Abstract
Lasiodiplodia species are commonly as endophytes, saprobes and pathogens in tropics and subtropics. During an investigation of Botryosphaeriaceae in Thailand, two Lasiodiplodia taxa were isolated. Morphological characteristics and phylogenetic analyses based on combined ITS, tef and tub2 sequence data support the establishment of a novel species, Lasiodiplodia chiangraiensis, isolated from woody hosts. Lasiodiplodia chiangraiensis is phylogenetically close to L. iraniensis and L. thailandica, but represents a distinct lineage. The new species could be distinguished from extant Lasiodiplodia species by its mature conidial dimensions. A detailed description and illustration are provided, as well as an updated phylogenetic tree (ITS, tef and tub2) including all species (with available molecular data) of Lasiodiplodia. In addition, the accepted genera in Botryosphaeriaceae based on recent studies are given.
References
Arx, J.A. von & Müller, E. (1954) Die Gattungen der amerosporen Pyrenomyceten. Beitrage zur Kryptogamenflora der Schweiz 11: 1–434.
Arx, J.A. von & Müller, E. (1975) A re-evaluation of the bitunicate ascomycetes with keys to families and genera. Studies in Mycology 9: 1–159.
Barr, M.E. (1987) Prodomus to the Class Loculoascomycetes Published by the author. Amherst, Massachusetts 168.
Burgess, T.I., Barber, P.A., Mohali, S., Pegg, G., de Beer, W. & Wingfield, M.J. (2006) Three new Lasiodiplodia spp. from the tropics, recognized based on DNA sequence comparisons and morphology. Mycologia 98: 423–435. https://doi.org/10.1080/15572536.2006.11832677
Burruano, S., Mondello, V., Conigliaro, G., Alfonzo, A., Spagnolo, A. & Mugnai, L. (2008) Grapevine decline in Italy caused by Lasiodiplodia theobromae. Phytopathologia Mediterranea 47: 132–136.
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
Chomnunti, P., Hongsanan, S., Aguirre-Hudson, B., Tian, Q., Peršoh, D., Dhami, M.K., Alias, A.S., Xu, J.C., Liu, X.Z., Stadler, M. & Hyde, K.D. (2014) The sooty moulds. Fungal Diversity 66: 1–36. https://doi.org/10.1007/s13225-014-0278-5
Clendinin, I. (1896) Lasiodiplodia Ellis. and Everh. n. gen. Botanical Gazette Crawfordsville 21: 92–93. https://doi.org/10.1086/327307
Crous, P.W., Slippers, B., Wingfield, M.J., Rheeder, J., Marasas, W.F.O., Philips, A.J.L., Alves, A., Burgess, T., Barber, P. & Groenewald, J.Z. (2006) Phylogenetic lineages in the Botryosphaeriaceae. Studies in Mycology 55: 235–253. https://doi.org/10.3114/sim.55.1.235
Dayarathne, M.C., Jones, E.B.G., Maharachchikumbura, S.S.N., Devadatha, B., Sarma, V.V., Khongphinitbunjong, K., Chomnunti, P. & Hyde, K.D. (2020) Morpho-molecular characterization of microfungi associated with marine based habitats. Mycosphere 11: 1–188. https://doi.org/10.5943/mycosphere/11/1/1
Denman, S., Crous, P.W., Taylor, J.E., Kang, J.C., Pascoe, I. & Wingfield, M.J. (2000) An overview of the taxonomic history of Botryosphaeria, and a re-evaluation of its anamorphs based on morphology and ITS rDNA phylogeny. Studies in Mycology 45: 129–140.
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
Dissanayake, A.J., Bhunjun, C.S., Maharachchikumbura, S.S.N. & Liu, J.K. (2020) Applied aspects of methods to infer phylogenetic relationships amongst fungi. Mycosphere 11: 2653–2677. https://doi.org/10.5943/mycosphere/11/1/19
Dou, Z.P., He, W. & Zhang, Y. (2017) Lasiodiplodia chinensis, a new holomorphic species from China. Mycosphere 8: 521–532. https://doi.org/10.5943/mycosphere/8/2/3
Fan, M.C., Yeh, H.C. & Hong, C.F. (2013) First report of Lasiodiplodia theobromae causing dieback of Aquilaria sinensis in Taiwan. Plant Disease 97: 690–691. https://doi.org/10.1094/PDIS-10-12-0998-PDN
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.
