Advertisement

Mycological Progress

, Volume 18, Issue 5, pp 683–701 | Cite as

Lasiodiplodia spp. associated with Aquilaria crassna in Laos

  • Yu Wang
  • Sen Lin
  • Lin Zhao
  • Xiang Sun
  • Wei He
  • Ying ZhangEmail author
  • Yu-Cheng DaiEmail author
Original Article
  • 17 Downloads

Abstract

Aquilaria (Thymelaeaceae) is a genus of evergreen trees, which is well-known in producing resinous heartwood (known as agarwood). Infection by Lasiodiplodia spp. has been reported effectively inducing the agarwood formation in members of Aquilaria. In this study, 12 taxa of Lasiodiplodia were retrieved from trunks of healthy, brown, and ligaloes tissue of Aquilaria crassna in Laos, of which eight species are new to science. Fungal identification was conducted using a combination of morphology and multi-locus phylogenetic analyses based on combined translation elongation factor 1-a sequence (tef1-a), internal transcribed spacer (ITS), ß-tubulin (TUB), and RNA polymerase II beta subunit (RPB2) nuDNA sequences. Cashew nut-shaped conidia and the baculate ornamentation on the conidia of Lasiodiplodia spp. are first reported in this study. Aquilaria crassna proved a good host for Lasiodiplodia, and the function of Lasiodiplodia spp. in inducing agarwood formation needs further study.

Keywords

Agarwood Botryosphaeriaceae Chinese medicine Fungal biodiversity New taxa 

Notes

Acknowledgements

Dr. Jinlong Zhang (KFBG) is acknowledged for host plant identification.

Funding information

This work was supported by the Fundamental Research Funds for the Central Universities (No. 2016ZCQ04), National Natural Science Foundation of China (General Program, 31770015, 31370063), NSFC Projects of International Cooperation and Exchanges (3155461143028), and National Science and Technology Foundation Project (2014FY210400).

Supplementary material

11557_2019_1481_MOESM1_ESM.jpg (5.7 mb)
ESM 1 (JPG 5851 kb)
11557_2019_1481_MOESM2_ESM.jpg (3.6 mb)
ESM 2 (JPG 3725 kb)
11557_2019_1481_MOESM3_ESM.jpg (5 mb)
ESM 3 (JPG 5128 kb)
11557_2019_1481_MOESM4_ESM.jpg (5.3 mb)
ESM 4 (JPG 5409 kb)

