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Penicillium Species Endophytic in Coffee Plants and Ochratoxin a Production

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Penicillium Species Endophytic in Coffee Plants and Ochratoxin a Production Mycologia, 98(1), 2006, pp. 31–42. # 2006 by The Mycological Society of America, Lawrence, KS 66044-8897 Penicillium species endophytic in coffee plants and ochratoxin A production Fernando E. Vega1 endophytes have been conducted in dozens of plants, Francisco Posada including many important agricultural commodities Insect Biocontrol Laboratory, U.S. Department of such as wheat (Larran et al 2002a), bananas (Poca- Agriculture, Agricultural Research Service, Bldg. 011A, sangre et al 2000, Cao et al 2002), soybeans (Larran et BARC-W, Beltsville, Maryland 20705 al 2002b) and tomatoes (Larran et al 2001), but Stephen W. Peterson coffee endophytes remain largely unexplored with Microbial Genomics and Bioprocessing Research Unit, the exception of bacterial endophytes (Vega et al National Center for Agricultural Utilization Research, 2005). U.S. Department of Agriculture, Agricultural Research Several species of Penicillium were isolated as part Service, 1815 N. University St., Peoria, Illinois 61604 of a large survey for fungal endophytes in coffee Thomas J. Gianfagna (Vega et al in prep). Members of this genus produce Fabio Chaves a variety of metabolites (Mantle 1987, Abramson Department of Biology and Pathology, Rutgers The State 1997, Samson and Frisvad 2004), and contamination University of New Jersey, 59 Dudley Road, New with one of these metabolites, ochratoxin A (OTA), Brunswick, New Jersey 08903 can be a problem in many commodities, including coffee (Bucheli and Taniwaki 2002), due to its possible adverse effect on human health. Species of Abstract: Tissues from Coffea arabica, C. congensis, C. Aspergillus are the main OTA producers in tropical dewevrei and C. liberica collected in Colombia, Hawaii and semi-tropical areas (Abramson 1997). Among and at a local plant nursery in Maryland were sampled Penicillium species, Pitt (1987) found that only P. for the presence of fungal endophytes. Surface verrucosum Dierckx produced OTA, while Larsen et al sterilized tissues including roots, leaves, stems and (2001) reported P. verrucosum and P. nordicum various berry parts were plated on yeast-malt agar. Dragoni & Cantoni as OTA producers. Here we DNA was extracted from a set of isolates visually report on the identity of Penicillium species occurring recognized as Penicillium, and the internal tran- as endophytes in coffee and on their OTA pro- scribed spacer region and partial LSU-rDNA was duction. amplified and sequenced. Comparison of DNA sequences with GenBank and unpublished sequences MATERIALS AND METHODS revealedthepresenceof11knownPenicillium species: P. brevicompactum, P. brocae, P. cecidicola, P. Sampling.—Apparently healthy coffee (Coffea spp.) citrinum, P. coffeae, P. crustosum, P. janthinellum, P. tissues were collected randomly in coffee plantations olsonii, P. oxalicum, P. sclerotiorum and P. steckii as in Hawaii (2003) and Colombia (2003) and from well as two possibly undescribed species near P. seedlings obtained at The Behnke Nurseries Co. in diversum and P. roseopurpureum. Ochratoxin A was Beltsville, Maryland (2004). The Maryland seedlings produced by only four isolates, one isolate each of P. were purchased by the Behnke Nurseries Co. from Colasanti’s Wholesale in Ontario Canada, which in turn brevicompactum, P. crustosum, P. olsonii and P. imports the seeds from Costa Rica and germinates them oxalicum. The role these endophytes play in the in North America. Tissues sampled consisted of leaves, biology of the coffee plant remains enigmatic. roots, stems and various parts of the coffee berry Key words: Coffea arabica, Coffea congensis, Coffea (crown, peduncle, pulp and seeds). dewevrei, Coffea liberica, endophytes, OTA Fungal isolation.—Tissues were washed individually in running tap water and moved to the laminar flow hood INTRODUCTION where sections were cut with a sterile scalpel. These sections were surface-sterilized by dipping in 0.5% Endophytes are fungi or bacteria that occur inside sodium hypochlorite for 2 min, 70% ethanol for plant tissues without causing any apparent symptoms 2 min and rinsing in sterile distilled water followed by (Wilson 1995). Several roles have been ascribed to drying on sterile filter paper (Arnold et al 2001). The fungal endophytes, including a role against insects edges of each sampled tissue were cut off and discarded (Breen 1994, Arnold and Lewis 2005). Surveys for and subsamples of the remaining tissue measuring approximately 2 3 3 mm were individually placed in Accepted for publication 19 Dec 2005. 5 cm diam petri dishes containing yeast-malt agar 1 Corresponding author. E-mail: [email protected] (YMA; Sigma Y-3127, Sigma-Aldrich Co., St. Louis, 31 32 MYCOLOGIA Missouri) to which 0.1% stock antibiotic solution was Minnesota) and OTA separated by isocratic C18 reverse added (stock: 0.02 g each tetracycline, streptomycin phase HPLC with a mobile phase of acetonitrile : water : and penicillin in 10 mL sterile distilled water, filter acetic acid (57 : 41 : 2) at 0.8 mL/min. OTA was quan- sterilized; from this 1 mL was added per liter of media). tified using a fluorescence detector (Shimadzu RF-10A, Columbia, Maryland) (excitation 330 nm and emission Fungal identification.