A multilocus timescale for oomycete evolution estimated under three distinct molecular clock models

BMC Evolutionary Biology

Jaime E Blair¹  Nahill H Matari¹ 

[1] Department of Biology, Franklin & Marshall College, Lancaster, PA, USA

关键词: Gene expression regulation;    Molecular clock;    Bayesian inference;    Divergence times;    Oomycetes;   

Others  :  856567
DOI  :  10.1186/1471-2148-14-101

 received in 2014-03-04, accepted in 2014-05-06,  发布年份 2014

【 摘 要 】

Background

Molecular clock methodologies allow for the estimation of divergence times across a variety of organisms; this can be particularly useful for groups lacking robust fossil histories, such as microbial eukaryotes with few distinguishing morphological traits. Here we have used a Bayesian molecular clock method under three distinct clock models to estimate divergence times within oomycetes, a group of fungal-like eukaryotes that are ubiquitous in the environment and include a number of devastating pathogenic species. The earliest fossil evidence for oomycetes comes from the Lower Devonian (~400 Ma), however the taxonomic affinities of these fossils are unclear.

Results

Complete genome sequences were used to identify orthologous proteins among oomycetes, diatoms, and a brown alga, with a focus on conserved regulators of gene expression such as DNA and histone modifiers and transcription factors. Our molecular clock estimates place the origin of oomycetes by at least the mid-Paleozoic (~430-400 Ma), with the divergence between two major lineages, the peronosporaleans and saprolegnialeans, in the early Mesozoic (~225-190 Ma). Divergence times estimated under the three clock models were similar, although only the strict and random local clock models produced reliable estimates for most parameters.

Conclusions

Our molecular timescale suggests that modern pathogenic oomycetes diverged well after the origin of their respective hosts, indicating that environmental conditions or perhaps horizontal gene transfer events, rather than host availability, may have driven lineage diversification. Our findings also suggest that the last common ancestor of oomycetes possessed a full complement of eukaryotic regulatory proteins, including those involved in histone modification, RNA interference, and tRNA and rRNA methylation; interestingly no match to canonical DNA methyltransferases could be identified in the oomycete genomes studied here.

