Fungal metabolic gene clusters-caravans traveling across genomes and environments

Frontiers in Microbiology

Volumn 6, Issue MAR, 2015, Pages

  Wisecaver, Jennifer H ^a   Rokas, Antonis ^a  

^a VANDERBILT UNIVERSITY   (United States)

Author keywords

Comparative genomics; Gene innovation; Horizontal gene transfer; Metabolic gene cluster; Microbial ecology; Physical linkage; Secondary metabolism; Specialized metabolism

Indexed keywords

VIRULENCE FACTOR;

ASPERGILLUS NIDULANS; BOTRYTIS CINEREA; EVOLUTIONARY ADAPTATION; FUNGAL METABOLISM; GENE CLUSTER; GENE FUNCTION; GENE LOCATION; GENETIC ANALYSIS; GENOME; HIGH THROUGHPUT SEQUENCING; HORIZONTAL GENE TRANSFER; METABOLIC GENE CLUSTER; METABOLISM; NONHUMAN; PENICILLIUM EXPANSUM; PENICILLIUM ROQUEFORTI; PHYLOGENOMICS; PODOSPORA ANSERINA; REVIEW;

FUNGI;

EID: 84927168286     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00161     Document Type: Review

References (107)

1. Abby, S. S., Tannier, E., Gouy, M., and Daubin, V. (2010). Detecting lateral gene transfers by statistical reconciliation of phylogenetic forests. BMC Bioinformatics 11:324. doi: 10.1186/1471-2105-11-324.
2. Akagi, Y., Akamatsu, H., Otani, H., and Kodama, M. (2009). Horizontal chromosome transfer, a mechanism for the evolution and differentiation of a plant-pathogenic fungus. Eukaryot. Cell 8, 1732-1738. doi: 10.1128/EC.00135-09.
3. Andersson, J. O. (2009). Gene transfer and diversification of microbial eukaryotes. Annu. Rev. Microbiol. 63, 177-193. doi: 10.1146/annurev.micro.091208.073203.
4. Andersson, J. O., Sjogren, A., Davis, L., Embley, T. M., and Roger, A. (2003). Phylogenetic analyses of diplomonad genes reveal frequent lateral gene transfers affecting eukaryotes. Curr. Biol. 13, 94-104. doi: 10.1016/S0960-9822(03)00003-4.
5. Ballester, A.-R., Marcet-Houben, M., Levin, E., Sela, N., Selma-Lázaro, C., Carmona, L., et al. (2014). Genome transcriptome, and functional analyses of Penicillium expansum provide new insights into secondary metabolism and pathogenicity. Mol. Plant Microbe Interact. 28, 232-248. doi: 10.1094/MPMI-09-14-0261-FI.
6. Blin, K., Medema, M. H., Kazempour, D., Fischbach, M. A., Breitling, R., Takano, E., et al. (2013). antiSMASH 2.0-a versatile platform for genome mining of secondary metabolite producers. Nucleic Acids Res. 41, W204-W212. doi: 10.1093/nar/gkt449.
7. Bobrowicz, P., Wysocki, R., Owsianik, G., Goffeau, A., and Ulaszewski, S. (1997). Isolation of three contiguous genes, ACR1, ACR2 and ACR3, involved in resistance to arsenic compounds in the yeast Saccharomyces cerevisiae. Yeast 13, 819-828.
8. Böhnert, H. U., Fudal, I., Dioh, W., Tharreau, D., Notteghem, J.-L., and Lebrun, M.-H. (2004). A putative polyketide synthase/peptide synthetase from Magnaporthe grisea signals pathogen attack to resistant rice. Plant Cell 16, 2499-2513. doi: 10.1105/tpc.104.022715.
9. Boschetti, C., Carr, A., Crisp, A., Eyres, I., Wang-Koh, Y., Lubzens, E., et al. (2012). Biochemical diversification through foreign gene expression in bdelloid rotifers. PLoS Genet. 8:e1003035. doi: 10.1371/journal.pgen.1003035.
10. Boschetti, C., Pouchkina-Stantcheva, N., Hoffmann, P., and Tunnacliffe, A. (2011). Foreign genes and novel hydrophilic protein genes participate in the desiccation response of the bdelloid rotifer Adineta ricciae. J. Exp. Biol. 214, 59-68. doi: 10.1242/jeb.050328.
