molbev.a004233 12519901 (Pubitemid 36077894)
17. Conspecific sperm and pollen precedence and speciation. Howard DJ, Annu Rev Ecol Syst 1999 30 109 132 10.1146/annurev.ecolsys.30.1.109 (Pubitemid 30065623)
18. Causes and consequences of variability in peptide mating pheromones of ascomycete fungi. Martin SH, Wingfield BD, Wingfield MJ, Steenkamp ET, Mol Biol Evol 2011 28 1987 2003 10.1093/molbev/msr022 21252281
19. The evolutionary trajectory of the mating-type (mat) genes in Neurospora relates to reproductive behavior of taxa. Wik L, Karlsson M, Johannesson H, BMC Evol Biol 2008 8 109 10.1186/1471-2148-8-109 18405383 (Pubitemid 351585479)
20. Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Butler G, Rasmussen MD, Lin MF, Santos MA, Sakthikumar S, Munro CA, Rheinbay E, Grabherr M, Forche A, Reedy JL, et al. Nature 2009 459 657 662 10.1038/nature08064 19465905
21. The evolution of sex: a perspective from the fungal kingdom. Lee SC, Ni M, Li W, Shertz C, Heitman J, Microbiol Mol Biol Rev 2010 74 298 340 10.1128/MMBR.00005-10 20508251
22. Evidence for diffusible, mating-type-specific trichogyne attractants in Neurospora crassa. Bistis GN, Exp Mycol 1983 7 292 295 10.1016/0147-5975(83) 90051-8
23. Pheromones are essential for male fertility and sufficient to direct chemotropic polarized growth of trichogynes during mating in Neurospora crassa. Kim H, Borkovich KA, Eukaryot Cell 2006 5 544 554 10.1128/EC.5.3.544-554.2006 16524909
24. A pheromone receptor gene, pre-1, is essential for mating type-specific directional growth and fusion of trichogynes and female fertility in Neurospora crassa. Kim H, Borkovich KA, Mol Microbiol 2004 52 1781 1798 10.1111/j.1365-2958.2004.04096.x 15186425 (Pubitemid 38822685)
25. Reproductive isolation and phylogenetic divergence in Neurospora: comparing methods of species recognition in a model eukaryote. Dettman JR, Jacobson DJ, Turner E, Pringle A, Taylor JW, Evolution 2003 57 2721 2741 14761052 (Pubitemid 38078354)
26. Reinforced postmating reproductive isolation barriers in Neurospora, an Ascomycete microfungus. Turner E, Jacobson DJ, Taylor JW, J Evol Biol 2010 23 1642 1656 10.1111/j.1420-9101.2010.02030.x 20546092
27. Genetic architecture of a reinforced, postmating, reproductive isolation barrier between Neurospora species indicates evolution via natural selection. Turner E, Jacobson DJ, Taylor JW, PLoS Genet 2011 7 1002204 10.1371/journal. pgen.1002204 21876674
28. Long-oligomer microarray profiling in Neurospora crassa reveals the transcriptional program underlying biochemical and physiological events of conidial germination. Kasuga T, Townsend JP, Tian CG, Gilbert LB, Mannhaupt G, Taylor JW, Glass NL, Nucleic Acids Res 2005 33 6469 6485 10.1093/nar/gki953 16287898 (Pubitemid 41806411)
29. The filamentous fungal gene expression database (FFGED). Zhang Z, Townsend JP, Fungal Genet Biol 2010 47 199 204 10.1016/j.fgb.2009.12.001 20025988
30. Resolution of large and small differences in gene expression using models for the Bayesian analysis of gene expression levels and spotted DNA microarrays. Townsend JP, BMC Bioinforma 2004 5 54 10.1186/1471-2105-5-54 (Pubitemid 38751282)
31. Bayesian analysis of gene expression levels: statistical quantification of relative mRNA level across multiple strains or treatments. Townsend JP, Hartl DL, Genome Biol 2002 3 ESEARCH0071 12537560
32. PAML: a program package for phylogenetic analysis by maximum likelihood. Yang Z, Comput Appl Biosci 1997 13 555 556 9367129 (Pubitemid 27480216)
33. PAML 4: phylogenetic analysis by maximum likelihood. Yang Z, Mol Biol Evol 2007 24 1586 1591 10.1093/molbev/msm088 17483113 (Pubitemid 47236688)