【 授权许可】

   
2014 Matari and Blair; licensee BioMed Central Ltd.

【 图 表 】

【 参考文献 】

• [1]Knoll AH: The fossil record of microbial life. In Fundamentals of Geobiology. Edited by Knoll AH, Canfield DE, Konhauser KO. Oxford: Wiley-Blackwell; 2012.
• [2]Zuckerkandl E, Pauling L: Molecular disease, evolution, and genic heterogeneity. In Horizons in Biochemistry. Edited by Kasha M, Pullman B. New York: Academic Press; 1962:189-225.
• [3]Zuckerkandl E, Pauling L: Evolutionary divergence and convergence in proteins. In Evolving Genes and Proteins. Edited by Bryson V, Vogel HJ. New York: Academic Press; 1965:97-166.
• [4]Kumar S: Molecular clocks: four decades of evolution. Nat Rev Genet 2005, 6(8):654-662.
• [5]Sanderson MJ: A nonparametric approach to estimating divergence times in the absence of rate constancy. Mol Biol Evol 1997, 14(12):1218-1231.
• [6]Sanderson MJ: Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol Biol Evol 2002, 19(1):101-109.
• [7]Thorne JL, Kishino H, Painter IS: Estimating the rate of evolution of the rate of molecular evolution. Mol Biol Evol 1998, 15(12):1647-1657.
• [8]Aris-Brosou S, Yang Z: Effects of models of rate evolution on estimation of divergence dates with special reference to the metazoan 18S ribosomal RNA phylogeny. Syst Biol 2002, 51(5):703-714.
• [9]Drummond AJ, Ho SYW, Phillips MJ, Rambaut A: Relaxed phylogenetics and dating with confidence. PLoS Biol 2006, 4(5):e88.
• [10]Drummond AJ, Suchard MA: Bayesian random local clocks, or one rate to rule them all. BMC Biol 2010, 8:114. BioMed Central Full Text
• [11]Ho SYW, Phillips MJ: Accounting for calibration uncertainty in phylogenetic estimation of evolutionary divergence times. Syst Biol 2009, 58(3):367-380.
• [12]Parham JF, Donoghue PCJ, Bell CJ, Calway TD, Head JJ, Holroyd PA, Inoue JG, Irmis RB, Joyce WG, Ksepka DT, Patané JSL, Smith ND, Tarver JE, van Tuinen M, Yang Z, Angielczyk KD, Greenwood JM, Hipsley CA, Jacobs L, Makovicky PJ, Müller J, Smith KT, Theodor JM, Warnock RCM, Benton MJ: Best practices for justifying fossil calibrations. Syst Biol 2012, 61(2):346-359.
• [13]Warnock RCM, Yang Z, Donoghue PCJ: Exploring uncertainty in the calibration of the molecular clock. Biol Lett 2012, 8(1):156-159.
• [14]Dick MW: Straminipilous Fungi. Dordrecht: Kluwer Academic Publishers; 2001.
• [15]Beakes GW, Glocklin SL, Sekimoto S: The evolutionary phylogeny of the oomycete "fungi". Protoplasma 2012, 249(1):3-19.
• [16]Cavalier-Smith T: Principles of protein and lipid targeting in secondary symbiogenesis: Euglenoid, Dinoflagellate, and Sporozoan plastid origins and the eukaryote family tree. J Eukaryot Microbiol 1999, 46(4):347-366.
• [17]Burki F, Shalchian-Tabrizi K, Minge M, Skjæveland Å, Nikolaev SI, Jakobsen KS, Pawlowski J: Phylogenomics reshuffles the eukaryotic supergroups. PLoS ONE 2007, 2(8):e790.
• [18]Adl SM, Simpson AGB, Lane CE, Lukeš J, Bass D, Bowser SS, Brown MW, Burki F, Dunthorn M, Hampl V, Heiss A, Hoppenrath M, Lara E, le Gall L, Lynn DH, McManus H, Mitchell EAD, Mozley-Stanridge SE, Parfrey LW, Pawlowski J, Rueckert S, Shadwick L, Schoch CL, Smirnov A, Spiegel FW: The Revised Classification of Eukaryotes. J Eukaryot Microbiol 2012, 59(5):429-514.
• [19]Fry W: Phytophthora infestans: the plant (and R gene) destroyer. Mol Plant Pathol 2008, 9(3):385-402.
• [20]Beakes GW, Sekimoto S: The evolutionary phylogeny of oomycetes - insights gained from studies of holocarpic parasites of algae and invertebrates. In Oomycete Genetics and Genomics: Diversity, Interactions, and Research Tools. Edited by Lamour K, Kamoun S. Hoboken, NJ: John Wiley & Sons, Inc; 2009:1-24.
• [21]Krings M, Taylor TN, Dotzler N: The fossil record of the Peronosporomycetes (Oomycota). Mycologia 2011, 103(3):445-457.
• [22]Taylor TN, Krings M, Kerp H: Hassiella monospora gen. et sp. nov., a microfungus from the 400 million year old Rhynie chert. Mycol Res 2006, 110(6):628-632.
• [23]Krings M, Taylor TN, Taylor EL, Kerp H, Hass H, Dotzler N, Harper CJ: Microfossils from the Lower Devonian Rhynie Chert with Suggested Affinities to the Peronosporomycetes. J Paleontol 2012, 86(2):358-367.
