Ranking higher taxa using divergence times: a case study in Dothideomycetes

Abstract

The current classification system for the recognition of taxonomic ranks among fungi, especially at high-ranking level, is subjective. With the development of molecular approaches and the availability of fossil calibration data, the use of divergence times as a universally standardized criterion for ranking taxa has now become possible. We can therefore date the origin of Ascomycota lineages by using molecular clock methods and establish the divergence times for the orders and families of Dothideomycetes. We chose Dothideomycetes, the largest class of the phylum Ascomycota, which contains 32 orders, to establish ages at which points orders have split; and Pleosporales, the largest order of Dothideomycetes with 55 families, to establish family divergence times. We have assembled a multi-gene data set (LSU, SSU, TEF1 and RPB2) from 391 taxa representing most family groups of Dothideomycetes and utilized fossil calibration points solely from within the ascomycetes and a Bayesian approach to establish divergence times of Dothideomycetes lineages. Two separated datasets were analysed: (i) 272 taxa representing 32 orders of Dothideomycetes were included for the order level analysis, and (ii) 191 taxa representing 55 families of Pleosporales were included for the family level analysis. Our results indicate that divergence times (crown age) for most orders (20 out of 32, or 63%) are between 100 and 220 Mya, while divergence times for most families (39 out of 55, or 71%) are between 20 and 100 Mya. We believe that divergence times can provide additional evidence to support establishment of higher level taxa, such as families, orders and classes. Taking advantage of this added approach, we can strive towards establishing a standardized taxonomic system both within and outside Fungi. In this study we found that molecular dating coupled with phylogenetic inferences provides no support for the taxonomic status of two currently recognized orders, namely Bezerromycetales and Wiesneriomycetales and these are treated as synonyms of Tubeufiales while Asterotexiales is treated as a synonym of Asterinales. In addition, we provide an updated phylogenetic assessment of Dothideomycetes previously published as the Families of Dothideomycetes in 2013 with a further ten orders and 35 families.

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References

  1. Ariyawansa HA, Tanaka K, Thambugala KM, Phookamsak R, Tian Q, Camporesi E, Hongsanan S, Monkai J, Wanasinghe DN, Mapook A (2014) A molecular phylogenetic reappraisal of the Didymosphaeriaceae (=Montagnulaceae). Fungal Divers 68:69–104

    Article  Google Scholar 

  2. Ariyawansa HA, Thambugala KM, Manamgoda DS, Jayawardena R, Camporesi E, Boonmee S, Wanasinghe DN, Phookamsak R, Hongsanan S, Singtripop C, Chukeatirote E (2015) Towards a natural classification and backbone tree for Pleosporaceae. Fungal Divers 71:85–139

    Article  Google Scholar 

  3. Beimforde C, Feldberg K, Nylinder S, Rikkinen J, Tuovila H, Dörfelt H, Gube M, Jackson DJ, Reitner J, Seyfullah LJ (2014) Estimating the Phanerozoic history of the Ascomycota lineages: combining fossil and molecular data. Mol Phylogenet Evol 78:386–398

    Article  PubMed  Google Scholar 

  4. Berbee ML, Taylor JW (1993) Dating the evolutionary radiations of the true fungi. Can J Bot 71:1114–1127

    Article  Google Scholar 

  5. Bezerra JD, Oliveira RJ, Paiva LM, Silva GA, Groenewald JZ, Crous PW, Souza-Motta CM (2017) Bezerromycetales and Wiesneriomycetales ord. nov. (class Dothideomycetes), with two novel genera to accommodate endophytic fungi from Brazilian cactus. Mycol Prog 16(4):1297–1309

    Article  Google Scholar 

  6. Boehm E, Mugambi G, Miller A, Huhndorf S, Marincowitz S, Spatafora J, Schoch C (2009) A molecular phylogenetic reappraisal of the Hysteriaceae, Mytilinidiaceae and Gloniaceae (Pleosporomycetidae, Dothideomycetes) with keys to world species. Stud Mycol 64:49–83

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. Boonmee S, Rossman AY, Liu JK, Li WJ, Dai DQ, Bhat JD, Jones EG, McKenzie EH, Xu JC, Hyde KD (2014) Tubeufiales, ord. nov., integrating sexual and asexual generic names. Fungal Divers 68:239–298

    Article  Google Scholar 

  8. Boonmee S, D’souza MJ, Luo Z, Pinruan U, Tanaka K, Su H, Bhat DJ, McKenzie EHC, Jones EBG, Taylor JE, Phillips AJL, Hirayama K, Eungwanichayapant PD, Hyde KD (2016) Dictyosporiaceae fam. nov. Fungal Divers 80:457–482

