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Richness of Nigrospora spp. (Apiosporaceae) in Manihot esculenta in Brazil and the description of three new species

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Abstract

Manihot esculenta, commonly known as cassava, is an important staple food in developing countries in Africa, Asia and Latin America. Despite its relevance, few surveys of endophytic fungi have been carried out on this plant. Nigrospora spp. have a wide range of hosts and can be found as saprobes, endophytes, and pathogens. Nigrospora has already been isolated from cassava plants in previous studies. However, its identification was made only at the genus level. In this study, healthy cassava stems were collected in the northeast region of Brazil from where specimens of this genus were obtained. The isolates were identified based on morphological features and phylogenetic analyses of internal transcribed spacer (ITS), part of the translation elongation factor 1 alpha (TEF1- α), and β-tubulin fragment (TUB2) genic regions. As a result, we report two new geographic occurrences of N. pyriformis, and N. vesicularifera, four new records of N. hainanensis, N. lacticolonia, N. pyriformis, and N. vesicularifera associated with cassava, and the description of three new species named N. endophytica, N. manihoticola and N. pernambucoensis.

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Data availability

Sequence data are deposited in GenBank (https://www.ncbi.nlm.nih.gov/genbank/), concatenated alignment is deposited in TreeBASE (http://www.treebase.org/). The ex-types and holotypes have been deposited in public collections (Micoteca URM Profa. Maria Auxiliadora de Queiroz Cavalcanti, and Herbário URM Pe. Camille Torrend, respectively) located at the Universidade Federal de Pernambuco (Recife, Brazil). New taxonomic descriptions and nomenclatures are deposited in MycoBank (www.mycobank.org).

References

  • Aguiar JLP, Sousa TCR, Lôbo CF (2013) A importância da mandioca. In JF Fialho, EA Vieira (eds), Mandioca no Cerrado: orientações técnicas, 2nd edn. Embrapa, Brasília, pp 14–26

  • Al-Nadabi H, Maharachchikumbura SSN, Al-Gahaffi ZS, Al-Hasani AS, Velazhahan R, Al-sadi AM (2020) Molecular identification of fungal pathogens associated with leaf spot disease of date palms (Phoenix dactylifera). All Life 13(1):587–597. https://doi.org/10.1080/26895293.2020.1835740

    Article  CAS  Google Scholar 

  • Ananya TS, Kindo AJ, Subramanian A, Suresh K (2014) Nigrospora sphaerica causing corneal ulcer in an immunocompetent woman: a case report. Int J Case Rep Images 5(10):675–679

    Article  Google Scholar 

  • Brito ACQ, Mello JF, Câmara MPS, Vieira JCB, Michereff SJ, Souza-Motta CMS, Machado AR (2020) Diversity and pathogenicity of Botryosphaeriaceae species associated with black root rot and stem cutting dry rot in Manihot esculenta in Brazil. Eur J Plant Pathol 157:583–598. https://doi.org/10.1007/s10658-020-02024-7

    Article  CAS  Google Scholar 

  • Carvalho PCL (2006) Classificação botânica. In: Mattos PLP, Farias ARN, Filho JRF (eds.). Mandioca: o produtor pergunta, a Embrapa responde. Embrapa Informação Tecnológica, Brasília, pp 18 – 21

  • Castellani A (1967) A maintenance and cultivation of the common pathogenic fungi of man in sterile distilled water. Further researches. Am J Trop Med Hyg 70:181–184

    Google Scholar 

  • Carbone I, Kohn LM (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91:553–556

    Article  CAS  Google Scholar 

  • Chen XYL, Zhang C, Yang H, Yang MF, Cernava T (2020) First Report of Leaf Spot on Chenopodium album Caused by Nigrospora pyriformis in China. Plant Dis. https://doi.org/10.1094/PDIS-07-19-1369-PDN

    Article  PubMed  Google Scholar 

  • Conforto C, Lima NB, Silva FJA, Câmara MPS, Maharachchikumbura S, Michereff SJ (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

    Article  CAS  Google Scholar 

  • Crous PW, Carnegie AJ, Sharma R et al (2019) Fungal Planet description sheets: 868–950. Persoonia 42:291–473. https://doi.org/10.3767/persoonia.2019.42.11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dawoud TM, Yassin MA, El-Samawaty ARM, Elgorban AM (2021) Silver nanoparticles synthesized by Nigrospora oryzae showed antifungal activity. Saudi J Biol Sci 28(3):1847–1852. https://doi.org/10.1016/j.sjbs.2020.12.036

    Article  CAS  PubMed  Google Scholar 

  • FAO (2013) Produzir mais com menos: Mandioca um guia para a intensificação sustentável da produção. http://www.fao.org/3/a-i2929o.pdf. Accessed 08 March 2018.