34. Gene birth, death, and divergence: The different scenarios of reproduction-related gene evolution. Tian X, Pascal G, Fouchecourt S, Pontarotti P, Monget P, Biol Reprod 2009 80 616 621 10.1095/biolreprod.108.073684 19129511
35. Relationship between phylogenetic distribution and genomic features in Neurospora crassa. Kasuga T, Mannhaupt G, Glass NL, PLoS One 2009 4 5286 10.1371/journal.pone.0005286 19461939
36. Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution. Anisimova M, Bielawski JP, Yang Z, Mol Biol Evol 2001 18 1585 1592 10.1093/oxfordjournals.molbev.a003945 11470850 (Pubitemid 32735106)
37. Evolution of primate gene expression. Khaitovich P, Enard W, Lachmann M, Paabo S, Nat Rev Genet 2006 7 693 702 10.1038/nrg1940 16921347 (Pubitemid 44260005)
38. Population genomics of the wild yeast Saccharomyces paradoxus: Quantifying the life cycle. Tsai IJ, Bensasson D, Burt A, Koufopanou V, Proc Natl Acad Sci USA 2008 105 4957 4962 10.1073/pnas.0707314105 18344325 (Pubitemid 351753853)
39. A genome-wide view of mutation rate co-variation using multivariate analyses. Ananda G, Chiaromonte F, Makova KD, Genome Biol 2011 12 27 10.1186/gb-2011-12-3-r27 21426544
40. Mutation rate variation in multicellular eukaryotes: causes and consequences. Baer CF, Miyamoto MM, Denver DR, Nat Rev Genet 2007 8 619 631 17637734 (Pubitemid 47077282)
41. tRNA gene number and codon usage in the C. elegans genome are co-adapted for optimal translation of highly expressed genes. Duret L, Trends Genet 2000 16 287 289 10.1016/S0168-9525(00)02041-2 10858656 (Pubitemid 30389593)
42. Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, Arabidopsis. Duret L, Mouchiroud D, Proc Natl Acad Sci USA 1999 96 4482 4487 10.1073/pnas.96.8.4482 10200288 (Pubitemid 29190362)
43. Synonymous codon usage in Escherichia coli: selection for translational accuracy. Stoletzki N, Eyre-Walker A, Mol Biol Evol 2007 24 374 381 17101719 (Pubitemid 46204370)
44. Mechanistic plasticity of sexual reproduction and meiosis in the Candida pathogenic species complex. Reedy JL, Floyd AM, Heitman J, Curr Biol 2009 19 891 899 10.1016/j.cub.2009.04.058 19446455
45. Sexual selection in mushroom-forming basidiomycetes. Nieuwenhuis BP, Debets AJ, Aanen DK, Proc Biol Sci 2011 278 152 157 10.1098/rspb.2010.1110 20630884
46. The fitness of filamentous fungi. Pringle A, Taylor JW, Trends Microbiol 2002 10 474 481 10.1016/S0966-842X(02)02447-2 12377558
47. Experimental evolution of a sexually selected display in yeast. Rogers DW, Greig D, P R Soc B 2009 276 543 549 10.1098/rspb.2008.1146
48. A Regulatory system controlling inhibition in sexual cycle of Neurospora. Howe HB, Prakash V, Can J Genet Cytol 1969 11 689 705 5370988
49. Phylogenetic and biological species diversity within the Neurospora tetrasperma complex. Menkis A, Bastiaans E, Jacobson DJ, Johannesson H, J Evol Biol 2009 22 1923 1936 10.1111/j.1420-9101.2009.01801.x 19682307
50. Multi-targeted priming for genome-wide gene expression assays. Adomas AB, Lopez-Giraldez F, Clark TA, Wang Z, Townsend JP, BMC Genomics 2010 11 477 10.1186/1471-2164-11-477 20716356
51. Molecular and functional analyses of poi-2, a novel gene highly expressed in sexual and perithecial tissues of Neurospora crassa. Kim H, Nelson MA, Eukaryot Cell 2005 4 900 910 10.1128/EC.4.5.900-910.2005 15879524 (Pubitemid 40697754)
52. A novel polyketide biosynthesis gene cluster is involved in fruiting body morphogenesis in the filamentous fungi Sordaria macrospora and Neurospora crassa. Nowrousian M, Curr Genet 2009 55 185 198 10.1007/s00294-009-0236-z 19277664
