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Applied and Environmental Microbiology, December 1999, p. 5571-5575, Vol. 65, No. 12
0099-2240/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Anastomosis Formation and Nuclear and Protoplasmic
Exchange in Arbuscular Mycorrhizal Fungi
Manuela
Giovannetti,*
Dario
Azzolini, and
Anna
Silvia
Citernesi
Dipartimento di Chimica e Biotecnologie
Agrarie, Centro di Studio per la Microbiologia del Suolo, CNR,
Università di Pisa, 56124 Pisa, Italy
Received 13 May 1999/Accepted 17 September 1999
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ABSTRACT |
We observed anastomosis between hyphae originating from the same
spore and from different spores of the same isolate of the arbuscular
mycorrhizal fungi Glomus mosseae, Glomus
caledonium, and Glomus intraradices. The percentage
of contacts leading to anastomosis ranged from 35 to 69% in hyphae
from the same germling and from 34 to 90% in hyphae from different
germlings. The number of anastomoses ranged from 0.6 to 1.3 per cm
(length) of hyphae in mycelia originating from the same spore. No
anastomoses were observed between hyphae from the same or different
germlings of Gigaspora rosea and Scutellospora
castanea; no interspecific or intergeneric hyphal fusions were
observed. We monitored anastomosis formation with time-lapse and
video-enhanced light microscopy. We observed complete fusion of hyphal
walls and the migration of a mass of particles in both directions
within the hyphal bridges. In hyphal bridges of G. caledonium, light-opaque particles moved at the speed of 1.8 ± 0.06 µm/s. We observed nuclear migration between hyphae of the
same germling and between hyphae belonging to different germlings of
the same isolate of three Glomus species. Our work suggests
that genetic exchange may occur through intermingling of nuclei during
anastomosis formation and opens the way to studies of vegetative
compatibility in natural populations of arbuscular mycorrhizal fungi.
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INTRODUCTION |
Arbuscular mycorrhizal (AM) fungi
are obligate symbionts that live in association with the roots of most
land plants and play a major role in nutrient uptake and in interplant
nutrient transfer (8, 27, 39). In experimental microcosms
and in the field, AM hyphal connections between roots are important for
the maintenance of stability and biodiversity in plant communities
(32, 36). Little is known about the dynamics of hyphal
growth during presymbiotic and symbiotic phases (24, 30,
31), and virtually nothing is known of the ability of these fungi
to form the hyphal networks through which nutrients are proposed to
flow. Although anastomoses occur widely between vegetative hyphae of
ascomycetes and basidiomycetes (1, 3, 17, 21), they are
believed to be lacking or rare in zygomycetes (5, 16), to
which AM fungi belong. The occurrence of anastomosis in AM fungi has
been mentioned by some authors (11, 15, 26, 40), but no
quantitative data are available on the frequency of hyphal fusions in
the different species, and, to our knowledge, no information has been
published on the cytological events involved.
In this study we monitored anastomosis between hyphae derived from
individually germinated spores of AM fungi via a combination of
time-lapse and video-enhanced light microscopy, image analysis, and
epifluorescence microscopy. Our main objectives were (i) to monitor
anastomosis formation in living hyphae; (ii) to detect cytoplasmic flow
and nuclear exchange between anastomosing hyphae; (iii) to determine
the occurrence and frequency of anastomosis between hyphae belonging to
the same and to different germinated spores of the same isolate of
Glomus mosseae, Glomus caledonium, Glomus
intraradices, Gigaspora rosea, or Scutellospora
castanea; and (iv) to determine the kind of interaction occurring
between hyphae belonging to different genera (Glomus versus
Gigaspora and Gigaspora versus
Scutellospora) and to different species of the same genus
(Glomus).
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MATERIALS AND METHODS |
Fungal material.
Spores of AM fungi were obtained from pot
cultures maintained in the collection of the Department of Chemistry
and Agricultural Biotechnology, University of Pisa, Pisa, Italy. The AM
fungi used were G. mosseae (Nicolson et Gerdemann) Gerdemann
et Trappe (Kent isolate) (Banque Européenne des Glomales [BEG]
code 12), G. caledonium (Nicolson et Gerdemann) Trappe et
Gerdemann (Rothamsted isolate) (BEG 20), G. intraradices
Schenck et Smith, isolated from Bourgogne, France (LPA 8), G. intraradices Schenck et Smith, isolated from Liguria, Italy (IMA
5), Glomus viscosum Nicolson (BEG 27), G. rosea
Nicolson et Gerdemann (BEG 9), and S. castanea Walker (BEG 1). Inocula of the G. intraradices French isolate, G. rosea, and S. castanea were kindly provided by V. Gianinazzi-Pearson, Laboratoire de Phytoparasitologie, Dijon, France.