    Article  Google Scholar 

  9. Crous PW, Slippers B, Wingfield MJ, Rheeder J, Marasas WFO, Philips AJL, Alves A, Burgess TI, Barber PA, Groenewald JZ (2006) Phylogenetic lineages in the Botryosphaeriacea. Stud Mycol 55:235–253

    Article  PubMed  PubMed Central  Google Scholar 

  10. Crous PW, Schoch C, Hyde K, Wood A, Gueidan C, De Hoog G, Groenewald J (2009) Phylogenetic lineages in the Capnodiales. Stud Mycol 64:17–47

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. Crous PW, Slippers B, Groenewald JZ, Wingfield MJ (2017) Botryosphaeriaceae: systematics, pathology, and genetics. Fungal Biol 121:305–306

    Article  PubMed  Google Scholar 

  12. Divakar PK, Crespo A, Kraichak E, Leavitt SD, Singh G, Schmitt G, Lumbsch HT (2017) Using a temporal phylogenetic method to harmonize familyand genus-level classification in the largest clade of lichen-forming fungi. Fungal Divers. doi:10.1007/s13225-017-0379-z

    Google Scholar 

  13. Doolittle RF, Feng DF, Tsang S, Cho G, Little E (1996) Determining divergence times of the major kingdoms of living organisms with a protein clock. Science 271:470

    CAS  Article  PubMed  Google Scholar 

  14. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4(5):e88

    Article  PubMed  PubMed Central  Google Scholar 

  15. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and BEAST 1.7. Mol Biol 29:1969–1973

    CAS  Article  Google Scholar 

  16. Gradstein F, Ogg J (2004) Geologic time scale 2004—why, how, and where next! Lethaia 37:175–181

    Article  Google Scholar 

  17. Graur D, Martin W (2004) Reading the entrails of chickens: molecular timescales of evolution and the illusion of precision. Trends Genet 20:80–86

    CAS  Article  PubMed  Google Scholar 

  18. Guatimosim E, Firmino AL, Bezerra JL, Pereira OL, Barreto RW, Crous PW (2015) Towards a phylogenetic reappraisal of Parmulariaceae and Asterinaceae (Dothideomycetes). Persoonia 35:230–241

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. Gueidan C, Ruibal C, de Hoog GS, Schneider H (2011) Rock-inhabiting fungi originated during periods of dry climate in the late Devonian and middle Triassic. Fungal Biol 115:987–996

    Article  PubMed  Google Scholar 

  20. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  21. Heckman DS, Geiser DM, Eidell BR, Stauffer RL, Kardos NL, Hedges SB (2001) Molecular evidence for the early colonization of land by fungi and plants. Science 293:1129–1133

    CAS  Article  PubMed  Google Scholar 

  22. Hedges SB, Kumar S (2004) Precision of molecular time estimates. Trends Genet 20:242–247

    CAS  Article  PubMed  Google Scholar 

  23. Hongsanan S, Li YM, Liu JK, Hofmann T, Piepenbring M, Bhat JD, Boonmee S, Doilom M, Singtripop C, Tian Q, Mapook A, Zeng XY, Bahkali AH, Xu JC, Mortimer PE, Wu HX, Yang JB, Hyde KD (2014) Revision of genera in Asterinales. Fungal Divers 68:1–68

    Article  Google Scholar 

  24. Hongsanan S, Tian Q, Bahkali AH, Yang JB, McKenzie EH, Chomnunti P, Hyde KD (2015) Zeloasperisporiales ord. nov., and two new species of Zeloasperisporium. Cryptogam Mycol 36:301–317

    Article  Google Scholar 

  25. Hyde KD, Jones EBG, Liu JK, Ariyawansa H, Boehm E, Boonmee S, Braun U, Chomnunti P, Crous PW, Dai DQ, Diederich P, Dissanayake A, Doilom M, Doveri F, Hongsanan S, Jayawardena R, Lawrey JD, Li YM, Liu YX, Lucking R, Monkai J, Muggia L, Nelsen MP, Pang KL, Phookamsak R, Senanayake IC, Shearer CA, Suetrong S, Tanaka K, Thambugala KM, Wijayawardene NN, Wikee S, Wu HX, Zhang Y, Aguirre-Hudson B, Alias SA, Aptroot A, Bahkali AH, Bezerra JL, Bhat DJ, Camporesi E, Chukeatirote E, Gueidan C, Hawksworth DL, Hirayama K, De Hoog S, Kang JC, Knudsen K, Li WJ, Li XH, Liu ZY, Mapook A, McKenzie EHC, Miller AN, Mortimer PE, Phillips AJL, Raja HA, Scheuer C, Schumm F, Taylor JE, Tian Q, Tibpromma S, Wanasinghe DN, Wang Y, Xu JC, Yacharoen S, Yan JY, Zhang M (2013) Families of Dothideomycetes. Fungal Divers 63:1–313