References

  1. Abdollahzadeh J, Javadi A, Goltapeh EM, Zare R, Phillips AJL (2010) Phylogeny and morphology of four new species of Lasiodiplodia from Iran. Persoonia 25:1–10CrossRefGoogle Scholar
  2. Alves A, Correia A, Luque J, Phillips AJL (2004) Botryosphaeria corticola, sp. nov. on Quercus species, with notes and description of Botryosphaeria stevensii and its anamorph, Diplodia mutila. Mycologia 96:16CrossRefGoogle Scholar
  3. Alves A, Correia A, Phillips AJL (2006) Multi-gene genealogies and morphological data support Diplodia cupressi sp. nov., previously recognized as D. pinea f. sp. cupressi, as a distinct species. Fungal Divers 23:1–15Google Scholar
  4. Alves A, Crous PW, Correia A, Phillips AJL (2008) Morphological and molecular data reveal cryptic speciation in Lasiodiplodia theobromae. Fungal Divers 28:1–13Google Scholar
  5. Begoude BAD, Slippers B, Wingfield MJ, Roux J (2010) Botryosphaeriaceae associated with Terminalia catappain Cameroon, South Africa and Madagascar. Mycol Progress 9:101–123CrossRefGoogle Scholar
  6. Bhattacharyya B, Datta A, Baruah HK (1952) On the formation and development of agaru in Aquilaria agallocha. Sci Cult 18:240–241Google Scholar
  7. Burgess TI, Barber PA, Mohali S, Pegg G, de Beer W, Wingfield MJ (2006) Three new Lasiodiplodia spp. from the tropics, recognized based on DNA sequence comparisons and morphology. Mycologia 98:423–435CrossRefGoogle Scholar
  8. Chungu D, Muimba-Kankolongo A, Wingfield MJ, Roux J (2010) Identification of fungal pathogens occurring in eucalypt and pine plantations in Zambia by comparing DNA sequences. Forestry 83:507–515CrossRefGoogle Scholar
  9. Coutinho IBL, Freire FCO, Lima CS, Lima JS, Goncalves FJT, Machado AR, Silva AMS, Cardoso JE (2017) Diversity of genus Lasiodiplodia associated with perennial tropical fruit plants in northeastern Brazil. Plant Pathol 66:90–104CrossRefGoogle Scholar
  10. Cruywagen EM, Slippers B, Roux J, Wingfield MJ (2017) Phylogenetic species recognition and hybridisation in Lasiodiplodia: a case study on species from baobabs. Fungal Biol 121:420–436CrossRefGoogle Scholar
  11. Cui JL, Guo SX, Xiao PG (2011) Antitumor and antimicrobial activities of endophytic fungi from medicinal parts of Aquilaria sinensis. J Zhejiang Univ Sci B 12:385–392CrossRefGoogle Scholar
  12. Damm U, Crous PW, Fourie PH (2007) Botryosphaeriaceae as potential pathogens of Prunus species in South Africa, with descriptions of Diplodia africana and Lasiodiplodia plurivora sp. nov. Mycologia 99:664–680CrossRefGoogle Scholar
  13. Dou ZP, He W, Zhang Y (2017) Lasiodiplodia chinensis sp. nov., a new holomorphic species from China. Mycosphere 8:521–532CrossRefGoogle Scholar
  14. Fan MC, Yeh HC, Hong CF (2013) First report of Lasiodiplodia theobromae causing dieback of Aquilaria sinensis in Taiwan. Plant Dis 97:690–691CrossRefGoogle Scholar
  15. Glass NL, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify y conserved genes from filamentous ascomycetes. Appl Environ Microbiol 61:1323–1330Google Scholar
  16. Gong LJ, Guo SX (2009) Endophytic fungi from Dracaena cambodiana and Aquilaria sinensis and their antimicrobial activity. Afr J Biotechnol 8:731–736Google Scholar
  17. Han XM, Liang L, Zhang Z (2014) Study of production of sesquiterpenes of Aquilaria senensis stimulated by Lasiodiplodia theobromae. China J Chin Mater Med 39:192–196Google Scholar
  18. Huelsenbeck JP, Ronquist F (2005) Bayesian analysis of molecular evolution using MrBayes. In: Nielsen R (ed) Statistical Methods in Molecular Evolution. Springer, New York, pp 183–232CrossRefGoogle Scholar
  19. Ismail AM, Cirvilleri G, Polizzi G, Crous PW, Groenewald JZ, Lombard L (2012) Lasiodiplodia species associated with dieback disease of mango (Mangifera indica) in Egypt. Australas Plant Pathol 41:649–660CrossRefGoogle Scholar
  20. Linaldeddu BT, Deidda A, Scanu B, Franceschini A et al (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 Divers 71:201–214CrossRefGoogle Scholar
  21. Liu JK, Phookamsak R, Doilom M, Wikee S, Li YM, Ariyawansha H, Boonmee S, Chomnunti P, Dai DQ, Bhat JD, Romero AI, Zhuang WY, Monkai J, Jones EBG, Chukeatirote E, Ko Ko TW, Zhao YC, Wang Y, Hyde KD (2012) Towards a natural classification of Botryosphaeriales. Fungal Divers 57:149–210CrossRefGoogle Scholar