Dynamics of anastomosis formation in living hyphae.
Spores
of G. caledonium and G. mosseae were surface
sterilized with 2% chloramine T supplemented with streptomycin (400 µg ml
1) for 20 min and then rinsed five times in
sterile distilled water. The spores were germinated on 20- by 20-mm
cellophane membranes (Hoefer, San Francisco, Calif.) and placed on a
thin layer of 1% water agar in 5.5-cm-diameter petri dishes for direct
observations of living hyphae under a Reichert-Jung (Vienna, Austria)
Polyvar microscope equipped with differential interference contrast
optics and epifluorescence optics. We monitored anastomosis formation in hyphal tips showing directed growth towards nearby hyphae, which
were growing at a distance of about 70 µm. To visualize the
establishment of protoplasmic continuity and the viability of
anastomosed hyphae, succinate dehydrogenase (SDH) activity was assessed
on germinated spores, which were stained, mounted on microscope slides,
and observed for the presence of formazan salt depositions in hyphal
bridges (38).
Nuclear migration and cytoplasmic flow through anastomoses.
We mounted cellophane membranes bearing germinated spores of G. caledonium and G. mosseae on microscope slides in
sterile distilled water. The coverslips were sealed with 1% water
agar, which was periodically wetted with sterile distilled water. The microchambers obtained were transferred to the Polyvar microscope and
observed for 2 h. Bright contrast images were acquired after regulation of the condenser diaphragm. The experiments were carried out
at room temperature (19 to 21°C). To monitor nuclei in hyphae during
anastomosis formation, 7- to 14-day-old germinated spores were mounted
on microscope slides in diaminophenylindole (DAPI) (Sigma, St. Louis,
Mo.) at 5 µg/ml of microscopy 1:1 water-glycerol and were observed
under epifluorescence by using the filter combination U1 (BP 330-380, LP 418, DS 420). Images were acquired with a Reichert 100× oil
immersion lens with a 1.25 numerical aperture. Time-lapse and
video-enhanced light microscopy was used to obtain images, which were
captured with a 3 charge-coupled device color video camera connected to
a videocassette recorder (Hi 8, EV-C2000E; SONY, Tokyo, Japan).
Selected frames were printed on a video graphic printer (UP-890 CE; SONY).
Occurrence and frequency of anastomoses.
Spores were rinsed
five times in sterile distilled water and were allowed to germinate
individually in sterile distilled water in microliter plates (Sigma).
Germinated spores were transferred to Millipore membranes
(0.45-µm-diameter pores), which were placed on moist, sterile quartz
sand in 9-cm-diameter petri dishes. After 7 to 14 days of incubation in
the dark at 28°C, mycelium growing on the membranes was stained with
Trypan Blue (0.05% in lactic acid), mounted on microscope slides, and
observed under the Polyvar light microscope. Hyphal length was assessed
by using Quantimet 500 image analysis software (Leica, Milan, Italy).
Pairings of individually germinated spores were made by placing
germinated spores approximately 1 cm apart on the membrane filter.
Findings are based on at least 10 germinated spores for anastomoses
within the same germling, 9 pairings for anastomoses between different germlings from the same isolate, and 9 sets of pairings for
interspecific and intergeneric anastomoses. Replicate experiments were
carried out on spores produced in different pot cultures (Table
1). The frequency of anastomosis was calculated by
determining the proportion of hyphal contacts which had anastomosed.
Chi-square analysis was used to determine the homogeneity of
anastomosis frequency data, and the chi-square test of independence was
performed to detect significant differences in anastomosis frequency
between hyphae from the same spores and hyphae from different spores.
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TABLE 1.
Anastomosis rate in mycelia originating from the same
spore or from different spores of the same isolate in five species of
AM fungi and numbers of anastomoses and hyphal contacts per centimeter
(length) of hypha in mycelia originating from the same spore
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RESULTS |
Dynamics of anastomosis formation in living hyphae.
