THE NUCLEAR CYCLE AND THE TERMINOLOGY OF SPORE STATES IN UREDINALES'
YASUYUKI
HIRATSUKA
Northern Forest Research Centre, Canadian Forestry Service,
Department of the Environment, Edimonton 70, Alberta
SUMMARY
The criteria for nomenclature of spore states in the Uredinales
should relate to their positions in the life cycle and be based on their
nuclearconditions. Definitions for five spore states are presentedbased on
these criteria. This system reflects the function of each spore state. On
the other hand, naming of the spore states based only on the external
morphology is not only impossible because of morphological variability
but illogical and creates confusion. Logically, names of the spore states
should be based on their true nature and the use of morphological terms
should be restricted to the description of spores and spore-producing
structures.
Terminology for the spore states of the rust fungi was proposed by
de Bary, Tulasne and others in the middle of the last century and modified by Arthur (1905, 1925, 1934), Azbukina (1970), Cummins (1959),
Cunningham (1930, 1931), Laundon (1967a), Savile (1968), and
others. Several names have been proposed for each spore state, such
as spermatia, pycnidiospores, pycniospores; aeciospores, aecidiospores;
uredospores, urediniospores, urediospores; teliospores, teleutospores;
sporidia or basidiospores. I use spermatia, aeciospores, urediniospores,
teliospores and basidiospores without critical considerations of etymology
or historical background. Not only several different terms are used for
one spore state but two different bases are applied in the definition and
terminology of spore states and, in certain cases, the same spore state
has been interpreted differently and called by different names. The
differences in definition and interpretation have been reflected in the
classification and nomenclature of some taxa.
The two different systems can be called the "ontogenic system" and
the "morphologic system." Current uredinologists use one or the other
system or mix the two, either consciously or unconsciously, in their
1 Based in part on a paper presented in the symposium on "Criteria and classi-
fication in the Heterobasidiomycetes"at the First International Mycological Congress, University of Exeter, England, September, 1971.
432
HIRATSUKA:
SPORE
STATES
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433
definition and nomenclature of spore states. However, using illogical
criteria or mixing the two different systems in definition and nomenclature of spore states creates confusion and thus in undesirable.
Cummins (1959) outlined the concept of the "ontogenic system" with
the statement, "Spore states are best considered to be 'positions' in the
life cycle rather than clearly recognizable morphological entities. Thus
a sorus may have the gross morphology of an uredium and yet be an
aecium, or a sorus may look like an aecial cup but actually be an uredium
or telium. In order to know what the fruiting structure really is, one
needs to know something of its ontogeny, i.e. one must know how it
originates, and what happens to the spores produced." The term
"ontogeny" in the preceding statement is misleading. It does not mean
the morphogenesis or the developmental morphology of each successive
spore state as the term originally implied, but it means the sequence
and function of spore states in the life cycle of the rust. I use the term
"ontogenic system" in the latter sense, knowing that the common meaning of the term is different, because several authors who discussed the
terminology of the rust fungi used the term in this sense (Azbukina,
1970; Cummins, 1959; Laundon, 1967a).
The "morphologic system" was applied mainly by early European
mycologists. It is represented by a recent paper by Laundon (1967a).
He stated that the ontogenic approach to terminology of rust fungi is
fundamentally illogical and causes difficulty and confusion. He suggested that the names of spore states be based on their visible morphology
and not on their invisible ontogeny. In other words, he suggested that
each spore state be defined and named by the morphology regardless of
what position in the life cycle the spore state occupies.
The nuclear cycle or the alternation of generations in rust fungi is
fairly well understood and the basic nuclear events are similar and stable
throughout the group regardless of modifications in their life cycles.
I believe that this basic nuclear cycle should be the basis for the definition and nomenclatureof spore states.
Major nuclear events in the life cycle of a rust fungus are nuclear
fusion, meiosis and dikaryotization (FIG. 1). Several spore states are
interpolated between haploid basidiospores which are meiospores and
nuclear fusion in teliospores. First, basidiospores initiate the haploid or
gametophytic state on which spermogonia may develop. Spermogonia
produce haploid spermatia which may or may not be functional for dikaryotization. Upon dikaryotization, dikaryotic spores are produced.
They germinate and initiate the dikaryotic or sporophytic state. One, or
rarely two (in the case of the presence of amphispores) repeating vege-
434
MYCOLOGIA, VOL.
65, 1973
DIKARYOTIZATiON
spermogonia
I0o
i? i
i
|
w~~~~~~~~~~~~$iBn~~~~~~~~~~~~~~~~~~~~
FIG. 1.
Nuclear cycle of a heteroecious pine s em rust (Croiartiium sp.).
tative spore states develop on the dikaryotic mycelium. The same mycelium also produces another kind of spore in which nuclear fusions
occur. These spores germinate and produce basidia.
