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Mycologia, 94(5), 2002, pp. 850-855.
© 2002 by The Mycological Society of America

Development of Acaulospora rehmii spore and hyphal swellings under root-organ culture


Yolande Dalpé 1

     Eastern Cereal and Oilseed Research Centre, Research Branch, Agriculture and Agri-Food Canada, Ottawa K1A OC6, Canada

Stéphane Declerck

     Université Catholique de Louvain, Mycothèque de l'Université Catholique de Louvain (MUCL 2), Unité de microbiologie, 3 Place Croix du Sud, 1348 Louvain-la-Neuve, Belgium

   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 

A strain of Acaulospora rehmii was, for the first time, successfully grown in vitro on Ri T-DNA transformed carrot roots allowing the in situ observation of Acaulospora spore development and of extraradical thin-walled hyphal swellings. The sporogenous hypha developed intercalarly along thin-walled coenocytic hyphae. The distal part of the sporogenous hypha swelled slightly as a sporiferous saccule primordium followed by the differentiation of a lateral spore primordium along the neck of the sporogenous hypha. Both structures matured simultaneously, and the sporiferous saccule began to collapse after spore maturation and complete differentiation of the spore wall. Several of the in situ observations on in vitro differentiated A. rehmii spores are concordant with previous ontogenic studies done on other Acaulospora species obtained from in vivo cultures. New and original observations on the early developmental stages of sporiferous saccules and spores and on the occurrence of small diameter intercalary hyphal swellings provide additional elements in the study of Acaulospora sporulation process and life cycle.

Key words: Acaulosporaceae, Glomerales, hyphal swellings, spore ontogenesis


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
The differentiation of Acaulospora spores is known to occur laterally along a sporogenous hypha at the neck of a fully inflated sporiferous saccule (Wu et al 1995Citation, Stürmer and Morton 1999Citation). At spore maturity, sporiferous saccules collapse, leaving empty shrunken saccules. The sporulation process of A. rehmii Sieverding & Toro as described by Sieverding and Toro (1987)Citation followed similar developmental stages. In their 1984 original description of A. appendicula Spain, Sieverding & Schenck, Schenck et al (1984)Citation described and illustrated, in addition to Acaulospora- type spores, two other fungal structures: a Glomus morphotype and a "vesicle-like" structure. Quite recently, A. appendicula has been put into synonymy with A. gerdemanii Schenck & Nicolson, with Glomus leptotichum Schenck & Smith (=G. fecundisporum Schenck & Smith) as a synanamorph (Morton et al 1997Citation). In the G. leptotichum synanamorph description, small diameter, thin-walled "vesicle-like" structures were mentioned to occur on hyphal branches that subtended glomoid spores. Based on molecular and subcellular characters, the dimorphic species A. gerdemanii-G. leptotichum was recently transferred to the family Archaeosporaceae as Archaeospora leptoticha (Schenck & Smith) Morton & Redecker (Morton and Redecker 2001Citation). Consequently, none of the remaining Acaulospora species were known to differentiate extraradical "vesicle-like" structures.

With arbuscular mycorrhizal (AM) fungi grown monoxenically on root-organ culture, continuous in situ observations of fungal colonies, mycelium organization, and sporulation steps can be followed non-destructively. Using this technology, original data on mycelium development (St-Arnaud et al 1996Citation, Bago et al 1998Citation), sporulation dynamics (Declerck et al 2000Citation, 2001Citation), and spore ontogeny (De Souza and Berbara 1999Citation, Pawlowska et al 1999Citation) have greatly improved our former understanding of AM fungi propagation processes and life cycles (Chabot et al 1992Citation, Strullu et al 1997Citation). Up to now, several Glomaceae and a few Gigasporaceae have been successfully cultivated in vitro on root-organ culture and are maintained in international culture collections (Declerck and Dalpé 2001Citation). Acaulospora rehmii Sieverding and Toro is the first Acaulosporaceae representative to have been successfully cultivated in vitro. The present study reports and illustrates in situ observations of A. rehmii sporiferous saccules, spores, and hyphal swellings developmental stages as observed on colonies grown monoxenically with Ri T-DNA transformed carrot roots cultures (Bécard and Piché 1992Citation).