    Article  Google Scholar 

  26. Hyde KD, Hongsanan S, Jeewon R, Bhat DJ, McKenzie EHC, Jones EBG, Phookamsak R, Ariyawansa HA, Boonmee S, Zhao Q, Abdel-Aziz FA, Abdel-Wahab MA, Banmai S, Chomnunti P, Cui BK, Daranagama DA, Das K, Dayarathne MC, de Silva NI, Dissanayake AJ, Doilom M, Ekanayaka AH, Gibertoni TB, Góes-Neto A, Huang SK, Jayasiri SC, Jayawardena RS, Konta S, Lee HB, Li WJ, Lin CG, Liu JK, Lu YZ, Luo ZL, Manawasinghe IS, Manimohan P, Mapook A, Niskanen T, Norphanphoun C, Papizadeh M, Perera RH, Phukhamsakda C, Richter C, de Santiago ALCMA, Drechsler-Santos ER, Senanayake IC, Tanaka K, Tennakoon TMDS, Thambugala KM, Tian Q, Tibpromma S, Thongbai B, Vizzini A, Wanasinghe DN, Wijayawardene NN, Wu HX, Yang J, Zeng XY, Zhang H, Zhang JF, Bulgakov TS, Camporesi E, Bahkali AH, Amoozegar AM, Araujo-Neta LS, Ammirati JF, Baghela A, Bhatt RP, Bojantchev S, Buyck B, da Silva GA, de Lima CLF, de Oliveira RJV, de Souza CAF, Dai YC, Dima B, Duong TT, Ercole E, Mafalda-Freire F, Ghosh A, Hashimoto A, Kamolhan S, Kang JC, Karunarathna SC, Kirk PM, Kytövuori I, Lantieri A, Liimatainen K, Liu ZY, Liu XZ, Lücking R, Medardi G, Mortimer PE, Nguyen TTT, Promputtha I, Raj KNA, Reck MA, Lumyong S, Shahzadeh-Fazeli SA, Stadler M, Soudi MR, Su HY, Takahashi T, Tangthirasunun N, Uniyal P, Wang Y, Wen TC, Xu JC, Zhang ZK, Zhao YC, Zhou JZ, Zhu L (2016) Fungal diversity notes 367–490: taxonomic and phylogenetic contributions to fungal taxa. Fungal Divers 80:1–270

    Article  Google Scholar 

  27. Hyde KD, Maharachchikumbura SSN, Hongsanan S, Samarakoon MC, Lücking R, Pem D, Harishchandra D, Jeewon R, Zhao RL, Xu JC, Liu JK, Al-Sadi AM, Bahkali AH, Elgorban AM (2017) The ranking of fungi—a tribute to David L. Hawksworth on his 70th birthday. Fungal Divers. doi:10.1007/s13225-017-0383-3

    Google Scholar 

  28. Jaklitsch WM, Fournier J, Dai DQ, Hyde KD, Voglmayr H (2015) Valsaria and the Valsariales. Fungal Divers 73:159–202

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  29. Jaklitsch WM, Olariaga I, Voglmayr H (2016) Teichospora and the Teichosporaceae. Mycol Prog 15:1–20

    Article  Google Scholar 

  30. James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan C, Fraker E, Miadlikowska J, Lumbsch HT, Rauhut A, Reeb V, Arnold AE, Amtoft A, Stajich JE, Hosaka K, Sung GH, Johnson D, O’Rourke B, Crockett M, Binder M, Curtis JM, Slot JC, Wang Z, Wilson AW, Schüssler A, Longcore JE, O’Donnell K, Mozley- Standridge S, Porter D, Letcher PM, Powell MJ, Taylor JW, White MM, Griffith GW, Davies DR, Humber RA, Morton JB, Sugiyama J, Rossman AY, Rogers JD, Pfister DH, Hewitt D, Hansen K, Hambleton S, Shoemaker RA, Kohlmeyer J, Volkmann- Kohlmeyer B, Spotts RA, Serdani M, Crous PW, Hughes KW, Matsuura K, Langer E, Langer G, Untereiner WA, Lücking R, Büdel B, Geiser DM, Aptroot A, Diederich P, Schmitt I, Schultz M, Yahr R, Hibbett DS, Lutzoni F, McLaughlin DJ, Spatafora JW, Vilgalys R (2006) Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 19:818–822

    Article  Google Scholar 

  31. Jeewon R, Hyde KD (2016) Establishing species boundaries and new taxa among fungi: recommendations to resolve taxonomic ambiguities. Mycosphere 7:1669–1677

