Fungal
Reproductive Processes
Mushroom
Sex
The physiological complexity of
the fungi is manifest in their diversity; there are estimated to be 1.5 million
different species of which only about 69,000 have been identified. These statistics are indicative of the
reproductive fecundity of the fungi in initiating and replicating a broad
taxonomy and of the limitations in our understanding of their nature, which
includes the physiology of the reproductive process. While the reproductive processes of the Kingdoms
Plantae and Animalia are well known, the fungi of the Kingdom Eumycota (also
known as Myceteae), are not. Sex refers to the division of living species
according to their reproductive roles, traditionally the female as the guardian
of the egg and the male as the purveyor of the sperm. This dichotomy is very
distinct in animals and to a somewhat lesser extent plants; in a perfect flower
both sexes are represented. Some fungi,
particularly the simpler and more primitive forms, have something more or less
analogous to male and female sexes. However, the more complicated forms like
the basidiomycete mushrooms have a much more complex relationship that involves
multiple combinations of paired individuals whose union results in
reproduction. In order to comprehend mushroom reproduction and attendant
“sexuality”, it is necessary to establish a lexical framework on which to base
the discussion.
The most important aspect of
reproduction is the transmission of the DNA code from one generation to the
next, as it critically establishes speciation and allows for random mutation.
Reproduction is initiated by the union of the male sperm and the female egg in
most animals, the pollen from the male anther and female pistil in (flowering)
plants, and by several variations on the theme; the end result is the same.
Both males and females carry the same number of chromosomes; the number varies
according to species (23 in humans) and is usually denoted simply by the letter
n; the single chromosome set cells are called haploid, derived from the Greek
word for ‘single’. When the two haploids combine, the result is 2n; a
fertilized egg or zygote – also a double haploid or diploid. The zygote, as the
only repository for all of the genetic information of the new organism, must grow
without losing the code. This is accomplished by mitosis, the division of the nucleus into two identical daughter
cells which have the same diploid 2n genetic makeup. The word was derived from
the Greek mitos meaning thread and
the Latin osis meaning process based
on observations of the thread-like chromosomes in the nuclei. As the diploid
nuclei continue to divide, the resultant cells differentiate according to the
established sequence of gene expression, the eventual result a fully grown individual
species. Reproduction of a new individual requires that the diploid 2n cell be
reduced to a haploid n cell in order for it to seek out a haploid cell of the
opposite sex. The reduction of a 2n diploid to an n haploid was termed meiosis, from the Greek meion meaning less and osis, meaning process; since this is a
homonym for mitosis, differentiating them is the pons asinorum of biology
students. With refinements in laboratory methods and instrumentation in the
late 19th Century, it was discovered that meiosis was a two-step
process so that four haploid cells were formed.
In summary, two n or haploid
nuclei combine to produce a 2n diploid which grows from one cell to many with mitosis; the 2n diploid cell reduces to
four n haploid cells by meiosis to
complete the cycle.
The fungi can be divided into two
generalized groups based on their reproductive strategies: sexual and asexual. In the mycological vernacular, sexual fungi
are sometimes referred to as the Fungi Perfecti and asexual as (naturally)
Fungi Imperfecti. On also occasionally finds the asexual fungi referred to as
Deuteromyctes from the Greek word deuesthai,
‘to be in need of’ and mycetes or
fungi, the etymological suggestion is that to be asexual is to need sex. More properly, the sexual fungus is called a teleomorph and the asexual fungus is
called an anamorph. This also makes good etymological sense since
teleo is the Greek word for ‘consummation’ or
‘completeness’ whereas ana means
simply ‘on’ or ‘up’, implying simplicity. Both teleomorphs and anamorphs
produce spores to execute the reproductive function. The sexual spores are
appropriately called teleospores;
they convey a genetic component from two separate parent entities (which really
should not be called male and female). Asexual spores are not called anaspores,
though they probably should be if language were based on logic, but rather mitospores, to indicate that they are
the product of mitotic or asexual division. Another name that one encounters
for asexual spores is conidium, which
comes from the Greek word konis,
meaning dust; these are asexual spores that are formed outside any enclosing
structure. Mushroom sex is complicated.
