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GALLEY the Southernmost Myco-Heterotrophic Plant, Arachnitis Allen Press x DTPro System GALLEY File # 20em Name /myco/96_520 08/02/2004 03:30PM Plate # 0-Composite pg 1141 # 1 Mycologia, 96(5), 2004, pp. 1141±1149. q 2004 by The Mycological Society of America, Lawrence, KS 66044-8897 The southernmost myco-heterotrophic plant, Arachnitis uni¯ora: root morphology and anatomy Laura S. DomõÂnguez1 niaceae p.p.-incl. Thismiaceae, Corsiaceae, Iridaceae Alicia SeÂrsic p.p., Orchidaceae p.p., Petrosaviaceae, Triuridaceae Instituto Multidisciplinario de BiologõÂa Vegetal -incl. Lacandoniaceae) and four in the Dicots (Gen- (IMBIV), C.C. 495, 5000 CoÂrdoba, Argentina tianaceae p.p. Monotropaceae, Polygalaceae p.p. and Pyrolaceae p.p.), comprising about 88 genera and 400 species (Maas et al 1986, RuÈbsamen 1986, Mab- Abstract: Root morphology and anatomy of the berly 1987, Dressler 1993, Leake 1994, Ibisch et al myco-heterotrophic Arachnitis uni¯ora (Corsiaceae) 1996). Four major types of mycorrhizal associations were studied in relation to their association with a have been described for myco-heterotrophs (after Glomus species (Glomeromycota). The mycorrhizal Leake 1994): arbutoid, monotropoid, orchid, and ar- features were studied in three distinctive stages of de- buscular (AM), whereas the arbutoid mycorrhiza Py- velopment: (i) shoot and ¯ower restricted to a small, rola may be without myco-heterotrophic species (Fur- underground bud; (ii) shoot and ¯ower bud up to nam and Trappe 1971). AM are formed by fungi be- 1.5 cm; and (iii) shoot and ¯ower already withered. longing to Phylum Glomeromycota (SchuÈssler et al The hyphae penetrate through and between the epi- 2001). Arbuscular mycorrhizal infection has been dermal and exodermal cells; the exodermis and out- shown or suggested to occur in species of the Bur- er cortical cells become colonized in an inter- and manniaceae, Corsiaceae, Gentianaceae, Polygalaceae, intracellular manner, with some coils being formed Pyrolaceae and Triuridaceae (van der Pijl 1934, in these layers. The fungi colonize the middle cortex, McLennan 1958, Terashita and Kawakami 1991, where intracellular vesicles in bundles are abundant. Leake 1994, Imhof 1997, Imhof and Weber 1997, Arbuscules are formed profusely at very early stages DomõÂnguez, et al 1998, Imhof 1998a, 1999a, b, c, of development, while in older stages they almost dis- DomõÂnguez and SeÂrsic 2001). Sequence analysis of appear and abundant vesicles are formed. Except for the ITS region recently has con®rmed the association some details, the pattern of root colonization corre- of Gentianaceae, Corsiaceae (Bidartondo et al 2002) sponds to a Paris-type. Presence of storage substances and Triuridaceae (Yamato 2001) with a lineage of (starch and oil) also was recorded. Starch is pro- AM fungi (Glomus). duced and stored within root cells, mainly in the out- Corsiaceae is a small family with three genera (Cor- er and inner root cortex. In senescent stages, plant sia Becc., Corsiopsis D.X. Zahng, R.M.K. Saunders & and fungal tissues collapse. C.M. Hu and Arachnitis Phil.) and 29 species all re- Key words: achlorophyllous plant, arbuscular my- stricted to the Southern Hemisphere. The 26 Corsia corrhiza, Corsiaceae species are native to Australasia, while the monotypic genus Corsiopsis inhabits China (RuÈbsamen 1986, Zhang & Saunders 1999). Arachnitis grows in Bolivia, INTRODUCTION in the Patagonian Nothofagus forests of Argentina Achlorophyllous vascular plants, which are unable to and Chile and in the Falkland Islands (Dimitri 1972, assimilate carbon by themselves and consequently de- Cribb et al 1995, Ibisch et al 1996). This genus is pend on their association with fungi for nourishment monotypic, with only A. uni¯ora Phil. It has been commonly were called ``saprophytic'' plants. This suggested recently that Corsiaceae is probably poly- misleading term, which implies that plants obtain car- phyletic and Arachnitis appears to be related to This- bohydrates directly from decaying organic matter, mia (Thismiaceae) in a larger clade that also includes nowadays is being replaced by the more precise term Burmanniaceae (Neyland and Henningan 2003). ``myco-heterotrophic'' (Leake 1994). Myco-hetero- The mycorrhizal associations of these achlorophyl- trophy has evolved many times and has been record- lous plants are poorly known with respect to their ed in 10 families: six within the Monocots (Burman- morphology, physiology and fungal symbiont. Taxo- nomical and biological studies of myco-heterotrophic Accepted for publication April 6, 2004. plants are dif®cult because they spend most of their 1 Corresponding author. E-mail: [email protected] lives underground, becoming visible only during the 1141 Allen Press x DTPro System GALLEY File # 20em Name /myco/96_520 08/02/2004 03:30PM Plate # 0-Composite pg 1142 # 2 1142 MYCOLOGIA FIGS. 1, 3±5. Plants and roots of Arachnitis uni¯ora. 1. Flowering plants in natural habitat. 