11. Boucher, Y., Douady, C. J., Papke, R. T., Walsh, D. A., Boudreau, M. E. R., Nesbø, C. L., et al. (2003). Lateral gene transfer and the origins of prokaryotic groups. Annu. Rev. Genet. 37, 283-328. doi: 10.1146/annurev.genet.37.050503.084247.
12. Bushley, K. E., and Turgeon, B. G. (2010). Phylogenomics reveals subfamilies of fungal nonribosomal peptide synthetases and their evolutionary relationships. BMC Evol. Biol. 10:26. doi: 10.1186/1471-2148-10-26.
13. Campbell, M. A., Rokas, A., and Slot, J. C. (2012). Horizontal transfer and death of a fungal secondary metabolic gene cluster. Genome Biol. Evol. 4, 289-293. doi: 10.1093/gbe/evs011.
14. Campbell, M. A., Staats, M., van Kan, J. A. L., Rokas, A., and Slot, J. C. (2013). Repeated loss of an anciently horizontally transferred gene cluster in Botrytis. Mycologia 105, 1126-1134. doi: 10.3852/12-390.
15. Capella-Gutierrez, S., Silla-Martinez, J. M., and Gabaldon, T. (2009). trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972-1973. doi: 10.1093/bioinformatics/btp348.
16. Carbone, I., and Ramirez-Prado, J. (2007). Gene duplication, modularity and adaptation in the evolution of the aflatoxin gene cluster. BMC Evol. Biol. 7:111. doi: 10.1186/1471-2148-7-111.
17. Cheeseman, K., Ropars, J., Renault, P., Dupont, J., Gouzy, J., Branca, A., et al. (2014). Multiple recent horizontal transfers of a large genomic region in cheese making fungi. Nat. Commun. 5, 2876. doi: 10.1038/ncomms3876.
18. Chen, K., Durand, D., and Farach-Colton, M. (2000). NOTUNG: A program for dating gene duplications and optimizing gene family trees. J. Comput. Biol. 7, 429-447. doi: 10.1089/106652700750050871.
19. Cohen, O., Gophna, U., and Pupko, T. (2011). The complexity hypothesis revisited: connectivity rather than function constitutes a barrier to horizontal gene transfer. Mol. Biol. Evol. 28, 1481-1489. doi: 10.1093/molbev/msq333.
20. Covert, S. F. (1998). Supernumerary chromosomes in filamentous fungi. Curr. Genet. 33, 311-319. doi: 10.1007/s002940050342.
21. Dagan, T., Artzy-Randrup, Y., and Martin, W. (2008). Modular networks and cumulative impact of lateral transfer in prokaryote genome evolution. Proc. Natl. Acad. Sci. U.S.A. 105, 10039-10044. doi: 10.1073/pnas.0800679105.
22. Danchin, E. G. J., Rosso, M.-N., Vieira, P., de Almeida-Engler, J., Coutinho, P. M., Henrissat, B., et al. (2010). Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. Proc. Natl. Acad. Sci. U.S.A. 107, 17651-17656. doi: 10.1073/pnas.1008486107.
23. Darling, A. E., Mau, B., and Perna, N. T. (2010). progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE 5:e11147. doi: 10.1371/journal.pone.0011147.
24. Dunning Hotopp, J. C., Clark, M. E., Oliveira, D. C. S. G., Foster, J. M., Fischer, P., Muñoz Torres, M. C., et al. (2007). Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317, 1753-1756. doi: 10.1126/science.1142490.
25. Field, B., and Osbourn, A. E. (2008). Metabolic diversification-independent assembly of operon-like gene clusters in different plants. Science 320, 543-547. doi: 10.1126/science.1154990.
26. Frey, M., Chomet, P., Glawischnig, E., Stettner, C., Grün, S., Winklmair, A., et al. (1997). Analysis of a chemical plant defense mechanism in grasses. Science 277, 696-699. doi: 10.1126/science.277.5326.696.
27. Garcia-Vallve, S., Romeu, A., and Palau, J. (2000). Horizontal gene transfer of glycosyl hydrolases of the rumen fungi. Mol. Biol. Evol. 17, 352-361. doi: 10.1093/oxfordjournals.molbev.a026315.
