Abstract
Eucalyptus globulus, an exotic species in Portugal, is one of the dominant and intensively managed forest species in the country. A disease syndrome characterised by leaf necrosis, stem girdling and cutting dieback in eucalyptus and associated with pestalotioid fungi has been detected in nurseries and young plantations in the last years. Twenty-seven isolates were recovered from diseased plants. Phylogenetic analysis based on internal transcribed spacers, partial translation elongation factor 1-α gene and partial β-tubulin gene sequence data grouped the isolates in five separate clades. Combining morphological, cultural and molecular data, five new species of Neopestalotiopsis are described, namely, Neopestalotiopsis eucalyptorum, Neopestalotiopsis hispanica, Neopestalotiopsis iberica, Neopestalotiopsis longiappendiculata and Neopestalotiopsis lusitanica.
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Data availability
Strains are available at MEAN (https://www.iniav.pt/recursos-geneticos-microbianos) and CBS (https://wi.knaw.nl/page/Collection) culture collections. Sequences are available at GenBank (https://www.ncbi.nlm.nih.gov/genbank) and alignments and trees are deposited in TreeBase (https://treebase.org).
References
Akaike H (1974) A new look at the statistical model identification. IEEE Trans Automat Contr 19:716–723. https://doi.org/10.1109/TAC.1974.1100705
Akinsanmi OA, Nisa S, Jeff-Ego OS et al (2017) Dry flower disease of macadamia in australia caused by Neopestalotiopsis macadamiae sp. nov. and Pestalotiopsis macadamiae sp. nov. Plant Dis 101:45–53. https://doi.org/10.1094/PDIS-05-16-0630-RE
Alfenas AC, Zauza EAV, Mafia RG, Assis TF (2009) Clonagem e doenças do eucalipto, 2nd edition. Editora UFV, Viçosa
Almeida FA, Araújo E, Gonçalves Junior H et al (2003) Diagnóstico e quantificação de doenças fúngicas da acerola no Estado da Paraíba. Fitopatol Bras 28:176–179. https://doi.org/10.1590/s0100-41582003000200010
Ayoubi N, Soleimani Pari S (2016) Morphological and molecular identification of Neopestalotiopsis mesopotamica causing tomato fruit rot. J Plant Dis Prot 123:267–271. https://doi.org/10.1007/s41348-016-0042-z
Bakry M, Bussières G, Lamhamedi MS et al (2011) A first record of Pestalotiopsis clavispora in argan mass cutting propagation: prevalence, prevention and consequences for plant production. Phytoprotection 90:117–120. https://doi.org/10.7202/045780ar
Barradas C, Phillips AJL, Correia A et al (2016) Diversity and potential impact of Botryosphaeriaceae species associated with Eucalyptus globulus plantations in Portugal. Eur J Plant Pathol 146:1–13. https://doi.org/10.1007/s10658-016-0910-1
Belisário R, Aucique-Pérez CE, Abreu LM et al (2020) Infection by Neopestalotiopsis spp. occurs on unwounded eucalyptus leaves and is favoured by long periods of leaf wetness. Plant Pathol 69:194–204. https://doi.org/10.1111/ppa.13132
Bezerra JDP, Machado AR, Firmino AL et al (2018) Mycological diversity description I. Acta Bot Brasilica 32:656–666. https://doi.org/10.1590/0102-33062018abb0154
Bragança H, Simões S, Onofre N et al (2007) Cryphonectria parasitica in Portugal: diversity of vegetative compatibility types, mating types, and occurrence of hypovirulence. For Pathol 37:391–402. https://doi.org/10.1111/j.1439-0329.2007.00513.x