2. Different stages of plant development: a. young specimen with turgent root system, shoot and ¯ower restricted to a small bud, b. shoot and ¯ower bud beginning to develop, basal part of the shoot with bracts (arrows), c. fully developed plant at fruit stage, d. senescent plant with dead shoot. 3. Turgent roots of young specimen. 4. Long and tapering root system of a withered plant. 5. Root surface with external hyphae (arrow). Scale bars: 1 5 5 cm; 2±4 5 0.5 cm; 5 5 200 mm. ¯owering and fruiting season. Some are mimetic with acetic acid (100%) : ethanol (96%) : water at 10:5:50:35, as the environment; thus collections of these plants are well as in glutaraldehyde (50%) and buffer pH 6.8 at 24: rare. 100, before being transferred to ethanol (70%) after 24 h In this work, presence and morphology of the my- (O'Brien and McCully 1981). Specimens examined. ARGENTINA. CHUBUT: Departa- corrhizal structures in three different stages of plant mento Lake Cholila, 41854942.10S, 72824924.60W, 7 Jan 1994, life cycle of A. uni¯ora are studied. AAC 525, (CORD). Additional specimens were ®xed at the same locality on 18 Jan 1998. NEUQUEÂN: Departamento 8 9 0 MATERIALS AND METHODS Los Lagos, Villa La Angostura, Laguna Verde, 40 46 37.9 S, 71839931.60W, elevation 813 m, 14±15 Dic 2001, AAC 1406, Plants of A. uni¯ora were collected from dense and shaded (CORD). RIÂO NEGRO: Departamento Bariloche. Road to forests, in loose organic soils, with abundant leaf and wood Llao Llao, Km. 6.5, 4187916.20S, 718 23931.20W. 14±15 Dec litter (FIG. 1). They co-exist with Austrocedrus chilensis 2001, AAC 1406, (CORD). (D.Don) Pic. Serm & Bizzarri and Nothofagus dombeyi In the laboratory, the roots were examined under a ste- (Mirb.) Oerst. trees and Osmorrhiza chilensis Hook & Arn., reomicroscope. Roots of ®ve plants at different stages of Berberis sp., Escallonia sp. as some species of the understory. development were embedded in synthetic resins following Individual plants were excavated and several whole root sys- the manufacturer's instructions (Kulzer Histo-Technique tems were detached for examination (n 5 45), while un- 7100), then cut into 4 mm thick sections (approximately 400 derground buds close to them also were preserved. Above- sections per root) and stained with Cresyl blue (Largent et ground parts of the plants were dried as herbarium speci- al 1977). Different stains also were tested for the fungal mens and the root systems preserved in formalin (40%) : symbiont (cotton blue and trypan blue) (Largent et al Allen Press x DTPro System GALLEY File # 20em Name /myco/96_520 08/02/2004 03:30PM Plate # 0-Composite pg 1143 # 3 DOMIÂNGUEZ AND SEÂRSIC:THE SOUTHERNMOST MYCO-HETEROTROPHIC PLANT 1143 1977). Lugol iodine solution was used to detect starch, and is an uneven row of more or less spherical cells (17± Sudan IV was used to detect oil content (Gerlach 1984). 50 mm diam). Lugol's stained transversal sections Macroscopic photographs were taken with a Leica M 420 showed that epidermal and exodermal cells do not photostereomicroscope. Sections were observed and pho- contain starch. The outer- and innermost cortical re- tographed with a Leitz DM LB photomicroscope. gions are characterized by an accumulation of high amounts of composite starch grains (FIGS. 22±23). In RESULTS the mid cortical parenchyma cells, where a profuse fungal colonization takes place, starch grains are Plant morphology.Ð-Roots of A. uni¯ora grow be- sparse. Oil globules were found inside and outside tween the mineral and organic soil horizons at the fungal hyphae, especially in the early stages of depths of ca 10±15 cm. The root system consists of a root development (FIG. 24). star-like conglomeration of (6)10(17) (n 5 5) tuber- ous roots (FIGS. 2±4); each root is about 5±10 mm The endophyte. Infection and development.ÐThe exter- 3 long 3±4 mm wide. No side roots or hairs were nally attached mycelium (FIG. 5) is characterized by observed. Root sprouts are found rarely. Fully devel- aseptate (a septum was seen only once), irregularly oped roots are bluntly tapering (FIG. 3). Root for- shaped, up to 1 mm thick-walled and rami®ed hyphae mation precedes shoot development. Once a clump (5±12 mm diam). No root-to-root attachments with of roots has developed completely, a shoot bud is neighboring plants were seen. The root surface does formed (FIG. 2a). The stem may grow from 6 cm up not show any particular coloration around the points to 40 cm, depending on plant populations, and pro- of hyphal penetration. duces a single zygomorphic ¯ower (FIG. 1, 2c). The Three distinctive stages of development were stud- shoot base is covered by 4±5 translucent bracts (FIG. ied: (i) shoot and ¯ower restricted to a small under- 2d). Stem and ¯ower are variable in color, being whit- ground bud (FIG. 2a); (ii) shoot and ¯ower bud be- ish, yellowish or purple. No odor was detected. The ginning to develop (FIG.
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