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Fungal isolate – A strain of Acaulospora rehmii (MUCL 43145; DAOM 229384) was isolated from rhizospheric soil of banana (AAB French plantain cv. Obino l'Ewai) in Cameroon. Bulk cultures were established on leek (Allium porrum L. var. Bleu de Solaise) plants grown on Terra green (Agsorb® 8/16 LVM-GA, Chicago, Illinois, USA) in a greenhouse (24/20 C day/night, with natural light). Plants were fertilized at regular intervals with Long Ashton solution (Hewitt 1966Citation) and rain water was applied every 2–3 d. After 6 mo culture, spores were gently extracted by wet sieving and used to establish new trap pot cultures on leek under the same growth conditions. After another 6 mo culture, spores were re-isolated by wet sieving and prepared for monoxenic culture.

Root-organ culture – Spores were transferred to the upper part of a sterilized (121 C for 15 min) 45 µm filter (Gelman Science, Michigan, USA) holder apparatus (VEL, Leuven, B) for surface sterilization. Spores were twice disinfected for 10 min in 2% chloramine T with 1–2 added drops of Tween 20, followed by a 10 min bath in an antibiotic solution (streptomycin 200 mg L-1 and gentamycine 100 mg L-1). The two disinfection steps were followed by triple rinsing with sterile (121 C for 15 min) de-ionized water. Surface disinfected spores were transferred to Petri plates (90-mm diam) containing a Strullu and Romand (1986)Citation (MSR) medium modified by Declerck et al (1998)Citation, solidified with 4 g L-1 Gel GroTM (ICN Biomedicals, Inc, Irvine, California, USA) and incubated in the dark at 27 C. Following germination, a plug of gel supporting a germinated spore was transferred with a 9-mm cork borer into the experimental Petri plate. An identical slice of agar had just been removed from the experimental plate so that the spore on the agar plug could be slid into the hole. An actively growing transformed carrot (Daucus carota L.) root (70 mm long) was placed in the vicinity of the spore. Petri plates were incubated in an inverted position in the dark at 27 C.

Microscopic observations – The development of fungal colonies and the differentiation of hyphal swellings, sporiferous saccules, and spores were followed for a 6 mo period. The rates of hyphal elongation and of cytoplasmic flow were estimated directly on Petri plates colonies under a Nikon SMZ-U dissecting microscope at 30 to 50x magnification. Hyphal apices or a group of well contrasted cytoplasmic granules were aligned to a precise micrometer position. The distance crossed by the chosen element was evaluated every 15 min for at least a 2 h period and the results extrapolated as µm h-1 growing speed. Terminology used to describe mycelium development are based on Bago et al (1998)Citation description of AM fungi in vitro development. Microscopic slides of hyphae, hyphal swellings and spores were mounted in Polyvinyl-lactic acid-glycerol media (PVLG) (Omar et al 1979Citation) and observations made under bright-field, differential interference contrast (DIC), and autofluorescence microscopy (Exciter filter 365 nm, Barrier filter, 420) respectively with Nikon Optiphot and Eclipse-800 compound microscopes. Photographs were taken using a Nikon CoolPix950 digital camera.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Spore germination – The first germinating spores were observed 15 d after incubation and others germinated during the 4–5 wk thereafter. Multiple germinations occurred in some of the spores giving rise to thin stunted hyphae which started to proliferate profusely when transferred in the vicinity of the host root. Several contact points with excised roots were observed within a few days after co-cultivation.