  • FAO (2017) Food outlook: Biannual report on global food markets November 2017. http://www.fao.org/3/a-I8080e.pdf. Accessed 10 April 2018.

  • 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(4):1323–1330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hartanti AT, Susanti FN, Prasasty VD, Radiastuti N (2021) Culturable endophytic fungal diversity in cassava tubers of Indonesia. Biodiversitas 22:1250–1260. https://doi.org/10.13057/biodiv/d220322

    Article  Google Scholar 

  • Hao Y, Aluthmuhandiram JVS, Chethana KWT, Manawasinghe IS, Li X, Liu M, Hyde KD, Phillips AJL, Zhang W (2020) Nigrospora species associated with various hosts from Shandong Peninsula, China. Mycobiology 48(3):169–183. https://doi.org/10.1080/12298093.2020.1761747

  • Hyde KD, Norphanphoun C, Maharachchikumbura SSN et al (2020) Refined families of Sordariomycetes. Mycosphere 11(1):305–1059. https://doi.org/10.5943/mycosphere/11/1/7

  • Jacobs K, Bergdahl DR, Wingfield MJ, Halik S, Seifert KA, Bright DE, Wingfield BD (2004) Leptographium wingfieldii introduced into North America and found associated with exotic Tomicus piniperda and native bark beetles. Mycol Res 108:411–418

    Article  PubMed  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Katoh K, Rozewicki J, Yamada KD (2017) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20(4):1160–1166. https://doi.org/10.1093/bib/bbx108

    Article  CAS  PubMed Central  Google Scholar 

  • Kee YJ, Hafifi ABM, Huda-Shakirah AR, Wong KL, Jin XL, Nordahliawate MSS, Zakaria L, Mohd MH (2019) First report of reddish brown spot disease of red-fleshed dragon fruit (Hylocereus polyrhizus) caused by Nigrospora lacticolonia and Nigrospora sphaerica in Malaysia. Crop Prot 122:165–170. https://doi.org/10.1016/j.cropro.2019.05.006

    Article  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2015) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0. Mol Biol Evol 33(7):1870–1874

    Article  Google Scholar 

  • Li H, Yan C, Tang Y, Ma X, Chen Y, Chen S, Lin M, Liu Z (2020) Endophytic bacterial and fungal microbiota in different cultivars of cassava (Manihot esculenta Crantz). J Microbiol 58(7):614–623. https://doi.org/10.1007/s12275-020-9565-x

    Article  CAS  PubMed  Google Scholar 

  • Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, LA, pp 1–8

  • Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808

    Article  PubMed  Google Scholar 

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

  • Ramírez-Camejo LA (2022) Diversity of culturable endophytic fungi vary through time in Manihot esculenta Crantz. Braz J Biol. https://doi.org/10.1590/1519-6984.253156

    Article  PubMed  Google Scholar 

  • Rayner RW (1970) A mycological colour chart. Commonwealth Mycological Institute and British Mycological Society, Kew, Surrey

  • Rannala B, Yang Z (1996) Probability distribution of molecular evolutionary trees: a new method of phylogenetic inference. J Mol Evol 43:304–311

    Article  CAS  PubMed  Google Scholar 

  • Raza M, Zhang ZF, Hyde KD, Diao YZ, Cai L (2019) Culturable plant pathogenic fungi associated with sugarcane in southern China. Fungal Diversity 99(1):1–104. https://doi.org/10.1007/s13225-019-00434-5(0123456789

