L.11-G.Biology
Mycology
D.Ebtihal Muiz
Rusts and Smuts
Rusts
Rusts are fungi of the order Uredinales (or Pucciniales). Many of
these species are plant parasites. Many of the rusts have two or more
hosts (heteroecious) and up to five spore stages. However, they most
commonly reproduce via asexual spore production. Their spores are
airborne and can travel great distances. They mostly cause foliar
infections. The group received its common name from the fact that some
species have a reddish spore stage, which resembles the corrosion process
known as rust. Rust occurs on many species of plant, but in most cases
any one species of rust can only infect one species of plant.
Rusts at their greatest complexity produce five different types of spores
on two different hosts in two unrelated host families. Such rusts are
heteroecious (requiring two hosts) and macrocyclic (producing all five
spores types). Wheat stem rust is an example.
By convention, the stages and spore states are numbered by Roman
numerals. Typically, basidiospores infect host one and the mycelium
forms pycnidia, called spermagonia, which are miniature, flask-shaped,
hollow, submicroscopic bodies embedded in host tissue (such as a leaf).
This stage, numbered "0," produces single-celled, minute spores that ooze
out in a sweet liquid and that act as nonmotile spermatia and also
protruding receptive hyphae. Insects and probably other vectors, such as
rain, carry the spermatia from spermagonia to spermagonia, cross
inoculating the mating types. Neither thallus is male or female. Once
crossed, the dikaryons are established and a second spore stage is formed,
numbered "I" and called aecia, which form dikaryotic aeciospores in dry
chains in inverted cup-shaped bodies embedded in host tissue. These
aeciospores then infect the second host genus and cannot infect the host
on which they are formed (in macrocyclic rusts). On the second host, a
repeating spore stage is formed, numbered "II," the uredospores in dry
pustules called uredinia. Urediospores are dikaryotic and can infect the
same host that produced them. They repeatedly infect this host over the
growing season. At the end of the season, a fourth spore type, the
teliospore, is formed. It is thicker-walled and serves to overwinter or to
survive other harsh conditions. It does not continue the infection process,
rather it remains dormant for a period and then germinates to form basidia
(stage "IV"), sometimes called a promycelium.
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In the Pucciniales (or Uredinales), the basidia are cylindrical and become
3-septate after meiosis, with each of the four cells bearing one
basidiospore each. The basidospores disperse and start the infection
process on host one again. Autoecious rusts complete their life cycles on
one host instead of two, and microcyclic rusts cut out one or more stages.
Uredinomycetes
Order: Uredinales (Rusts)
This class is composed of a single order of obligate parasites that are
pathogenic to ferns, gymnosperms and flowering plants. Basidiocarps are
not produced in this order and the life cycle is quite different than that of
the Basidiomycetes. In Puccinia graminis (Wheat Rust), the species that
will be used as the representative for this order, there are five spore stages
that are produced and two hosts are required in the completion ofthe life
cyle. The five stages produced are:
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Stage 0:Spermagonium
Stage I: Aecium
Stage II: Uredium
Stage III: Telium
Stage IV: Basidium
As a means of comparing the life cycle of Puccinia graminis with that of
the mushroom life cycle, a summary of the life cycle will begin with the
basidiospore.
Basidium (Stage IV)
Puccinia graminis is heterothallic and basidia produce basidiospores
that are of two mating types, designated as a1 and a2, Basidiospores are
capable of only infecting the leaves of Berberis sp. (barberry), the
alternative host for this species. Species that require two hosts to
complete their life cycles are said to be heteroecious. The cells of the
teliospore germinates to produce a short germ tube that will develop into
a basidium that is essentially transversely septate.
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Figure 1: Basidia and basidiospores are produced
from germinating teliospores. The basidium is very
similar in appearance to the transversely septate
basidia that is present in the Auriculariales of the
Basidiomycetes
Spermogonium (Stage 0)
The spermogonium stage (Fig. 2) produces the sex organs in rusts.
They are produced on the upper surface of the Berberis (barberry) leaf.
Since the spermogonia are derived from basidiospores, they are of two
mating types. They are flasked-shaped and produce spore-like spermatia
which ooze out, from the neck, in a sweet-smelling nectar. Also growing
from the necks are receptive hyphae. The spermogonia are visited by
flies which are attracted by the nectar secretions, and as they visit
different spermagonia, spermatia of both mating types, adhere to their
bodies and are transferred to receptive hyphae of the other mating types.