28. Gladyshev, E. A., Meselson, M., and Arkhipova, I. R. (2008). Massive horizontal gene transfer in bdelloid rotifers. Science 320, 1210-1213. doi: 10.1126/science.1156407.
29. Glass, N. L., Jacobson, D. J., and Shiu, P. (2000). The genetics of hyphal fusion and vegetative incompatibility in filamentous ascomycete fungi. Annu. Rev. Genet. 34, 165-186. doi: 10.1146/annurev.genet.34.1.165.
30. Gogarten, J. P., and Townsend, J. P. (2005). Horizontal gene transfer, genome innovation and evolution. Nat. Rev. Microbiol. 3, 679-687. doi: 10.1038/nrmicro1204.
31. Gojkovic, Z., Knecht, W., Zameitat, E., Warneboldt, J., Coutelis, J. B., Pynyaha, Y., et al. (2004). Horizontal gene transfer promoted evolution of the ability to propagate under anaerobic conditions in yeasts. Mol. Genet. Genomics 271, 387-393. doi: 10.1007/s00438-004-0995-7.
32. Goodwin, S. B., M'barek, S. B., Dhillon, B., Wittenberg, A. H. J., Crane, C. F., Hane, J. K., et al. (2011). Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis. PLoS Genet. 7:e1002070. doi: 10.1371/journal.pgen.1002070.
33. Graham, L. A., Lougheed, S. C., Ewart, K. V., and Davies, P. L. (2008). Lateral transfer of a lectin-like antifreeze protein gene in fishes. PLoS ONE 3:e2616. doi: 10.1371/journal.pone.0002616.
34. Greene, G. H., McGary, K. L., Rokas, A., and Slot, J. C. (2014). Ecology drives the distribution of specialized tyrosine metabolism modules in fungi. Genome Biol. Evol. 6, 121-132. doi: 10.1093/gbe/evt208.
35. Haggerty, L. S., Jachiet, P.-A., Hanage, W. P., Fitzpatrick, D. A., Lopez, P., O'Connell, M. J., et al. (2014). A pluralistic account of homology: adapting the models to the data. Mol. Biol. Evol. 31, 501-516. doi: 10.1093/molbev/mst228.
36. Hall, C., Brachat, S., and Dietrich, F. S. (2005). Contribution of horizontal gene transfer to the evolution of Saccharomyces cerevisiae. Eukaryot. Cell 4, 1102-1115. doi: 10.1128/EC.4.6.1102-1115.2005.
37. Hall, C., and Dietrich, F. S. (2007). The reacquisition of biotin prototrophy in Saccharomyces cerevisiae involved horizontal gene transfer, gene duplication and gene clustering. Genetics 177, 2293-2307. doi: 10.1534/genetics.107.074963.
38. Han, Y., Liu, X., Benny, U., Kistler, H. C., and VanEtten, H. D. (2001). Genes determining pathogenicity to pea are clustered on a supernumerary chromosome in the fungal plant pathogen Nectria haematococca. Plant J. 25, 305-314. doi: 10.1046/j.1365-313x.2001.00969.x.
39. He, C., Rusu, A. G., Poplawski, A. M., Irwin, J. A., and Manners, J. M. (1998). Transfer of a supernumerary chromosome between vegetatively incompatible biotypes of the fungus Colletotrichum gloeosporioides. Genetics 150, 1459-1466.
40. Hittinger, C. T., Rokas, A., and Carroll, S. B. (2004). Parallel inactivation of multiple GAL pathway genes and ecological diversification in yeasts. Proc. Natl. Acad. Sci. U.S.A. 101, 14144-14149. doi: 10.1073/pnas.0404319101.
41. Hu, J., Chen, C., Peever, T., Dang, H., Lawrence, C., and Mitchell, T. (2012). Genomic characterization of the conditionally dispensable chromosome in Alternaria arborescens provides evidence for horizontal gene transfer. BMC Genomics 13:171. doi: 10.1186/1471-2164-13-171.
42. Hu, X., Xiao, G., Zheng, P., Shang, Y., Su, Y., Zhang, X., et al. (2014). Trajectory and genomic determinants of fungal-pathogen speciation and host adaptation. Proc. Natl. Acad. Sci. U.S.A. 111, 16796-16801. doi: 10.1073/pnas.1412662111.