  22. Machado AR, Pinho DB, Pereira OL (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 Divers 67:1–17CrossRefGoogle Scholar
  23. Marques MW, Lima NB, Jr MADM, Barbosa MAG, Souza BO, Michereff SJ, Phillips AJL, Camara MPS (2013) Species of Lasiodiplodia associated with mango in Brazil. Fungal Divers 61:181–193Google Scholar
  24. Michalak S (2012) RaxmlGUI: a graphical front-end for RAxML. Org Divers Evol 12:335–337CrossRefGoogle Scholar
  25. Mohamed R, Jong PL, Zali MS (2010) Fungal diversity in wounded stems of Aquilaria malaccensis. Fungal Divers 43:67–74CrossRefGoogle Scholar
  26. Netto MSB, Assunção IP, Lima GSA, Marques MW, Lima WG, Monteiro JHA, Balbino VQ, Michereff SJ, Phillips AJL, Câmara MPS (2014) Species of Lasiodiplodia associated with papaya stem-end rot in Brazil. Fungal Divers 67:127–141CrossRefGoogle Scholar
  27. Netto MSB, Lima WG, Correia KC, da Silva CF, Thon M, Martins RB et al (2017) Analysis of phylogeny, distribution, and pathogenicity of Botryosphaeriaceae species associated with gummosis of Anacardium in Brazil, with a new species of Lasiodiplodia. Fungal Biol 121:437–451CrossRefGoogle Scholar
  28. Niekerk JMV, Crous PW, Groenewald JZ, Fourie PH, Halleen F (2004) DNA phylogeny, morphology and pathogenicity of Botryosphaeria species on grapevines. Mycologia 96:18Google Scholar
  29. Nobuchi T, Siripatanadilok S (1991) Preliminary observation of Aquilaria crassna wood associated with the formation of aloeswood. Kyoto Univ For 63:226–235Google Scholar
  30. Osorio JA, Crous CJ, Beer ZWD, Wingfield MJ, Roux J (2016) Endophytic Botryosphaeriaceae, including five new species, associated with mangrove trees in South Africa. Fungal Biol 121:361–393CrossRefGoogle Scholar
  31. Page RD (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358Google Scholar
  32. Pavlic D, Slippers B, Coutinho TA, Gryenhout M et al (2004) Lasiodiplodia gonubiensis sp. nov., a new Botryosphaeria anamorph from native Syzygium cordatum in South Africa. Stud Mycol 50:313–322Google Scholar
  33. Pavlic D, Wingfield MJ, Slippers B, Barber PA, Hardy GESJ, Burgess T (2008) New species of the Botryosphaeriaceae discovered on baobabs and other native trees in Western Australia. Mycologia 100:851–866CrossRefGoogle Scholar
  34. Pavlic D, Slippers B, Coutinho TA, Wingfield MJ (2010) Botryosphaeriaceae occurring on native Syzygium cordatum in South Africa and their potential threat to Eucalyptus. Plant Pathol 56:624–636CrossRefGoogle Scholar
  35. Phillips AJL, Alves A, Correia A, Luque J (2005) Two new species of Botryosphaeria with brown, 1-septate ascospores and Dothiorella anamorphs. Mycologia 97:17CrossRefGoogle Scholar
  36. Phillips AJL, Alves A, Pennycook SR, Johnston PR, Crous PW (2008) Resolving the phylogenetic and taxonomic status of dark-spored teleomorph genera in the Botryosphaeriaceae. Persoonia 21:29–55CrossRefGoogle Scholar
  37. Phillips AJL, Alves A, Abdollahzadeh J, Slippers B, Wingfield MJ, Groenewald JZ, Crous PW (2013) The Botryosphaeriaceae: genera and species known from culture. Stud Mycol 76:51–167CrossRefGoogle Scholar
  38. 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 53:793–808CrossRefGoogle Scholar
  39. Prasher IB, Singh G (2014) Lasiodiplodia indica—a new species of coelomycetous mitosporic fungus from India. Kavaka 43:64–69Google Scholar
  40. Premalatha K, Kalra A (2013) Molecular phylogenetic identification of endophytic fungi isolated from resinous and healthy wood of Aquilaria malaccensis, a red listed and highly exploited medicinal tree. Fungal Ecol 6:205–211CrossRefGoogle Scholar
  41. Rahayu G, Putridan JAL (2007) Acremonium and methyl-jasmonate induce terpenoid formation in agarwood tree (Aquilaria crassna). In: Makalahdi presenta sikandalam 3rd Asian conference on crop protection, Jogyakarta, 22–24 Aug 2007Google Scholar
  42. Rodríguez-Gálvez E, Guerrero P, Barradas C, Crous PW, Alves A (2017) Phylogeny and pathogenicity of Lasiodiplodia species associated with dieback of mango in Peru. Fungal Biol 121:452–465CrossRefGoogle Scholar
  43. Ronquist F, Huelsenbeck JP (2003) MrBayes 3.0: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefGoogle Scholar