The anamorphs largely occupy the
netherworld of the Kingdom Eumycota, which is taxonomically comprised of three
phyla. The primitive Phylum Chytridiomycota (one species of chytrid is
responsible for the recent decimation of many amphibian species in Central
America and Australia – the frog die-off) is comprised of species which have
asexual zoospores that move with a whip-like flagellum. The Phylum Zygomycota
is a complex group that includes the bread molds and the soil fungi that are
the predominant in the establishing mycorrhizal relationships with plant roots.
Zygomycetes propagate by both teleospores and mitospores; they are classified
by the unique sexual phase that results from a physical conjugation (the Greek
word for union is zygoma) of two
separate fungi. However, it is the third
and most physically obvious Phylum Dikaryomycota which is comprised of the
cup-like Subphylum Ascomycotina and the true mushroom Subphylum Basidiomycotina
that have the more confusingly exasperating reproductive systems. The
ascomycetes and the basidiomycetes can have both an anamorph and a teleomorph,
in which case the two taken together may be called a holomorph. Some species
exist only as anamorphs, some (so far as is known) exist only as teleomorphs,
and some have part of the life cycle as anamorph and part as teleomorph.
Deciphering the complexities of the holomorph which can involve multiple hosts
and multiple physical forms is a seemingly Sisyphean task, though it has been
worked out for a few species – where there is some agronomic significance. A
case in point is the basidiomycete species Puccinia
graminis subspecies tritici, more
commonly known as wheat rust. The life cycle starts when a teleospore
germinates on a barberry (Berberis),
a popular garden shrub (the Japanese barberry, B. thunbergii has escaped cultivation and become an invasive
species) to form a brown pustule that doesn’t harm the barberry, but which
emits sexual spores that germinate on wheat plants (Triticum) and form anamorphs that create more spores that can cause
massive wheat crop damage by investing acres of (amber waves of) grain. During the late summer, the fungus shifts to
the production of teleospores that are dispersed in search of the barberry.
Because of this, a barberry eradication program was initiated by the U. S
Department of Agriculture in 1918 that continued until 1975, destroying an
estimated 100 million plants. There are likely thousands of holomorphs (an
anamorph and a teleomorph) that have yet to be fully characterized, if even
known to exist. The fungal world is complex.
Since anamorphs are asexual,
there is no question about sex; there is none. When a mitospore comes to rest
in a provident environment, it germinates to create a filamentous tendril
called a hypha (from the Greek hyphos,
meaning web) that grows in what is called the assimilative mode. Assimilation is
the process by which food is changed from the form in which it is found into
the form in which it can be used; it is the fungal equivalent of plant
vegetative growth. As assimilative
growth continues, the bundles of hyphae eventually form a tangled “web” called
a mycelium, which comes from a combination of Greek words that translate
loosely as “folded warty fungus.” In the
case of the fungi, assimilation is most generally in the form of the secretion
of enzymes from the hyphal tip that break down the plant or animal nutrients
into a form that can be used by the fungus for growth. The hypha extends,
becoming ramose to exploit new resources, until the host is invested and growth
ceases. Reproduction occurs when there is sufficient energy available for the
production of spores, and, most importantly, when the food source is depleted.
The process of spore formation among anamorphs is generally straight forward.