53. Multiple layers of temporal and spatial control regulate accumulation of the fruiting body-specific protein APP in Sordaria macrospora and Neurospora crassa. Nowrousian M, Piotrowski M, Kuck U, Fungal Genet Biol 2007 44 602 614 10.1016/j.fgb.2006.09.009 17092746 (Pubitemid 46809817)
54. Characterization of mat A-2, mat A-3 and Delta matA mating-type mutants of Neurospora crassa. Ferreira AVB, An ZQ, Metzenberg RL, Glass NL, Genetics 1998 148 1069 1079 9539425 (Pubitemid 28169019)
55. Multiple functions of mfa-1, a putative pheromone precursor gene of Neurospora crassa. Kim H, Metzenberg RL, Nelson MA, Eukaryot Cell 2002 1 987 999 10.1128/EC.1.6.987-999.2002 12477799 (Pubitemid 36557719)
56. A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Colot HV, Park G, Turner GE, Ringelberg C, Crew CM, Litvinkova L, Weiss RL, Borkovich KA, Dunlap JC, Proc Natl Acad Sci USA 2006 103 10352 10357 10.1073/pnas.0601456103 16801547 (Pubitemid 44051170)
57. Regulation of melanin biosynthesis via the dihydroxynaphthalene pathway is dependent on sexual development in the ascomycete Sordaria macrospora. Engh I, Nowrousian M, Kuck U, FEMS Microbiol Lett 2007 275 62 70 10.1111/j.1574-6968. 2007.00867.x 17681008 (Pubitemid 47390096)
58. A multilocus genealogical approach to phylogenetic species recognition in the model eukaryote Neurospora. Dettman JR, Jacobson DJ, Taylor JW, Evolution 2003 57 2703 2720 14761051 (Pubitemid 38078353)
59. Neurospora V. A synthetic medium favoring sexual reproduction. Westergaard M, Mitchell HK, Am J Bot 1947 34 573 577 10.2307/2437339
60. A convenient growth medium for Neurospora (medium N). Vogel, Microbiol Genet Bull 1956 13 42 43
61. Ascus and ascospore morphogenesis. Read ND, Beckett A, Mycol Res 1996 100 1281 1314 10.1016/S0953-7562(96)80057-8
62. RNA extraction, probe preparation, and competitive hybridization for transcriptional profiling using Neurospora crassa long-oligomer DNA microarrays. Clark TA, Guilmette JM, Renstrom D, Townsend JP, Fungal Genetics Reports 2008 55 18 28
63. Enabling a community to dissect an organism: overview of the Neurospora functional genomics project. Dunlap JC, Borkovich KA, Henn MR, Turner GE, Sachs MS, Glass NL, McCluskey K, Plamann M, Galagan JE, Birren BW, et al. Adv Genet 2007 57 49 96 17352902
64. A comprehensive phylogeny of Neurospora reveals a link between reproductive mode and molecular evolution in fungi. Nygren K, Strandberg R, Wallberg A, Nabholz B, Gustafsson T, Garcia D, Cano J, Guarro J, Johannesson H, Mol Phylogenet Evol 2011 59 649 663 10.1016/j.ympev.2011.03.023 21439389
65. Using DNA microarrays to study gene expression in closely related species. Oshlack A, Chabot AE, Smyth GK, Gilad Y, Bioinformatics 2007 23 1235 1242 10.1093/bioinformatics/btm111 17384014 (Pubitemid 47050539)
66. Biologically meaningful expression profiling across species using heterologous hybridization to a cDNA microarray. Renn SCP, Aubin-Horth N, Hofmann HA, BMC Genomics 2004 5 42 10.1186/1471-2164-5-42 15238158 (Pubitemid 39565312)
67. Yale microarray experimental design, home of the filamentous fungal microarray database http://www.yale.edu/townsend/Links/ffdatabase/downloads.html
68. Multifactorial experimental design and the transitivity of ratios with spotted DNA microarrays. Townsend JP, BMC Genomics 2003 4 41 10.1186/1471-2164-4-41 14525623 (Pubitemid 39565279)
69. The filamentous fungal gene expression database http://bioinfo.townsend. yale.edu/online.jsp
