Abstract
Botryosphaeria is a commonly encountered and economically important genus whose species are widely distributed phytopathogens as well as endophytes, necrotrophs and saprobes. We herein provide insights into botryosphaeriaceous microfungi associated with Magnolia species in Thailand. Phylogeny based on combined ITS, tef1 and tub2 sequences coupled with their morphological characteristics verified the status of the new collection as new host records of Botryosphaeria kuwatsukai and B. puerensis from Magnolia species. Prior to this investigation, only a few Botryosphaeria species have been discovered in Thailand. This is the first account of B. kuwatsukai from Magnolia species as well as the first geographical record in Thailand. Furthermore, we reveal endophytic and saprobic B. puerensis in Thailand for the first time and its first association with Magnolia species. Along with the host associations and geographic distributions, we also emphasized the lifestyles of Botryosphaeria species that are used in the current phylogenetic analyses.
References
Abdollahzadeh, J., Zare, R. & Phillips, A.J. (2013) Phylogeny and taxonomy of Botryosphaeria and Neofusicoccum species in Iran, with description of Botryosphaeria scharifii sp. nov. Mycologia 105: 210–220. https://doi.org/10.3852/12-107
Alves, A., Correia, A., Luque, J. & Phillips, A. (2004) Botryosphaeria corticola, sp. nov. on Quercus species, with notes and description of Botryosphaeria stevensii and its anamorph, Diplodia mutila. Mycologia 96: 598–613. https://doi.org/10.1080/15572536.2005.11832956
Ariyawansa, H.A., Hyde, K.D., Liu, J.K., Wu, S.P. & Liu, Z.Y. (2016) Additions to karst Fungi 1: Botryosphaeria minutispermatia sp. nov., from Guizhou Province, China. Phytotaxa 275 (1): 35–44. https://doi.org/10.11646/phytotaxa.275.1.4
Barr, M.E. (1972) Preliminary studies on the Dothideales in temperate North America. Contributions from the University of Michigan Herbarium 9: 523–638.
Barr, M.E. (1987) Prodromus to Class Loculoascomycetes. University of Massachusetts, Amherst, MA.
Carbone, I. & Kohn, L.M. (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91: 553–556. https://doi.org/10.1080/00275514.1999.12061051
Cesati, V. & De Notaris, G. (1863) Schema di classificazione degli sferiacei italici aschigeri piu’ omeno appartenenti al genere Sphaeria nell’antico significato attribuitoglide Persoon. Commentario della Società Crittogamologica Italiana 14: 177–240.
Chen, Y.Y., Dissanayake, A.J., Liu, Z.Y. & Liu, J.K.J. (2020) Additions to Karst Fungi 4: Botryosphaeria spp. associated with woody hosts in Guizhou province, China including B. guttulata sp. nov. Phytotaxa 454 (3): 186–202. https://doi.org/10.11646/phytotaxa.454.3.2
Crous, P.W., Slippers, B., Wingfield, M.J., Rheeder, J., Marasas, W.F.O., Phillips, A., Alves, A., Burgess, T.I., Barber, P.A. & Groenewald, J.Z. (2006) Resolving phylogenetic lineages in the Botryosphaeriaceae. Studies in Mycology 55: 235–253. https://doi.org/10.3114/sim.55.1.235
Darge, W.A. & Woldemariam, S.S. (2021) Botryosphaeria tree fungal pathogens and their diversity. International Journal of Phytopathology 10: 49–56. https://doi.org/10.33687/phytopath.010.01.3447
Desprez-Loustau, M.L., Marcais, B., Nageleisen, L.M., Piou, D. & Vannini, A. (2006) Interactive effects of drought and pathogens in forest trees. Annals of Forest Science 63: 597–612. https://doi.org/10.1051/forest:2006040
Dissanayake, A.J., Phillips, A.J.L., Hyde, K.D. & Li, X.H. (2016) Botryosphaeriaceae: Current status of genera and species. Mycosphere 7: 1001–1073. https://doi.org/10.5943/mycosphere/si/1b/13
Dou, Z.P., Zhao, L., He, W. & Zhang, Y. (2021) Two novel species of Botryosphaeria causing stem canker of blueberries from China. Mycosystema 40: 473–486. https://doi.org/10.13346/j.mycosystema.200333
Farr, D.F. & Rossman, A.Y. (2022) Fungal Databases, U.S. National Fungus Collections, ARS, USDA. Available from: https://nt.ars-grin.gov/fungaldatabases/ (accessed 19 September 2022)
Glass, N.L. & Donaldson, G.C. (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Applied and Environmental Microbiology 61: 1323–1330. https://doi.org/10.1128/aem.61.4.1323-1330.1995
Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 1999 41: 95–98.