This begins the dikaryon stage of the life cycle.
Figure 2. The spermogonium stage of Puccinia
graminis forms on the upper surface of the Berberis
leaf. Structure on the lower surface of the leaf is the
aecium, the next spore stage in the life cycle. This
spore stage does not form unless spermatia of one
mating strain fertilize the receptive hyphae of a
different mating strain.
Figure 3: A high magnification of the spermogonium
stage. The spermogonium is flask-shaped. The
spermatia are borne at the base of the spermogonium.
The upright hyphae are the receptive hyphae.
Aecium (Stage I)
The aecium stage is directly linked to the spermagonium stage. When
spermatia are transfered to compatible receptive hyphae, this begins the
dikaryotic stage of the life cycle and directly produces the aecium on the
lower surface of the barberry leaf. The aecium is an upside-down,sac3
shaped structure (Fig. 4)in which chains of aeciospores are formed.The
aeciospores burst through the lower surface of the leaf and are dispersed
by wind.
Figure 4. Aecium stage emerging from the lower surface of
the Berberis leaf. The aeciospores are borne in chains and
are held together by little rectangular cells called
disjunctors.
Uredium (Stage II)
The aeciospores cannot reinfect the barberry host. Instead infection can
only occur on the primary host, Triticum aestivum (wheat), where a new
dikaryotic infection occurs. When two hosts are required in the
completion of a rust life cycle, the rust is said to be heteroecious. The
wheat is said to be the primary host while barberry is said to be the
alternate host. The dikaryons infect the wheat stems and leaves and will
form uredia that contain orange-brown urediospores (Fig. 5). This order
is commonly called the rusts because of the orange-brown (rusty) colored
pustules that form on the wheat plant after the urediospores have broken
through the epidermal surface. The urediospores are comparable to
conidia in that they will reinfect wheat plants and produce more uredia
and ureiospores. This stage begins during summer and continues until late
summer in North America.
Figure 5. A prepared slide showing the rust spores as
they break the host epidermis. This is the repeating
stage of the life cycle and continually reinfects wheat
from early spring to summer.
Telium (Stage III)
Towards the end of summer, the uredium begins to produce
teliospores (Fig. 6), a dark, thick-walled, two celled spore. Teliospores
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do not produce telia! It is the uredium that gradually becomes a telium by
producing more and more teliospores. Because of the color of the
teliospores,the telium is black. Following karyogamy, the teliospore
overwinters. Meiosis takes place in each cell of the teliospore, in
spring,and germinates to form the promycelium (=basidium). The
promycelium becomes transversely septate, forming four cells. Each cell
produce a sterigma and a basidiospore, and this now completes the life
cycle.
Figure 6. Teliospores, on the wheat plant. The
teliospores are dark, two celled, thick walled spores.
These spores overwinter before producing the
basidiospore stage.
Comparison of the Puccinia graminis and mushroom life cycle
The monokaryon derived from the basidiospore, in the rusts, are
heterothallic as in the mushroom life cycle. However, the dikaryon phase
and its formation, in the life cycle of the rusts, is extended and more
complex in comparison:
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In the rusts, the monokaryons, derived from germination of
basidiospore, produce sex organs, i.e. spermogonium with
spermatia and receptive hyphae.The monokaryons in the
mushroom life cycle does not produce sex organs and fusion takes
place between hyphal cells of compatible monokaryons.
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The dikaryon of the rusts produces three spore stages:
aeciospore,urediospore and teliospore, with a change in host from
barberry to wheat following the aecium stage. The dikaryon in the
mushroom life cycle does not produce additional spore stages prior
to basidia and basidiospore formation unless an asexual stage is
present, in which case conidia are produced.
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Basidiocarp formation is absent in the rusts.
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Smuts
Smuts (mostly Ustilaginomycetes of the class Teliomycetae) cause
plant disease, and commonly affect grasses, notably including cereal
crops such as maize. They initially attack the plant's reproductive system,
forming galls which darken and burst, releasing fungal spores which
infect other plants nearby.