43. Huang, J. (2013). Horizontal gene transfer in eukaryotes: the weak-link model. Bioessays 35, 868-875. doi: 10.1126/science.1142490.
44. Hull, E. P., Green, P. M., Arst, H. N., and Scazzocchio, C. (1989). Cloning and physical characterization of the L-proline catabolism gene cluster of Aspergillus nidulans. Mol. Microbiol. 3, 553-559. doi: 10.1111/j.1365-2958.1989.tb00201.x.
45. Hurst, L., Pal, C., and Lercher, M. (2004). The evolutionary dynamics of eukaryotic gene order. Nat. Rev. Genet. 5, 299-310. doi: 10.1038/nrg1319.
46. Itkin, M., Heinig, U., Tzfadia, O., Bhide, A. J., Shinde, B., Cardenas, P. D., et al. (2013). Biosynthesis of antinutritional alkaloids in solanaceous crops is mediated by clustered genes. Science 341, 175-179. doi: 10.1126/science.1240230.
47. Jain, R., Rivera, M. C., and Lake, J. A. (1999). Horizontal gene transfer among genomes: the complexity hypothesis. Proc. Natl. Acad. Sci. U.S.A. 96, 3801-3806. doi: 10.1073/pnas.96.7.3801.
48. Jain, R., Rivera, M. C., Moore, J. E., and Lake, J. A. (2003). Horizontal gene transfer accelerates genome innovation and evolution. Mol. Biol. Evol. 20, 1598-1602. doi: 10.1093/molbev/msg154.
49. Jargeat, P., Rekangalt, D., Verner, M., Gay, G., Debaud, J., Marmeisse, R., et al. (2003). Characterisation and expression analysis of a nitrate transporter and nitrite reductase genes, two members of a gene cluster for nitrate assimilation from the symbiotic basidiomycete Hebeloma cylindrosporum. Curr. Genet. 43, 199-205. doi: 10.1007/s00294-003-0387-2.
50. Katoh, K., and Standley, D. M. (2013). MAFFT Multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772-780. doi: 10.1093/molbev/mst010.
51. Keeling, P. J., and Palmer, J. D. (2008). Horizontal gene transfer in eukaryotic evolution. Nat. Rev. Genet. 9, 605-618. doi: 10.1038/nrg2386.
52. Keller, N., and Hohn, T. (1997). Metabolic pathway gene clusters in filamentous fungi. Fungal Genet. Biol. 21, 17-29. doi: 10.1006/fgbi.1997.0970.
53. Keller, N., Turner, G., and Bennett, J. (2005). Fungal secondary metabolism-from biochemistry to genomics. Nat. Rev. Microbiol. 3, 937-947. doi: 10.1038/nrmicro1286.
54. Khaldi, N., Collemare, J., Lebrun, M.-H., and Wolfe, K. H. (2008). Evidence for horizontal transfer of a secondary metabolite gene cluster between fungi. Genome Biol. 9:R18. doi: 10.1186/gb-2008-9-1-r18.
55. Khaldi, N., and Wolfe, K. H. (2011). Evolutionary origins of the fumonisin secondary metabolite gene cluster in Fusarium verticillioides and Aspergillus niger. Int. J. Evol. Biol. 2011, 423821-423827. doi: 10.4061/2011/423821.
56. Kishino, H., and Hasegawa, M. (1989). Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea. J. Mol. Evol. 29, 170-179. doi: 10.1007/BF02100115.
57. Kloesges, T., Popa, O., Martin, W., and Dagan, T. (2011). Networks of gene sharing among 329 proteobacterial genomes reveal differences in lateral gene transfer frequency at different phylogenetic depths. Mol. Biol. Evol. 28, 1057-1074. doi: 10.1093/molbev/msq297.
58. Koonin, E. V., Makarova, K. S., and Aravind, L. (2001). Horizontal gene transfer in prokaryotes: quantification and classification. Annu. Rev. Microbiol. 55, 709-742. doi: 10.1146/annurev.micro.55.1.709.
59. Kroken, S., Glass, N., Taylor, J., Yoder, O., and Turgeon, B. (2003). Phylogenomic analysis of type I polyketide synthase genes in pathogenic and saprobic ascomycetes. Proc. Natl. Acad. Sci. U.S.A. 100, 15670-15675. doi: 10.1073/pnas.2532165100.