Bragança H, Diogo ELF, Neves L et al (2016) Quambalaria eucalypti a pathogen of Eucalyptus globulus newly reported in Portugal and in Europe. For Pathol 46:67–75. https://doi.org/10.1111/efp.12221
Branco M, Bragança H, Sousa E, Phillips AJL (2014) Pests and diseases in Portuguese forestry: current and new threats. In: Reboredo F (ed) Forest Context and Policies in Portugal-Present and Future Challenges World Forests 19. Springer International Publishing Switzerland, Switzerland, pp 117–154
Carbone I, Kohn LM (1999) A method for designing primer sets for speciation studies in filamentous fungi. Mycologia 91:553–556
Chen Y, Zeng L, Shu N et al (2018) Pestalotiopsis-like species causing gray blight disease on Camellia sinensis in China. Plant Dis 102:1–28. https://doi.org/10.1094/PDIS-05-17-0642-RE
Conforto C, Lima NB, Silva FJA et al (2019) Characterization of fungal species associated with cladode brown spot on Nopalea cochenillifera in Brazil. Eur J Plant Pathol 155:1179–1194. https://doi.org/10.1007/s10658-019-01847-3
Crous PW, Gams W, Stalpers JA et al (2004) MycoBank: an online initiative to launch mycology into the 21st century. Stud Mycol 50:19–22 (https://doi.org/citeulike-article-id:9861703)
Crous PW, Summerell BA, Swart L et al (2011) Fungal pathogens of Proteaceae. Persoonia 27:20–45. https://doi.org/10.3767/003158511X606239
Crous PW, Wingfield MJ, Le RJJ et al (2015) Fungal planet description sheets: 371–399. Persoonia 35:264–327
Crous PW, Wingfield MJ, Chooi Y-H et al (2020) Fungal planet description sheets: 1042–1111. Persoonia - Mol Phylogeny Evol Fungi 44:301–459. https://doi.org/10.3767/persoonia.2020.44.11
Diogo ELF, Santos JM, Phillips AJL (2010) Phylogeny, morphology and pathogenicity of Diaporthe and Phomopsis species on almond in Portugal. Fungal Divers 44:107–115. https://doi.org/10.1007/s13225-010-0057-x
Espinoza JG, Briceño EX, Keith LM, Latorre BA (2008) Canker and twig dieback of blueberry caused by Pestalotiopsis spp. and a Truncatella sp. in Chile. Plant Dis 92:1407–1414. https://doi.org/10.1094/PDIS-92-10-1407
FAO (2001) Mean annual volume increment of selected industrial forest & plantation species by L. Ugalde & D. Pérez, forest plantation thematic papers, Working Paper 1. Forest Resources Development Service, Forest Resources Division. FAO, Rome, 27 pp. http://www.fao.org/3/a-ac121e.pdf. Accessed 8 Feb 2021
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution (NY) 39:783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
Ferreira MC, Ferreira GW, Fonseca N (1994). Manual de Sanidade dos Viveiros Florestais, IEADR, Lisboa
Freitas EFS, Da Silva M, Barros MVP, Kasuya MCM (2019) Neopestalotiopsis hadrolaeliae sp. nov., a new endophytic species from the roots of the endangered orchid Hadrolaelia jongheana in Brazil. Phytotaxa 416:211–220. https://doi.org/10.11646/phytotaxa.416.3.2
Gerardo-Lugo SS, Tovar-Pedraza JM, Maharachchikumbura SSN et al (2020) Characterization of Neopestalotiopsis species associated with mango grey leaf spot disease in Sinaloa, Mexico. Pathogens 9:1–17. https://doi.org/10.3390/pathogens9100788
Glass NL, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol 61:1323–1330
Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174. https://doi.org/10.1007/BF02101694
ICNF (2019) 6,º Inventário Florestal Nacional (IFN6) - 2015 Relatório Final. Instituto de Conservação da Natureza e Florestas, Lisboa. www2.icnf.pt/portal/florestas/ifn/ifn6. Accessed 16 Mar 2021
