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Kroken, S. and Taylor, J. W. 2000 Phylogenetic Species, Reproductive Mode, and Specificity of the Green Alga Trebouxia Forming Lichens with the Fungal Genus Letharia Author(s): Scott Kroken and John W. Taylor Source: The Bryologist, Vol. 103, No. 4 (Winter, 2000), pp. 645-660 Published by: American Bryological and Lichenological Society Stable URL: http://www.jstor.org/stable/3244330 . Accessed: 19/07/2011 18:28 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at . http://www.jstor.org/action/showPublisher?publisherCode=abls. Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. American Bryological and Lichenological Society is collaborating with JSTOR to digitize, preserve and extend access to The Bryologist. http://www.jstor.org The Bryologist 103(4), pp. 645-660 Copyright ? 2000 by the American Bryological and Lichenological Society, Inc. Phylogenetic Species, Reproductive Mode, and Specificity of the Green Alga Trebouxia Forming Lichens with the Fungal Genus Letharia SCOTTrrKROKEN1 AND JOHN W. TAYLOR2 Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720 U.S.A. 1e-mail: kroken@ nature.berkeley.edu, 2jtaylor@ socrates.berkeley.edu Abstract. The green algal symbionts of the lichenized fungus Letharia are identified as mem- bers of the morphospecies Trebouxia jamesii, based on ITS sequences that place them in a mo- lecularly diverse clade with other lichen algae also identified as T. jamesii. However, based on additional sequence from a second locus, actin, T. jamesii is seen to consist of many phylogenetic species. A clade of six to seven closely related phylogenetic species of T. jamesii are symbiotic with five of the six phylogenetic species of Letharia. Within this broad level of specificity, there are also narrower patterns of specificity. For example, three cryptic species of T. jamesii were found only in two species of Letharia in California, a pattern that may be due either to bioge- ography, or to Letharia phylogenetically tracking Trebouxia. Allopatric Letharia vulpina has switched to a genetically distant phylogenetic species within the T. jamesii morphospecies, sug- gesting that habitat plays a role in specificity. One phylogenetic species of T. jamesii was found to have a recombining population structure, as two alleles of two loci were found in all four pairwise combinations among the haploid genotypes of that species. This result suggests that Trebouxia, a genus in which sexual structures have never been observed, is nevertheless recom- bining. Trebouxia (sensu lato, including Asterochloris) 'gracilis,' and L. 'rugosa' are always apotheciate, is the photobiont found in 20% of all lichens (Ram- and sometimes also isidiate. Letharia vulpina and bold & Triebel 1992). Trebouxia is in the order Tre- L. 'lupina' are always sorediate and rarely apothe- bouxiophyceae (Friedl 1995), which includes the ciate. symbiotic algae for 50-70% of all lichen species In spite of the fact that 20% of all described spe- (Ahmadjian 1982), including the Lecanorales cies of fungi are lichenized, their photobionts re- (Friedl & Btidel 1996). In this study, we determine main poorly understood in terms of the number and the identity and phylogeny of green algal symbionts identity of species, the reproductive mode of those of the lichenized fungus Letharia, compare the al- species, and the degree of specificity in the asso- gal phylogeny to the fungal phylogeny to examine ciations between lineages of photobionts and lich- patterns of specificity (the range and taxonomic re- enized fungi. Approximately 13,500 lichen species latedness of acceptable partners, Rambold et al. have been named, corresponding to the diversity of 1998), and investigate the population structure of the fungal component (Hawksworth 1988). Of the algae to determine if recombination contributes these, 12,500 lichen species have a green alga as a to the reproduction of lichenized algae. The study photobiont and 1,000 lichen species have a cya- uses variation in DNA-based loci to identify phy- nobacterium (Tschermak-Woess 1988). The photo- logenetic species using concordance of gene gene- bionts of most lichen species have been assigned to alogies, and to infer reproductive mode from com- a genus based on morphology. However, only 200 parison among gene genealogies within phyloge- photobionts have been described to species, also netic species. This same approach has been used to based on morphology, with 100 species of cyano- study the speciation and reproductive mode of bacteria, and 100 species of green algae (Tscher- Letharia (Kroken & Taylor 2001). mak-Woess 1988). If these morphological species Letharia was selected for this study among the are indeed phylogenetic species, then for each cy- many members of the largest order of lichens, the anobacterial photobiont there would be 10 compat- Lecanorales, because we have shown that it is com- ible fungi, and for each green algal photobiont there posed of at least six phylogenetic species (Kroken would be 1,250 compatible fungi! However, each & Taylor 2001). To permit comparison of myco- photobiont species as defined by morphology may biont and phycobiont, the six fungal species are comprise many cryptic species that are compatible provisionally identified as follows. Letharia 'luci- only with a much smaller range of fungal species. da' is strictly apotheciate. Letharia 'barbata,' L. DNA sequence data are being used to determine the 0007-2745/00/645-660$1.75/0 646 THE BRYOLOGIST [VOL. 103 157 bases 202 bases 9 A1TCT3T 738 5'14769 ~'~actin primermap67 A 7Z3 Ai783 1122 3' ACT2T ACT4T FIGURE1. Primer map for type I actin. identity of photobiont species and their specificity each 1.5-mL microcentrifuge tube containing one ml of purified water, 10 pL of algal cells and 50 pL of PVPP to lichenized fungi. One such study used DNA se- (polyvinylpolypyrrolidone) powder were added. The open quence data to suggest specificity among strains of tubes were secured in a floating rack and placed into a the cyanobacterium Nostoc and species of the Pel- beaker of boiling water for two min., and then placed on tigeralean lichenized fungi in the genera Peltigera ice to chill. One pL of the resulting solution was used and Nephroma (Paulsrud & Lindblad 1998). directly as template for each PCR reaction. Primer design, PCR and DNA sequencing.-Algal-spe- Most green algae include both clonal and sexual cific primers were necessary to amplify Trebouxia DNA reproduction in their life cycles. However, physical from the whole lichen DNA extracts. PCR primers were evidence of sex (e.g., fusion of gametes, meiotic designed to amplify ITS from the nuclear ribosomal array, tetrads) has not been observed in any green algal and a fragment of the actin gene that contained two in- were to photobiont (Friedl & Rokitta 1997), and the green trons. Fungal sequences aligned algal sequences available in Genbank to identify primer sites that would algal class Trebouxiophyceae has been described as discriminate against fungal ITS. The algal-specific ITS "sexual unknown" It reproduction (Friedl 1995). primers ITS 1T (gga agg ate att gaa tct ate gt), ITS2T (ttc has been suggested that the fungus suppresses sex- get gcg ttc ttc ate gtt), ITS3T (aac gat gaa gaa cgc age ual reproduction in the phycobiont to prevent it gaa), and ITS4T (ggt tcg ctc gcc get act a) are based on nuclear ribosomal from the from producing novel genotypes that would be less sequences Trebouxiophyceae, including species of and (Bhat- suited to This effect Trebouxia Asterochloris symbiosis (Ahmadjian 1993a). tacharya et al. 1996; Friedl 1995; Friedl & Rokitta 1997; has been demonstrated for the bacterium Wolbachia Friedl & Zeltner 1994). The initial set of heterologous that infects female wasps and in which sexual re- algal-specific actin primers were based on sequences from combination is suppressed, thereby causing the Chlorella vulgaris (Chow & Chan 1997), a member of the (Friedl & Zeltner wasps to reproduce parthenogenetically (Rousset et Trebouxiophyceae 1994),Chlamydomon- as reinhardtii (Sugase et al. 1996) a member of the Chlo- al. be 1992). Although clonality may advantageous rophyceae (Friedl & Zeltner 1994), and several represen- over short periods, clonal lineages are predicted to tative fungal actin sequences. The Trebouxia-specific actin be doomed for extinction (Muller 1964), and no class I primers ACT1T (cac acr gtr ccc ate tay gag g), green alga has been demonstrated to have a clonal ACT2T (agg tag ctc ata gtt ctt ctc aat), and ACT3T (acy att gag aag aac tat gag cta), ACT4T (gtt gaa cag cac ctc population structure. With molecular methods, we agg gca) are based on Trebouxia sequence obtained from no longer need to observe sex directly to negate the the initial primers (Fig. 1). hypothesis of clonality, because we can infer that PCR was performed to bias the reaction toward algal recombination is or is not occurring based on com- amplicons with a TD62 (touchdown) program that con- parison of genotypes. sists of initial two min. treatment at 940C, followed by of 10 cycles of one min. at 94?C, one min.
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