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Molecular Characterisation of Fungal Endophytic Morphospecies Associated with the Indigenous Forest Tree, 5 Theobroma Gileri, in Ecuador

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Molecular Characterisation of Fungal Endophytic Morphospecies Associated with the Indigenous Forest Tree, 5 Theobroma Gileri, in Ecuador mycological research 112 (2008) 852–860 journal homepage: www.elsevier.com/locate/mycres Molecular characterisation of fungal endophytic morphospecies associated with the indigenous forest tree, 5 Theobroma gileri, in Ecuador Sarah E. THOMASa,*, Jayne CROZIERa,y, M. Catherine AIMEb,z, Harry C. EVANSa, Keith A. HOLMESa,x aCABI Europe-UK, Silwood Park, Buckhurst Road, Ascot, Berkshire SL5 7TA, UK bUnited States Department of Agriculture-Agricultural Research Service, Systematic Botany and Mycology Laboratory, Beltsville, MD 20705, USA article info abstract Article history: Fungal endophytes were isolated from healthy stems and pods of Theobroma gileri, an alter- Received 24 April 2007 native host of the frosty pod rot pathogen of cacao. Non-sporulating isolates were grouped Received in revised form into 46 different morphological species according to their colony morphology. Many of these 3 January 2008 morphospecies were assumed to be basidiomycetes and, therefore, were of particular inter- Accepted 10 January 2008 est. Basidiomycetous endophytes have received far less attention than ascomycetes and also Corresponding Editor: have potential as biological control agents of the basidiomycetous pathogens of T. cacao: Mon- Barbara Schulz iliophthora roreri (frosty pod rot pathogen) and M. perniciosa (witches’ broom disease). The mor- phospecies were further characterised by molecular analyses. Amplification of the nuLSU Keywords: was undertaken for phylogenetic placement of these non-sporulating cultures and revealed Agaricomycotina a total of 31 different taxa of which 15 were basidiomycetes belonging to the class Agaricomy- Basidiomycota cetes, and 16 ascomycetes primarily belonging to the Sordariomycetes. Biological control ª 2008 The British Mycological Society. Published by Elsevier Ltd. All rights reserved. Cocoa Endophyte Phytopathogens rDNA phylogeny Theobroma cacao Neotropics Introduction west Ecuador and Colombia, an area of high plant endemism (Dodson & Gentry 1991). T. gileri appears confined between Theobroma gileri (Malvaceae) is an understorey tree in submon- 550–700 m a.s.l. and can be abundant in ravines and rocky tane forests of the Choco´ phytogeographic region of north- slopes, often reaching a height of between 15–20 m (Evans 5 Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture. * Corresponding author. Tel.: þ44 (0) 1491829149; fax: þ44 (0) 1491829123. E-mail address: [email protected] y Present address: CABI Caribbean & Latin America, CATIE, Turrialba, 7170, Costa Rica. z Present address: Department of Plant Pathology and Crop Physiology, Louisiana State University AgCenter, 302 Life Sciences Bldg., Baton Rouge, LA 70803, USA. x Present address: CABI Caribbean & Latin America Gordon Street, Curepe, Trinidad & Tobago. 0953-7562/$ – see front matter ª 2008 The British Mycological Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.mycres.2008.01.008 Molecular characterisation of fungal endophytic morphospecies 853 et al. 2003). Interest in this species of Theobroma and its associ- evolutionarily isolated from T. cacao, which appears to have ated mycoflora originated when it was identified as a forest originated east of the Andes (Motomayor et al. 2002). This iso- host of one of the major basidiomycete pathogens of the com- lation supports the hypothesis that this Theobroma species mercially cultivated T. cacao (Baker et al. 1954). may be a source of novel fungal endophytes, with potential T. cacao is the source of the internationally traded commod- as biocontrol agents. Its isolated forest habitat and non-culti- ity, cocoa. In Latin America production of cocoa is currently vated status may have enabled T. gileri to retain its rich myco- affected by the basidiomycetous pathogens Moniliophthora per- flora, which has been lost by cultivated T. cacao; this is niciosa (causal agent of witches’ broom disease) and M. roreri supported by the previous study on T. gileri endophytes (Evans (causal agent of frosty pod rot). Conventional control et al. 2003). approaches have proved unable to halt the advance of these In a survey undertaken in Ecuador in 1999, Evans et al. diseases, especially frosty pod rot, which was identified in (2003) located the type locality of T. gileri in order to isolate po- 2005 as having reached as far north as Mexico (Phillips-Mora tential classical biological control agents for frosty pod rot. et al. 2006). M. roreri is also posing a direct threat to Bolivia Fungal endophytes were isolated from the stems and pods and Brazil from its