Hopkins KE, McQuilken MP (2000) Characteristics of Pestalotiopsis associated with hardy ornamental plants in the UK. Eur J Plant Pathol 106:77–85. https://doi.org/10.1023/A:1008776611306
Hu H, Jeewon R, Zhou D et al (2007) Phylogenetic diversity of endophytic Pestalotiopsis species in Pinus armandii and Ribes spp.: evidence from rDNA and β-tubulin gene phylogenies. Fungal Divers 24:1–22
Huannaluek N, Jayawardena RS, Maharachchikumbura SSN, Harishchandra DL (2021) Additions to pestalotioid fungi in Thailand: Neopestalotiopsis hydeana sp nov Pestalotiopsis hydei sp. nov. Phytotaxa 479:23–43. https://doi.org/10.11646/phytotaxa.479.1.2
Ismail AM, Cirvilleri G, Polizzi G (2013) Characterisation and pathogenicity of Pestalotiopsis uvicola and Pestalotiopsis clavispora causing grey leaf spot of mango (Mangifera indica L.) in Italy. Eur J Plant Pathol 135:619–625. https://doi.org/10.1007/s10658-012-0117-z
Jayawardena RS, Liu M, Maharachchikumbura SSN et al (2016) Neopestalotiopsis vitis sp. nov. causing grapevine leaf spot in China. Phytotaxa 258:63–74. https://doi.org/10.11646/phytotaxa.258.1.4
Jayawardena RS, Hyde KD, Jeewon R et al (2019) One stop shop II: taxonomic update with molecular phylogeny for important phytopathogenic genera: 26–50 (2019). Fungal Divers 94:41–129. https://doi.org/10.1007/s13225-019-00418-5
Jiang N, Bonthond G, Fan XL et al (2018) Neopestalotiopsis rosicola sp. nov. causing stem canker of Rosa chinensis in China. Mycotaxon 133:271–283. https://doi.org/10.5248/133.271
Jiang N, Fan X, Tian C (2021) Identification and characterization of leaf-inhabiting fungi from Castanea plantations in China. J Fungi 7:64. https://doi.org/10.3390/jof7010064
Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20:1160–1166. https://doi.org/10.1093/bib/bbx108
Kumar V, Cheewangkoon R, Gentekaki E et al (2019) Neopestalotiopsis alpapicalis sp. Nov. a new endophyte from tropical mangrove trees in Krabi province (Thailand). Phytotaxa 393:251–262. https://doi.org/10.11646/phytotaxa.393.3.2
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Liu F, Hou L, Raza M, Cai L (2017) Pestalotiopsis and allied genera from Camellia, with description of 11 new species from China. Sci Rep 7:866. https://doi.org/10.1038/s41598-017-00972-5
Liu F, Bonthond G, Groenewald JZ et al (2019) Sporocadaceae, a family of coelomycetous fungi with appendage-bearing conidia. Stud Mycol 92:287–415. https://doi.org/10.1016/j.simyco.2018.11.001
Lin HF, Chen TH, Da LS (2011) The antifungal mechanism of Bacillus subtilis against Pestalotiopsis eugeniae and its development for commercial applications against wax apple infection. African J Microbiol Res 5:1723–1728. https://doi.org/10.5897/AJMR10.169
Ma X-Y, Maharachchikumbura SSNN, Chen B-W et al (2019) Endophytic pestalotiod taxa in Dendrobium orchids. Phytotaxa 419:268–286. https://doi.org/10.11646/phytotaxa.419.3.2
Maharachchikumbura SSN, Guo L-D, Chukeatirote E et al (2011) Pestalotiopsis —morphology, phylogeny, biochemistry and diversity. Fungal Divers 50:167–187. https://doi.org/10.1007/s13225-011-0125-x
Maharachchikumbura SSN, Guo L-DD, Cai L et al (2012) A multi-locus backbone tree for Pestalotiopsis, with a polyphasic characterization of 14 new species. Fungal Divers 56:95–129. https://doi.org/10.1007/s13225-012-0198-1