In the simplest case, structures called conidiophores grow directly on the
hypha and produce conidia, the mitospores of the anamorph. In some cases, a
simple, specialized spore bearing body called a sporangium will be created. In
either case, prodigious quantities of spores are produced, and this is the key
to the success of the fungi. The
miniscule size of the spore permits airborne transmission over great distances
and their ubiquity helps to ensure that at least one will be successful. For
the asexual anamorphs, this is all that it takes. It is much harder for the
sexual fungi. One may well posit that it makes no sense to invoke the
complexities of sexuality when asexuality is so fecund. It is important to keep
in mind that asexuality brooks very little, if any variation, whereas variation
is the province and provenance of sexuality. Organisms can only evolve to
changing environmental conditions efficiently and effectively only with the
evolution that sexuality provides. And
the environment is always changing.
Sexual reproduction in the dicaryomycotan
fungi is simultaneously very simple and very complicated. According to Nicholas Money in Mr.
Bloomfield’s Garden, “sexual behavior in mushroom-forming fungi spans
monogamy and civility, to group sex and slaughter.” Bryce Kendrick in The
Fifth Kingdom has a more nuanced view in noting that “reproduction in fungi
frequently involves sex, though their sexual behavior is sometimes
obscure.” The hidden sex of spore
producing species has a turbid history; mosses, ferns, algae and fungi were at
one point classified as in a subkingdom called Cryptogamia (literally hidden
life). Before the invention of the microscope, spores were essentially
invisible; the reproduction of any of the cryptogams was accordingly shrouded
in the aura of thaumaturgic intrigue. For example, the absence of
visible seeds in ferns led to some interesting interpretations as to the nature
of fern propagation. As the fern was clearly a plant, then it must have a seed,
and, by syllogistic logic, since the "fern seed" could not be seen,
it was claimed by some early herbalists that it must be invisible. This
ultimately led to a widely held belief that the invisibility of the fern seed
conveyed invisibility to the bearer of the seed, but only if the seeds were
collected at midnight on Midsummer Night's Eve, June 23, also known as the eve
of Saint John, the shortest night of the year.
Mushrooms, whose reproductive mechanisms were even more obscure than
those of the ferns, were seen as even more mysterious, a perspective enhanced
by their seemingly chthonian appearance overnight, sometimes in fairy ring
circles.
The simple part of mushroom
sexuality is that they do not have any specialized sex organs. Any of the
filamentous hyphae can engage in sexual union if approached with a sexually
compatible hypha from another individual. The complicated part is that there
may be many different pairing combinations that are sexually compatible, just
as there will be many that are not. When the hyphae from two incompatible forms
make contact, the result is a fungal battle for territory, the two strains defending their borders with
melanin barriers; trees that are subject to fungal hegemony have patterned wood
whose whorls and shadings afford an aesthetic effect employed by wood carvers. When
the hyphae of two sexually compatible individuals make contact, the
reproductive process begins. The complexity is in the breadth and extent of
sexually compatibility. The multiple sexes of the basidiomycete fungi were
first discovered by the German botanist Karl Johannes Kniep during the First
World War through the evaluation of the fungus Schizophyllum commune, known as the common split gill. The choice
of this fungus was not serendipitous; S.
commune is distributed worldwide and grows throughout the year, a
consequence of its high spore germination rate and its ability to thrive in a
fairly broad range of environmental conditions. Kniep found that, unlike
animals and plants that have one set of genes for each of the male and female
genders, most fungi have two sets of genes which are called ‘mating type factors’;
he called them A and B, a designation that has persisted. Over the last
century, work with S. commune has
revealed that there are about 340 A factors, and 64 B factors, which results in
something like 21,000 possible “sexual” pairings. There have been estimates
made for other fungi, but it should be recognized that the only way to
determine if two types are compatible is to pair them to see what happens, a
daunting and painstaking laboratory assignment. For most mushrooms, the number
of mating factors, or sexes, is a matter of conjecture. It is likely, however,
to be significantly more than two.