Hongsanan, S., Hyde, K.D., Phookamsak, R., Wanasinghe, D.N., McKenzie, E.H.C., Sarma, V.V., Lücking, R., Boonmee, S., Bhat, J.D., Liu, N.G., Tennakoon, D.S., Pem, D., Karunarathna, A., Jiang, S.H., Jones, G.E.B., Phillips, A.J.L., Manawasinghe, I.S., Tibpromma, S., Jayasiri, S.C., Sandamali, D., Jayawardena, R.S., Wijayawardene, N.N., Ekanayaka, A.H., Jeewon, R., Lu, Y.Z., Phukhamsakda, C., Dissanayake, A.J., Zeng, X.Y., Luo, Z.L., Tian, Q., Thambugala, K.M., Dai, D.Q., Samarakoon, M.C., Chethana, K.W.T., Ertz, D., Doilom, M., Liu, J.K., Pérez-Ortega, S., Suija, A., Senwanna, C., Wijesinghe, S.N., Niranjan, M., Zhang, S.N., Ariyawansa, H.A., Jiang, H.B., Zhang, J.F., Norphanphoun, C., de Silva, N.I., Thiyagaraja, V., Zhang, H., Bezerra, J.D.P., Miranda-González, R., Aptroot, A., Kashiwadani, H., Harishchandra, D., Sérusiaux, E., Abeywickrama, P.D., Bao, D.F., Devadatha, B., Wu, H.X., Moon, K.H., Gueidan, C., Schumm, F., Bundhun, D., Mapook, D., Monkai, J., Bhunjun, C.S., Chomnunti, P., Suetrong, S., Chaiwan, N., Dayarathne, M.C., Yang, J., Rathnayaka, A.R., Xu, J.C., Zheng, J.S., Liu, G., Feng, Y. & Xie, N. (2020) Refined families of Dothideomycetes: orders and families incertae sedis in Dothideomycetes. Fungal Diversity 105: 17–318. https://doi.org/10.1007/s13225-020-00462-6
Ismail, A.M., Cirvilleri, G., Polizzi, G., Crous, P.W., Groenewald, J.Z. & Lombard, L. (2012) Lasiodiplodia species associated with dieback disease of mango (Mangifera indica) in Egypt. Australasian Plant Pathology 41: 649–660. https://doi.org/10.1007/s13313-012-0163-1
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.L., 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
Jiang, N., Wang, X.W., Liang, Y.M. & Tian, C.M. (2018) Lasiodiplodia cinnamomi sp. nov. from Cinnamomum camphora in China. Mycotaxon 133: 249–259. https://doi.org/10.5248/133.249
Li, W.J., Liu, J.K., Bhat, D.J., Camporesi, E., Xu, J.C. & Hyde, K.D. (2014) Introducing the novel species, Dothiorella symphoricarposicola, from snowberry in Italy. Cryptogamie, Mycologie 35: 257–270. https://doi.org/10.7872/crym.v35.iss3.2014.257
Linaldeddu, B.T., Deidda, A., Scanu, B., Franceschini, A., Serra, S., Berraf-Tebbal, A., Boutiti, M.Z., Ben Jamâa, M.L. & Phillips, A.J.L. (2015) Diversity of Botryosphaeriaceae species associated with grapevine and other woody hosts in Italy, Algeria and Tunisia, with descriptions of Lasiodiplodia exigua and Lasiodiplodia mediterranea sp. nov. Fungal Diversity 71: 201–214. https://doi.org/10.1007/s13225-014-0301-x
Liu, J.K., Chomnunti, P., Cai, L., Phookamsak, R., Chukeatirote, E., Jones, E.B.G., Moslem, M. & Hyde, K.D. (2010) Phylogeny and morphology of Neodeightonia palmicola sp. nov. from palms. Sydowia 62: 261?276.
Liu, J.K., Phookamsak, R., Doilom, M., Wikee, S., Li, Y.M., Ariyawansha, H.A., Boonmee, S., Chomnunti, P., Dai, D.Q., Bhat, D.J., Romero, A.I., Zhuang, W.Y., Monkai, J., Jones, E.B.G., Chukeatirote, E., Ko Ko, T.W., Zhao, Y.C., Wang, Y. & Hyde, K.D. (2012) Towards a natural classification of Botryosphaeriales. Fungal Diversity 57: 149–210. https://doi.org/10.1007/s13225-012-0207-4
Luo, M., Dong, Z.Y., Bin, S.Y. & Lin, J.T. (2011) First report of fruit rot disease on pomelo caused by Lasiodiplodia theobromae in China. Plant Disease 95: 1190–1190. https://doi.org/10.1094/PDIS-03-11-0214
Machado, A.R., Pinho, D.B. & Pereira, O.L. (2014) Phylogeny, identification and pathogenicity of the Botryosphaeriaceae associated with collar and root rot of the biofuel plant Jatropha curcas in Brazil, with a description of new species of Lasiodiplodia. Fungal Diversity 67: 231–247. https://doi.org/10.1007/s13225-013-0274-1
Marques, M.W., Lima, N.B., de Morais, M.A., Barbosa, M.A.G., Souza, B.O., Michereff, S.J., Phillips, A.J.L. & Câmara, M.P.S. (2013) Species of Lasiodiplodia associated with mango in Brazil. Fungal Diversity 61: 181–93. https://doi.org/10.1007/s13225-013-0231-z
Mohali, S., Encinas, O. & Mora, N. (2002) Manchado azul en madera de Pinus oocarpa y Azadirachta indica en Venezuela. Fitopatologia Venezolana 15: 30–32.
