Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2023-02-07
Page range: 227–240
Abstract views: 64
PDF downloaded: 1

Interesting Botryosphaeria (Botryosphaeriaceae) associated with Magnolia species in Thailand: Additions of two new host records with their lifestyles

Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand, Research Center of Microbial Diversity and Sustainable Utilization, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand
University of Lisbon, Faculty of Sciences, Biosystems and Integrative Sciences Institute (BioISI), Campo Grande, 1749-016 Lisbon, Portugal
Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand, Research Center of Microbial Diversity and Sustainable Utilization, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand
Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand, Research Center of Microbial Diversity and Sustainable Utilization, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand
Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand, Research Center of Microbial Diversity and Sustainable Utilization, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand
Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand, Research Center of Microbial Diversity and Sustainable Utilization, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand, Academy of Science, Royal Society of Thailand, Bangkok 10300, Thailand
Fungi Botryosphaeriaceae endophytes phylogeny saprobes taxonomy

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

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