• [24]Krings M, Taylor TN, Dotzler N, Decombeix A-L: Galtierella biscalithecae nov. gen. et sp., a Late Pennsylvanian endophytic water mold (Peronosporomycetes) from France. Comptes Rendus Palevol 2010, 9(1–2):5-11.
• [25]Strullu-Derrien C, Kenrick P, Rioult JP, Strullu DG: Evidence of parasitic Oomycetes (Peronosporomycetes) infecting the stem cortex of the Carboniferous seed fern Lyginopteris oldhamia. Proc R Soc B Biol Sci 2011, 278(1706):675-680.
• [26]Stidd BM, Cosentino K: Albugo-like oogonia from the American Carboniferous. Science 1975, 190(4219):1092-1093.
• [27]Dotzler N, Krings M, Agerer R, Galtier J, Taylor TN: Combresomyces cornifer gen. sp. nov., an endophytic peronosporomycete in Lepidodendron from the Carboniferous of central France. Mycol Res 2008, 112(9):1107-1114.
• [28]Schwendemann AB, Taylor TN, Taylor EL, Krings M, Dotzler N: Combresomyces cornifer from the Triassic of Antarctica: Evolutionary stasis in the Peronosporomycetes. Rev Palaeobot Palynol 2009, 154(1–4):1-5.
• [29]Krings M, Taylor TN, Dotzler N: Fungal endophytes as a driving force in lan plant evolution: evidence from the fossil record. In Biocomplexity of Plant-Fungal Interactions. Edited by Southworth D. Ames, Iowa: John Wiley & Sons, Inc; 2012.
• [30]Berney C, Pawlowski J: A molecular time-scale for eukaryote evolution recalibrated with the continuous microfossil record. Proc R Soc B Biol Sci 2006, 273(1596):1867-1872.
• [31]Parfrey LW, Lahr DJG, Knoll AH, Katz LA: Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc Natl Acad Sci 2011, 108(33):13624-13629.
• [32]Hackett JD, Yoon HS, Butterfield NJ, Sanderson MJ, Bhattacharya D, Falkowski PG, Knoll AH: Plastid endosymbiosis: sources and timing of the major events. In Evolution of Primary Producers in the Sea. Burlington, MA: Elsevier Academic Press; 2007:109-132.
• [33]Phillips N, Calhoun S, Moustafa A, Bhattacharya D, Braun EL: Genomic insights into evolutionary relationships among heterokont lineages emphasizing the Phaeophyceae. J Phycol 2008, 44(1):15-18.
• [34]Brown JW, Sorhannus U: A molecular genetic timescale for the diversification of autotrophic stramenopiles (Ochrophyta): substantive underestimation of putative fossil ages. PLoS ONE 2010, 5(9):e12759.
• [35]Siomi H, Siomi MC: On the road to reading the RNA-interference code. Nature 2009, 457(7228):396-404.
• [36]Vetukuri RR, Avrova AO, Grenville-Briggs LJ, Van West P, Soderbom F, Savenkov EI, Whisson SC, Dixelius C: Evidence for involvement of Dicer-like, Argonaute and histone deacetylase proteins in gene silencing in Phytophthora infestans. Mol Plant Pathol 2011, 12(8):772-785.
• [37]Kemen E, Gardiner A, Schultz-Larsen T, Kemen AC, Balmuth AL, Robert-Seilaniantz A, Bailey K, Holub E, Studholme DJ, MacLean D, Jones JDG: Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana. PLoS Biol 2011, 9(7):e1001094.
• [38]Cock JM, Sterck L, Rouze P, Scornet D, Allen AE, Amoutzias G, Anthouard V, Artiguenave F, Aury J-M, Badger JH, Beszteri B, Billiau K, Bonnet E, Bothwell JH, Bowler C, Boyen C, Brownlee C, Carrano CJ, Charrier B, Cho GY, Coelho SM, Collen J, Corre E, Da Silva C, Delage L, Delaroque N, Dittami SM, Doulbeau S, Elias M, Farnham G, et al.: The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 2010, 465(7298):617-621.
• [39]Baxter L, Tripathy S, Ishaque N, Boot N, Cabral A, Kemen E, Thines M, Ah-Fong A, Anderson R, Badejoko W, Bittner-Eddy P, Boore JL, Chibucos MC, Coates M, Dehal P, Delehaunty K, Dong S, Downton P, Dumas B, Fabro G, Fronick C, Fuerstenberg SI, Fulton L, Gaulin E, Govers F, Hughes L, Humphray S, Jiang RHY, Judelson H, Kamoun S: Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome. Science 2010, 330(6010):1549-1551.
• [40]Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K, Kuo A, Maheswari U, Martens C, Maumus F, Otillar RP, Rayko E, Salamov A, Vandepoele K, Beszteri B, Gruber A, Heijde M, Katinka M, Mock T, Valentin K, Verret F, Berges JA, Brownlee C, Cadoret J-P, Chiovitti A, Choi CJ, Coesel S, De Martino A, Detter JC, Durkin C, Falciatore A, et al.: The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 2008, 456(7219):239-244.