Mycelium and hyphal swellings (HS) development – Runner hyphae were coenocytic, hyaline, straight, 6.2–7.0 µm in diam, with 0.8–1.0 µm thick walls. They spread on the culture medium surface at a mean speed rate of 58 µm h-1 (35–82 µm h-1) and branched regularly, at acute angles, into thinner secondary and tertiary branches (2.5–6.0 µm diam) (Fig. 1). Hypha diameter decreased proportionally with each branching level and flowing cytoplasm was observed in hyphae as thin as 2.5 µm in diam. Even though mycelium spread over all the gel-Gro surface, the hyphal network remained sparse. Branched absorbing structures (BAS) (Bago et al 1998Citation) were observed along runner and branched hyphae. Several hyphae penetrated root tissue and sparse arbuscules formed inside roots, but no vesicles were detected. During mycelium spread and after root contact, intercalary small diameter, thin walled hyphal swellings (HS) developed along both runner and branched hyphae (Figs. 1–3). Intercalary hyphal swellings were hyaline, globose to ovoid, 20–35 µm in diam surrounded by a single wall slightly thickened (1.2–1.4 (–2.4) µm) compared to the hyphal wall from which they originated (Figs. 2–3). With time, the cytoplasm contained in the distal side of HS flowed backwards to the swelling leaving an empty, septate, distal hypha that collapsed (Fig. 2). Hyphal swellings remained unchanged for the life of the colony and within a single colony, their number remained consistently higher, by about ten times, than the number of differentiated Acaulospora spores, yet all the sporiferous saccules observed gave rise to fully developed spores. No physical relationship between HS and spores has ever been detected, both structures always occurred on different "mother" hyphae.



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  		 FIGS. 1–7. Acaulospora rehmii. 1. General view of intercalary hyphal swellings along branched hyphae. 2. Closer view of an intercalary hyphal swelling with a septum closing the distal hypha. 3. Row of three hyphal swellings along hypha with thickened walls. 4. Intercalary fusiform inflated sporogenous hypha (SH) containing granular cytoplasm. 5. Sporogenous hypha (SH) inflating into a claviform sporiferous saccule primordium (SSP). 6. Side view of a sporogenous hypha (SH) bearing a spore primordia (SP) with a fine branch tortuous hypha (BH) adjacent to the SP. 7. Oblique view of a spore primordium (SP) at the neck of the sporiferous saccule primordium (SSP). Scale bars: 1 = 120 µm; 2 = 10 µm; 3 = 60 µm; 4–7 = 30 µm

 
Sporiferous saccule primordium development – The early stages of sporogenous hypha (SH) differentiation occurred either along runner or secondary branch hyphae. Cytoplasm first increased in density within a 120–230 µm long somewhat inflated hyphal region (Fig. 4) and autofluoresced under U.V. light. In 5 to 10 d, the condensed cytoplasm became granular in appearance. The SH apex inflated into a fusiform to claviform shape (Figs. 4–5) that was referred to as sporiferous saccule primordium (SSP). The single wall of the SSP thickened from 1.0–1.2 µm up to 1.6–1.9 µm. Cytoplasm from both distal and proximal hyphal attachments flowed into the sporogenous structure at a rate of 30–42 µm h-1. Septa were gradually differentiated along the distal hyphal attachment, leaving an empty filament which usually remained attached to the SSP until spore expansion was terminated. At spore primordium differentiation, the SSP may remain fusiform to claviform (Fig. 6) or slightly swollen into a globose structure, up to 24–30 µm in diam (Fig. 7).

