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Regional Specialization of Sarcodes Sanguinea Regional Specialization of Sarcodes sanguinea (Ericaceae) on a Single Fungal Symbiont from the Rhizopogon ellenae (Rhizopogonaceae) Species Complex Author(s): Annette M. Kretzer, Martin I. Bidartondo, Lisa C. Grubisha, Joseph W. Spatafora, Timothy M. Szaro and Thomas D. Bruns Source: American Journal of Botany, Vol. 87, No. 12 (Dec., 2000), pp. 1778-1782 Published by: Botanical Society of America, Inc. Stable URL: http://www.jstor.org/stable/2656828 Accessed: 12-12-2015 01:10 UTC Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at http://www.jstor.org/page/ info/about/policies/terms.jsp 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]. Botanical Society of America, Inc. is collaborating with JSTOR to digitize, preserve and extend access to American Journal of Botany. http://www.jstor.org This content downloaded from 160.36.178.25 on Sat, 12 Dec 2015 01:10:22 UTC All use subject to JSTOR Terms and Conditions AmericanJournal of Botany87(12): 1778-1782. 2000. REGIONAL SPECIALIZATION OF SARCODES SANGUINEA (ERICACEAE) ON A SINGLE FUNGAL SYMBIONT FROM THE RHIZOPOGON ELLENAE (RHIZOPOGONACEAE) SPECIES COMPLEX' ANNETTE M. KRETZER,2'5'6 MARTIN I. BIDARTONDO,3'5 LISA C. GRUBISHA,4 JOSEPH W. SPATAFORA,2 TIMOTHY M. SZARO,4 AND THOMAS D. BRUNS4 2OregonState University, Department of Botanyand PlantPathology, 2082 CordleyHall, Corvallis,Oregon 97331-2902 USA; 3Universityof Californiaat Berkeley,Department of EnvironmentalScience, Policy and Management,111 KoshlandHall, Berkeley,California 94720-3102 USA; and 4Universityof Californiaat Berkeley,Department of Plantand MicrobialBiology, 111 KoshlandHall, Berkeley,California 94720-3102 USA We have sampledthe mycorrhizalroots of 76 snow plants(Sarcodes san?guinea,Monotropoideae, Ericaceae) in two areas of the SierraNevada of Californiathat are - 180 km apart.To identifythe fungal symbionts associated with these plants, we firstanalyzed restrictionfragment length polymorphisms (RFLPs) of the internaltranscribed spacer region (ITS) of the fungalnuclear ribosomal repeat.Fungal ITS-RFLPs were successfullyproduced from 57 of the 76 plantssampled, and all symbiontsshared the same DNA fragmentpattern. The morphologyof S. sanguineamycorrhizae was consistentwith that expected from a Rhizopogonspecies in section Amnylopogon.To confirmand refinethis identification, a total of six fungalITS sequenceswere determined from S. sanguineamy- corrhizae.These sequenceswere analyzedtogether with eight existing and eightnewly determined ITS sequencesfrom Rhizopogon sectionAnmylopogon. The newlydetermined sequences include an ITS sequencefrom the fungal symbiont of pine drops(Pterospora andromedea,Monotropoideae, Ericaceae), a plantthat was previouslyreported to be exclusivelyassociated with the Rhizopogon subcaerulescensgroup. When these sequences were analyzed together, the Sarcodes symbionts grouped tightly with several collections of R. ellenae includingthe holotype,one collectionof R. idahoensis,and one collectionof R. semireticulatus.A differentlineage comprised collections of R. subgelatinosus, R. subcaerulescens, anothercollection of R. semireticulatus, and the Pterospora symbiont. We concludethat S. sanguineaassociates exclusively with a singlespecies in theR. ellenae speciescomplex throughout our sampling range.These resultsindicate a muchhigher level of specificityin S. sanguineathan was previouslyreported and confirmthe emerging patternthat nonphotosynthetic, monotropoid plants generally associate very specifically with a narrowrange of ectomycorrhizalfungi. Key words: monotropoidmycorrhizae; Pterospora andromedea; Rhizopogon; Sarcodes san?guinea; specificity(host). The snow plant,Sarcodes sanguinea,is the onlymember thatemerged from these studies was thatin contrastto pho- of a monospecificgenus in the Monotropoideae(Ericaceae) tosyntheticmycorrhizal plants, which typically associate with and occursthroughout the Sierra Nevada of Californiaas well largenumbers of distantlyrelated fungi, most monotropes ap- as in southernOregon, western Nevada, and northernMexico pear to associatewith specific groups of closelyrelated ecto- (Wallace,1975). Like othermembers of theMonotropoideae, mycorrhizalfungi: Monotropa uniflora was foundassociated it is nonphotosyntheticand mustreceive all of itscarbon from withtaxa in the Russulaceae,while Pterospora andromedea fungalroot symbionts. The rootsof S. sanguineaare coralloid, was foundonly in symbiosiswith the Rhizopogon subcaeru- fleshy,and surroundedby a fungalmantle except for the tips, lescensspecies group.Recently, Lefevre, Carter, and Molina which are