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The Relationship of Endophytic Fungi to the Gametophyte of the Fern Schizaea Pusilla

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The Relationship of Endophytic Fungi to the Gametophyte of the Fern Schizaea Pusilla The Relationship of Endophytic Fungi to the Gametophyte of the Fern Schizaea pusilla Lucinda J. Swatzell; Martha J. Powell; John Z. Kiss International Journal of Plant Sciences, Vol. 157, No. 1. (Jan., 1996), pp. 53-62. Stable URL: http://links.jstor.org/sici?sici=1058-5893%28199601%29157%3A1%3C53%3ATROEFT%3E2.0.CO%3B2-0 International Journal of Plant Sciences is currently published by The University of Chicago Press. Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/about/terms.html. 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/journals/ucpress.html. 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. The JSTOR Archive is a trusted digital repository providing for long-term preservation and access to leading academic journals and scholarly literature from around the world. The Archive is supported by libraries, scholarly societies, publishers, and foundations. It is an initiative of JSTOR, a not-for-profit organization with a mission to help the scholarly community take advantage of advances in technology. For more information regarding JSTOR, please contact [email protected]. http://www.jstor.org Sun Mar 2 20:08:26 2008 Int. J. Plant Sci. 157(1):53-62. 1996. O 1996 by The University of Chicago. All rights reserved. 1058-5893/96/5701-0007$02.00 THE RELATIONSHIP OF ENDOPHYTIC FUNGI TO THE GAMETOPHYTE OF THE FERN SCHIZAEA PUSILLA LUCINDA J. SWATZELL,' MARTHA J. POWELL,2 AND JOHN Z. KISS Department of Botany, Miami University, Oxford, Ohio 45056 Schizaea pusilla is a rare and threatened fern restricted in North America to acidic bogs of Nova Scotia, Newfound- land, and New Jersey. The gametophyte lives in close association with two endophytic fungi. To characterize the nature of this fern's relationship with these fungi, we introduced axenic gametophytes to bog soil for colonization. Following colonization, the endophytic fungi were isolated and reintroduced to axenic gametophytes. The gametophytes introduced to bog soil were colonized by an aseptate fungus that formed vesicles and arbuscules within the gametophyte. However, culture of colonized gametophytes produced two fungal isolates: an aseptate fungus (fungus B) and a septate fungus (fungus A). Upon reintroduction of fungal isolates to axenically grown gametophytes, the aseptate fungus demonstrated a positive growth response to the presence of the gametophytes and colonized the gametophytes without harm to the host. The septate fungus did not exhibit any specific recognition but contacted the gametophytes randomly, leaving a large percentage of the host nonviable. We propose that the relationship of the septate fungus to the gametophyte of S. pusilla is nonmycorrhizal while the relationship of the aseptate fungus to the gametophyte is mycorrhizal. Further- more, based on lack of nutrient availability in local soils, formation of specialized structures in the gametophyte for harboring fungi, and dependence of the fern on fungal presence for completion of its life cycle, we propose that S. pusilla maintains an obligatory relationship with the aseptate mycorrhizal fungus. Introduction direction as their initial cells in the spore (von Aderkas and Raghavan 1985). The rhizoid, however, rapidly Symbioses between fungi and lower vascular plants turns toward the substrate (Britton and Taylor 1901) are common and range from obligatory in the Psilo- and the apical protonemal cell orients in a negatively phyta to facultative in leptosporangiate ferns (Boullard phototropic direction by the three- to four-cell stage of 1979). Among leptosporangiate ferns, sporophytes gametophyte development (Kiss 1994). (compared to gametophytes) are more commonly found Gametophytes develop rhizoidophores (fig. I), in association with mycorrhizal fungi (Boullard 1979; which are large, highly vacuolate, specialized struc- Bonfante-Fasolo 1984). However, continuous relation- tures that begin as single spherical cells on the fila- ships between fungal symbionts and ferns throughout mentous gametophyte (von Aderkas and Raghavan both phases have been reported in Schizaeaceae, Glei- 1985). Rhizoidophores develop two to three rhizoids, cheniaceae, and Hymenophyllaceae (Boullard 1979). Of divide longitudinally, and form receptacles for an en- the schizaeaceous ferns, gametophytes of Actinostachys dophytic and purported symbiotic fungus (Britton and spp. (Bierhorst 1968, 1975), Lygodium (Warrington Taylor 