So, what happens when two hypha like
each other? They mate. What this means for fungi is that the two hyphae merge
to form a single cell; the union to form into a single cytoplasm is called
plasmogamy. Since each of the two “sexes” are haploid (n), this results in two
nuclei inside one cell (n + n). This is not the same as diploid (2n) because
the nuclei remain distinct and separate. The cell with two different nuclei is
called a dikaryon, from which the Phylum name Dikaryomycota originates; karyon is the Greek word for nut and in
the lexicon of biology, it is the nucleus of a cell. The double nucleus
dikaryon hypha can and does continue to grow by assimilation in a manner that
is one of the most unusual aspects of fungal physiology. The process starts
when each of the two compatible nuclei divides by mitosis, retaining their
haploid genetics so that two of each type is created. One of the nuclei pairs
separates so that one nucleus is at the tip of the hypha and the other, sister
nucleus is at the back. The second nuclei pair also separates, but in this case
one moves into a bulbous growth that protrudes from the side of the hypha while
the other stays behind. As a new cell wall forms between the two sets of nuclei,
the bulbous region clamps onto the hyphal wall on the other side of the septa,
forming what is prosaically called a clamp connection. The clamp connection
opens to allow the two separate nuclei to form an identical dikaryon and then
closes so that at the end of the process there is a dikaryon in each of the two
separated cells. Laboratory observation has revealed that most basidiomycetes
produce a new clamp connection about once every hour and that the mitotic
division that creates the paired nuclei takes about 3 minutes. A sexually
compatible dikaryon can continue to grow using clamp connections indefinitely
as long as there is a nutritive source. Note that a 2n diploid has not yet been
formed and meiosis, and therefore sex, has not yet occurred, just a lot of
foreplay.
When environmental conditions are
amenable for the successful dispersion of the sexually engendered spores, the
reproductive cycle begins. It is the mechanics of the sexual process that
differentiates the Subphylum
Basidiomycotina from the Subphylum Ascomycotina; the former produce 4 spores on
a structure called a basidium and the latter produce 8 spores on a structure
called an ascus; the subphylum names are derived from the names of the two
different spore containments. The conversion of the dikaryon into sexual spores
by meiosis does not occur until the fungus is ready, a determination based on
some means of determining temperature and moisture that registers the
propensity for the spores to germinate if created. In the ascomycetes, the dikaryon undergoes a
nuclear transition from n + n to the diploid 2n which rapidly undergoes meiosis
to create four nuclei that divide by mitosis to create the 8 spores. The
ascomycetes, which include the succulent edible morels and truffles, are mostly
small, brightly colored cups like the Scarlet Cup (Sarcoscypha coccinea) or irregular stalks like the Orange Earth
Tongue (Microglossum rufum); their
taxonomy is established by the manner in which they release their spores from
the ascus.
The basidiomyctes are the largest
and most complex organisms of the Kingdom Eumycota; they are evident for their
visible mushroom fruiting bodies. The reproductive machinations of
basidiomycetes are essentially the same as those of the ascomycetes - a 2n
diploid forms and divides by meiosis to create 4 haploid spores, stopping short
of the final octal mitosis of the ascomycetes. The key difference is that in
the basidiomycetes, a nascent, hypogeal reproductive fruiting body called the
primordium is formed by the mycelium. It is only at the point of reproductive
imminence that meiosis occurs; four club-shaped basidia are produced at the end
of selected hyphae so that each of the four haploid spores will be separately
housed and ready for dispersal. Fungi thus spend almost all of their lives as
haploids contrasted to animals and plants that live almost wholly as diploids The spore producing surface is called
the hymenium; for gilled mushrooms it is on both sides of the adjacent gills,
for mushrooms with pores, it is the surface of the vertical tubes. The fully formed hypogeal mushroom primordium
is now reproductively and physiologically ready to break the surface of the
ground and open to expose its spore laden gills to the winds of chance
dispersion. The impetus for this reproductive consummation is environmental.
Mushrooms make their epigeal appearance soon after a rain as the conditions for
spore germination are likely to be good. They also appear when their food
source is threatened which may occur due to disease, death, fire, or, when that
source is nutritionally depleted. If the spores germinate and find a mate, then
fungal life goes on.