Exceptions to this general pattern are the existence of species that
have a monokaryotic life cycle throughout and produce two basidiospores
instead of the usual four. Apparently no nuclear fusion or meiosis takes
place in these cases (Jackson, 1931). They can be considered as variations from the basic cycle.
On the basis of the nuclear cycle, each spore state can be defined as
follows:
Teliospores are basidia-producing spores.
Basidiospores are monokaryotic spores produced on basidia usually as
the result of meiosis.
Spermatia are monokaryotic gametes.
Aeciospores are nonrepeating vegetative spores produced usually from
the result of dikaryotization and germinate to initiate dikaryotic
mycelium, thus usually associated with spermogonia.
Urediniospores are repeating vegetative spores produced usually on
dikaryotic mycelium.
HIRATSUKA:
SPORE STATES IN UREDINALES
435
According to this definition all basidia-producing spores regardless of
morphology are called teliospores and this will correspond to the "perfect state" of Uredinales defined in the International Code of Botanical
Nomenclature (1966, Article 59). This is also equivalent to "probasidium" defined by Donk (1954) and Talbot (1954).
There are so many morphological variations of teliospores that it is
impossible to define this spore state based on morphology or morphological types. Even in morphologic definition as proposed by Laundon
(1967a), the only definite statement is "teliospores always produce
basidia on germination" which is a purely ontogenical definition.
Some morphological variations of teliospores are illustrated in FIG. 2.
Teliospores may be one- (FIG. 2A, B), two- (FIG. 2C, D, H) or multicelled spores (FIG. 2E, F, G, I, J) produced on pedicels. They may be
a single layer of cells (FIG. 2K, L) or a multilayer of cells (FIG. 2M, N)
without pedicels. They may be produced in chains (FIG. 20, P, Q, R)
with or without peridial cells or intercellary cells. The surface of teliospores may be smooth (FIG. 2D, E), echinulate (FIG. 2H), verrucose
(FIG. 2A), reticulate or striate (FIG. 2B). They may be thick walled
and heavily pigmented (FIG. 2A, B, H, I) or thin walled and hyaline
(FIG. 2Q, R).
It is evident that teliospores cannot be defined by morphology and
thus the basidia-producing spores of endo species should be called teliospores even though they resemble aeciospores of related species. Most of
the endo species produce typical basidia and basidiospores but in case of
species in Endocronartium they do not produce basidiospores. Spores
of E. harknessii (J. P. Moore) Y. Hiratsuka and E. pini (Pers. emend.
Kleb.) Y. Hiratsuka produce septate germ tubes with a single nucleus
in each cell (Hiratsuka et al., 1966; Hiratsuka, 1968; Hiratsuka, 1969).
Even in this case the basic nuclear events occur and although basidiospores are not produced, germ tubes are considered to be basidia and
therefore the spores should be called teliospores (FIG. 3).
Based on the nuclear cycle, aeciospores and urediniospores are
defined as follows. Aeciospores are nonrepeating vegetative spores produced usually by dikaryotization and which germinate to initiate dikaryotic mycelium. They usually are associated with spermogonia. Urediniospores are repeating vegetative spores produced on dikaryotic mycelium.
On the other hand, definite statements in the definitions of aeciospores
and urediniospores in Laundon's "morphologic system" are: "Aeciospores are borne in chains and unicellular" and "Urediniospores are always unicellular and borne singly on pedicels." However, those definitions are in direct contradiction with the morphological definition of
436
MYCOLOGIA,VOL. 65, 1973
FIG.2. Morphologicalvariations of telial states of Uredinales. A. Pileolaria
brevipes Berk. & Rav. B. Trachysporaintrusa (Grev.) Arth. C. Dasyspora gregaria (Kunze) P. Henn. D. Diorchidiella australe (Speg.) Lindq. E. Ravenelia
mera Cumm. F. Chrysella mikaniae Syd. G. Kuehneola uredinis (Lk.) Arth.
H. Prospodium appendiculatum (Wint.) Arth. I. Sphaerophragmium acaciae
(Cke.) Magn. J. Cumminsinaclavispora Petr. K. Melampsorellasymphyti Bubak. L. Chrysocelis lupini Lagh. & Diet. M. Goplana dioscoreae Cumm. N.
Lipocystis caesalpiniae (Arth.) Cumm. 0. Phragmidiella markhamiae P. Henn.
P. Didymopsora africana Cumm. Q. Dietelia verruciformis (P. Henn.) P. Henn.
R. Endophylloides portoricensis Whet. & Olive. (Reproduced with permission
from Cummins, 1959).
teliospores, because, as I pointed out in previous paragraphs, many teliospores are produced either in chains or singly on pedicels.