Spore development – Concurrently with early SSP differentiation, a protuberance (7–10 µm in diameter), densely filled with cytoplasmic material developed laterally along the SH (Figs. 6, 7). Such lateral protuberances were considered spore primordia (SP). During the first 7 to 10 d after occurrence, SP inflated and reached up to 30 µm in diameter. Fine branch hyphae (BH), straight or tortuous, developed along the sporogenous hyphae, adjacent to the SP (Fig. 6). Septa never were detected along the sporogenous hypha. Both the sporiferous saccule and spore expanded simultaneously and no cytoplasmic movement from the saccule to the spore was detectable. At maximum spore expansion, the SH was elongated and funnel shaped, with diam increasing from 4–6 µm at the proximal hyphae level to 18–25 µm near the sporiferous saccules (SS) (Fig. 8). Sporiferous saccule (SS) reached a maximum of 115–152 µm in diam, concurrently with spore maximum size, after which the SS collapse (Fig. 9). At full differentiation, spores were globose, pale yellow to yellow, 112–162 µm diam, typically ornamented (Fig. 10), sessile on the subtending hypha, autofluorescent under UV light (Fig. 9), and the opening was 2.9–3.4 µm wide (Fig. 11). Spore wall was up to 9.5 µm thick, consisting of an external hyaline layer (L1) common with the SH wall, and remaining intact all through the differentiation process (Fig. 11), a laminate layer up to 7.5 µm thick including ornamentations (L2), and a third membrane-like layer (L3). Flexible inner walls (iw1 and iw2) were detectable only on spores bearing a collapsed sporiferous saccule (Fig. 11). Stages of spore wall differentiation were comparable to those described for A. laevis and A. spinosa (Stürmer and Morton 1999Citation). No orb and no spore germination were observed in any of the in vitro differentiated spores.



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  		 FIGS. 8–11. Acaulospora rehmii. 8. Well developed sporiferous saccule (SS) and spore with denser cytoplasm inside spore and adjacent portion of sporogenous hypha (SH). 9. Ultra-violet autofluorescence of a crushed mature spore still attached to a shrivelled sporiferous saccule (SS). 10. Surface ornamentation of a mature spore showing typical labyrinthiform ridges. 11. Close view of spore wall layers of a mature spore still attached to its sporiferous saccule (SS). Note the three outer walls (L1, L2, L3) and the two inner walls (iw1, iw2). Scale bars: 8, 9 = 60 µm; 10 = 10 µm; 11 = 25 µm

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
The in vitro monoxenic propagation of A. rehmii extended the range of genera that are, up to now, cultivated on root-organ culture (Fortin et al 2002) and suggests that additional species from the genera Scutellospora, Entrophospora, Archaeospora, and Paraglomus may be successfully propagated in vitro. With in vitro cultures, non-destructive observations of fungal colonies permits in situ recording of developmental stages. Comparisons between in vivo (pot) and in vitro (root-organ) cultures help to differentiate traits dependant on environmental growth constraints from functional and evolutionary ones. Differences between those two growing modalities are that the first reflects conditions (whole plant partner), close to natural ones, with substrate, edaphic, and contamination constraints, whereas the other is artificial, with physiological constraints due to the absence of the whole plant, but with constant substrate composition, and no surrounding contamination. The characters observed from in vitro culture of Acaulospora rehmii did not vary significantly from those observed in pot cultures (Sieverding and Toro 1987Citation, Stürmer and Morton 1999Citation), but gave additional information on the proliferation of HS and on the sporiferous saccule developmental sequences.

Hyphal swelling development – The first structures to be differentiated after A. rehmii established contact with excised roots were hyphal swellings. Their abundance in the gel-Gro medium was interpreted to be a fungal response to a functional symbiotic association. These thin-walled globose structures closely resembled juvenile spores of Glomus. During the 6 mo growing period of observations, none of them reached diameter greater than 35 µm and none matured as glomoid spores.

