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Trichoderma Stromaticum and Its Overseas Relatives

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Trichoderma Stromaticum and Its Overseas Relatives Mycol Progress (2012) 11:215–254 DOI 10.1007/s11557-011-0743-4 ORIGINAL ARTICLE Trichoderma stromaticum and its overseas relatives Gary J. Samuels & Adnan Ismaiel & Jorge de Souza & Priscila Chaverri Received: 1 October 2010 /Revised: 25 January 2011 /Accepted: 26 January 2011 /Published online: 22 February 2011 # Springer-Verlag (outside the USA) 2011 Abstract Trichoderma stromaticum, T. rossicum and new- stromaticum in tropical America. The closest relatives of T. ly discovered species form a unique lineage in Tricho- stromaticum are collected in Africa and Thailand; somewhat derma. Phylogenetic and phenotypic diversity in more distantly related are T. rossicum and T. barbatum,both Trichoderma stromaticum are examined in the light of found in north temperate regions. reported differences in ecological parameters and AFLP patterns. Multilocus phylogenetic analysis using 4 genes (tef1, Keywords Hypocreales . Theobroma cacao . Pleomorphic rbp2, cal, chi18-5) did not reveal phylogenetic basis for the fungi . Species concepts . Species complex . Hypocrea . two reported divergent AFLP patterns or for ecological Hypocreaceae . Cacao . Biological control . Biogeography. parameters; however, this analysis does indicate incomplete Systematics speciation with one supported clade derived from within T. stromaticum that corresponds to AFLP Group 2 of de Souza Taxonomic novelties Trichoderma barbatum . et al. (2006, Phytopathology 96:61–67). Trichoderma T. caesareum . T. floccosum . T. ivoriense . T. lanuginosum . stromaticum is known only from tropical America and is T. vermipilum typically found in association with Theobroma cacao infected with Moniliophthora perniciosa. It is reported here for the first time on pseudostromata of M. roreri in Peru. Strains of T. Introduction stromaticum also have been isolated as endophytes from stems of Theo. cacao. There are no recognized close relatives of T. Witches’ Broom Disease has caused considerable eco- nomic and social disruption in South America, but especially in the Brazilian state of Bahia (see reviews G. J. Samuels (*) : A. Ismaiel Systematic Mycology and Microbiology Lab, and references in de Souza et al. 2006, 2008; Loguercio United States Department of Agriculture, et al. 2009a, b). The pathogen, Moniliophthora perniciosa, Agriculture Research Service, infects cacao trees when basidiospores germinate and Rm 304, B-011A, 10300 Baltimore Ave, penetrate all meristematic tissues, including pods and Beltsville, MD 20705, USA e-mail: [email protected] flower cushions, leading to hypertrophy and hyperplasia and loss of apical dominance (witches’ broom formation) J. de Souza and loss of fruit. The pathogen ultimately produces small Centro de Ciências Agrárias Biológicas e Ambientais (CCABA), mushrooms on the infected dead brooms and infected pods Universidade Federal do Recôncavo da Bahia (UFRB), Centro, Cruz das Almas, BA 44380-000, Brazil that continue the disease cycle (Purdy and Schmidt 1996; Hebbar et al. 2002;deSouzaetal.2006, 2008; Meinhardt P. Chaverri et al. 2008). Trichoderma stromaticum colonizes dead Department of Plant Sciences and Landscape Architecture, brooms and other tissue infected with M. perniciosa and University of Maryland, 2112 Plant Sciences Building, destroys the basidiocarps of the pathogen thereby reducing College Park, MD 20742, USA the inoculum (Bastos 1996;Hjorthetal.2003). A 216 Mycol Progress (2012) 11:215–254 biological control product ‘Trichovab®,’ which is based on Morphological analyses asinglestrainofT. stromaticum, hasbeenusedonan experimental scale in Brazil since 1996 (de Souza et al. Observations of microscopic characters were made from 2006).Thestrainusedinthisproduct(‘TVC’)was cultures grown on CMD or SNA (low nutrient agar; originally isolated in the Brazilian Amazonian region Nirenberg 1976), less frequently from potato dextrose agar (Pará State) but its efficacy is subject to environmental (PDA; Difco). Cultures to be used for micromorphological conditions (Sanogo et al. 2002; Loguercio et al. 2009a, b) observations were incubated at 25°C under alternating cool and its effectiveness is greatly enhanced when it is applied white fluorescent light/darkness. in combination with farm sanitation and copper-based Material to be used for microscopic measurements was fungicides (Medeiros et al. 2010). first immersed in 3% (aq.) potassium hydroxide (KOH), de Souza et al. (2006) found that a large collection of which was replaced with water or more KOH as the strains of T. stromaticum from Brazil, Ecuador and preparation dried. Observations were made with differential Colombia could be divided between two amplified interference contrast, phase contrast or bright