    Google Scholar 

  32. Katoh K, Toh H (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9:286–298

    CAS  Article  PubMed  Google Scholar 

  33. Kirk PM, Ainsworth GC, Cannon PF, Minter DW (2008) Ainsworth & Bisby’s dictionary of the fungi, 10th edn. CAB International, Wallingford

    Google Scholar 

  34. Li GJ, Hyde KD, Zhao RL, Hongsanan S, Abdel-Aziz FA, Abdel-Wahab MA, Alvarado P, Alves-Silva G, Ammirati JF, Ariyawansa HA, Baghela A, Bahkali AH, Beug M, Bhat DJ, Bojantchev D, Boonpratuang T, Bulgakov TS, Camporesi E, Boro MC, Ceska O, Chakraborty D, Chen JJ, Chethana KWT, Chomnunti P, Consiglio G, Cui BK, Dai DQ, Dai YC, Daranagama DA, Das K, Dayarathne MC, Crop ED, De Oliveira RJV, de Souza CAF, de Souza JI, Dentinger BTM, Dissanayake AJ, Doilom M, Drechsler-Santos ER, Ghobad-Nejhad M, Gilmore SP, Goes-Neto A, Gorczak M, Haitjema GH, Hapuar-achchi KK, Hashimoto A, He MQ, Henske JK, Hirayama K, Iribarren MJ, Jayasiri SC, Jayawardena RS, Jeon SJ, Jerônimo GH, Jesus AL, Jones EBG, Kang JC, Karunarathna SC, Kirk PM, Konta S, Kuhnert E, Langer E, Lee HS, Lee HB, Li WJ, Li XH, Liimatainen K, Lima DX, Lin CG, Liu JK, Liu XZ, Liu ZY, Luangsa-ard JJ, Lücking R, Lumbsch HT, Lumyong S, Leaño EM, Marano AV, Matsumura M, McKenzie EHC, Mongkol-samrit S, Mortimer PE, Nguyen TTT, Niskanen T, Norphan-phoun C, O’Malley MA, Parnmen S, Pawłowska J, Perera RH, Phookamsak R, Phukhamsakda C, Pires-Zottarelli CLA, Raspé O, Reck MA, Rocha SCO, de Santiago ALCMA, Senanayake IC, Setti L, Shang QJ, Singh SK, Sir EB, Solomon KV, Song J, Srikitikulchai P, Stadler M, Suetrong S, Takahashi H, Takahashi T, Tanaka K, Tang LP, Thambugala KM, Thanakitpipattana D, Theodorou MK, Thongbai B, Thummarukcharoen T, Tian Q, Tibpromma S, Verbeken A, Vizzini A, Vlasák J, Voigt K, Wanasinghe DN, Wang Y, Weerakoon G, Wen HA, Wen TC, Wijayawardene NN, Wongkanoun S, Wrzosek M, Xiao YP, Xu JC, Yan JY, Yang J, Yang SD, Hu Y, Zhang JF, Zhao J, Zhou LW, Persoh D, Phillips AJL, Maharachchikumbura SSN (2016) Fungal diversity notes 253–366: taxonomic and phylogenetic contributions to fungal taxa. Fungal Divers 78:1–237

    Article  Google Scholar 

  35. Liu JK, Phookamsak R, Jones EBG, Zhang Y, Ko-Ko TW, Hu HL, Boonmee S, Doilom M, Chukeatirote E, Bahkali AH, Wang Y, Hyde KD (2011) Astrosphaeriella is polyphyletic, with species in Fissuroma gen. nov., and Neoastrosphaeriella gen. nov. Fungal Divers 51:135–154

    Article  Google Scholar 

  36. Liu JK, Phookamsak R, Doilom M, Wikee S, Li YM, Ariyawansha H, Boonmee S, Chomnunti P, Dai DQ, Bhat JD, Romero AI, Zhuang WY, Monkai J, Jones EBG, Chukeatirote E, Ko-Ko TW, Zhao YC, Wang Y, Hyde KD (2012) Towards a natural classification of Botryosphaeriales. Fungal Divers 57:149–210

    Article  Google Scholar 

  37. Liu JK, Phookamsak R, Dai DQ, Tanaka K, Jones EBG, Xu JC, Chukeatirote E, Hyde KD (2014) Roussoellaceae, a new pleosporalean family to accommodate the genera Neoroussoella gen. nov., Roussoella and Roussoellopsis. Phytotaxa 181:001–033