    Article  Google Scholar 

  • Rivera MF, Laberry R, Lozano JC (1993) Evidences for Endophytes Parasiting Traditional Clones of Cassava (Manihot esculenta crantz). In: Roca WM, Thro AM (Eds) Proceedings of the first international scientific meeting of the cassava Biotechnology network, Cartagena, Colombia 25–28 August 1992. Centro Internacional de Agricultura Tropical (CIAT), pp 335–339

  • Ronquist F, Heulsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Santos DV, Silva RMF, Aguilera P, Silva GA, Bezerra JL, Oliveira RJV (2021) First occurrence of Nigrospora lacticolonia Mei Wang & L. Cai (Xylariales, Ascomycota) in the Neotropical Region. Check List 17(4):1243–1248. https://doi.org/10.15560/17.4.1243

  • Stamatakis A (2014) RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun X, Guo LD, Hyde KD (2011) Community composition of endophytic fungi in Acer truncatum and their role in decomposition. Fungal Divers 47:85–95. https://doi.org/10.1007/s13225-010-0086-5

    Article  Google Scholar 

  • Wang M, Liu F, Crous PW, Cai L (2017) Phylogenetic reassessment of Nigrospora: Ubiquitous endophytes, plant and human pathogens. Persoonia 39:118–142. https://doi.org/10.3767/persoonia.2017.39.06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, USA, pp 315–322

    Google Scholar 

  • Wu Z, Xie Z, Wu M, Li X, Li W, Ding W, She Z, Li C (2018) New Antimicrobial Cyclopentenones from Nigrospora sphaerica ZMT05, a Fungus Derived from Oxya chinensis Thunber. J Agric Food Chem 66(21):5368–5372. https://doi.org/10.1021/acs.jafc.8b01376

    Article  CAS  PubMed  Google Scholar 

  • Zhang ZF, Zhou SY, Eurwilaichitr L, Ingsriswang S, Raza M, Chen Q, Zhao P, Liu F, Cai L (2021) Culturable mycobiota from Karst caves in China II, with descriptions of 33 new species. Fungal Diversity 106:29–136. https://doi.org/10.1007/s13225-020-00453-7

    Article  Google Scholar 

  • Zheng T, Zhao L, Huang M, Deng J, Wang Y (2021) First report of leaf spot caused by Nigrospora hainanensis on Oxalis corymbosa in China. Plant Dis. https://doi.org/10.1094/PDIS-10-21-2149-PDN

    Article  PubMed  Google Scholar 

  • Zimmerman A (1902) Ueber einige an tropischen Kulturpflanzen beobachtete Pilze III. Zentralblatt Für Bakteriologie, Parasitenkunde 8:216–221

    Google Scholar 

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Acknowledgements

Amanda C.Q. Brito thanks the Fundação de Amparo à Ciência e Tecnologia de estado de Pernambuco (FACEPE) for a doctoral fellowship (2019−2023); A.R. Machado and C.M. Souza-Motta also acknowledge the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the research fellowships. We are grateful to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Fundação de Apoio à Ciência e Tecnologia do Estado de Pernambuco (FACEPE), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Pró-Reitoria de Pesquisa e Inovação of the Universidade Federal de Pernambuco (PROPESQI-UFPE) for financial support, and Micoteca URM Profa. Maria Auxiliadora de Queiroz Cavalcanti of the Universidade Federal de Pernambuco for the assistance in the execution of this study.

Funding

This work was financial supported by research fellowship from CNPq-407539/2018–2; doctoral fellowship from FACEPE IBPG-0099–5.01/19; and financial supported by CAPES and PROPESQI-UFPE.

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All authors contributed to the conception and design of the manuscript. ARM guided and supervised this research. CMSM revised the data. ACQB, JFM, AEAS, SSN, and ARM collected the samples used in this study. JFM did the molecular lab work. ACQB performed the morphological and phylogenetic analyses, done the illustrations, and wrote the first draft. All authors contributed to its development and completion. All authors read and approved the final manuscript.

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Correspondence to Amanda Cupertino de Queiroz Brito.

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de Queiroz Brito, A.C., de Mello, J.F., de Almeida Souza, A.E. et al. Richness of Nigrospora spp. (Apiosporaceae) in Manihot esculenta in Brazil and the description of three new species. Mycol Progress 22, 37 (2023). https://doi.org/10.1007/s11557-023-01887-4

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