Hara, K. (1930) Pathologia Agriculturalis Plantarum. Yokendo, Tokyo, pp. 481–483. [in Japanese]
Hattori, Y., Ando, Y., Sasaki, A., Uechi, N. & Nakashima, C. (2021) Taxonomical study of noteworthy species of Botryosphaeria in Japan. Mycobiology 49: 122–132. https://doi.org/10.1080/12298093.2021.1895486
Hsieh, W. & Chen, C. (1994) Sivanesania, a new botryosphaeriaceous ascomycete genus on Rubus from Taiwan. Mycological Research 98: 44–46.
Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755. https://doi.org/10.1093/bioinformatics/17.8.754
Inderbitzin, P., Bostock, R.M., Trouillas, F.P. & Michailides, T.J. (2010) A six-locus phylogeny reveals high species diversity in Botryosphaeriaceae from California almond. Mycologia 102: 1350–1368. https://doi.org/10.3852/10-006
Index Fungorum (2022) Available from: http://www.indexfungorum.org/names/names.asp (accessed 30 September 2022)
Jayasiri, S.C., Hyde, K.D., Ariyawansa, H.A., Bhat, J., Buyck, B., Cai, L., Dai, Y.C., Abd Elsalam, K.A., Ertz, D., Hidayat, I., Jeewon, R., Jones, E.B.G., Bahkali, A.H., Karunarathna, S.C., Liu, J.K., Luangsa-ard, J.J., Lumbsch, H.T., Maharachchikumbura, S.S.N., McKenzie, E.H.C., Moncalvo, J.M., Ghobad-Nejhad, M., Nilsson, H., Pang, K., Pereira, O.L., Phillips, A.J.L., Raspé, O., Rollins, A.W., Romero, A.I., Etayo, J., Selçuk, F., Stephenson, S.L., Suetrong, S., Taylor, J.E., Tsui, C.K.M., Vizzini, A., Abdel-Wahab, M.A., Wen, T.C., Boonmee, S., Dai, D.Q., Daranagama, D.A., Dissanayake, A.J., Ekanayaka, A.H., Fryar, S.C., Hongsanan, S., Jayawardena, R.S., Li, W.J., Perera, R.H., Phookamsak, R., De Silva, N.I., Thambugala, K.M., Tian, Q., Wijayawardene, N.N., Zhao, R.L., Zhao, Q., Kang, J.C. & Promputtha, I. (2015) The Faces of Fungi database: fungal names linked with morphology, phylogeny and human impacts. Fungal Diversity 74: 3–18. https://doi.org/10.1007/s13225-015-0351-8
Lazzizera, C., Frisullo, S., Alves, A. & Phillips, A.J.L. (2008) Morphology, phylogeny and pathogenicity of Botryosphaeria and Neofusicoccum species associated with drupe rot of olives in southern Italy. Plant Pathology 57: 948–956. https://doi.org/10.1111/j.1365-3059.2008.01842.x
Li, G.Q., Liu, F.F., Li, J.Q., Liu, Q.L. & Chen, S.F. (2018) Botryosphaeriaceae from Eucalyptus plantations and adjacent plants in China. Persoonia-Molecular Phylogeny and Evolution of Fungi 40: 63–95. https://doi.org/10.3767/persoonia.2018.40.03
Li, G.Q., Slippers, B., Wingfield, M.J. & Chen, S.F. (2020) Variation in Botryosphaeriaceae from Eucalyptus plantations in Yunnan Province in southwestern China across a climatic gradient. IMA Fungus 11: 1–49. https://doi.org/10.1186/s43008-020-00043-x