The characteristic part of the life cycle of smuts is the thick-walled, often
darkly pigmented, ornate, teliospore, which serves to survive harsh
conditions such as overwintering and also serves to help disperse the
fungus as dry diaspores. The teliospores are initially dikaryotic but
become diploid via karyogamy. Meiosis takes place at the time of
germination. A promycelim is formed that consists to a short hypha
(equated to a basidium).
In some smuts, such as Ustilago maydis, the nuclei migrate into the
promycelium that becomes septate, and haploid yeast-like
conidia/basidiospores (sometimes called sporidia) bud off laterally from
each cell. In various smuts, the yeast phase may proliferate, or they may
fuse, or they may infect plant tissue and become hyphal. In other smuts,
such as Tilletia caries, the elongated haploid basidiospores form apically,
often in compatible pairs that fuse centrally resulting in "H"-shaped
diaspores, which are by then dikaryotic. Dikaryotic conidia may then
form. Eventually, the host is infected by infectious hyphae. Teliospores
form in host tissue. Many variations on these general themes occur.
Smuts with both a yeast phase and an infectious hyphal stage are
examples of dimorphic Basidiomycota. In plant parasitic taxa, the
saprotrophic phase is normally the yeast, while the infectious stage is
hyphal. However, there are examples of animal and human parasites
where the species are dimorphic but it is the yeast-like state that is
infectious. The genus Filobasidiella forms basidia on hyphae, but the
main infectious stage is more commonly known by the anamorphic yeast
name Cryptococcus (e.g., Cryptococcus neoformans and Cryptococcus
gattii).
The dimorphic Basidiomycota with yeast stages and the pleiomorphic
rusts are examples of fungi with anamorphs, which are the asexual stages.
Some Basidiomycota are only known as anamorphs. Many are yeasts,
collectively called basidiomycetous yeasts to differentiate them from
ascomycetous yeasts in the Ascomycota. Aside from yeast anamorphs,
and uredinia, aecia, and pycnidia, some Basidiomycota form other
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distinctive anamorphs as parts of their life cycles. Examples are Collybia
tuberosa, with its apple-seed-shaped and colored sclerotium;
Dendrocollybia racemosa, with its sclerotium and its Tilachlidiopsis
racemosa conidia; Armillaria, with their rhizomorphs; Hohenbuehelia,
with their Nematoctonus nematode infectious, state; and the coffee leaf
parasite, Mycena citricolor and its Decapitatus flavidus propagules called
gemmae
Ustomycetes
Order: Ustilaginales (Smuts)
This class is composed of several orders, but we will only consider
the order Ustilaginales. Species in this order are composed entirely of
fungi that are parasitic on flowering plants. However, unlike the rusts, the
smuts are not obligate parasites throughout its entire life cycle. Only the
dikaryon stage is obligately parasitic. The monokaryon stage, which is
yeast, is saprobic. Thus, they are dimorphic. There are not many species
of smuts that occur in Hawaii. Two species that are relatively common
are: Ustilago cynadontis, Bermuda Grass Smut (Fig. 1) and U. maydis,
Corn Smut (Fig. 2).
Figure 1: Ustilago cynadontis, Bermuda Grass Smut.
The black powdery spores are the teliospores It is this
dirty, powdery stage that led to this group of fungi
being called smut.
Figure 2: Ustilago maydis, the Corn Smut. This
species can be found where corn is grown in Hawaii.
The Ustilaginales is similar to the rusts in two significant characteristics:
both lack a basidiocarp, during sexual reproduction and produce their
basidia from germinating teliospores. However, the smuts do not have sex
organs nor do they produce multiple spore stages as is the case of the
rusts.
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The life cycle is simple and more similar to the Basidiomycetes. We will
describe the life cycle of Ustilago maydis, the corn smut, as an explane of
a smut life cycle. There are, it should be noted that there are several
variations of life cycle.
Following dispersal of the basidiospores, the spores typically germinate
by budding to produce yeast cells, which are saprobic. When the yeast
cells contact a compatible mating strains, dikaryon formation will occur.
Once the dikaryon has formed, it becomes an obligate parasite and must
have a host. Once in the host, the mycelial cells become rounded and
break apart to give rise to the thick-walled teliospore stage.
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