Netto, M.S.B., Assunção, I.P., Lima, G.S.A., Marque, M.W., Lima, W.G., Monteiro, J.H.A., Balbino, Valdir de Q., Michereff, S.J., Phillips, A.J.L. & Câmara, M.P.S. (2014) Species of Lasiodiplodia associated with papaya stem-end rot in Brazil. Fungal Diversity 67: 127–141. https://doi.org/10.1007/s13225-014-0279-4
Nylander, J.A., Ronquist, J.P., Huelsenbeck, F. & Nieves-Aldrey, J.L. (2004) Bayesian phylogenetic analysis of combined data. Systematic Biology 53: 47–67. https://doi.org/10.1080/10635150490264699
Phillips, A.J.L., Oudemans, P.V., Correia, A. & Alves, A. (2006) Characterisation and epitypification of Botryosphaeria corticis, the cause of blueberry cane canker. Fungal Diversity 21: 141–155.
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 76: 51–167. https://doi.org/10.3114/sim0021
Phillips, A.J.L., 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
Prasher, I.B. & Singh, G. (2014) Lasiodiplodia indica — a new species of coelomycetous mitosporic fungus from India. Kavaka 43: 64–69.
Punithalingam, E. (1980) Plant diseases attributed to Botryodiplodia theobromae Pat. Cramer, Vaduz.
Rodríguez-Gálveza, E., Guerrero, P., Barradas, C., Crous, P.W. & Alves, A. (2017) Phylogeny and pathogenicity of Lasiodiplodia species associated with dieback of mango in Peru. Fungal Biology 121: 452–465. http://dx.doi.org/10.1016/j.funbio.2016.06.004
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna. S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542. https://doi.org/10.1093/sysbio/sys029
Sakalidis, M.L., Ray, J.D., Lanoiselet, V., Hardy, G.E.S. & Burgess, T.I. (2011) Pathogenic Botryosphaeriaceae associated with Mangifera indica in the Kimberley region of Western Australia. European Journal of Plant Pathology 130: 379–391. https://doi.org/10.1007/s10658-011-9760-z
Silvestro, D. & Michalak, I. (2012) RAxML-GUI: a graphical front-end for RAxML. Organisms Diversity and Evolution 12: 335–337. https://doi.org/10.1007/s13127-011-0056-0
Sinha, B., Lalhruaitluangi, C., Devi, P.S., Singh, R.K., Singh, A.H., Singh, K.M. & Amaresan, N. (2018) First report of Lasiodiplodia theobromae causing dieback in tree bean (Perkia roxburghii) in Manipur. Plant Disease Research 33: 222–224.
Slippers, B., Johnson, G.I., Crous, P.W., Coutinho, T.A., Wingfield, B.D. & Wingfield, M.J. (2005) Phylogenetic and morphological re-evaluation of the Botryosphaeria species causing diseases of Mangifera indica. Mycologia 97: 99–110. https://doi.org/10.1080/15572536.2006.11832843
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
Slippers, B., Boissin, E., Phillips, A.J.L., Groenewald, J.Z, Lombard, L., 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
Smith, H., Wingfield, M.J., Coutinho, T.A. & Crous, P.W. (1996) Sphaeropsis sapinea and Botryosphaeria dothidea endophytic in Pinus spp. and Eucalyptus spp. in South Africa. South African Journal of Botany 62: 86–88. https://doi.org/10.1016/S0254-6299(15)30596-2
Swofford, D.L. (2002) PAUP*: Phylogenetic Analysis Using Parsimony and other methods, version 4.0 b10. Sunderland, MA, Sinauer Associates.