    Article  Google Scholar 

  38. Liu JK, Hyde KD, Jones EBG, Ariyawansa HA, Bhat DJ, Boonmee S, Maharachchikumbura SSN, McKenzie EHC, Phookamsak R, Phukhamsakda C, Shenoy BD, Abdel-Wahab MA, Buyck B, Chen J, Chethana KWT, Singtripop C, Dai DQ, Dai YC, Daranagama DA, Dissanayake AJ, Doilom M, D’souza MJ, Fan XL, Goonasekara ID, Hirayama K, Hongsanan S, Jayasiri SC, Jayawardena RS, Karunarathna SC, Li WJ, Mapook A, Norphanphoun C, Pang KL, Perera RH, Peršoh D, Pinruan U, Senanayake IC, Somrithipol S, Suetrong S, Tanaka K, Thambugala KM, Tian Q, Tibpromma S, Udayanga D, Wijayawardene NN, Wanasinghe D, Wisitrassameewong K, Zeng XY, Abdel-Aziz FA, Adamčík S, Bahkali AH, Boonyuen N, Bulgakov T, Callac P, Chomnunti P, Greiner K, Hashimoto A, Hofstetter V, Kang JC, Lewis J, Li XH, Liu XZ, Liu ZY, Matsumura M, Mortimer PE, Rambold G, Randrianjohany E, Sato G, Sri-Indrasutdhi V, Tian CM, Verbeken A, von Brackel W, Wang Y, Wen TC, Xu JC, Yan JY, Zhao RL, Camporesi E (2015) Fungal diversity notes 1–110: taxonomic and phylogenetic contributions to fungal species. Fungal Divers 72:1–197

    CAS  Article  Google Scholar 

  39. Liu NG, Ariyawansa HA, Hyde KD, Maharachchikumbura SSN, Zhao RL, Phillips AJL, Jayawardena RS, Thambugala KM, Dissanayake AJ, Wijayawardene NN, Liu JK, Liu ZY, Jeewon R, Jones EBG, Jumpathong J (2016) Perspectives into the value of genera, families and orders in classification. Mycosphere 7:1649–1668. doi:10.5943/mycosphere/7/11/3

    Google Scholar 

  40. Lücking R, Huhndorf S, Pfister DH, Plata ER, Lumbsch HT (2009) Fungi evolved right on track. Mycologia 101:810–822

    Article  PubMed  Google Scholar 

  41. Lumbsch HT, Huhndorf SM (2010) Myconet volume 14. Part one. Outline of Ascomycota—2009. Fieldiana (Life Earth Sci) 1:1–42

    Article  Google Scholar 

  42. Maharachchikumbura SSN, Hyde KD, Jones EBG, McKenzie EHC, Huang SK, Abdel-Wahab MA, Daranagama DA, Dayarathne M, D’souza MJ, Goonasekara ID, Hongsanan S, Jayawardena RS, Kirk PM, Konta S, Liu JK, Liu ZY, Norphanphoun C, Pang KL, Perera RH, Senanayake IC, Shang QJ, Shenoy BD, Xiao YP, Bahkali AH, Kang JC, Somrothipol S, Suetrong S, Wen TC, Xu JC (2015) Towards a natural classification and backbone tree for Sordariomycetes. Fungal Divers 72:199–301

    Article  Google Scholar 

  43. Maharachchikumbura SSN, Hyde KD, Jones EBG, McKenzie EHC, Bhat DJ, Dayarathne MC, Huang SK, Norphanphoun C, Senanayake IC, Perera RH, Shang QJ, Xiao YP, D’souza MJ, Hongsanan S, Jayawardena RS, Daranagama DA, Konta S, Goonasekara ID, Zhuang WY, Jeewon R, Phillips AJL, Abdel-Wahab MA, Al-Sadi AM, Bahkali AH, Boonmee S, Boonyuen N, Cheewangkoon R, Dissanayake AJ, Kang JC, Li QR, Liu JK, Liu XZ, Liu ZY, Luangsa-ard JJ, Pang KL, Phookamsak R, Promputtha I, Suetrong S, Stadler M, Wen TC, Wijayawardene NN (2016) Families of Sordariomycetes. Fungal Divers 79:1–317

    Article  Google Scholar 

  44. Mapook A, Hyde KD, Hongsanan S, Phukhamsakda C, Li JF, Boonmee S (2016) Palawaniaceae fam. nov., a new family (Dothideomycetes, Ascomycota) to accommodate Palawania species and their evolutionary time estimates. Mycosphere 7:1732–1745

    Google Scholar 

  45. McPeek MA, Brown JM (2007) Clade age and not diversification rate explains species richness among animal taxa. Am Nat 169:E000

    Article  Google Scholar 

  46. Mugambi GK, Huhndorf SM (2009) Molecular phylogenetics of Pleosporales: Melanommataceae and Lophiostomataceae re-circumscribed (Pleosporomycetidae, Dothideomycetes, Ascomycota). Stud Mycol 64:103–121