—Penicillium strains were identified 460 nm). The minimum detectable amount was based on the DNA sequence of a ca 1200 nucleotide 0.01 ng. Three sample replicates were analyzed for each sequence fragment containing the ITS1, 5.8S rDNA, isolate. An OTA (Sigma-Aldrich Co., St. Louis, Missouri) ITS2 and D1–D2 region of LSU rDNA (ID region, standard curve was prepared for quantification and Peterson 2000, Peterson et al 2003). Briefly, DNA was Aspergillus ochraceus Wilhelm was used as a positive isolated from mycelium harvested from agar cultures control (kindly provided by J. White, Rutgers Universi- and broken mechanically with glass beads. Proteins ty). Aspergillus westerdijkiae Frisvad & Samson, a species were extracted using phenol-chloroform, nucleic acids known to produce ochratoxins and which has been were precipitated with ethanol, pelleted, redissolved in isolated from surface-disinfected green coffee beans in TE buffer (10 mM Tris, 1 mM EDTA pH 8.0) and India (Frisvad et al 2004) also was used as a positive further purified by adsorption to silica in the presence control. The A. westerdijkiae strains were isolated from of concentrated NaI (Peterson 2000). Purified DNA was a coffee berry borer parasitoid (Prorops nasuta Water- stored in TE buffer at 220 C. ston; Hymenoptera: Bethylidae) and from a coffee berry The ID region was amplified using primers ITS-5 (White borer (Hypothenemus hampei (Ferrari); Coleoptera: Cur- et al 1990) and D2R (Peterson et al 2003), standard buffer culionidae), both collected at the National Coffee (White et al 1990) and Taq polymerase (RedTaq, Sigma, St. Research Center (CENICAFE´ ) in Chinchina´, Caldas, Louis). The thermal profile was 96 C 2 min, followed by 35 Colombia (Peterson et al 2005a). cycles of 96 C 30 s, 51 C 30 s, 72 C 90 s and a final extension of 5 min at 72 C. Amplicon quality was assessed by agarose gel electrophoresis and ethidium bromide staining. Ampli- RESULTS cons were purified using Millipore Multiscreen PCR clean- up plates (Millipore, Billerica, Massachusetts). Comparison of ID region sequences with GenBank Sequencing reactions were performed on both strands of and unpublished sequences revealed the presence of each amplicon using ABI Big-Dye reaction kit 3.1 (Applied 13 Penicillium species endophytic in Coffea arabica: P. Biosystems, Foster City, California); excess dye was removed sp. (near P. diversum Raper & Fennell), P. brevicom- by ethanol precipitation. DNA sequences were read on an pactum Dierckx, P. brocae Peterson et al, P. cecidicola ABI 3730 DNA (Applied Biosystems, Foster City, California) Seifert et al, P. citrinum Thom, P. coffeae Peterson et sequencer. Complementary strands of the DNA were al, P. crustosum Thom, P. janthinellum Biourge, P. aligned and corrected using Sequencher (Gene Codes olsonii Bainier & Sartory, P. oxalicum Currie & Thom, Corp., Ann Arbor, Michigan). BLAST was implemented P. sclerotiorum Beyma, P. sp. (near P. roseopurpureum locally and a database of Penicillium sequences was Dierckx), and P. steckii Zalessky (TABLE I). P. olsonii assembled from published sequences of ex-type cultures (GenBank) and unpublished sequences of other ex-type was also identified in C. liberica Bull ex Hiern, C. isolates (Peterson 2000, unpubl). If an unknown sequence dewevrei DeWild & Durand, and C. congensis from the was a perfect match to the sequence from an ex-type Kona Experimental Station in Kona, Hawaii (TA- culture, the unknown was assigned to that species. BLE I). The sequences of six isolates identified as P. Sequences were also compared to all GenBank accessions brevicompactum differed from the sequence of the ex- using BLAST. Sequences of the isolates reported here are type isolate at 0, 1 or 2 base positions with total deposited in GenBank and accession numbers are listed similarity of 1138, 1139 or 1140 matches out of 1140 (TABLE I). Fungal isolates are accessioned in the ARS bases. Each of these sequences had been found Culture Collection (NRRL) Peoria, Illinois. Some isolates previously to be representative of the species in also were examined for phenotypic characters and keyed genealogical concordance phylogenetic species rec- using Pitt et al (1990) or Ramirez (1982). ognition (GCPSR) study (Peterson 2004). Sequences Ochratoxin A detection.—All the isolates listed (TABLE I) from the 13 isolates identified as P. olsonii were were tested for OTA presence. OTA was extracted and identical with the sequence from an ex-type isolate analyzed using the methodology of Bragulat et al (1140 bases) and were representative of variation (2001). Three agar plugs (0.5 mm diam 3 0.5 mm found in the species (Peterson 2004). Three isolates length) were removed from the fungal cultures growing possessed sequences identical to the ID region on YMA for three months and added to an HPLC sequence (1110 bases) of P. citrinum ex-type and (Shimadzu LC-AT, Columbia, Maryland) autosampler vial (33 mm 3 10 mm) of known weight and are identified as such.
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