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729. https://doi.org/10.1093/molbev/mst197
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 34: 87–99. http://dx.doi.org/10.3767/003158515X685841
Wang, Y., Lin, S., Zhao, L., Sun, X., He, W., Zhang, Y. & Dai, Y.C. (2019) Lasiodiplodia spp. associated with Aquilaria crassna in Laos. Mycological Progress 18: 683–701. https://doi.org/10.1007/s11557-019-01481-7
White, T.J., Bruns, T., Lee, S. & Taylor, J.L. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innes, M.A., Gelfand, D.H., Snisky, J.J. & White, T.J. (Eds.) PCR protocols: a guide to methods and applications. Academic, San Diego, pp. 315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1
Wijayawardene, N.N., Hyde, K.D., Al-Ani, L.K.T., Tedersoo, L., Haelewaters, D., Rajeshkumar, K.C., Zhao, R.L., Aptroot, A., Leontyev, D.V., Saxena, R.K., Tokarev, Y.S., Dai, D.Q., Letcher, P.M., Stephenson, S.L., Ertz, D., Lumbsch, H.T., Kukwa, M., Issi, I.V., Madrid, H., Phillips, A.J.L., Selbmann, L., Pfliegler, W.P., Horváth, E., Bensch, K., Kirk, P.M., Kolar?íková, K., Raja, H.A., Radek, R., Papp, V., Dima, V., Ma, J., Malosso, E., Takamatsu, S., Rambold, G., Gannibal, P.B., Triebel, D., Gautam, A.K., Avasthi, S., Suetrong, S., Timdal, E., Fryar, S.C., Delgado, G., Réblová, M., Doilom, M., Dolatabadi, S., Paw?owska, J.Z., Humber, R.A., Kodsueb, R., Sánchez-Castro, I., Goto, B.T., Silva, D.K.A., de Souza, F.A., Oehl, F., da Silva, G.A., Silva, I.R., B?aszkowski, J., Jobim, K., Maia, L.C., Barbosa, F.R., Fiuza, P.O., Divakar, P.K., Shenoy, B.D., Castañeda-Ruiz, R.F., Somrithipol, S., Lateef, A.A., Karunarathna, S.C., Tibpromma, S., Mortimer, P.E., Wanasinghe, D.N., Phookamsak, R., Xu, J., Wang, Y., Tian, F., Alvarado, P., Li, D.W., Kušan, I., Matoc?ec, N., Mešicì, A., Tkalc?ec, Z., Maharachchikumbura, S.S.N., Papizadeh, M., Heredia, G., Wartchow, F., Bakhshi, M., Boehm, E., Youssef, N., Hustad, V.P., Lawrey, J.D., Santiago, A.L.C.M.A., Bezerra, J.D.P., Souza-Motta, C.M., Firmino, A.L., Tian, Q., Houbraken, J., Hongsanan, S., Tanaka, K., Dissanayake, A.J., Monteiro, J.S., Grossart, H.P., Suija, A., Weerakoon, G., Etayo, J., Tsurykau, A., Vázquez, V., Mungai, P., Damm, U., Li, Q.R., Zhang, H., Boonmee, S., Lu, Y.Z., Becerra, A.G., Kendrick, B., Brearley, F.Q., Motieju?naite?, J., Sharma, B., Khare, R., Gaikwad, S., Wijesundara, D.S.A., Tang, L.Z., He, M.Q., Flakus, A., Rodriguez-Flakus, P., Zhurbenko, M.P., McKenzie, E.H.C., Stadler, M., Bhat, D.J., Liu, J.K., Raza, M., Jeewon, R., Nassonova, E.S., Prieto, M., Jayalal, R.G.U., Erdog?du, M., Yurkov, A., Schnittler, M., Shchepin, O.N., Novozhilov, Y.K., Silva-Filho, A.G.S., Gentekaki, E., Liu, P., Cavender, J.C., Kang, Y., Mohammad, S., Zhang, L.F., Xu, R.F., Li, Y.M., Dayarathne, M.C., Ekanayaka, A.H., Wen, T.C., Deng, C.Y., Pereira, O.L., Navathe, S., Hawksworth, D.L., Fan, X.L., Dissanayake, L.S., Kuhnert, E., Grossart, H.P. & Thines, M. (2020) Outline of Fungi and fungus-like taxa. Mycosphere 11: 1060–1456. https://doi.org/10.5943/mycosphere/11/1/8
Wright, A.F. & Harmon, P.F. (2009) First report of Lasiodiplodia theobromae associated with stem blight of southern highbush blueberries in Florida. Plant Disease 93: 962–962. https://doi.org/10.1094/PDIS-93-9-0962C
Zhang, W., Groenewald, J.Z., Lombard, L., Schumacher, R.K., Phillips, A.J.L., & Crous, P.W. (2020) Evaluating species in Botryosphaeriales. Persoonia 46: 63–115. https://doi.org/10.3767/persoonia.2021.46.03
Zhao, L., Wang, Y., He, W. & Zhang, Y. (2019) Stem blight of blueberry caused by Lasiodiplodia vaccinii sp. nov. in China. Plant Disease 103: 2041–2050. https://doi.org/10.1094/PDIS-01-19-0079-RE