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  47. Nelsen M, Lücking R, Grube M, Mbatchou J, Muggia L, Plata ER, Lumbsch H (2009) Unravelling the phylogenetic relationships of lichenised fungi in Dothideomyceta. Stud Mycol 64:135–144

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  48. Padovan ACB, Sanson GF, Brunstein A, Briones MR (2005) Fungi evolution revisited: application of the penalized likelihood method to a Bayesian fungal phylogeny provides a new perspective on phylogenetic relationships and divergence dates of Ascomycota groups. J Mol Evol 60:726–735

    CAS  Article  PubMed  Google Scholar 

  49. Pérez-Ortega S, Suija A, Crespo A, de los Ríos A (2014) Lichenicolous fungi of the genus Abrothallus (Dothideomycetes: Abrothallales ordo nov.) are sister to the predominantly aquatic Janhulales. Fungal Divers 64:295–304

    Article  Google Scholar 

  50. Pérez-Ortega S, Garrido-Benavent I, Grube M, Olmo R, de los Ríos A (2016) Hidden diversity of marine borderline lichens and a new order of fungi: Collemopsidiales (Dothideomyceta). Fungal Divers 80:285–300

    Article  Google Scholar 

  51. Phookamsak R, Liu JK, McKenzie EH, Manamgoda DS, Ariyawansa H, Thambugala KM, Dai DQ, Camporesi E, Chukeatirote E, Wijayawardene NN, Bahkali AH, Mortimer PE, Xu JC, Hyde KD (2014) Revision of Phaeosphaeriaceae. Fungal Divers 68:159–238

    Article  Google Scholar 

  52. Phookamsak R, Norphanphoun C, Tanaka K, Dai DQ, Luo ZL, Liu JK, Su HY, Bhat DJ, Bahkali AH, Mortimer PE, Xu JC, Hyde KD (2015) Towards a natural classification of Astrosphaeriella-like species; introducing Astrosphaeriellaceae and Pseudoastrosphaeriellaceae fam. nov and Astrosphaeriellopsis, gen. nov. Fungal Divers 74:143–197

    Article  Google Scholar 

  53. Phukhamsakda C, Hongsanan S, Ryberg M, Ariyawansa H, Chomnunti P, Bahkali A, Hyde KD (2016) The evolution of Massarineae with Longipedicellataceae fam. Nov. Mycosphere 7:1713–1731

    Google Scholar 

  54. Prieto M, Wedin M (2013) Dating the diversification of the major lineages of Ascomycota (Fungi). PLoS ONE 8:e65576

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  55. Raja HA, El-Elimat T, Oberlies NH, Shearer CA, Miller AN, Tanaka K, Hashimoto A, Fournier J (2015) Minutisphaerales (Dothideomycetes, Ascomycota): a new order of freshwater ascomycetes including a new family, Minutisphaeraceae, and two new species from North Carolina, USA. Mycologia 107:845–862

    CAS  Article  PubMed  Google Scholar 

  56. Rambaut A (2009) FigTree 1.2.2. http://tree.bio.ed.ac.uk/software/figtree/

  57. Rambaut A, Suchard M, Drummond AJ (2013) Tracer 1.6 http://tree.bio.ed.ac.uk/software/tracer/

  58. Redecker D, Kodner R, Graham LE (2000) Glomalean fungi from the Ordovician. Science 289:1920–1921

    CAS  Article  PubMed  Google Scholar 

  59. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572

    CAS  Article  PubMed  Google Scholar 

  60. Rutschmann F, Eriksson T, Salim KA, Conti E (2007) Assessing calibration uncertainty in molecular dating: the assignment of fossils to alternative calibration points. Syst Biol 56:591–608

    CAS  Article  PubMed  Google Scholar 

  61. Samarakoon M, Hyde KD, Promputtha I, Hongsanan S, Ariyawansa HA, Maharachchikumbura SSN, Daranagama A, Stadler M, Mapook A (2016) Evolution of Xylariomycetidae (Ascomycota: Sordariomycetes). Mycosphere 7:1746–1791

    Google Scholar 

  62. Sauquet H, Ho SYW, Gandolfo MA, Jordan GJ, Wilf P, Cantrill DJ, Bayly MJ, Bromham L, Brown GK, Carpenter RJ, Lee DM, Murphy DJ, Sniderman JMK, Udovicic F (2012) Testing the impact of calibration on molecular divergence times using a fossil-rich group: the case of Nothofagus (Fagales). Syst Biol 61:289–313

    Article  PubMed  Google Scholar 

  63. Schoch CL, Shoemaker RA, Seifert KA, Hambleton S, Spatafora JW, Crous PW (2006) A multigene phylogeny of the Dothideomycetes using four nuclear loci. Mycologia 98:1041–1052