Maharachchikumbura SSN, Guo L-D, Chukeatirote E, Hyde KD (2014a) Improving the backbone tree for the genus Pestalotiopsis; addition of P. steyaertii and P. magna sp. nov. Mycol Prog 13:617–624. https://doi.org/10.1007/s11557-013-0944-0
Maharachchikumbura SSN, Hyde KD, Groenewald JZ et al (2014b) Pestalotiopsis revisited. Stud Mycol 79:121–186. https://doi.org/10.1016/j.simyco.2014.09.005
Maharachchikumbura SSN, Larignon P, Hyde KD et al (2016) Characterization of Neopestalotiopsis, Pestalotiopsis and Truncatella species associated with grapevine trunk diseases in France. Phytopathol Mediterr 55:380–390
Metz AM, Haddad A, Worapong J et al (2000) Induction of the sexual stage of Pestalotiopsis microspora, a taxol-producing fungus. Microbiology 146(Pt 8):2079–2089
Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: 2010 Gateway Computing Environments Workshop (GCE). IEEE, New Orleans, pp 1–8. https://doi.org/10.1109/GCE.2010.5676129
Mishra Y, Singh A, Batra A, Sharma MM (2014) Understanding the biodiversity and biological applications of endophytic fungi: a review. J Microb Biochem Technol s8:1–11. https://doi.org/10.4172/1948-5948.S8-004
Morales-Rodríguez C, Dalla Valle M, Aleandri MP, Vannini A (2019) Pestalotiopsis biciliata, a new leaf pathogen of Eucalyptus spp. recorded in Italy. For Pathol 49:1–7. https://doi.org/10.1111/efp.12492
Norphanphoun C, Jayawardena RS, Chen Y et al (2019) Morphological and phylogenetic characterization of novel pestalotioid species associated with mangroves in Thailand. Mycosphere 10:531–578. https://doi.org/10.5943/mycosphere/10/1/9
Nylander JAA (2004) MrModeltest v2. program distributed by the author. Evolutionary Biology Centre, Uppsala University. https://www.abc.se/_nylander/mrmodeltest2/mrmodeltest2.html
O’Donnell K, Kistler HC, Cigelnik E, Ploetz RC (1998) Multiple evolutionary origins of the fungus causing Panama disease of banana: concordant evidence from nuclear and mitochondrial gene genealogies. Proc Natl Acad Sci 95:2044–2049. https://doi.org/10.1073/pnas.95.5.2044
Old KM, Lee SS, Sharma JK, Yuan ZQ (2000) A manual of diseases of tropical acacias in Australia, South-East Asia and India. Center for International Forestry Research (CIFOR). Jakarta, Indonesia
Pirralho M, Flores D, Sousa VB et al (2014) Evaluation on paper making potential of nine Eucalyptus species based on wood anatomical features. Ind Crops Prod 54:327–334. https://doi.org/10.1016/j.indcrop.2014.01.040
Qi M, Xie C-X, Chen Q-W, Yu Z-D (2021) Pestalotiopsis trachicarpicola, a novel pathogen causes twig blight of Pinus bungeana (Pinaceae: Pinoideae) in China. Antonie Van Leeuwenhoek 114:1–9. https://doi.org/10.1007/s10482-020-01500-8
Rannala B, Yang Z (1996) Probability distribution of molecular evolutionary trees: a new method of phylogenetic inference. J Mol Evol 43:304–311. https://doi.org/10.1007/BF02338839
Rayner RW (1970) A mycological color chart. Commonwealth Mycological Institute, Kew
Ronquist F, Teslenko M, van der Mark P et al (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Santos GS, Mafia RG, Aguiar AM et al (2020) Stem rot of eucalyptus cuttings caused by Neopestalotiopsis spp. in Brazil. J Phytopathol 168:311–321. https://doi.org/10.1111/jph.12894
Silva MRC, Diogo E, Bragança H et al (2015) Teratosphaeria gauchensis associated with trunk, stem and foliar lesions of Eucalyptus globulus in Portugal. For Pathol 45:224–234. https://doi.org/10.1111/efp.12160