Liu, J.K., Phookamsak, R., Doilom, M., Wikee, S., Li, Y.M., Ariyawansha, H., Boonmee, S., Chomnunti, P., Dai, D.Q., Bhat, J.D. & Romero, A.I. (2012) Towards a natural classification of Botryosphaeriales. Fungal Diversity 57: 149–210. https://doi.org/10.1007/s13225-012-0207-4
Mehl, J.W., Slippers, B., Roux, J. & Wingfield, M.J. (2017) Overlap of latent pathogens in the Botryosphaeriaceae on a native and agricultural host. Fungal Biology 121: 405–419. https://doi.org/10.1016/j.funbio.2016.07.015
Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Gateway Computing Environments Workshop (GCE): 1–8. https://doi.org/10.1109/GCE.2010.5676129
Miura, M. (1917) Ringo no Byoki. Shokabo, Tokyo, pp. 106–109. [in Japanese]
Moral, J., Morgan D., Trapero A. & Michailides, T.J. (2019) Ecology and epidemiology of diseases of nut crops and olives caused by Botryosphaeriaceae fungi in California and Spain. Plant Disease 103: 1809–1827. https://doi.org/10.1094/PDIS-03-19-0622-FE
Nose, T. (1933) On the ring rot of pears and the causal organism, especially on its perfect generation Physalospora piricola. Annals of the Agricultural Experiment Station 7: 156–163. [in Japanese]
Pennycook, S.R. & Samuels, G.J. (1985) Botryosphaeria and Fusicoccum species associated with ripe fruit rot of Actinidia deliciosa (Kiwifruit) in New Zealand. Mycotaxon 24: 445–458.
Phillips, A.J.L., Alves, A., Abdollahzadeh, J., Slippers, B., Wingfield, M.J., Groenewald, J.Z. & Crous, P.W. (2013) The Botryosphaeriaceae: genera and species known from culture. Studies in Mycology 55: 53–63. https://doi.org/10.3114/sim0021
Phillips, A.J.L., Alves, A., Pennycook, S.R., Johnston, P.R., Ramaley, A., Akulov, A. & Crous, P.W. (2008) Resolving the phylogenetic and taxonomic status of darkspored teleomorph genera in the Botryosphaeriaceae. Persoonia 21: 29–55. https://doi.org/10.3767/003158508X340742
Phillips, A.J., Hyde, K.D., Alves, A. & Liu, J.K. (2019) Families in Botryosphaeriales: a phylogenetic, morphological and evolutionary perspective. Fungal Diversity 94: 1–22. https://doi.org/10.1007/s13225-018-0416-6
Posada, D. & Crandall, K.A. (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817–818. https://doi.org/10.1093/bioinformatics/14.9.817
Qiu, Y., Savocchia, S., Steel, C.C. & Ash, G.J. (2008) Botryosphaeria dothidea associated with grapevine trunk disease in south-eastern Australia. Australasian Plant Pathology 37: 482–485. https://doi.org/10.1071/AP08045
Rambaut, A. & Drummond, A. (2008) FigTree: Tree figure drawing tool, version 1.2. 2. Institute of Evolutionary Biology, University of Edinburgh.