    CAS  Article  PubMed  Google Scholar 

  64. Schoch CL, Crous PW, Groenewald JZ, Boehm EWA, Burgess TI, de Gruyter J, de Hoog GS, Dixon LJ, Grube M, Gueidan C, Harada Y, Hatakeyama S, Hirayama K, Hosoya T, Huhndorf SM, Hyde KD, Jones EBG, Kohlmeyer J, Kruys Å, Li YM, Lücking R, Lumbsch HT, Marvanová L, Mbatchou JS, McVay AH, Miller AN, Mugambi GK, Muggia L, Nelsen MP, Nelson P, Owensby CA, Phillips AJL, Phongpaichit S, Pointing SB, Pujade-Renaud V, Raja HA, Rivas Plata E, Robbertse B, Ruibal C, Sakayaroj J, Sano T, Selbmann L, Shearer CA, Shirouzu T, Slippers B, Suetrong S, Tanaka K, Volkmann-Kohlmeyer B, Wingfield MJ, Wood AR, Woudenberg JHC, Yonezawa H, Zhang Y, Spatafora JW (2009a) A class-wide phylogenetic assessment of Dothideomycetes. Stud Mycol 64:1–15

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  65. Schoch CL, Sung GH, López-Giráldez F, Townsend JP, Miadlikowska J, Hofstetter V, Robbertse B, Mathen PB, Kauff F, Wang Z, Gueidan CC, Andrie RM, Trippe K, Ciufetti LM, Wynns A, Fraker E, Hodkinson BP, Bonito G, Groenewald JZ, Arzanlou M, De-Hoog GS, Crous PW, Hewitt D, Pfister DH, Peterson K, Gryzenhout M, Wingfield MJ, Aptroot A, Suh SO, Blackwell M, Hillis DM, Griffith GW, Castlebury LA, Rossman AY, Lumbsch HT, Lücking R, Büdel B, Rauhut A, Diederich P, Ertz D, Geiser DM, Hosaka K, Inderbitzin P, Kohlmeyer J, Volkmann-Kohlmeyer B, Mostert L, O’Donnell K, Sipman H, Rogers J, Shoemaker RA, Sugiyama J, Summerbell RC, Untereiner W, Johnston PR, Stenroos S, Zuccaro A, Dyer PS, Crittenden PD, Cole MS, Hansen K, Trappe JM, Yahr R, Lutzoni FO, Spatafora JW (2009b) The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. Syst Biol 58:224–239

    CAS  Article  PubMed  Google Scholar 

  66. Shearer CA, Raja HA, Miller AN, Nelson P, Tanaka K, Hirayama K, Marvanová L, Hyde KD, Zhang Y (2009) The molecular phylogeny of freshwater Dothideomycetes. Stud Mycol 64:145–153

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  67. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57:758–771. doi:10.1080/10635150802429642

    Article  PubMed  Google Scholar 

  68. Suetrong S, Schoch CL, Spatafora JW, Kohlmeyer J, Volkmann-Kohlmeyer B, Sakayaroj J, Phongpaichit S, Tanaka K, Hirayama K, Jones EBG (2009) Molecular systematics of the marine Dothideomycetes. Stud Mycol 64:155–173

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  69. Tanaka K, Hirayama K, Yonezawa H, Hatakeyama S, Harada Y, Sano T, Shirouzu T, Hosoya T (2009) Molecular taxonomy of bambusicolous fungi: Tetraplosphaeriaceae, a new pleosporalean family with Tetraploa-like anamorphs. Stud Mycol 64:175–209

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  70. Tanaka K, Hirayama K, Yonezawa H, Sato G, Toriyabe A, Kudo H, Hashimoto A, Matsumura M, Harada Y, Kurihara Y (2015) Revision of the Massarineae (Pleosporales, Dothideomycetes). Stud Mycol 82:75–136

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  71. Taylor JW, Berbee ML (2006) Dating divergences in the Fungal Tree of Life: review and new analyses. Mycologia 98:838–849

    Article  PubMed  Google Scholar 

  72. Thambugala KM, Hyde KD, Tanaka K, Tian Q, Wanasinghe DN, Ariyawansa HA, Jayasiri SC, Boonmee S, Camporesi E, Hashimoto A, Hirayama K, Schumacher RK, Promputtha I, Liu ZY (2015) Towards a natural classification and backbone tree for Lophiostomataceae, Floricolaceae, and Amorosiaceae fam. nov. Fungal Divers 74:199–266

