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SORUS DEVELOPMENT, SPORE MORPHOLOGY,
AND NUCLEAR CONDITION OF GYMNO­
SPORANGIUM GAEUMANNII SSP.
ALBERTENSE
YASUYUKI HIRATSUKA
Northern Forest Research Centre, Canadian Forestry Service
Department of the Environment, Edmonton, Alberta
SUMMARY
A needle rust of Juniperus communis L. var. depressa Pursh, Gymno­
sporangium gaeumannii Zogg spp. albertense Parmelee, can sporulate
annually on the same site of a needle for up to three or possibly more
years. The first sorus develops subepidermally and sporulates by pushing
up the epidermal layer. In the second year, a new sporogenous layer de­
velops under the old one and sporulates by pushing it up as the epidermal
layer was pushed up a year before. Occasionally, a third sporogenous
layer is produced under the second a year later.· Six morphologically
distinct spores are present in this fungus: (1) pedicellate, 1-celled, multi­
pored, verrucose spores, (2) pedicellate, 2-celled multipored, verrucose
spores, (3) pedicellate, 1-celled, single-pored, smooth spores, (4) pedicellate
2-celled, single-pored, smooth spores, (5) pedicellate, 2-celled spores
with one multipored, verrucose cell, and one single-pored, smooth cell, and
(6) nonpedicellate, verrucose, hyaline spores. Regardless of the number of
cells in a spore, the multipored, verrucose cells have two nuclei, which
upon germination migrate into the germ tube without nuclear fusion or
division.
The single-pored, smooth cells have one large nucleus and
germinate to produce basidia and basidiospores. Thus the 2-celled, multi­
pored spores should be called urediniospores rather than teliospores.
Parmelee (1969) described a rust fungus, Gymnosporangium gaeu­
Zogg ssp. albertense Parmelee, on Juniperus communis L. var.
depressa Pursh based on several specimens collected in Banff and Jasper
National Parks, Alberta, Canada. He indicated that it resembled the
telial state of Gymnosporangium cornutum Arth. ex Kern but it had
predominantly single-celled urediniospores rather than 2-celled telio­
spores. There is a similarity between this fungus and G. gaeumannii
Zogg ssp. gaeumannii which has been reported only from the Swiss
Alps (Zogg, 1949; Holm, 1968), but according to Parmelee (1969,
1971) the two differ in urediniospore germ pore numbers (mostly
6-8 for G. gaeumannii gaeumannii and mostly 10-12 for G. gaeumannii
mannii
albertense) .
137
MYCOLOGIA, VOL. 65, 1973
138
In both subspecies, several unusual spore types besides predominant
multipored, single-celled urediniospores have been recorded.
The true
nature of each of those spore types has not been known, although several
authors predicted it without germination experiment or cytological study
(Holm,
1968, 1969;
Kern,
1970;
Parmelee,
1971;
Zogg,
1949).
Sori of this fungus are usually found on 2-6-year-old needles but
the mechanism of overwintering or phenology of sorus development has
not been known.
MATERIALS AND METHODS
About 30 specimens, including the holotype and paratypes, of Gymno­
sporangium gaeumannii ssp. albertense collected in various locations in
Banff and Jasper National Parks, Alberta, Canada, at different times of
the year were studied.
For germination and cytological studies, fresh
spores were dispersed onto microscope slides coated with 0.3% water
agar and then incubated at 15 C.
After germ tubes had developed to
the suitable stage, slides were dried on a slide warmer adjusted to 50 C
and fixed in Singleton's fixative (Singleton,
with HCl-Giemsa after hydrolizing for
1953).
They were stained
5-6 min at 60 C in HC!.
RESULTS AND DISCUSSION
Sorus developmen t.
-
Only one kind of sorus is produced (FIG. 1).
It is subepidermal and contains several different kinds of spores.
No
bounding structures, such as pseudoperidium or peripheral paraphyses,
are present.
Infection to initiate a new sorus probably occurs during
the summer on the current year or l-year-old needles.
The first sorus
develops subepidermally during the winter and in the spring it sporulates
by pushing up the epidermal layer (FIG. 2).
side.
It opens up usually at one
Spores develop continually until late in the growing season of
the host.