• [41]Lamour KH, Mudge J, Gobena D, Hurtado-Gonzales OP, Schmutz J, Kuo A, Miller NA, Rice BJ, Raffaele S, Cano LM, Bharti AK, Donahoo RS, Finley S, Huitema E, Hulvey J, Platt D, Salamov A, Savidor A, Sharma R, Stam R, Storey D, Thines M, Win J, Haas BJ, Dinwiddie DL, Jenkins J, Knight JR, Affourtit JP, Han CS, Chertkov O: 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):1350-1360.
• [42]Haas BJ, Kamoun S, Zody MC, Jiang RHY, Handsaker RE, Cano LM, Grabherr M, Kodira CD, Raffaele S, Torto-Alalibo T, Bozkurt TO, Ah-Fong AMV, Alvarado L, Anderson VL, Armstrong MR, Avrova A, Baxter L, Beynon J, Boevink PC, Bollmann SR, Bos JIB, Bulone V, Cai G, Cakir C, Carrington JC, Chawner M, Conti L, Costanzo S, Ewan R, Fahlgren N, et al.: Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 2009, 461(7262):393-398.
• [43]Tyler BM, Tripathy S, Zhang X, Dehal P, Jiang RHY, Aerts A, Arredondo FD, Baxter L, Bensasson D, Beynon JL, Tyler BM, Tripathy S, Zhang X, Dehal P, Jiang RHY, Aerts A, Arredondo FD, Baxter L, Bensasson D, Beynon JL, Chapman J, Damasceno CMB, Dorrance AE, Dou D, Dickerman AW, Dubchak IL, Garbelotto M, Gijzen M, Gordon SG, Govers F, et al.: Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 2006, 313(5791):1261-1266.
• [44]Levesque CA, Brouwer H, Cano L, Hamilton J, Holt C, Huitema E, Raffaele S, Robideau G, Thines M, Win J, Levesque CA, Brouwer H, Cano L, Hamilton J, Holt C, Huitema E, Raffaele S, Robideau G, Thines M, Win J, Zerillo M, Beakes G, Boore J, Busam D, Dumas B, Ferriera S, Fuerstenberg S, Gachon C, Gaulin E, Govers F, et al.: Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire. Genome Biol 2010, 11(7):R73. BioMed Central Full Text
• [45]Jiang RHY, de Bruijn I, Haas BJ, Belmonte R, Löbach L, Christie J, van den Ackerveken G, Bottin A, Bulone V, Díaz-Moreno SM, Dumas B, Fan L, Gaulin E, Govers F, Grenville-Briggs LJ, Horner NR, Levin JZ, Mammella M, Meijer HJG, Morris P, Nusbaum C, Oome S, Phillips AJ, van Rooyen D, Rzeszutek E, Saraiva M, Secombes CJ, Seidl MF, Snel B, Stassen JHM, et al.: Distinctive expansion of potential virulence genes in the genome of the oomycete fish pathogen Saprolegnia parasitica. PLoS Genet 2013, 9(6):e1003272.
• [46]Stover NA, Krieger CJ, Binkley G, Dong Q, Fisk DG, Nash R, Sethuraman A, Weng S, Cherry JM: Tetrahymena Genome Database (TGD): a new genomic resource for Tetrahymena thermophila research. Nucleic Acids Res 2006, 34(S1):D500-D503.
• [47]Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou S, Allen AE, Apt KE, Bechner M, Brzezinski MA, Chaal BK, Chiovitti A, Davis AK, Demarest MS, Detter JC, Glavina T, Goodstein D, Hadi MZ, Hellsten U, Hildebrand M, Jenkins BD, Jurka J, Kapitonov VV, Kröger N, Lau WWY, Lane TW, Larimer FW, Lippmeier JC, Lucas S, et al.: The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 2004, 306(5693):79-86.
• [48]Battistuzzi FU, Filipski A, Hedges SB, Kumar S: Performance of relaxed-clock methods in estimating evolutionary divergence times and their credibility intervals. Mol Biol Evol 2010, 27(6):1289-1300.
• [49]Grenville-Briggs L, Gachon CMM, Strittmatter M, Sterck L, Küpper FC, van West P: A Molecular Insight into Algal-Oomycete Warfare: cDNA Analysis of Ectocarpus siliculosus Infected with the Basal Oomycete Eurychasma dicksonii. PLoS ONE 2011, 6(9):e24500.
• [50]Sekimoto S, Hatai K, Honda D: Molecular phylogeny of an unidentified Haliphthoros-like marine oomycete and Haliphthoros milfordensis inferred from nuclear-encoded small- and large-subunit rRNA genes and mitochondrial-encoded cox2 gene. Mycoscience 2007, 48(4):212-221.
• [51]Jiang RHY, Tyler BM: Mechanisms and evolution of virulence in oomycetes. Annu Rev Phytopathol 2012, 50(1):295-318.
• [52]Bell CD, Soltis DE, Soltis PS: The age and diversification of the angiosperms re-revisited. Am J Bot 2010, 97(8):1296-1303.