1901). Upon colonization by the fungus, rhi- 1972), Schizaea jistulosa, Schizaea melanesica, Schi- zoidophores fill with fungal elements. The rhizoids zaea dichotoma (Bierhorst 1966, 1967, 1968), Schizaea collapse and the purported symbiont is presumed to robusta, Schizaea rupestris (Bierhorst 1971), and Schi- function in absorption of water and nutrients (Britton zaea pusilla (Britton and Taylor 1901) all associate with and Taylor 1901). Britton and Taylor (1901) observed fungal symbionts. Of these Schizaea species, S. mela- structures resembling vesicles in colonized rhizoido- nesica and S. pusilla exhibit continuous relationships phores and noted the continuance of colonization with their endophytic fungi throughout both the game- throughout the gametophyte and sporophyte stages. In tophyte and sporophyte phases instead of facultative re- addition, these workers recorded the presence of a sec- lationships only in the sporophyte stage. Of particular ond endophyte in the gametophytes. 1n their paper, one interest in this article is the gametophyte of S. pusilla endophytic fungus is recorded and illustrated as asep- and its fungal associations. tate and the other fungus is illustrated as septate. How- Schizaea pusilla is a rare and threatened fern re- ever, these endophytes remain unidentified and un- stricted in North America to acidic bogs of New Jer- characterized to a further degree. In addition, it is not sey, Nova Scotia, and Newfoundland (Montgomery known which endophyte bears the vesicle-like struc- and Fairbrothers 1992). The life cycle of S. pusilla is tures, and the function of these structures is unclear. described in detail by Britton and Taylor (1901). Schi- To further characterize the endophytic fungi of S. zaea pusilla is one of the few ferns that maintains a pusilla and to elucidate the nature of their relationship completely filamentous and uniseriate gametophyte to this fern, we examined the endophytes within col- throughout its development (Kiss et al. 1995). In S. onized gametophytes and in isolated cultures. pusilla, following germination of the spore, the first protonemal and rhizoidal cells are oriented in the same Material and methods 'Author for correspondence and reprints. Fax: 513-529-4243. 2Present address: Department of Biology, James Madison Univer- Spores, gametophytes, and sporophytes of Schizaea pus- sity, Harrisonburg, Virginia 22807. illa and soil samples were collected from Webb's Mill Bog, Manuscript received May 1995; revised manuscript received August Ocean County, New Jersey, in September 1993, July 1994, 1995. and September 1994. 54 INTERNATIONAL JOURNAL OF PLANT SCIENCES .. - Petri dish . ,--= ../ - axenic * gametophytes sterile filter paper /-\ Petri dish with bog soil Fi. 2 Bog soil culture used in colonization experiments. Bog soil samples approximately 7-8 cm deep were separated into distinct soil layers. The bottom layer, which had a high sand content, was placed into the bottom of a petri dish (diameter = 9 cm). A middle layer with a high clay and organic content was then removed from the samples, homogenized into a paste, and packed into petri dishes Fig. 1 Field-collected gametophyte viewed with stereomicroscope. Subterranean filament cells are typically etiolated or devoid of con- above the sandy layer. The top layer of the samples, which was tents (SbF). Branches of filament cells beneath the substrate produce largely organic material, also was homogenized and placed in the rhizoidophores (Rp), from which two to three rhizoids (Rh) develop. petri dishes above the two previous layers and gently packed. A Rhizoids are often surrounded by brown masses of fungal hyphae (H). sterilized #I Whatman filter paper disk was placed directly above Branches of filament cells growing above the substrate (SrF) are the soil surface, and axenically grown gametophytes were washed with sterilized distilled H,O onto the filter paper. Bog soil cultures bright green and filled with chloroplasts. Solid line = approximate were sealed with Parafilm to avoid desiccation. soil level. Bar = 1.0 mm. growth were excised and placed on new medium) were made on resultant fungal growth. Tip cultures and the resultant COLONIZATION.Spores were surface sterilized with 0.4% fungal isolates were maintained on cornmeal agar with the (vlv) sodium hypochlorite for 20 min and cultured axenically above antibiotics (pH 4.5) under continuous illumination of on a modified Knop's medium (pH 4.5) with 1.2% (wlv) 2.2 hmol m-2 s-I at 21°C. Subcultures of fungal isolates were sucrose and 1.2% (wlv) agar (Guiragossian and Koning established on Sabouraud Dextrose Agar
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