70. Statistical significance for genomewide studies. Storey JD, Tibshirani R, Proc Natl Acad Sci USA 2003 100 9440 9445 10.1073/pnas.1530509100 12883005 (Pubitemid 37033947)
71. Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Diatchenko L, Lau YF, Campbell AP, Chenchik A, Moqadam F, Huang B, Lukyanov S, Lukyanov K, Gurskaya N, Sverdlov ED, Siebert PD, Proc Natl Acad Sci USA 1996 93 6025 6030 10.1073/pnas.93.12.6025 8650213 (Pubitemid 26190796)
72. Base-calling of automated sequencer traces using phred. II. Error probabilities. Ewing B, Green P, Genome Res 1998 8 186 194 9521922 (Pubitemid 28177230)
73. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Ewing B, Hillier L, Wendl MC, Green P, Genome Res 1998 8 175 185 9521921 (Pubitemid 28177229)
74. The UniVec database http://www.ncbi.nlm.nih.gov/VecScreen/UniVec.html
75. Neurospora crassa database, Broad Institute http://www.broadinstitute. org/annotation/genome/neurospora/MultiHome.html
76. JGI, Neurospora discreta FGSC 8579 mat A http://genome.jgi-psf.org/ Neudi1/Neudi1.home.html
77. JGI, Neurospora tetrasperma FGSC 2508 mat A http://genome.jgi-psf.org/ Neute1/Neute1.home.html
78. Massive changes in genome architecture accompany the transition to self-fertility in the filamentous fungus Neurospora tetrasperma. Ellison CE, Stajich JE, Jacobson DJ, Natvig DO, Lapidus A, Foster B, Aerts A, Riley R, Lindquist EA, Grigoriev IV, Taylor JW, Genetics 2011 189 55 69 10.1534/genetics.111.130690 21750257
79. Automatic genome-wide reconstruction of phylogenetic gene trees. Wapinski I, Pfeffer A, Friedman N, Regev A, Bioinformatics 2007 23 549 i558 10.1093/bioinformatics/btm193 17646342 (Pubitemid 47244442)
80. Basic Local Alignment Search Tool. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, J Mol Biol 1990 215 403 410 2231712
81. A greedy algorithm for aligning DNA sequences. Zhang Z, Schwartz S, Wagner L, Miller W, J Comput Biol 2000 7 203 214 10.1089/10665270050081478 10890397 (Pubitemid 30412170)
82. Multiple alignment of DNA sequences with MAFFT. Katoh K, Asimenos G, Toh H, Methods Mol Biol 2009 537 39 64 10.1007/978-1-59745-251-9-3 19378139
83. Improved accuracy of multiple ncRNA alignment by incorporating structural information into a MAFFT-based framework. Katoh K, Toh H, BMC Bioinforma 2008 9 212 10.1186/1471-2105-9-212 (Pubitemid 351715980)
84. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Talavera G, Castresana J, Syst Biol 2007 56 564 577 10.1080/10635150701472164 17654362 (Pubitemid 47171631)
85. Controlling the false discovery rate-a practical and powerful approach to multiple testing. Benjamini Y, Hochberg Y, J Roy Stat Soc B Met 1995 57 289 300
86. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Hall TA, Nucl Acids Symp Ser 1999 41 95 98
87. Bayes empirical Bayes inference of amino acid sites under positive selection. Yang ZH, Wong WSW, Nielsen R, Mol Biol Evol 2005 22 1107 1118 10.1093/molbev/msi097 15689528 (Pubitemid 40471423)
88. SMART 6: recent updates and new developments. Letunic I, Doerks T, Bork P, Nucleic Acids Res 2009 37 229 D232 10.1093/nar/gkn808 18978020
89. Improved prediction of signal peptides: SignalP 3.0. Bendtsen JD, Nielsen H, von Heijne G, Brunak S, J Mol Biol 2004 340 783 795 10.1016/j.jmb.2004.05. 028 15223320 (Pubitemid 38829638)
90. A sensitive predictor for potential GPI lipid modification sites in fungal protein sequences and its application to genome-wide studies for Aspergillus nidulans, Candida albicans, Neurospora crassa, Saccharomyces cerevisiae and Schizosaccharomyces pombe. Eisenhaber B, Schneider G, Wildpaner M, Eisenhaber F, J Mol Biol 2004 337 243 253 10.1016/j.jmb.2004.01.025 15003443 (Pubitemid 38293395)