Spatiotemporal studies made it possible to monitor anastomosis
formation, which took about 35 min after a hyphal tip showed directed
growth towards another hypha, in G. caledonium and G. mosseae mycelia. Complete fusion of hyphal walls and cytoplasmic flow between fused hyphae were observed. We observed protoplasmic continuity, the characteristic feature of true vegetative hyphal fusion, as SDH activity in all the anastomoses. Depositions of formazan
salt were detected in anastomosing hyphae and in hyphal bridges (Fig.
1).
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FIG. 1.
Micrograph showing complete fusion of hyphal walls and
the establishment of protoplasmic continuity in two anastomosing hyphae
of G. mosseae, visualized by histochemical localization of
SDH activity. Depositions of formazan salt are evident in hyphal
bridges. Bar, 10 µm.
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Nuclear migration and cytoplasmic flow through anastomoses.
DAPI staining and epifluorescence microscopy showed that hyphal
anastomosis involved the migration of nuclei via the fusion bridge.
Migration occurred between hyphae belonging to the same germling (Fig.
2a and b) and between hyphae belonging to
different germlings of the same isolate (Fig. 2c and d).
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FIG. 2.
Localization of nuclear migration between two
anastomosing hyphae of G. caledonium belonging to the same
germling (a and b) and to different germlings of the same isolate (c
and d). (a) Light micrograph illustrating the site of hyphal fusion.
(b) Epifluorescence image of the same field, showing an elongated
nucleus (stained with DAPI) in the middle of the fusion bridge. Bar, 7 µm. (c and d) Epifluorescence microscopy of the nuclei within fusion
bridges (arrows). Bar, 12 µm.
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We used time-lapse and video-enhanced microscopy to detect protoplasmic
streaming inside the hyphae and to monitor the trajectory
of a mass of
particles (e.g., vacuoles, mitochondria, nuclei,
and fat droplets)
migrating in both directions within the protoplasm
and through
anastomoses (Fig.
3). The mass streaming
of particles
occurred at a speed of 1.8 ± 0.06 µm/s (mean ± standard error
of the mean [SEM]) in hyphal bridges of
G. caledonium.
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FIG. 3.
Protoplasmic flow subsequent to anastomosis in G. caledonium, visualized over time by video-enhanced light
microscopy. Cytoplasmic continuity is established between two fused
hyphae, evidenced by the bidirectional movement of particles
(arrowheads). (a and b) A large, light-opaque particle migrating from
one hypha to the other via the fusion bridge (arrows). Time sequence: 0 (a) and 2 (b) s. (c and d) Two coupled light-opaque particles migrating
in the opposite direction, via the fusion bridge (arrows). Time
sequence: 0 (c) and 2 (d) s. Bar, 3.8 µm.
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Occurrence and frequency of anastomoses.
We observed
anastomoses between hyphae belonging to the same germinated spore
and between different spores of the same isolate in all three
Glomus species. The percentage of anastomoses between hyphae from the same germling ranged from 35% in G. caledonium to 69% in the Italian isolate of G. intraradices (Table 1), and the number of anastomoses ranged from
0.62 ± 0.06 (mean ± SEM) to 1.3 ± 0.23 per cm
(length) of hyphae (Table 1). Hyphal fusions also occurred readily
between hyphae belonging to different germlings from the same isolate.
The anastomosis rate ranged from 34% in G. caledonium to
90% in the Italian isolate of G. intraradices (Table 1).
No anastomoses were observed between hyphae belonging to the same
germling of
G. rosea or
S. castanea (Table
1). No
fusions
were detected in more than 220 hyphal contacts between
germlings
of
G. rosea. No fusions were detected in more than
460 hyphal
contacts between germlings of
S. castanea.
No anastomoses were observed in pairings between germlings of different
species of AM fungi:
G. mosseae and
G. caledonium (0 fusions, 90 contacts),
G. mosseae and
G. rosea (0 fusions,
140 contacts),
G. caledonium
and
G. rosea (0 fusions, 232 contacts),
and
G. rosea and
S. castanea (0 fusions, 98
contacts).
During interspecific and intergeneric hyphal interactions, the
responses ranged from no contact interference, when hyphae
simply
appeared to overgrow each other, to contact responses such
as formation
of hyphal swellings devoid of protoplasm and septate
(Fig.
4) or growth of one hypha along the other
without anastomosis
formation.
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FIG. 4.
Interactions between hyphae originating from two
different species of AM fungi, G. mosseae (upper arrow) and
G. viscosum (arrowhead). Note the formation of a hyphal
swelling which becomes empty and septate without any anastomosis
formation (lower arrow). Bar, 20 µm.