Some examples of spore states of rusts are arranged according to the
ontogenic system in FIG. 4. To make my point clear, I chose four examples from heteroecious species because in those cases alternation of
HIRATSUKA:
SPORE
STATES
IN
437
UREDINALES
NUCLEARFUSION
/ (3
aecioid teliospores
00
(
MEI0I
O TA^^---X
0I
0 * I *I
DIKARYOTIZATION
0olo1
oI
PINE
spermogonia
o !
MEIOSIS
*
I
/
FIG. 3. Nuclear cycle of an autoecious pine stem rust (Endocronartiumsp.).
generations is clearly recognizable and the gametophytic state and the
sporophytic state occur on two different plant species. However, the
same principle can be applied to the autoecious species. In the case of
Puccinia graminis Pers., Cronartium ribicola J. C. Fisch., or many
other so-called "typical" long cycle, heteroecious species, aeciospores are
produced in chains and urediniospores are produced singly on pedicels.
It is also true that most aeciospores are verrucose and most urediniospores are echinulate. However, in such genera as Chrysomyxa and
Coleosporium, not only aeciospores but also repeating spore states on
alternate hosts are produced in chains. In the ontogenic system, this
spore state should be called urediniospores but in the morphologic system they are called aeciospores because they are produced in chains.
On the other hand, a rust on Tsuga which has been known as Uredo
holwayi Arth. in western North America has pedicellate spores associated with spermogonia. This spore state is now connected to Pucciniastrum vaccinii (Wint.) JCrst. which has a pedicellate spore state and
intraepidermal teliospores on Vaccinium spp. (Hiratsuka, 1965). In
the ontogenic system, the spores on Tsuga are called aeciospores although they are produced singly on pedicels. In the morphologic system, however, this state on Tsuga would be called urediniospores.
To call the uredinial states of Chrysomyxa and Coleosporium aecia
just because they are produced in chains or the aecial state of Pucciniastrum vaccinii uredinia just because spores are produced singly on
438
4MYCOLOGIA,VOL.
65. 1973
FIG. 4. Spore states of four groups of heteroecious rusts arranged according
to the "ontogenic system." Dotted area defined as aecia and cross-hatched area
as uredinia.
pedicels, results in calling two biologically and functionally different
spore states by the same name (FIG. 5).
In the cases of aecidioid uredinia or secondary aecia, and uredinoid
aecia or primary uredinia in autoecious species, separation of the two
spore states is more difficult. But in most cases, so-called uredinoid
aecia or primary uredinia and true uredinia are morphologically distinct
in some degree although both are produced singly on pedicels. Differences are especially noticeable in such genera as Ravenelia, Uropyxis,
Pileolaria and Prospodium but are by no means rare in Puccinia-Uromyces. The differences are usually in wall thickness, pigmentation or
size of spores but sometimes in surface ornamentation and shape of
spores (Pileolaria spp., J. F. Hennen, personal communication), or in
the positions of the sori (section Cyathospora of Prospodium; Cummins, 1940).
Hiratsuka (1973) found that in Gymnosporangium gaeumannii Zogg
ssp. albertense Parmelee (Parmelee, 1969) the sorus is mainly composed
of pedicellate, one-celled, multipored, verrucose spores (FIG. 6A) but
also contained five other types of spores. They are: (1) pedicellate,
HIRATSUKA:
SPORE
STATES
IN
UREDINALES
439
one-celled, single-pored, smooth spores (FIG. 6B); (2) pedicellate,
two-celled, multipored, verrucose spores (FIG. 6C); (3) pedicellate,
two-celled, single-pored, smooth spores (FIGS. 6D); (4) pedicellate,
two-celled spores with one multipored, verrucose cell and one singlepored, smooth cell (FIG. 6E, F) ; and (5) nonpedicellate verrucose, hyaline spores. Each type of spore was germinated, except the last which
did not germinate, and the nuclear condition of the spore was studied. It
was found that regardless of the number of cells in a spore (one or two)
the multipored, verrucose cells had two nuclei and upon germination
the two nuclei simply migrated into the germ tube. The single-pored,
smooth cells had one large nucleus and germinated to produce fourcelled basidia and basidiospores (FIG. 6). It was concluded that the
two-celled, multipored, verrucose spores were not teliospores as predicted by Holm (1968) but were urediniospores as predicted by Parmelee (1971) and Kern (1970).
This example also supports the ontogenic system because two-celled
urediniospores are not allowed in morphological definitions. I expect
more examples of this kind will be found when the germination of
state
Gametophytic
Spermogonia
.
..................
..................
.... H........
Chrysomyxa
spp.
---- - - - - - - - - - - -'-
.................
..................
................
state
Telia
/
/
....
W
..".'%
...'...*.._.........''...*.. '.
spp.
Uredinia
'. .'..* Aecia '.*..
.
Puccinia
Sporophytic
o~OO
..................
..................
..................
...
..
.........