• [53]Luis P, Gauthier A, Trouvelot S, Poinssot B, Frettinger P: Identification of Plasmopara viticola genes potentially involved in pathogenesis on grapevine suggests new similarities between oomycetes and true Fungi. Phytopathology 2013, 103(10):1035-1044.
• [54]Morris PF, Schlosser LR, Onasch KD, Wittenschlaeger T, Austin R, Provart N: Multiple horizontal gene transfer events and domain fusions have created novel regulatory and metabolic networks in the oomycete genome. PLoS ONE 2009, 4(7):e6133.
• [55]Richards TA, Soanes DM, Jones MDM, Vasieva O, Leonard G, Paszkiewicz K, Foster PG, Hall N, Talbot NJ: Horizontal gene transfer facilitated the evolution of plant parasitic mechanisms in the oomycetes. Proc Natl Acad Sci 2011, 108(37):15258-15263.
• [56]Belbahri L, Calmin G, Mauch F, Andersson JO: Evolution of the cutinase gene family: evidence for lateral gene transfer of a candidate Phytophthora virulence factor. Gene 2008, 408(1–2):1-8.
• [57]Collins L, Chen XS: Ancestral RNA: The RNA biology of the eukaryotic ancestor. RNA Biol 2009, 6(5):495-502.
• [58]Katz LA: Origin and diversification of eukaryotes. Annu Rev Microbiol 2012, 66(1):411-427.
• [59]Shabalina SA, Koonin EV: Origins and evolution of eukaryotic RNA interference. Trends Ecol Evol 2008, 23(10):578-587.
• [60]van West P, Kamoun S, van’t Klooster JW, Govers F: Internuclear gene silencing in Phytophthora infestans. Mol Cell 1999, 3(3):339-348.
• [61]van West P, Shepherd SJ, Walker CA, Li S, Appiah AA, Grenville-Briggs LJ, Govers F, Gow NAR: Internuclear gene silencing in Phytophthora infestans is established through chromatin remodelling. Microbiology 2008, 154(5):1482-1490.
• [62]Spangler M: Cytosine methylation of Phytophthora sojae by methylated DNA immunoprecipitation. In MS thesis. Biological Sciences Department: Bowling Green State Universit; 2012.
• [63]Goll MG, Bestor TH: Eukaryotic cytosine methyltransferases. Annu Rev Biochem 2005, 74(1):481-514.
• [64]De Riso V, Raniello R, Maumus F, Rogato A, Bowler C, Falciatore A: Gene silencing in the marine diatom Phaeodactylum tricornutum. Nucleic Acids Res 2009, 37(14):e96.
• [65]Montsant A, Allen AE, Coesel S, Martino AD, Falciatore A, Mangogna M, Siaut M, Heijde M, Jabbari K, Maheswari U, Rayko E, Vardi A, Apt KE, Berges JA, Chiovitti A, Davis AK, Thamatrakoln K, Hadi MZ, Lane TW, Lippmeier JC, Martinez D, Parker MS, Pazour GJ, Saito MA, Rokhsar DS, Armbrust EV, Bowler C: Identification and comparative genomic analysis of signaling and regulatory components in the diatom Thalassiosira pseudonana. J Phycol 2007, 43(3):585-604.
• [66]del Campo J, Sieracki ME, Molestina R, Keeling P, Massana R, Ruiz-Trillo I: The others: our biased perspectives of eukaryotic genomes. Trends Ecol Evol 2014, 29(5):252-259.
• [67]Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer ELL, Eddy SR, Bateman A, Finn RD: The Pfam protein families database. Nucleic Acids Res 2012, 40(D1):D290-D301.
• [68]Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG: Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23(21):2947-2948.
• [69]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony methods. Mol Biol Evol 2011, 28(10):2731-2739.
• [70]Drummond AJ, Suchard MA, Xie D, Rambaut A: Bayesian Phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 2012, 29(8):1969-1973.
• [71]Rambaut A, Drummond AJ: Tracer version 1.5, available at. http://tree.bio.ed.ac.uk/software/tracer/ webcite
• [72]Rambaut A, Drummond AJ: FigTree version 1.4, available at. http://tree.bio.ed.ac.uk/software/figtree webcite
• [73]Kooistra W, Gersonde R, Medlin LK, Mann DG: The origin and evolution of the Diatoms: their adaptation to a planktonic existence. In Evolution of Primary Producers in the Sea. Edited by Falkowski PG, Knoll AH. Burlington, MA: Elsevier Academic Press; 2007:207-249.
• [74]Sims PA, Mann DG, Medlin LK: Evolution of the diatoms: insights from fossil, biological and molecular data. Phycologia 2006, 45(4):361-402.
• [75]Matari N, Blair JE: Data from: a multilocus timescale for oomycete evolution estimated under three distinct molecular clock models. Dryad Digital Repository 2014. http://dx.doi.org/10.5061/dryad.39mc5 webcite