Senanayake, I.C., Rathnayaka, A.R., Marasinghe, D.S., Calabon, M.S., Gentekaki, E., Lee, H.B., Hurdeal, V.G., Pem, D., Dissanayake, L.S., Wijesinghe, S.N. & Bundhun, D. (2020) Morphological approaches in studying fungi: Collection, examination, isolation, sporulation and preservation. Mycosphere 11: 2678–2754. https://doi.org/10.5943/mycosphere/11/1/20
Shoemaker, R.A. (1964) Conidial states of some Botryosphaeria species on Vitis and Quercus. Canadian Journal of Botany 42: 1297–1301. https://doi.org/10.1139/b64-12
Slippers, B., Boissin, E., Phillips, A.J.L., Groenewald, J.Z., Wingfield, M.J., Postma A., Burgess, T. & Crous, P.W. (2013). Phylogenetic lineages in the Botryosphaeriales: A systematic and evolutionary framework. Studies in Mycology 76: 31–49. https://doi.org/10.3114/sim0020
Slippers, B., Johnson, G.I. & Crous, P.W. (2005) Phylogenetic and morphological reevaluation of the Botryosphaeria species causing diseases of Mangifera indica. Mycologia 97: 99–110. https://doi.org/10.1080/15572536.2006.11832843
Slippers, B., Crous, P.W., Denman, S., Coutinho, T.A., Wingfield, B.D. & Wingfield, M.J. (2004) Combined multiple gene genealogies and phenotypic characters differentiate several species previously identified as Botryosphaeria dothidea. Mycologia 96: 83–101. https://doi.org/10.1080/15572536.2005.11833000
Slippers, B., Roux, J., Wingfield, M.J., Van der Walt, F.J.J., Jami, F., Mehl, J.W.M. & Marais, G.J. (2014) Confronting the constraints of morphological taxonomy in the Botryosphaeriales. Persoonia-Molecular Phylogeny and Evolution of Fungi 33: 155–168. https://doi.org/10.3767/003158514X684780
Slippers, B. & Wingfield, M.J. (2007) Botryosphaeriaceae as endophytes and latent pathogens of woody plants: diversity, ecology and impact. Fungal Biology Reviews 21: 90–106. https://doi.org/10.1016/j.fbr.2007.06.002
Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690. https://doi.org/10.1093/bioinformatics/btl446
Stamatakis, A., Hoover, P. & Rougemont, J. (2008) A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology 57: 758–771. https://doi.org/10.1080/10635150802429642
Taylor, K., Barber, P.A., Hardy, G.E.S.J. & Burgess, T.I. (2009) Botryosphaeriaceae from tuart (Eucalyptus gomphocephala) woodland, including descriptions of four new species. Mycological Research 113: 337–353. https://doi.org/10.1016/j.mycres.2008.11.010
Theissen, F. & Sydow, H. (1915) Die Dothideales. Kritischsystematische Originalunter suchungen (Continuatio). Annales Mycologici 13: 431–746.
Theissen, F. & Sydow, H. (1918) Vorentwürfe zu den Pseudosphaeriales. Annales Mycologici 16: 1–34.
Trakunyingcharoen, T., Lombard, L., Groenewald, J.Z., Cheewangkoon, R., To-Anun, C. & Crous, P.W. (2015) Caulicolous Botryosphaeriales from Thailand. Persoonia-Molecular Phylogeny and Evolution of Fungi 34: 87–99. https://doi.org/10.3767/003158515X685841
von Höhnel, F. (1909) Fragmente zur Mykologie (VII. Mitteilung, Nr. 289 bis 353). Sitzungsberichte der Kaiserlichen Akademie der Wissenschaften. Mathematisch-Naturwissenschaftliche Classe 1118: 813–904
White, T.J., Bruns, T., Lee, S.J.W.T. & Taylor, J. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis, M.A., Gelfand, D.H., Sninsky, J.J. & White, T.J. (Eds.) PCR Protocols: a guide to methods and applications. Academic Press, San Diego, CA, USA, pp. 315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1
Wijayawardene, N.N., Hyde, K.D., Wanasinghe, D.N., Papizadeh, M., Goonasekara, I.D., Camporesi, E., Bhat, D.J., McKenzie, E.H., Phillips, A.J., Diederich, P. & Tanaka, K. (2016) Taxonomy and phylogeny of dematiaceous coelomycetes. Fungal Diversity 77: 1–316. https://doi.org/10.1007/s13225-016-0360-2
Xu, C., Wang, C., Ju, L., Zhang, R., Biggs, A.R., Tanaka, E., Li, B. & Sun, G. (2015) Multiple locus genealogies and phenotypic characters reappraise the causal agents of apple ring rot in China. Fungal Diversity 71: 215–231. https://doi.org/10.1007/s13225-014-0306-5