    Article  Google Scholar 

  73. Tian Q, Liu JK, Hyde KD, Wanasinghe DN, Boonmee S, Jayasiri SC, Luo ZL, Taylor JE, Phillips AJ, Bhat DJ, Li WJ, Ariyawansa H, Thambugala KM, Jones EBG, Chomnunti P, Bahkali AH, Xu JC, Camporesi E (2015) Phylogenetic relationships and morphological reappraisal of Melanommataceae (Pleosporales). Fungal Divers 74:267–324

    Article  Google Scholar 

  74. Wijayawardene NN, Crous PW, Kirk PM, Hawksworth DL, Boonmee S, Braun U, Dai DQ, Dsouza MJ, Diederich P, Dissanayake A, Doilom M, Hongsanan S, Jones EBG, Groenewald JZ, Jayawar-dena R, Lawrey JD, Liu JK, Lücking R, Madrid H, Manamgoda DS, Muggia L, Nelsen MP, Phookamsak R, Suetrong S, Tanaka K, Thambugala KM, Wanasinghe DN, Wikee S, Zhang Y, Aptroot A, Ariyawansa HA, Bahkali AH, Bhat DJ, Gueidan C, Chomnunti P, De Hoog GS, Knudsen K, Li WJ, McKenzie EHC, Miller AN, Phillips AJL, Piątek M, Raja HA, Shivas RS, Slippers B, Taylor JE, Tian Q, Wang Y, Woudenberg JHC, Cai L, Jaklitsch WM, Hyde KD (2014) Naming and outline of Dothideomycetes–2014 including proposals for the protection or suppression of generic names. Fungal Divers 69:1–55

    Article  PubMed  PubMed Central  Google Scholar 

  75. Zhang Y, Schoch CL, Fournier J, Crous PW, De Gruyter J, Woudenberg JHC, Hirayama K, Tanaka K, Pointing SB, Spatafora JW, Hyde KD (2009) Multi-locus phylogeny of Pleosporales: a taxonomic, ecological and evolutionary re-evaluation. Stud Mycol 64:85–102

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  76. Zhang Y, Crous PW, Schoch CL, Hyde KD (2012) Pleosporales. Fungal Divers 53:1–221

    CAS  Article  PubMed  Google Scholar 

  77. Zhao RL, Zhou JL, Chen J, Margaritescu S, Sánchez-Ramirez S, Hyde KD, Callac P, Parra LA, Li GJ, Moncalvo JM (2016) Towards standardizing taxonomic ranks using divergence times-a case study for reconstruction of the Agaricus taxonomic system. Fungal Divers 78:239–292. doi:10.1007/s13225-016-0357-x

    Article  Google Scholar 

  78. Zhao RL, Li GJ, Sánchez-Ramírez S, Stata M, Moncalvo J-M, Yang ZL, Wu G, Dai YC, He SH, Cui BK, Zhou JL, Wu F, He MQ, Hyde KD (2017) A six-genes phylogenetic overview of Basidiomycota and allied phyla with estimated divergence times of higher taxa and a phyloproteomics perspective. Fungal Divers. doi:10.1007/s13225-017-0381-5

    Google Scholar 

  79. Zhaxybayeva O, Gogarten JP (2002) Bootstrap, Bayesian probability and maximum likelihood mapping: exploring new tools for comparative genome analyses. BMC Genomics 3:4

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was funded by grants of the National Natural Science Foundation of China (NSFC 31210103919; 31600032; 31360015), Science and Technology Foundation of Guizhou Province (LH [2015]7061) and the Research of Featured Microbial Resources and Diversity Investigation in Southwest Karst area (Project No. 2014FY120100.). Jian-Kui Liu thanks Dr. Bang Feng (Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, China) for his valuable help with phylogenetic analysis. Dr. Rui-Lin Zhao and Dr. H.A. Ariyawansa are thanked for their valuable suggestions. Dr. Hong Luo is thanked for commenting the manuscript. K.D. Hyde thanks the Chinese Academy of Sciences, Project Number 2013T2S0030, for the award of Visiting Professorship for Senior International Scientists at Kunming Institute of Botany. K.D. Hyde also extends his appreciation to the Thailand Research Fund (TRF) Grant (RSA5980068) and National Research Council of Thailand (NRCT) for Grants (60201000201; 592010200112). Alan JL Phillips acknowledges the support from Biosystems and Integrative Sciences Institute (BioISI, FCT/UID/Multi/04046/2013).

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Correspondence to Qi Zhao.

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Liu, JK., Hyde, K.D., Jeewon, R. et al. Ranking higher taxa using divergence times: a case study in Dothideomycetes. Fungal Diversity 84, 75–99 (2017). https://doi.org/10.1007/s13225-017-0385-1

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Keywords

  • BEAST
  • Clade age
  • Classification
  • Calibration
  • Family
  • Order
  • Phylogeny
  • Pleosporales