Structures similar to HS have been regularly observed either from in vivo or in vitro cultures. Hyphal swelling structures extracted from in vivo cultures have been referred to as "juvenile spores" of Glomus globiferum Koske and Walker (Wu and Sylvia 1993Citation). "Thin-walled inflated structures" were described from the periphery of Sclerocystis coremioides Berk. & Broome sporocarps (Wu 1993Citation). "Vesicles" were also observed on branched subtending hyphae of the glomoid spores of A. leptoticha synanamorph (Morton et al 1997Citation). However, in contrast to A. rehmii HS which remained single-walled, A. leptoticha "vesicles" were surrounded by a double wall, and as such were quite similar to the G. leptotichum synanamorph spores. Several in vitro cultures of Glomus species strains differentiated HS. With G. intraradices Schenck & Smith (Chabot et al 1992Citation) and G. clarum Nicol. & Schenck (DeSouza and Berbara 1999Citation), HS expanded into mature spores. However, with G. mosseae (Nicol. & Gerd.) Gerd. & Trappe, the in vitro differentiated HS remained unchanged over all colony expansion (Mosse and Hepper 1975Citation, Douds 1997Citation). These so called "vegetative spores" were attributed survival and propagation potential at the same level as mature spores. When species with large-size, pigmented spores were grown in in vitro culture (e.g., G. monosporum, G. caledonium, Dalpé & Declerck unpubl) both HS and specific glomoid spores were differentiated simultaneously on the same hyphae, similar to what has been observed with G. leptotichum synanamorph (Morton et al 1997Citation). As HS were observed mainly occuring with large-size spore species, growing either under in vitro and in vivo conditions, their differentiation may be interpreted as a pre-sporulation step. The HS may play the role of a transitory stage of colony development potentially insuring energy storage to support further sporulation, such as the role attributed to auxiliary cells of Gigasporaceae (Pearson and Schweiger 1993Citation). The HS may also be considered as immature glomoid spores; their occurrence and abundance in in vitro cultures together with mature acaulosporoid spores suggest a failure of the fungal-root thallus to support their complete maturation. Successful in vitro cultivation of additional Acaulospora species would help determine whether all Acaulospora species form HS.

Spore development – From the vegetative hypha to the mature spore, four stages of differentiation were observed: (1) intercalary differentiation of a sporogenous hypha, (2) spore primordium budding along the sporogenous hypha, (3) simultaneous swelling of sporiferous saccule and spore, and finally, (4) sporiferous saccule shriveling at spore maturity. Mature spores of A. rehmii differentiated under in vitro conditions did not differ morphologically from pot-culture extracted ones, and spore wall maturation followed the same stages of development as described for A. laevis Gerd. & Trappe and A. spinosa Walker & Trappe (Stürmer and Morton 1999Citation). Contrary to the observations of Wu et al (1995)Citation on Entrophospora kentinensis Wu & Liu spore ontogenesis, the sporogenous hypha of A. rehmii was never closed by a septum. Only the dense granular cytoplasm accumulated at the sporogenous hypha and saccule delimited the spore complex borders. Mature spores maintained their turgor and never showed any sign of plasmolysis. This may explain why no germination orb was observed on mature spores, as this structure seems to become detectable only at spore senescence (Spain 1992Citation, Stürmer and Morton 1999Citation).

The simultaneous swelling of sporiferous saccule and spore as well as the absence of detectable cytoplasmic movement from the saccule to the spore during maturation does not provide many clues for determining the function of the saccule in spore development. One hypothesis is that the initiation of spore primordia may require a certain concentration of cytoplasmic material and that the sporiferous saccule would play the role of a cytoplasmic reservoir. The variety of morphologies adopted by the sporogenous hypha and the sporiferous saccule during expansion can be attributed to the plasticity of these thin-walled structures, plasticity which is enhanced by the lack of physical constraints imposed by the gel media compared to the more compacted solid root substrate of pot culture. The in vitro cultivation of A. morrowae Spain & Schenck, (Wu unpubl) revealed close similarities in spore ontogeny sequences with the one here described for A. rehmii. Successful cultivation of additional Acaulospora representatives will allow comparisons of developmental patterns but required an improved mastery of in vitro cultivation.


   ACKNOWLEDGMENTS
 
This work was supported by a grant from EC: INCO-DC ERBIC18*CT970208. S.D. gratefully acknowledges the financial support from the Belgian Federal Office for Scientific, Technical, and Cultural affairs (OSTC, contract BCCM C2/10/007). Thanks are addressed to R. Fogain (CARBAP Cameroon) for providing A. rehmii strain, to S. Seguin for technical assistance, to manuscript reviewers for their fruitful comments, and to the director of MUCL for the facilities provided and for continuous encouragement.


   FOOTNOTES
 
1 Corresponding author, Email: dalpey{at}em.agr.ca Back

2 Part of the Belgian coordinated collections of microorganisms (BCCM) Back

Accepted for publication May 13, 2002.


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
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