base in Peru (Evans 2002a). Biological con- of T. gileri. A rich endophytic assemblage was obtained that trol, in particular classical biological control, is a management consisted of 373 isolates (Evans et al. 2003). With the aid of option being pursued (Holmes et al. 2004). Classical biocontrol morphological keys, 258 of these were identified at least to ge- aims to redress the ecological imbalance by introducing nus level. The taxonomic range of endophytic fungi isolated coevolved natural enemies, selected for specificity and bio- was different from previously documented studies of tree en- control activity, from the evolutionary centre of origin of the dophytes with the majority of isolates belonging to ana- invasive, alien pest or pathogen. This strategy has tradition- morphs of the Hypocreales, as well as to basidiomycete ally been exploited for the control of invasive alien weeds, orders (Evans et al. 2003). However, it was not possible to iden- using both insect and fungal agents (Evans 2002b; McFadyen tify 115 (31 %) of the isolates collected as they did not sporulate 1998) as well as against exotic arthropods (Greathead 1995). on artificial culture media. These were grouped into 46 ‘mor- T. gileri was first described from north-west Ecuador in the phological species’ according to their colony characteristics early 1950s (Cuatrecasas 1953, 1964) and was subsequently (Fig 1). reported to occur along the Pacific slopes of the Andes up to This paper reports on the subsequent molecular character- northern Colombia (Baker et al. 1954). This means that T. gileri, isation undertaken to identify these 46 morphospecies iso- which grows in the Choco´ phytogeographic region that is a rec- lated from healthy stems and pods of T. gileri in native ognised biodiversity ‘hotspot’ (Myers et al. 2000), has been forest. This paper has given special consideration to the Fig 1 – Morphospecies isolated from stems of Theobroma gileri. 854 S. E. Thomas et al. phylogenetic breadth of the basidiomycete endophytes identi- et al. (2003). This subsequent study focuses on the 115 isolates fied as these have been less well studied in comparison with that failed to form fruiting structures in culture, or only pro- ascomycetes and may be useful as potential novel biocontrol duced arthrosporic stages. These isolates were grouped into agents for the basidiomycetous pathogens of T. cacao. 46 morphospecies according to their colony characteristics and a representative isolate of each was selected for molecu- lar analysis. All isolates are stored under oil or at 10 C as DIS Methods codes at CABI, UK (Tables 1 and 2). Selection of endophytic fungi DNA extraction, PCR amplification, and rDNA sequencing of endophytic morphospecies Details on the endophyte isolation techniques and the two study sites, one on the northwestern slopes of the Andes in DNA was extracted from the fungal isolates using a MoBio the Ecuadorian Province Esmeraldas and the other in the UltraClean Plant DNA Isolation Kit (MoBio Laboratories, Sol- neighbouring Pichincha Province, can be found in Evans ana Beach, CA). An agar block (ca 5mm 5mm 2 mm) Table 1 – Identification of T. gileri basidiomycetes isolates based on LSU rDNA sequence data Isolate Genbank Tentative Nearest Query Max Site/Tissue code no. identification match coverage (%) identity (%) Esmeraldas Pichincha Stem Pod Stem Pod DIS 360d DQ674802 Coprinellus sp. AY207180.1 99 99 + ÀÀÀ Coprinellus disseminatus DIS 274g – Coprinellus sp. + ÀÀÀ DIS 320g – Coprinellus sp. ÀÀ+ À DIS 337bii – Coprinellus sp. ÀÀ+ À DIS 355e – Coprinellus sp. ÀÀ+ À DIS 357aii – Coprinellus sp. ÀÀ+ À DIS 276d DQ674804 Ganoderma sp. DQ208418.1 100 99 À + ÀÀ Fomes fomentarius DIS 276b – Ganoderma sp. À + ÀÀ DIS 276f – Ganoderma sp. À + ÀÀ DIS 358a DQ674805 Lachnocladiaceae sp. DQ094786.1 100 97 + ÀÀÀ Peniophora cinerea DIS 360e DQ674807 Lentinus sp. 1 AF261563.1 100 98 + ÀÀÀ Lentinus squarrosulus DIS 326i DQ674806 Lentinus sp. 2 AF261563.1 100 98 + ÀÀÀ Lentinus squarrosulus DIS 274b DQ674808 Melanotus AF261511.1 93 100 + ÀÀÀ subcuneiformis Melanotus subcuneiformis DIS 330i DQ674803 Meripilus sp. AY684166.1 100 95 À + ÀÀ Albatrellus higanensis DIS 276i DQ674809 Phlebioid sp. EU118665.1 100 99 À + ÀÀ Scopuloides hydnoides DIS 330fi DQ674810 Piptoporus sp. AY684164.1 100 96 À + ÀÀ Fomitopsis pinicola DIS 360aii DQ674813 Polyporaceae sp. 1 DQ208421.1 100 97 + ÀÀÀ Fomes fomentarius DIS 357f – Polyporaceae sp. 1 ÀÀ+ À DIS 328b DQ674812 Polyporaceae sp. 2 DQ208421.1 100 97 + ÀÀÀ Fomes fomentarius DIS 227b – Polyporaceae sp. 2 ÀÀ+ À DIS 274c – Polyporaceae sp. 2 + ÀÀÀ DIS 356a – Polyporaceae sp. 2 ÀÀ+ À DIS 357b – Polyporaceae sp. 2 ÀÀ+ À DIS 229c DQ674811 Polyporaceae sp. 3 AY684163.1 100 97 ÀÀ+ À Ganoderma tsugae DIS 359c DQ674814 cf. Pycnoporus sp. AY586703.1 100 98 + ÀÀÀ Pycnoporus cinnabarinus DIS 372b DQ674815 Schizophyllum sp.
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