field micros- fragment length polymorphism (AFLP) groups that corre- copy. Helicon Focus® version 4.21.5 Pro (MP) (Helicon lated with a number of biological differences (de Souza Soft, www.heliconfocus.com) was used to produce some et al. 2006; 2008; Loguercio et al. 2009a, b)andthefact composite images. To make sections of perithecial collec- that a Hypocrea teleomorph, H. stromatica JL Bezerra tions, small pieces of substratum with one or two stromata et al. (Bezerra et al. 2003) is known for Group 2. These were rehydrated in 3% KOH. These were supported in differences suggest that T. stromaticum as it is currently Tissue-Tek® O.C.T. compound (Miles, Elkhart, IN, USA) understood is composed of at least two cryptic species. In on the stage of an IEC-CTF microtome cryostat; sections the present work, we apply multilocus phylogenetic and were made at a thickness of ca. 15 μm. Permanent classical mycological analyses to a collection of strains of preparations were made following Volkmann-Kohlmeyer T. stromaticum to clarify the taxonomy of this species. and Kohlmeyer (1996). InthecourseoftaxonomicworkwithTrichoderma/ Where possible, 30 units of each parameter were Hypocrea, we have collected or received from collabo- measured for each collection using Scion Image for rators many strains, which are routinely identified through Windows® (www.scioncorp.com). The continuous measure- DNA sequence analysis. Several of these are closely ments are reported as extremes in brackets with the range related to T. stromaticum and are included in the present calculated as mean plus and minus standard deviation. work. Computation of descriptive statistics, including 95% confi- dence intervals (ci), was performed using Systat 10 (Systat Software, San José, CA, USA). Materials and methods Growth rates were determined on PDA and SNA at 15, 20, 25, 30 and 35°C in darkness (with intermittent light). Cultures used Measurements were made at intervals of 24 up to 96 h. Colony characters were taken from colonies incubated on Although the primary emphasis of the present work is T. PDA and SNA at 25°C with alternating cool white stromaticum, related strains and species were included fluorescent light and darkness (12 h:12 h) after 7−10 days; when their close relationship to T. stromaticum was these conditions are referred to in descriptions as ‘under revealed during on-going taxonomic studies of Tricho- light.’ Color standards are from Kornerup and Wanscher derma. The strains used in this study are cited in Table 1. (1978, K&W). These include several cultures cited by de Souza et al. (2006) and perithecial collections. Cultures and perithecial DNA extraction, PCR and sequencing specimens of Trichoderma stromaticum and other species were collected by the authors in Brazil (Bahia), Cameroon, DNA from all strains included in this study was extracted Ecuador and Thailand. Cultures were also provided by using ArchivePure DNA cell/Tissue kit from 5 PRIME colleagues in Austria, Canada, Côte d’Ivoire, Ecuador, (Gaithersburg, MD, USA). The primers and their sequences Peru, Republic of South Africa, Russia, U.K., and USA. used in this study are given in Table 2. The primers for ITS Single ascospores were isolated from perithecial collections and α-actin (act) were described previously (Samuels and on cornmeal agar (Difco or BD BBL, Franklin Lakes, NJ, Ismaiel 2009). A portion of translation elongation factor 1- USA)+2% (w/v) dextrose (CMD) with the use of a α (tef1) was amplified using the primers Ef728M and Ef-2. micromanipulator. Representative cultures are deposited in Ef7-28 M is a modified version of EF728F (Carbone and Centraalbureau voor Schimmelcultures (CBS, Utrecht, and Kohn 1999) where nucleotide #4 is changed from C to Y= The Netherlands). C/T. This modification was necessary to make the primer Mycol Progress (2012) 11:215 Table 1 Trichoderma strains used in the research Species Strain T. stromaticum strain Provenance GenBank accession numbers code and AFLP groupa cal chi18-5 rbp2 tef1 ITS T. barbatum G.J.S. 04-308=CBS 125733 Tb USA: MI HQ342352 HQ342483 HQ342286 HQ342223 HQ342417 T. barbatum DAOM 230008 Russia: Siberia HQ342353 HQ342484 HQ342287 HQ342224 HQ342418 T. caesareum G.J.S. 01-225=CBS 124369 T Thailand: Khao Yai HQ342345 HQ342476 HQ342279 HQ342216 HQ342410 – Natl Park T. floccosum G.J.S. 01-238=CBS 124372 T Thailand: Khao Yai Natl Park HQ342347 HQ342478 HQ342281 HQ342218 HQ342412 254 T. ivoriense G.J.S. 01-312=CBS 125734 T Côte d’Ivoire HQ342346 HQ342477 HQ342280 HQ342217 HQ342411 T. lanuginosum G.J.S. 01-174=CBS 126100 Cameroon: Reserve Faunal du Dja HQ342349 HQ342480 HQ342283 HQ342220 HQ342414 T. lanuginosum G.J.S. 01-176=CBS 125718 T Cameroon: Reserve Faunal du Dja HQ342350 HQ342481 HQ342284 HQ342221 HQ342415 T. medusae G.J.S. 01-171=CBS 125719 T Cameroon: Reserve Faunal du Dja HQ342343 HQ342474 HQ342277
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