  44. Rosado AWC, Machado AR, Freire FCO, Pereira OL (2016) Phylogeny, identification, and pathogenicity of Lasiodiplodia associated with postharvest stem-end rot of coconut in Brazil. Plant Dis 100:561–568CrossRefGoogle Scholar
  45. Sakalidis ML, Hardy GE, Burgess TI (2011) Use of the Genealogical Sorting Index (GSI) to delineate species boundaries in the Neofusicoccum parvum-Neofusicoccum ribis species complex. Mol Phylogenet Evol 60:333–344CrossRefGoogle Scholar
  46. Sangareswari M, Parthiban KT, Kanna SU, Karthiba L, Saravanakumar D (2016) Fungal microbes associated with agarwood formation. Am J Plant Sci 7:1445–1452CrossRefGoogle Scholar
  47. Slippers B, Crous PW, Denman S, Coutinho TA, Wingfield WMJ (2004) Combined multiple gene genealogies and phenotypic characters differentiate several species previously identified as Botryosphaeria dothidea. Mycologia 96:83–101CrossRefGoogle Scholar
  48. Slippers B, Crous PW, Jami F, Groenewald JZ, Wingfield MJ (2017) Diversity in the Botryosphaeriales: looking back, looking forward. Fungal Biol 121:307–321CrossRefGoogle Scholar
  49. Smith H, Wingfield MJ, Coutinho TA, Crous PW (1996) Sphaeropsis sapinea and Botryosphaeria dothidea endophytic in Pinus spp. and Eucalyptus spp. in South Africa. S Afr J Bot 62:86–88CrossRefGoogle Scholar
  50. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:88–90CrossRefGoogle Scholar
  51. Swofford DL (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, SunderlandGoogle Scholar
  52. Tamuli P, Boruah P, Nath SC, Leclercq P (2005) Essential oil of eaglewood tree: a product of pathogenesis. J Essent Oil Res 17:601–604CrossRefGoogle Scholar
  53. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefGoogle Scholar
  54. Tian JJ, Gao XX, Zhang WM, Wang L, Qu LH (2013) Molecular identification of endophytic fungi from Aquilaria sinensis and artificial agarwood induced by pinholes-infusion technique. Afr J Biotechnol 12:3115–3131Google Scholar
  55. Trakunyingcharoen T, Cheewangkoon R, To-Anun C, Crous PW, VanNiekerk JM, Lombard L (2014) Botryosphaeriaceae associated with diseases of mango (Mangifera indica). Australas Plant Pathol 43:425–438Google Scholar
  56. Trakunyingcharoen T, Lombard L, Groenewald JZ, Cheewangkoon R, To-Anun C, Crous PW (2015) Caulicolous Botryosphaeriales from Thailand. Persoonia 34:87–99CrossRefGoogle Scholar
  57. Urbez-Torres JR, Peduto F, Striegler RK, Urrea-Romero KE, Rupe JC, Cartwright RD et al (2012) Characterization of fungal pathogens associated with grapevine trunk diseases in Arkansas and Missouri. Fungal Divers 52:169–189CrossRefGoogle Scholar
  58. White TJ, Bruns T, Lee S, Taylor JL (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innes MA, Gelfand DH, Snisky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic, San Diego, pp 315–322Google Scholar
  59. Wu ZC, Li DL, Chen YC, Zhang WM (2010) A new isofuranonaphthalenone and benzopyrans from the endophytic fungus Nodulisporium sp. A4 from Aquilaria sinensis. Helv Chim Acta 93:920–924CrossRefGoogle Scholar
  60. Yang T, Groenewald JZ, Cheewangkoon R, Jami F, Abdollahzadeh J, Lombard L, Crous PW (2017) Families, genera and species of Botryosphaeriales. Fungal Biol 121:322–346CrossRefGoogle Scholar
  61. Zhang Y, Wang HK, Fournier J, Crous PW, Jeewon R, Pointing SB, Hyde KD (2009) Towards a phylogenetic clarification of Lophiostoma / Massarina and morphologically similar genera in the Pleosporales. Fungal Divers 38:225–251Google Scholar
  62. Zhang Z, Han XM, Wei JH, Xue J, Yang Y, Liang L, Li XJ, Guo QM, Xu YH, Gao ZH (2014) Compositions and antifungal activities of essential oils from agarwood of Aquilaria sinensis (Lour.) Gilg induced by Lasiodiplodia theobromae (Pat.) Griffon & Maubl. J Braz Chem Soc 25:20–26Google Scholar

Copyright information

© German Mycological Society and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Beijing Advanced Innovation Center for Tree Breeding by Molecular DesignBeijing Forestry UniversityBeijingPeople’s Republic of China
  2. 2.Institute of MicrobiologyBeijing Forestry UniversityBeijingPeople’s Republic of China
  3. 3.Beijing Key Laboratory for Forest Pest ControlBeijing Forestry UniversityBeijingPeople’s Republic of China
  4. 4.State Key Laboratory of Mycology, Institute of MicrobiologyChinese Academy of SciencesBeijingPeople’s Republic of China

Personalised recommendations