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DISCUSSION |
Anastomosis formation and the cytological events involved have
been studied extensively in ascomycetes and basidiomycetes (1, 3,
17, 21, 25). Anastomoses are believed to be lacking or rare in
zygomycetes (5, 16), although their occurrence in AM fungi
has been mentioned by others (11, 15, 26, 40). In this
report, we present evidence for anastomosis formation between hyphae
originating from the same spore and from different spores in one
isolate of G. mosseae, one isolate of G. caledonium, and two different isolates of G. intraradices. The frequency of anastomoses per contacts in hyphae
from the same germling was comparable to that found within
self-anastomosing isolates of Rhizoctonia solani
more than
50% (19). The number of anastomoses per centimeter (length)
of hypha ranged from 0.62 to 1.3, corresponding to 0.22 to 0.45 fusions
per mm2, as worked out from hyphal density data
(13). These values are lower than those observed in fungi
that are able to grow saprophytically, such as Gibberella
fujikuroi6.9 to 8.1 fusions per mm2 in
self-compatible strains (6)but still significant when the
poor growth ability of the presymbiotic mycelium of AM fungi is
considered (2, 24).
In the three Glomus species, hyphal fusions occur regularly
in mycelia originating from different spores. In G. mosseae
the frequency of anastomosis formation between hyphae from different germlings was not statistically different from that for mycelia originating from the same germling, whereas G. intraradices and G. caledonium showed significantly
higher and lower frequencies of anastomosis per contact, respectively,
in hyphae originating from different spores. No anastomoses were
observed between hyphae from the same or different germlings of
G. rosea and S. castanea, and this characteristic
may be another difference between the Glomineae and Gigasporineae
families (37).
During interspecific and intergeneric interactions, no hyphal fusions
were detected, suggesting that hyphae recognize species-level differences and confirming previous qualitative findings
(40). The ability to discriminate self from other at the
intraspecific level, however, remains to be demonstrated. The use of
tests based on vegetative compatibility may lead to the identification
of genetically different isolates in population studies of pathogenic, saprophytic, and ectomycorrhizal fungi (3, 7, 9, 20-22, 29,
35). Our work opens the way to studies of vegetative
compatibility in natural populations of AM fungi. For example,
different isolates of G. mosseae, a species of worldwide
distribution, could be paired with known tester strains to
determine if they are genetically isolated as indicated by vegetative compatibility.
AM fungi are ancient obligate biotrophs (18) which, although
lacking host-regulated spore germination (14), have survived for 400 million years (28, 33, 37). We suggest that the ability of germlings to form anastomoses with compatible hyphae may
affect the fitness of Glomus species; the young mycelium
produced by spores germinating in the absence of the host may connect
to a mycelial network as soon as the germ tube contacts a compatible mycelium, increasing its chance to colonize host roots. The formation of anastomoses also can restore protoplasmic continuity in damaged hyphae (10).
We obtained direct evidence for nuclear exchange between hyphae from
the same germling and between hyphae of different germlings of the same
isolate in three Glomus species. Nuclei from single spores
of Glomus species may be heterogeneous, based on variation in molecular characters (23, 34, 41). Since
Glomus spores are multinucleate and may contain 1,000 to
5,000 nuclei per spore (4, 12, 42), some researchers have
suggested that these spores are heterokaryotic (23, 34). Our
results suggest that genetic exchange may occur through intermingling
of nuclei during anastomosis formation between different germlings of
the same isolate. This exchange could result in information flow, as
well as physiological and genetic integration, between mycelia
belonging to different germlings.
Lack of knowledge of the genetics of AM fungi and our inability to
culture them in axenic culture make it difficult to discern the
mechanism by which genetic exchange occurs. Further studies are needed
in order to understand how these obligate symbionts maintain genetic
diversity within spores.
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ACKNOWLEDGMENT |
This work was partly supported by a University of Pisa grant
(Fondo di Ateneo).
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FOOTNOTES |
*
Corresponding author. Mailing address: Dipartimento di
Chimica e Biotecnologie Agrarie, Via del Borghetto 80, 56124 Pisa, Italy. Phone: 39-050-571561. Fax: 39-050-571562. E-mail:
mgiova{at}agr.unipi.it.
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Applied and Environmental Microbiology, December 1999, p. 5571-5575, Vol. 65, No. 12
0099-2240/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