Yamada, K.D., Tomii, K. & Katoh, K. (2016) Application of the MAFFT sequence alignment program to large data-reexamination of the usefulness of chained guide trees. Bioinformatics 32: 3246–3251. https://doi.org/10.1093/bioinformatics/btw412
Zhang, W., Groenewald, J.Z., Lombard, L., Schumacher, R.K., Phillips, A.J.L. & Crous, P.W. (2021) Evaluating species in Botryosphaeriales. Persoonia-Molecular Phylogeny and Evolution of Fungi 46: 63–115. https://doi.org/10.3767/persoonia.2021.46.03
Zhou, Y., Dou, Z., He, W., Zhang, X. & Zhang, Y. (2016) Botryosphaeria sinensia sp. nov., a new species from China. Phytotaxa 245 (1): 43–50. https://doi.org/10.11646/phytotaxa.245.1.4
Zhou, Y.P., Zhang, M., Dou, Z.P. & Zhang, Y. (2017) Botryosphaeria rosaceae sp. nov. and B. ramosa, new botryosphaeriaceous taxa from China. Mycosphere 8: 162–171. https://doi.org/10.5943/mycosphere/8/2/2
Alves, A., Correia, A., Luque, J. & Phillips, A. (2004) Botryosphaeria corticola, sp. nov. on Quercus species, with notes and description of Botryosphaeria stevensii and its anamorph, Diplodia mutila. Mycologia 96: 598–613. https://doi.org/10.1080/15572536.2005.11832956
Ariyawansa, H.A., Hyde, K.D., Liu, J.K., Wu, S.P. & Liu, Z.Y. (2016) Additions to karst Fungi 1: Botryosphaeria minutispermatia sp. nov., from Guizhou Province, China. Phytotaxa 275 (1): 35–44. https://doi.org/10.11646/phytotaxa.275.1.4
Barr, M.E. (1972) Preliminary studies on the Dothideales in temperate North America. Contributions from the University of Michigan Herbarium 9: 523–638.
Barr, M.E. (1987) Prodromus to Class Loculoascomycetes. University of Massachusetts, Amherst, MA.
Carbone, I. & Kohn, L.M. (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91: 553–556. https://doi.org/10.1080/00275514.1999.12061051
Cesati, V. & De Notaris, G. (1863) Schema di classificazione degli sferiacei italici aschigeri piu’ omeno appartenenti al genere Sphaeria nell’antico significato attribuitoglide Persoon. Commentario della Società Crittogamologica Italiana 14: 177–240.
Chen, Y.Y., Dissanayake, A.J., Liu, Z.Y. & Liu, J.K.J. (2020) Additions to Karst Fungi 4: Botryosphaeria spp. associated with woody hosts in Guizhou province, China including B. guttulata sp. nov. Phytotaxa 454 (3): 186–202. https://doi.org/10.11646/phytotaxa.454.3.2
Crous, P.W., Slippers, B., Wingfield, M.J., Rheeder, J., Marasas, W.F.O., Phillips, A., Alves, A., Burgess, T.I., Barber, P.A. & Groenewald, J.Z. (2006) Resolving phylogenetic lineages in the Botryosphaeriaceae. Studies in Mycology 55: 235–253. https://doi.org/10.3114/sim.55.1.235
Darge, W.A. & Woldemariam, S.S. (2021) Botryosphaeria tree fungal pathogens and their diversity. International Journal of Phytopathology 10: 49–56. https://doi.org/10.33687/phytopath.010.01.3447
Desprez-Loustau, M.L., Marcais, B., Nageleisen, L.M., Piou, D. & Vannini, A. (2006) Interactive effects of drought and pathogens in forest trees. Annals of Forest Science 63: 597–612. https://doi.org/10.1051/forest:2006040
Dissanayake, A.J., Phillips, A.J.L., Hyde, K.D. & Li, X.H. (2016) Botryosphaeriaceae: Current status of genera and species. Mycosphere 7: 1001–1073. https://doi.org/10.5943/mycosphere/si/1b/13
Dou, Z.P., Zhao, L., He, W. & Zhang, Y. (2021) Two novel species of Botryosphaeria causing stem canker of blueberries from China. Mycosystema 40: 473–486. https://doi.org/10.13346/j.mycosystema.200333
Farr, D.F. & Rossman, A.Y. (2022) Fungal Databases, U.S. National Fungus Collections, ARS, USDA. Available from: https://nt.ars-grin.gov/fungaldatabases/ (accessed 19 September 2022)
Glass, N.L. & Donaldson, G.C. (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Applied and Environmental Microbiology 61: 1323–1330. https://doi.org/10.1128/aem.61.4.1323-1330.1995
Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 1999 41: 95–98.