uncolonized.Although the importanceof fungal (1998) foundAllotropa virgata to be specificallyassociated root symbiontsfor the nutritionof monotropoidplants has with Tricholomamagnivelare. This patternof specificityis been recognizedfor a long time (e.g., Kamienski,1881; also observedin nonphotosyntheticorchids (Taylor and Bruns, Francke,1934), the fungi involved are just startingto be iden- 1997), and so it appearsthat specific fungal associations are tifiedthrough the use ofmolecular techniques. Cullings, Szaro, thenorm in nonphotosyntheticmycorrhizal plants. and Bruns(1996) sampledseveral monotropoid taxa mostly in Sarcodessanguinea so farappeared to be theonly exception the westernUnited States and used partialsequence analysis to thispattern. Cullings, Szaro, and Bruns(1996) reportedthat as well as oligonucleotideprobing of themitochondrial large it associatedwith at least threedistantly related lineages of 12 indi- subunitrDNA to identifythe fungalsymbionts. The picture fungiwithin the Hymenomycetes. Furthermore, only vidual plantswere sampled;thus the diversityof associates could have been underestimated.None of thesymbionts of S. Manuscriptreceived 24 August1999; revision accepted 17 February2000. sanguineawas identifiedto species level, and only one fell The authorsthank Jim Trappe and his groupfor help in collectingand identifyinghypogeous fungi in the SierraNational Forest, and the Harry withina lineageknown to be ectomycorrhizalat the timeof ThiersHerbarium at San FranciscoState University for collection loans. The publication.For thesereasons we decidedto investigatethe studywas supportedin partby USDA ForestBiology competitive grant num- mycorrhizalassociates of S. sanguineamore closely. ber 9600479 and in partby cooperativeagreement number PSW-94-0023CA MATERIALS AND METHODS withthe USDA ForestService. 5 These authorshave contributedequally to thisstudy. Sampling-Rootballsof S. sanguineawere sampled by digginga hole next 6 Authorfor reprint requests. to a floweringplant and by carefullyfollowing the inflorescence to locatethe 1778 This content downloaded from 160.36.178.25 on Sat, 12 Dec 2015 01:10:22 UTC All use subject to JSTOR Terms and Conditions December 2000] KRETZER ET AL.-HOST SPECIFICITY IN SARCODES 1779 TABLE 1. Sarcodes sanguinea rootballssampled. No. pop- No. No. symbionts Location Year ulations plants identified Shaver Lake Area "high-density"sited 1995 1 15 15a LakeTahoe 1997 11 9b Basin along McKinley grove roade 1996 3 13 9a along roads no. 168 and 801 1996 6 15 13a near the USFS Dinkey Creek 1997 1 1 lb Shaver Lake work station indicatecountieswhereSarcdesang Area Lake Tahoe Basin 1997 6 21 bOa (+lc) Total 17 76 58 (76%) a Identifiedby RFLP analysis afterdirect amplification of the fungal ITS region fromS. sanguinea roots. b Identifiedby RFLP analysis of fungalcultures derived from S. san- guinea roots. c One symbiontfrom the Lake Tahoe populationswas identifieddi- % rectlyby sequencing of the fungalITS region withoutRFLP analysis. SAW~~~~~~~~~~~~~...''..... .K d This site is located at 119007'50" W and 37009'06" N. The spatial distributionof Abies magnificaectomycorrhizae around S. sanguinea rootballs has also been studied at this site and is being reportedin an accompanyingpaper. e Between Dinkey Creek and McKinley Grove. fBetween Shaver Lake and HuntingtonLake, and betweenHunting- ton Lake and Mono Hot Springs. rootball;small pieces of rootswere removed, rinsed in watel;and eitherused forculturing or lyophilizedfor molecular analysis. In the springof 1995, 1996, and 1997, we sampleda totalof 64 S. san- GibcoBRL, GrandIsland, New York,and 2% NuSieve agarosefrom FMC guinearootballs for direct identification ofthe fungal symbiont based on poly- BioProducts,Rockland, Maine, USA) and visualizedwith ethidium bromide. merasechain reaction (PCR) withfungus-specific primers. The plantsorigi- PCR were for a PCR natedfrom 16 populationsin two areas of the SierraNevada of Califomia products prepared sequencing using QlAquick puri- ficationkit (QIAGEN, Valencia,California, USA). Nucleotide were (Table 1, Fig. 1). Plantssampled within a populationwere 5-100 m apart, sequences determined the reactiontermination method fluorescencela- and populationswere 5-180 kmapart. Twelve additional plants were sampled by cyclic using beled reactionsand the in thespring of 1997 at the "high-densitysite" and at one othersite (Table dideoxyribonucleotidetriphosphates. Sequencing pro- were instructionsfor the 1) forcultivation of thefungal symbiont from S. sanguinearoots (and sub- cessingof reactionproducts performedfollowing sequentidentification of thecultured mycelium). ABI
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