60. Lawrence, D. P., Kroken, S., Pryor, B. M., and Arnold, A. E. (2011). Interkingdom gene transfer of a hybrid NPS/PKS from bacteria to filamentous ascomycota. PLoS ONE 6:e28231. doi: 10.1371/journal.pone.0028231.
61. Lee, J. M. (2003). Genomic gene clustering analysis of pathways in eukaryotes. Genome Res. 13, 875-882. doi: 10.1101/gr.737703.
62. Li, F.-W., Villarreal, J. C., Kelly, S., Rothfels, C. J., Melkonian, M., Frangedakis, E., et al. (2014). Horizontal transfer of an adaptive chimeric photoreceptor from bryophytes to ferns. Proc. Natl. Acad. Sci. U.S.A. 111, 6672-6677. doi: 10.1073/pnas.1319929111.
63. Loftus, B., Anderson, I., Davies, R., Alsmark, U. C. M., Samuelson, J., Amedeo, P., et al. (2005). The genome of the protist parasite Entamoeba histolytica. Nature 433, 865-868. doi: 10.1038/nature03291.
64. Ma, L.-J., van der Does, H. C., Borkovich, K. A., Coleman, J. J., Daboussi, M.-J., Di Pietro, A., et al. (2010). Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464, 367-373. doi: 10.1038/nature08850.
65. Marcet-Houben, M., and Gabaldon, T. (2010). Acquisition of prokaryotic genes by fungal genomes. Trends Genet. 26, 5-8. doi: 10.1016/j.tig.2009.11.007.
66. Matasyoh, J. C., Dittrich, B., Schueffler, A., and Laatsch, H. (2011). Larvicidal activity of metabolites from the endophytic Podospora sp. against the malaria vector Anopheles gambiae. Parasitol. Res. 108, 561-566. doi: 10.1007/s00436-010-2098-1.
67. Moore, G. G., Collemare, J., and Lebrun, M. H. (2014). "Evolutionary mechanisms involved in development of fungal secondary metabolite gene clusters, " in Natural Products Discourse, Diversity, and Design, eds A. Osbourn, R. J. Goss, and G. T. Carter (Hoboken, NJ: John Wiley & Sons, Inc.), 343-356. doi: 10.1111/j.1365-2958.2008.06422.x.
68. Moran, N. A., and Jarvik, T. (2010). Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science 328, 624-627. doi: 10.1126/science.1187113.
69. Moran, Y., Fredman, D., Szczesny, P., Grynberg, M., and Technau, U. (2012). Recurrent horizontal transfer of bacterial toxin genes to eukaryotes. Mol. Biol. Evol. 29, 2223-2230. doi: 10.1093/molbev/mss089.
70. Nakamura, Y., Itoh, T., Matsuda, H., and Gojobori, T. (2004). Biased biological functions of horizontally transferred genes in prokaryotic genomes. Nat. Genet. 36, 760-766. doi: 10.1038/ng1381.
71. Novo, M., Bigey, F., Beyne, E., Galeote, V., Gavory, F., Mallet, S., et al. (2009). Eukaryote-to-eukaryote gene transfer events revealed by the genome sequence of the wine yeast Saccharomyces cerevisiae EC1118. Proc. Natl. Acad. Sci. U.S.A. 106, 16333-16338. doi: 10.1073/pnas.0904673106.
72. Ochman, H., Lawrence, J., and Groisman, E. (2000). Lateral gene transfer and the nature of bacterial innovation. Nature 405, 299-304. doi: 10.1038/35012500.
73. Patron, N. J., Waller, R. F., Cozijnsen, A. J., Straney, D. C., Gardiner, D. M., Nierman, W. C., et al. (2007). Origin and distribution of epipolythiodioxopiperazine (ETP) gene clusters in filamentous ascomycetes. BMC Evol. Biol. 7:174. doi: 10.1186/1471-2148-7-174.
74. Pombert, J.-F., Selman, M., Burki, F., Bardell, F. T., Farinelli, L., Solter, L. F., et al. (2012). Gain and loss of multiple functionally related, horizontally transferred genes in the reduced genomes of two microsporidian parasites. Proc. Natl. Acad. Sci. U.S.A. 109, 12638-12643. doi: 10.1073/pnas.1205020109.