By the end of the fall, most of the spores are discharged and
a cushion of sporogenous layer consisting of basal cells and old pedicels
remains.
Under this spent sporogenous layer, together with one or
two layers of host cells, a new or second sporogenous layer develops
during the ensuing winter (FIG.
3).
This layer pushes up the old
sporogenous layer in the same way as the epidermis was lifted up and
ruptured the previous year.
Occasionally, a third sporogenous layer
may be formed under the second sporogenous layer a year later (FIG. 4).
This is the third successive annual sporulation on the same site.
In
this case the rust stayed alive at least 4 years on the same needle,
139
HIRATSUKA: GVMNOSPORANGIUM
FIG. 1.
Sori of Gymllosporongium gaeumannii ssp. albertense
needles of Juniperus communis var. depressa.
hence may be termed perennial.
on
X 13.
This unusual sorus development ex­
plains the mechanism of survival and overwintering of this rust, and
it also explains why the sori are found regularly on older needles.
Spore morphology.-The most common type of spore is single-celled,
multipored
(8-12 germ pores), pedicellate, dark yellow-brown with
verrucose wall ornamentation (FIG. Sa).
all through the sporulation period.
These spores are produced
During the first few weeks after
sorus development, the same sorus may also yield I-celled (FIG. Sb)
and 2-celled (FIG. 6)
smooth spores with one germ pore per cell.
MYCOLOGIA, VOL. 65, 1973
140
FIGs. 2-4.
tense.
Sorus development of Gymnosporangium gaeumannii ssp. alber­
2. Subepidermal sorus.
3.
a.
Early development of second sporulation.
h. Almost spent previous year's sporogenous layer. 4. a. New sporogenous layer.
h. Spent previous year's sporogenous layer. c. Spent 2-year-old sporogenous layer.
Epidermal layer covering the sorus has gone. All X 850.
These are the teliospores as in Parmelee's original 1969 description.
Except that the pedicel is not gelatinous, they are typical of teliospores
of Gymnosporangium.
The frequency of this type of spore in a sorus
HIRATSUKA: GYMNOSPORANGIUM
FIGS. 5-8.
tense.
5.
a.
smooth spore.
141
Spore morphology of Gymnosporangium gaeumannii ssp. alb er­
A I-celled, multi pored, verrucose spore. h. A I-celled, single-pored,
6. Three 2-celled, single-pored, smooth spores and one I-celled,
7. a. A 2-celled, multipored, verrucose spore. h. A
multipored, verrucose spore.
I-celted, verrucose, hyaline spore.
8.
a. A 2-celted, pediceltate spore with one
multipored, verrucose celt and one single-pored smooth cell.
pored, verrucose spore.
h. A I-celted, multi­
All X 850.
differs from sorus to sorus but very few have been found later in the
sporulation period.
During the period when teliospores occur fre­
quently, two other kinds of spores may occur.
Firstly, there are 2-
celled, multipored spores which look like doubles of single-celled, multi­
pored spores (FIG . 7a).
Secondly, there are 2-celled spores having one
multipored cell and one single-pored cell (FIG. 8).
The two kinds of
142
MYCOLOGIA, VOL. 65, 1973
FIGs. 9--13. Nuclear condition of Gymllosporangium gaclllnanllii
9. a. A young 2-celled, multipored, verrucose spore with two
cell. h. Two I-celled, multipored verrucose spores with two nuclei
10. A young 2-celled spore with one multipored, verrucose cell with
tense.
and one single-pored, smooth cell with one large nucleus.
11.
single-pored, smooth spores with one large nucleus per each cell.
multipored, verrucose spore with two nuclei.
verrucose cell with two migrating nuclei.
pored, smooth cell.
ssp. alber­
nuclei per
per spore.
two nuclei
a. Three 2-celled,
h. One I-celled,
12. A germ tube from a multipored,
13. A 4-celled basidium from a single­
All X 850 except FIG. 12, X 610.
143
HIRATSUKA: GYMNOSPORANGIUM
cells differ not only in germ pore numbers but in the surface configura­
tion.
Multipored cells are verrucose and single-pored cells are smooth.
The same sorus may contain hyaline and nonpedicellate spores
(FIG. 7b).
They look somewhat like peridial cells of certain rust fungi but they are
produced throughout the sorus and not around it.