Hara, K. (1930) Pathologia Agriculturalis Plantarum. Yokendo, Tokyo, pp. 481–483. [in Japanese]
Hattori, Y., Ando, Y., Sasaki, A., Uechi, N. & Nakashima, C. (2021) Taxonomical study of noteworthy species of Botryosphaeria in Japan. Mycobiology 49: 122–132. https://doi.org/10.1080/12298093.2021.1895486
Hsieh, W. & Chen, C. (1994) Sivanesania, a new botryosphaeriaceous ascomycete genus on Rubus from Taiwan. Mycological Research 98: 44–46.
Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755. https://doi.org/10.1093/bioinformatics/17.8.754
Inderbitzin, P., Bostock, R.M., Trouillas, F.P. & Michailides, T.J. (2010) A six-locus phylogeny reveals high species diversity in Botryosphaeriaceae from California almond. Mycologia 102: 1350–1368. https://doi.org/10.3852/10-006
Index Fungorum (2022) Available from: http://www.indexfungorum.org/names/names.asp (accessed 30 September 2022)
Jayasiri, S.C., Hyde, K.D., Ariyawansa, H.A., Bhat, J., Buyck, B., Cai, L., Dai, Y.C., Abd Elsalam, K.A., Ertz, D., Hidayat, I., Jeewon, R., Jones, E.B.G., Bahkali, A.H., Karunarathna, S.C., Liu, J.K., Luangsa-ard, J.J., Lumbsch, H.T., Maharachchikumbura, S.S.N., McKenzie, E.H.C., Moncalvo, J.M., Ghobad-Nejhad, M., Nilsson, H., Pang, K., Pereira, O.L., Phillips, A.J.L., Raspé, O., Rollins, A.W., Romero, A.I., Etayo, J., Selçuk, F., Stephenson, S.L., Suetrong, S., Taylor, J.E., Tsui, C.K.M., Vizzini, A., Abdel-Wahab, M.A., Wen, T.C., Boonmee, S., Dai, D.Q., Daranagama, D.A., Dissanayake, A.J., Ekanayaka, A.H., Fryar, S.C., Hongsanan, S., Jayawardena, R.S., Li, W.J., Perera, R.H., Phookamsak, R., De Silva, N.I., Thambugala, K.M., Tian, Q., Wijayawardene, N.N., Zhao, R.L., Zhao, Q., Kang, J.C. & Promputtha, I. (2015) The Faces of Fungi database: fungal names linked with morphology, phylogeny and human impacts. Fungal Diversity 74: 3–18. https://doi.org/10.1007/s13225-015-0351-8
Lazzizera, C., Frisullo, S., Alves, A. & Phillips, A.J.L. (2008) Morphology, phylogeny and pathogenicity of Botryosphaeria and Neofusicoccum species associated with drupe rot of olives in southern Italy. Plant Pathology 57: 948–956. https://doi.org/10.1111/j.1365-3059.2008.01842.x
Li, G.Q., Liu, F.F., Li, J.Q., Liu, Q.L. & Chen, S.F. (2018) Botryosphaeriaceae from Eucalyptus plantations and adjacent plants in China. Persoonia-Molecular Phylogeny and Evolution of Fungi 40: 63–95. https://doi.org/10.3767/persoonia.2018.40.03
Li, G.Q., Slippers, B., Wingfield, M.J. & Chen, S.F. (2020) Variation in Botryosphaeriaceae from Eucalyptus plantations in Yunnan Province in southwestern China across a climatic gradient. IMA Fungus 11: 1–49. https://doi.org/10.1186/s43008-020-00043-x
Liu, J.K., Phookamsak, R., Doilom, M., Wikee, S., Li, Y.M., Ariyawansha, H., Boonmee, S., Chomnunti, P., Dai, D.Q., Bhat, J.D. & Romero, A.I. (2012) Towards a natural classification of Botryosphaeriales. Fungal Diversity 57: 149–210. https://doi.org/10.1007/s13225-012-0207-4
Mehl, J.W., Slippers, B., Roux, J. & Wingfield, M.J. (2017) Overlap of latent pathogens in the Botryosphaeriaceae on a native and agricultural host. Fungal Biology 121: 405–419. https://doi.org/10.1016/j.funbio.2016.07.015
Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Gateway Computing Environments Workshop (GCE): 1–8. https://doi.org/10.1109/GCE.2010.5676129
Miura, M. (1917) Ringo no Byoki. Shokabo, Tokyo, pp. 106–109. [in Japanese]
Moral, J., Morgan D., Trapero A. & Michailides, T.J. (2019) Ecology and epidemiology of diseases of nut crops and olives caused by Botryosphaeriaceae fungi in California and Spain. Plant Disease 103: 1809–1827. https://doi.org/10.1094/PDIS-03-19-0622-FE
Nose, T. (1933) On the ring rot of pears and the causal organism, especially on its perfect generation Physalospora piricola. Annals of the Agricultural Experiment Station 7: 156–163. [in Japanese]
Pennycook, S.R. & Samuels, G.J. (1985) Botryosphaeria and Fusicoccum species associated with ripe fruit rot of Actinidia deliciosa (Kiwifruit) in New Zealand. Mycotaxon 24: 445–458.