75. Proctor, R. H., Van Hove, F., Susca, A., Stea, G., Busman, M., van der Lee, T., et al. (2013). Birth, death and horizontal transfer of the fumonisin biosynthetic gene cluster during the evolutionary diversification of Fusarium. Mol. Microbiol. 90, 290-306. doi: 10.1111/mmi.12362.
76. Qi, X., Bakht, S., Leggett, M., Maxwell, C., Melton, R., and Osbourn, A. (2004). A gene cluster for secondary metabolism in oat: implications for the evolution of metabolic diversity in plants. Proc. Natl. Acad. Sci. U.S.A. 101, 8233-8238. doi: 10.1073/pnas.0401301101.
77. Ricard, G., McEwan, N., Dutilh, B., Jouany, J., Macheboeuf, D., Mitsumori, M., et al. (2006). Horizontal gene transfer from bacteria to rumen ciliates indicates adaptation to their anaerobic, carbohydrates-rich environment. BMC Genomics 7:22. doi: 10.1186/1471-2164-7-22.
78. Richards, T. A., Leonard, G., Soanes, D. M., and Talbot, N. J. (2011). Gene transfer into the fungi. Fungal Biol. Rev. 25, 98-110. doi: 10.1016/j.fbr.2011.04.003.
79. Richards, T. A., Soanes, D. M., Foster, P. G., Leonard, G., Thomton, C. R., and Talbot, N. J. (2009). Phylogenomic analysis demonstrates a pattern of rare and ancient horizontal gene transfer between plants and fungi. Plant Cell 21, 1897-1911. doi: 10.1105/tpc.109.065805.
80. Rokas, A., Williams, B. L., King, N., and Carroll, S. B. (2003). Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 425, 798-804. doi: 10.1038/nature02053.
81. Salichos, L., and Rokas, A. (2013). Inferring ancient divergences requires genes with strong phylogenetic signals. Nature 497, 327-331. doi: 10.1038/nature12130.
82. Sanderson, M. J., Thorne, J. L., Wikström, N., and Bremer, K. (2004). Molecular evidence on plant divergence times. Am. J. Bot. 91, 1656-1665. doi: 10.3732/ajb.91.10.1656.
83. Scazzocchio, C. (2014). Fungal biology in the post-genomic era. Fungal Biol. Biotechnol. 1, 7. doi: 10.1186/s40694-014-0007-6.
84. Schmitt, I., and Lumbsch, H. T. (2009). Ancient horizontal gene transfer from bacteria enhances biosynthetic capabilities of fungi. PLoS ONE 4:e4437. doi: 10.1371/journal.pone.0004437.
85. Schönknecht, G., Chen, W.-H., Ternes, C. M., Barbier, G. G., Shrestha, R. P., Stanke, M., et al. (2013). Gene transfer from bacteria and archaea facilitated evolution of an extremophilic eukaryote. Science 339, 1207-1210. doi: 10.1126/science.1231707.
86. Schumacher, J., Gautier, A., Morgant, G., Studt, L., Ducrot, P.-H., Le Pêcheur, P., et al. (2013). A functional bikaverin biosynthesis gene cluster in rare strains of Botrytis cinerea is positively controlled by VELVET. PLoS ONE 8:e53729. doi: 10.1371/journal.pone.0053729.
87. Shimodaira, H. (2002). An approximately unbiased test of phylogenetic tree selection. Syst. Biol. 51, 492-508. doi: 10.1080/10635150290069913.
88. Shimodaira, H., and Hasegawa, M. (1999). Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 16, 1114-1116. doi: 10.1093/oxfordjournals.molbev.a026201.
89. Shimodaira, H., and Hasegawa, M. (2001). CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17, 1246-1247. doi: 10.1093/bioinformatics/17.12.1246.
90. Slot, J. C., and Hibbett, D. S. (2007). Horizontal transfer of a nitrate assimilation gene cluster and ecological transitions in fungi: a phylogenetic study. PLoS ONE 2:e1097. doi: 10.1371/journal.pone.0001097.
91. Slot, J. C., and Rokas, A. (2010). Multiple GAL pathway gene clusters evolved independently and by different mechanisms in fungi. Proc. Natl. Acad. Sci. U.S.A. 107, 10136-10141. doi: 10.1073/pnas.0914418107.