The interesting problem here is the nomenclature and definition of
each spore type.
With the European subspecies, Holm
(1968, 1969)
concluded that since multipored, 2-celled spores are very similar to
the teliospores of Gymnosporangium multiporum Kern, these spores
should be considered as teliospores and since the predominant single­
celled multipored spores are identical with the cells of 2-celled spores,
he suggested calling them teliospores also.
But, Kern
(1970)
stated
that the 2-celled multipored spores in the species may be regarded as
bicellular urediniospores rather than teliospores.
He also noted that
teliospore germination in G. multiporum had not been shown and
therefore he referred to the "alleged" teliospores of G. multiporum.
(1971)
(1970) and
Parmelee
had independently reached the same conclusion as
Kern
also noted that teliospores of G. multiporum were
smooth whereas the 2-celled urediniospores of G. gaeumannii were
verrucose.
Nuclear condition and germination of spores.-To find out the real
nature of each type of spore I germinated them and observed their
nuclear conditions before and after germination.
The I-celled, multipored spores had two nuclei (FIGS. 9b,
1 1b)
and
upon germination the two nuclei migrated into the germ tube and no
nuclear fusion or division occurred (FIG. 12).
The 2-celled, multipored spores also had two nuclei in each cell of
the spores (FIG. 9a) and the two nuclei migrated into germ tubes and
no nuclear fusion or division occurred.
The I-celled and 2-celled, single-pored, smooth spores had one large
nucelus per cell (FIG. 11a).
Upon germination, the nucleus migrated
into the germ tube, then divided twice and produced a 4-celled basidium
(FIG.
13)
which later produced four basidiospores.
The 2-celled spores, having a combination of multipored verrucose
and single-pored smooth cells, had two nuclei in each multipored cell
and one large nucleus in each single-pored cell (FIG. 10).
In other
words, the nuclear condition was also the combination of the two kinds
of cells and reflects a uredinial and telial morphology.
I did not observe
the germination of the two kinds of cells at the same time, but multi­
pored cells germinated with the two nuclei migrating into a long germ
144
MYCOLOGIA, VOL. 65, 1973
tube.
Probably the single-pored smooth cells germinate to produce
basidia and basidiospores.
The I-celled, hyaline, notlpedicellate spores did not germinate.
summary, regardless of the number of cells in
a
In
spore, multipored, ver­
rucose cells have two nuclei and upon germination the two nuclei
simply migrate into the germ tube forming a dikaryon typical of the
uredinial state.
The single-pored, smooth cells had one large nucleus
and germinated to produce basidia and basidiospores which were typical
of the telial state.
From the results, 2-celled multipored spores should
be considered as urediniospores as predicted by Kern
Parmelee
(1971)
(1970)
rather than as teliospores as predicted by
and
Holm
(1968).
ACKNOWLEDGMENTS
I wish to thank Mr. P. J. Maruyama for his excellent technical
assistance, and Dr. J. A. Parmelee, Plant Research Institute, Ottawa,
and Dr. G. B. Cummins, Tucson, Arizona, for critical review of the
manuscript.
LITERATURE CITED
Holm, L.
1968.
Etudes Uredinologiques. 8.
une espece primitive?
.
--
Etudes Uredinologiques.
1969.
Gymnosporangium
gaeumannii­
Svensk Bot. Tidskr. 62: 463-466.
des
Gymnosporangiu1l!.
The uredial stage in Gymnosporangium.
Bull. Torrey Bot.
9.
Sur
I'uredo
Svensk Bot. Tidskr. 63: 349-358.
Kern, F. D.
1970.
Club 97: 159-161.
Parmelee, J. A.
1969.
Gymnosporangium gaeumannii in North America.
Mycol­
ogia 61: 401-404.
--.
1971.
The genus Gymnosporangium in western Canada.
49: 903-926.
Singleton, J. R.
crassa.
Zogg,
H.
1953.
Canad. ]. Bot.
Chromosome morphology and the ascus of Neurospora
Amer.]. Bot. 40: 124-144.
1949.
"Ober ein neucs Urcdo-bildendes Gymnosporangium:
sporangium gaeumannii.
Ber. Schweiz. Bot. Ges. 59: 421-426.
Accepted for publication April 13, 1972.
Gymno­