Phillips, A.J.L., Alves, A., Abdollahzadeh, J., Slippers, B., Wingfield, M.J., Groenewald, J.Z. & Crous, P.W. (2013) The Botryosphaeriaceae: genera and species known from culture. Studies in Mycology 55: 53–63. https://doi.org/10.3114/sim0021
Phillips, A.J.L., Alves, A., Pennycook, S.R., Johnston, P.R., Ramaley, A., Akulov, A. & Crous, P.W. (2008) Resolving the phylogenetic and taxonomic status of darkspored teleomorph genera in the Botryosphaeriaceae. Persoonia 21: 29–55. https://doi.org/10.3767/003158508X340742
Phillips, A.J., Hyde, K.D., Alves, A. & Liu, J.K. (2019) Families in Botryosphaeriales: a phylogenetic, morphological and evolutionary perspective. Fungal Diversity 94: 1–22. https://doi.org/10.1007/s13225-018-0416-6
Posada, D. & Crandall, K.A. (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817–818. https://doi.org/10.1093/bioinformatics/14.9.817
Qiu, Y., Savocchia, S., Steel, C.C. & Ash, G.J. (2008) Botryosphaeria dothidea associated with grapevine trunk disease in south-eastern Australia. Australasian Plant Pathology 37: 482–485. https://doi.org/10.1071/AP08045
Rambaut, A. & Drummond, A. (2008) FigTree: Tree figure drawing tool, version 1.2. 2. Institute of Evolutionary Biology, University of Edinburgh.
Senanayake, I.C., Rathnayaka, A.R., Marasinghe, D.S., Calabon, M.S., Gentekaki, E., Lee, H.B., Hurdeal, V.G., Pem, D., Dissanayake, L.S., Wijesinghe, S.N. & Bundhun, D. (2020) Morphological approaches in studying fungi: Collection, examination, isolation, sporulation and preservation. Mycosphere 11: 2678–2754. https://doi.org/10.5943/mycosphere/11/1/20
Shoemaker, R.A. (1964) Conidial states of some Botryosphaeria species on Vitis and Quercus. Canadian Journal of Botany 42: 1297–1301. https://doi.org/10.1139/b64-12
Slippers, B., Boissin, E., Phillips, A.J.L., Groenewald, J.Z., Wingfield, M.J., Postma A., Burgess, T. & Crous, P.W. (2013). Phylogenetic lineages in the Botryosphaeriales: A systematic and evolutionary framework. Studies in Mycology 76: 31–49. https://doi.org/10.3114/sim0020
Slippers, B., Johnson, G.I. & Crous, P.W. (2005) Phylogenetic and morphological reevaluation of the Botryosphaeria species causing diseases of Mangifera indica. Mycologia 97: 99–110. https://doi.org/10.1080/15572536.2006.11832843
Slippers, B., Crous, P.W., Denman, S., Coutinho, T.A., Wingfield, B.D. & Wingfield, M.J. (2004) Combined multiple gene genealogies and phenotypic characters differentiate several species previously identified as Botryosphaeria dothidea. Mycologia 96: 83–101. https://doi.org/10.1080/15572536.2005.11833000
Slippers, B., Roux, J., Wingfield, M.J., Van der Walt, F.J.J., Jami, F., Mehl, J.W.M. & Marais, G.J. (2014) Confronting the constraints of morphological taxonomy in the Botryosphaeriales. Persoonia-Molecular Phylogeny and Evolution of Fungi 33: 155–168. https://doi.org/10.3767/003158514X684780
Slippers, B. & Wingfield, M.J. (2007) Botryosphaeriaceae as endophytes and latent pathogens of woody plants: diversity, ecology and impact. Fungal Biology Reviews 21: 90–106. https://doi.org/10.1016/j.fbr.2007.06.002
Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690. https://doi.org/10.1093/bioinformatics/btl446
Stamatakis, A., Hoover, P. & Rougemont, J. (2008) A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology 57: 758–771. https://doi.org/10.1080/10635150802429642
Taylor, K., Barber, P.A., Hardy, G.E.S.J. & Burgess, T.I. (2009) Botryosphaeriaceae from tuart (Eucalyptus gomphocephala) woodland, including descriptions of four new species. Mycological Research 113: 337–353. https://doi.org/10.1016/j.mycres.2008.11.010
Theissen, F. & Sydow, H. (1915) Die Dothideales. Kritischsystematische Originalunter suchungen (Continuatio). Annales Mycologici 13: 431–746.