? r 1 1Oi
; Fc '
-- - - - - - -
iV I
FN^P
-
'
.................
..................
FIG. 5. Spore states of four groups of heteroecious rusts arranged according
to the "morphologic system." Dotted area defined as aecia and cross-hatched area
as uredinia.
440
MYCOLOGIA,VOL. 65, 1973
.
.I
~A ~
B
:-?
-1
~ ~~~~ ~ ~ ~ ~~~~~~
c
OQ;;,
r~
C~~~~~~~~~~~~~~~~~~~~~_s~Sp
i,-
F
K
~~ ~ ~
S-
*~~~~~~~~~~~~~~~~~~~~~1
FIG. 6. Morphological variations of spores of Gvymzosporanlgium gaeumannii
ssp. albertense and their nuclear conditions. A. One-celled, multipored, verrucose
spore. B. One-celled, single-pored, smooth spore. C. Two-celled, multipored,
verrucose spore. D. Two-celled, single-pored, smooth spore. E. Two-celled spore
with a multipored, verrucose cell and a single-pored, smooth cell. F. Same as E
except for the relative position of the two kinds of cells.
spores is studied. Peterson (1967) also reported occasional two-celled
urediniospores in Uredo cupressicola Peterson.
Germination and cytological studies of many poorly known rusts
are necessary to find out the real nature of their spore states. Also,
detailed morphological studies are important to accurately describe the
spore state involved. In this respect, Hughes (1970) compared the
spore formation of various rust fungi and applied the concepts and terms
developed for the Hyphomycetes. He concluded that spermatia are
phialospores, aeciospores are meristem arthrospores, urediniospores are
sympodioconidia, and teliospores are produced either as terminal, chlamydospore-like cells of hyphae of determinate growth, as sympodioconidia, or as meristem arthrospores. Catenulate urediniospores of
Chrysomyxa, Coleosporium and other so-called aecioid urediniospores
should belong to meristem arthrospores, and aeciospores of Pucciniastrum vaccinii and other so-called uredinioid aeciospores should belong
HIRATSUKA:
SPORE STATES IN UREDINALES
441
to Sympodioconidia. He also pointed out that the urediniospores of
Kernkampella breyniae-patensis (Mundk. & Thirum.) Rajendren, described by Rajendren (1970), have still another type of spore formation.
In this species, the urediniospores are discharged by breaks across the
middle of the pedicels, the sporogenous cells then grow through the
persistent half of the pedicel and produce a new urediniospore at the
apex of the proliferation. This phenomenon is repeated and the old,
lower parts of earlier pedicels appear as collars around the base of
newly forming urediniospores. Aeciospores of Dasyspora gregaria
(Kunze) P. Henn. are produced terminally on the short branches of
hyphae which develop superficially. This may be another different type
of aeciospore formation. Careful examinations may reveal additional
modes of spore formation in rust fungi.
Modified terms were proposed for several situations by the advocates
of both systems. Laundon (1967a) uses telial aecia (aecia behaving
like telia) for the basidia-producing spore state of endocyclic species,
uredial aecia (aecia behaving like uredia) for the catenulate repeating
vegetative spore state, and aecial uredia (uredia behaving like aecia) for
the pedicellate nonrepeating vegetative spore state. Cummins (1959)
uses aecidioid telia (Aecidium-like telia), caeomoid telia (Caeoma-like
telia), aecidioid uredia (Aecidium-like uredia) and uredinoid aecia
(Uredo-like aecia). These names reflect the consideration of the true
nature of spore states in the morphologic system and the consideration
of the morphology in the ontogenic system. However, Laundon's system is misleading, inaccurate, and undesirable because the same terms
are used both ontogenically and morphologically. Cummins' system of
referring the morphological types of form-genera together with the names
of spore states based on the position in the life cycle is the most desirable
one. According to this scheme telia of Endophyllum, Kunkelia, and
Endocronartium should be called aecidioid telia, caeomoid telia and
peridermioid telia respectively and the use of aecioid telia (Hiratsuka,
1969) should be avoided. At the present time, however, form-genera
of Uredinales are not well defined morphologically, especially in the
genus Uredo which includes most of the uredinial species. More accurate description of spore states will be possible when the imperfect states
are studied carefully and when the genera are segregated according to
their morphology and relationship as suggested by Laundon (1967b).
ACKNOWLEDGMENTS
I thank Dr. G. B. Cummins (Tucson, Arizona, U. S. A.), Dr. N.
Hiratsuka (Tokyo, Japan) and Dr. J. F. Hennen (Purdue University,
MYCOLOGIA,VOL. 65, 1973
442
Lafayette, Indiana, U. S. A.) for critical review of the manuscript and
valuable suggestions.
LITERATURE
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--,
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1968.
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HIRATSUKA:
SPORE STATES IN UREDINALES
443
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Accepted for publicationJune 10, 1972.