92. Slot, J. C., and Rokas, A. (2011). Horizontal transfer of a large and highly toxic secondary metabolic gene cluster between fungi. Curr. Biol. 21, 134-139. doi: 10.1016/j.cub.2010.12.020.
93. Soanes, D., and Richards, T. A. (2014). Horizontal gene transfer in eukaryotic plant pathogens. Ann. Rev. Phytopathol. 52, 583-614. doi: 10.1146/annurev-phyto-102313-050127.
94. Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312-1313. doi: 10.1093/bioinformatics/btu033.
95. Stolzer, M., Lai, H., Xu, M., Sathaye, D., Vernot, B., and Durand, D. (2012). Inferring duplications, losses, transfers and incomplete lineage sorting with nonbinary species trees. Bioinformatics 28, I409-I415. doi: 10.1093/bioinformatics/bts386.
96. Szklarczyk, D., Franceschini, A., Wyder, S., Forslund, K., Heller, D., Huerta-Cepas, J., et al. (2015). STRING v10: protein-protein interaction networks, integrated over the tree of life. Nuc. Acids Res. 43, D447-D452. doi: 10.1093/nar/gku1003.
97. Temporini, E. D., and Vanetten, H. D. (2004). An analysis of the phylogenetic distribution of the pea pathogenicity genes of Nectria haematococca MPVI 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. doi: 10.1007/s00294-004-0506-8.
98. Tiburcio, R. A., Lacerda Costa, G. G., Carazzolle, M. F., Costa Mondego, J. M., Schuster, S. C., Carlson, J. E., et al. (2010). Genes acquired by horizontal transfer are potentially involved in the evolution of phytopathogenicity in Moniliophthora perniciosa and Moniliophthora roreri, two of the major pathogens of cacao. J. Mol. Evol. 70, 85-97. doi: 10.1007/s00239-009-9311-9.
99. Treangen, T. J., and Rocha, E. P. C. (2011). Horizontal transfer, not duplication, drives the expansion of protein families in prokaryotes. PLoS Genet. 7:e1001284. doi: 10.1371/journal.pgen.1001284.
100. van den Berg, M. A., Albang, R., Albermann, K., Badger, J. H., Daran, J.-M., Driessen, A. J. M., et al. (2008). Genome sequencing and analysis of the filamentous fungus Penicillium chrysogenum. Nat. Biotechnol. 26, 1161-1168. doi: 10.1038/nbt.1498.
101. van der Does, H. C., and Rep, M. (2012). Horizontal transfer of supernumerary chromosomes in fungi. Methods Mol. Biol. 835, 427-437. doi: 10.1007/978-1-61779-501-5_26.
102. Vernot, B., Stolzer, M., Goldman, A., and Durand, D. (2007). Reconciliation with non-binary species trees. Comput. Syst. Bioinform. Conf. 6, 441-452. doi: 10.1142/9781860948732_0044.
103. Wenzl, P., Wong, L., Kwang-won, K., and Jefferson, R. A. (2005). A functional screen identifies lateral transfer of β-glucuronidase (gus) from bacteria to fungi. Mol. Biol. Evol. 22, 308-316. doi: 10.1093/molbev/msi018.
104. Winzer, T., Gazda, V., He, Z., Kaminski, F., Kern, M., Larson, T. R., et al. (2012). A Papaver somniferum 10-gene cluster for synthesis of the anticancer alkaloid noscapine. Science 336, 1704-1708. doi: 10.1126/science.1220757.
105. Wisecaver, J. H., Slot, J. C., and Rokas, A. (2014). The evolution of fungal metabolic pathways. PLoS Genet. 10:e1004816. doi: 10.1371/journal.pgen.1004816.
106. Wong, S., and Wolfe, K. H. (2005). Birth of a metabolic gene cluster in yeast by adaptive gene relocation. Nat. Genet. 37, 777-782. doi: 10.1038/ng1584.
107. Yue, J., Hu, X., Sun, H., Yang, Y., and Huang, J. (2012). Widespread impact of horizontal gene transfer on plant colonization of land. Nat. Commun. 3, 1152. doi: 10.1038/ncomms2148.