Theissen, F. & Sydow, H. (1918) Vorentwürfe zu den Pseudosphaeriales. Annales Mycologici 16: 1–34.
Trakunyingcharoen, T., Lombard, L., Groenewald, J.Z., Cheewangkoon, R., To-Anun, C. & Crous, P.W. (2015) Caulicolous Botryosphaeriales from Thailand. Persoonia-Molecular Phylogeny and Evolution of Fungi 34: 87–99. https://doi.org/10.3767/003158515X685841
von Höhnel, F. (1909) Fragmente zur Mykologie (VII. Mitteilung, Nr. 289 bis 353). Sitzungsberichte der Kaiserlichen Akademie der Wissenschaften. Mathematisch-Naturwissenschaftliche Classe 1118: 813–904
White, T.J., Bruns, T., Lee, S.J.W.T. & Taylor, J. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis, M.A., Gelfand, D.H., Sninsky, J.J. & White, T.J. (Eds.) PCR Protocols: a guide to methods and applications. Academic Press, San Diego, CA, USA, pp. 315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1
Wijayawardene, N.N., Hyde, K.D., Wanasinghe, D.N., Papizadeh, M., Goonasekara, I.D., Camporesi, E., Bhat, D.J., McKenzie, E.H., Phillips, A.J., Diederich, P. & Tanaka, K. (2016) Taxonomy and phylogeny of dematiaceous coelomycetes. Fungal Diversity 77: 1–316. https://doi.org/10.1007/s13225-016-0360-2
Xu, C., Wang, C., Ju, L., Zhang, R., Biggs, A.R., Tanaka, E., Li, B. & Sun, G. (2015) Multiple locus genealogies and phenotypic characters reappraise the causal agents of apple ring rot in China. Fungal Diversity 71: 215–231. https://doi.org/10.1007/s13225-014-0306-5
Yamada, K.D., Tomii, K. & Katoh, K. (2016) Application of the MAFFT sequence alignment program to large data-reexamination of the usefulness of chained guide trees. Bioinformatics 32: 3246–3251. https://doi.org/10.1093/bioinformatics/btw412
Zhang, W., Groenewald, J.Z., Lombard, L., Schumacher, R.K., Phillips, A.J.L. & Crous, P.W. (2021) Evaluating species in Botryosphaeriales. Persoonia-Molecular Phylogeny and Evolution of Fungi 46: 63–115. https://doi.org/10.3767/persoonia.2021.46.03
Zhou, Y., Dou, Z., He, W., Zhang, X. & Zhang, Y. (2016) Botryosphaeria sinensia sp. nov., a new species from China. Phytotaxa 245 (1): 43–50. https://doi.org/10.11646/phytotaxa.245.1.4
Zhou, Y.P., Zhang, M., Dou, Z.P. & Zhang, Y. (2017) Botryosphaeria rosaceae sp. nov. and B. ramosa, new botryosphaeriaceous taxa from China. Mycosphere 8: 162–171. https://doi.org/10.5943/mycosphere/8/2/2