Silva AC, Diogo E, Henriques J et al (2020) Pestalotiopsis pini sp. nov., an emerging pathogen on stone pine (Pinus pinea L.). Forests 11:1–17. https://doi.org/10.3390/f11080805
Silvério ML, de Cavalcanti MA, Q, Silva GA da, et al (2016) A new epifoliar species of Neopestalotiopsis from Brazil. Agrotópica 28:151–158
Solarte F, Muñoz CG, Maharachchikumbura SSN, Álvarez E (2018) Diversity of Neopestalotiopsis and Pestalotiopsis spp., causal agents of guava scab in Colombia. Plant Dis 102:49–59. https://doi.org/10.1094/PDIS-01-17-0068-RE
Song YU, Geng KUN, Zhang BIN et al (2013) Two new species of Pestalotiopsis from Southern China. Phytotaxa 126:22–30. https://doi.org/10.11646/phytotaxa.126.1.2
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Stergiopoulos L, Gordon TR (2014) Cryptic fungal infections: the hidden agenda of plant pathogens. Front Plant Sci 5:10–13. https://doi.org/10.3389/fpls.2014.00506
Stone JK, Polishook JD, White JF (2004) Endophytic fungi. In: Biodiversity of Fungi. Elsevier, Burlington, pp 241–270
Swofford DL (2002) Phylogenetic analysis using parsimony. Sinauer Associates, Sunderland
Tejesvi MV, Kini KR, Prakash HS et al (2007) Genetic diversity and antifungal activity of species of Pestalotiopsis isolated as endophytes from medicinal plants. Fungal Divers 24:37–54
Tibpromma S, Hyde KD, McKenzie EHC et al (2018) Fungal diversity notes 840–928: micro-fungi associated with Pandanaceae. Fungal Divers 93:1–160. https://doi.org/10.1007/s13225-018-0408-6
Vaidya G, Lohman DJ, Meier R (2011) SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 27:171–180. https://doi.org/10.1111/j.1096-0031.2010.00329.x
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols. Academic Press, San Diego, pp 315–322
Xu J, Yang X, Lin Q (2014) Chemistry and biology of Pestalotiopsis-derived natural products. Fungal Divers 66:37–68. https://doi.org/10.1007/s13225-014-0288-3
Acknowledgements
The authors would like to thank to Joana Henriques for help on molecular biology, to Isabel Lourenço and Florinda Medeiros for assistance in the Mycology laboratory. We also thank Ana Reis, from Altri Florestal, for providing one sample and Saowaluck Tibpromma, Kunming Institute for Botany, China, for sending sequences before they were made available in GenBank. Alan JL Phillips acknowledges the support from UIDB/04046/2020 and UIDP/04046/2020 Centre grants from FCT, Portugal (to BioISI).
Funding
This work was funded by a collaborative protocol, “Estudo das Doenças do eucalipto – prospecção e controlo” established between INIAV, the RAIZ Institute and Altri Florestal.
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H.B., E.D., C.I.G. and C.V. designed the experiments; E.D. and A.C.S. performed morphological and phylogenetic analysis; C.I.B and E.D. wrote the first draft of the manuscript; H.B and A.J.L.P. reviewed and edited the manuscript. HB and A.J.L.P. supervised the study. All authors have read, edited and approved the final manuscript.
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Diogo, E., Gonçalves, C.I., Silva, A.C. et al. Five new species of Neopestalotiopsis associated with diseased Eucalyptus spp. in Portugal. Mycol Progress 20, 1441–1456 (2021). https://doi.org/10.1007/s11557-021-01741-5
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DOI: https://doi.org/10.1007/s11557-021-01741-5