International Journal of Medicinal Mushrooms, Vol. 7, pp. 79–101 (2005)
© 2005 by Begell House, Inc. 79
Principles of Mushroom Developmental Biology
Faculty of Life Sciences, e University of Manchester, Manchester, UK
Address all correspondence to D. Moore, Faculty of Life Sciences, e University of Manchester, 1.800 Stopford Building,
Oxford Road, Manchester M13 9PT, UK; firstname.lastname@example.org
ABSTRACT: Research done over the last century has persistently indicated major diﬀ erences between
fungi, animals, and plants. Unfortunately, for most of that time fungi have been considered, quite errone-
ously, to be closely related to plants; as observations have been constrained to comply with this funda-
mental error, a proper appreciation of fungal developmental biology has been seriously inhibited. During
the ﬁ nal quarter of the 20 century, the phylogenetic status of the true fungi as an independent Kingdom
of eukaryotes became clear. In this review, I bring together some of the observations, old and recent, that
contribute to our current understanding of the way that fungi construct multicellular structures.
KEY WORDS: morphogenesis, fungi, tissues, fruit bodies, cell interactions, morphogens, diﬀ erentia-
GUI: graphical user interface; PCD: programmed cell death
Development is formally deﬁ ned as the process of
change and growth within an organism during the
transition from embryo to adult. is deﬁ nition im-
mediately illustrates a major challenge faced by any
mycologist interested in development, which is the
speciﬁ cation of “embryo”—reﬂ ecting the fact that
most developmental biologists deal with animal
systems. e challenge occurs because the con-
cepts and vocabulary of development derive mostly
from animal embryology and reﬂ ect the interactive
behavior of animal cells. Plants have made some
contribution to theoretical developmental biology,
which is ﬁ tting for organisms with cell biology so
diﬀ erent from that of animals, but there is no par-
allel representation of fungal development. is is
an unfortunate deﬁ ciency, given that fungi diﬀ er so
much from both animals and plants.
I should stress that I am referring speciﬁ cally to
the poor contribution made by studies of multicel-
lular development in fungi (the true analogue of ani-
mal embryology). ere is an irony in the fact that so
much of what we know about eukaryotic molecular
cell biology, cell structure, and the cell cycle derives
from work with yeast. In many ways this creates a
false sense of satisfaction for mycologists, but very
little of this knowledge has a real bearing on fungal
morphogenesis, even though those interested in
the yeast/ﬁ lamentous transition, in particular, use
the word and write conﬁ dently about hyphal “mor-
phogenesis” (Harris et al., 1999; Gancedo, 2001;
Mösch, 2002; Warenda and Konopka, 2002; Seiler
and Plamann, 2003).
is verges on being a misnomer for the reason
that what they describe would be called cell diﬀ eren-
tiation in any other organism. e word morphogen-
esis is generally used to encompass the development
of the body form of a multicellular animal or plant
(fungi do not feature in such deﬁ nitions!). e key
80 International Journal of Medicinal Mushrooms
problems in morphogenesis have always related to
the interactions between cells from which the pat-
ternings of cell populations arise and from which
the morphology of the embryo emerges.
Regrettably, it is still often necessary to remind
people that fungi are not plants. Indeed, this simple
biological fact is not explicitly included in any of the
curriculum speciﬁ cations used now, in 2004–2005,
as the basis for teaching science to students up to
the age of 16 in schools in the United Kingdom.
Consequently, there are a great many people, young
and old alike, who, if they ever do think about it at
all, will be ﬁ rmly convinced that fungi are plants.
Peculiar plants, perhaps, but plants nevertheless. is
notion, of course, is completely wrong.
Plants, animals, and fungi should now be clearly un-
derstood to form three quite distinct Kingdoms of eu-
karyotic organisms (Whitaker, 1969; Margulis, 1974,
1992; Cavalier-Smith, 1981, 1987, 2002; Margulis
and Schwartz, 1982). is arrangement is reﬂ ected in
current ideas about the early evolution of eukaryotes,
in which the major Kingdoms are thought to have
separated at some protistan level (Moore, 1998, Chap.
1; Feoﬁ lova, 2001; Margulis, 2004).
A major aspect of the original deﬁ nition of the
Kingdoms (Whitaker, 1969) was their means of
nutrition (plants use radiant energy, animals engulf
food particles, fungi absorb digestive products), and
this apparently simple basis for separation embraces
numerous correlated diﬀ erences in structure and life
style strategy. Other noncorrelated diﬀ erences also
emerge, and among these is the way in which multi-
cellular architectures can be organized. Even in lower
animals, a key feature of embryo development is the
movement of cells and cell populations (Duband
et al., 1986; Blelloch et al., 1999); evidently, cell
migration (and everything that controls it) plays a
central role in animal morphogenesis. Being encased
in walls, plant cells have little scope for movement,
and their changes in shape and form are provided
for by control of the orientation and position of
the mitotic division spindle and, consequently, the
orientation and position of the daughter cell wall,
which forms at the spindle equator (Gallagher and
Fungal cells are also encased in walls, of course;
but their basic structural unit, the hypha, has two
peculiarities requiring that fungal morphogenesis be
totally diﬀ erent from plant morphogenesis. ese
are that a hypha grows only at its apex (Bartnicki-
Garcia, 2002; Momany, 2002), and that cross walls
form only at right angles to the long axis of the
hypha (Harris, 2001). e consequence of these
features is that no amount of cross wall formation
(cell division) in fungi will turn one hypha into two
hyphae (Fıeld et al., 1999; Howard and Gow, 2001;
Momany, 2001; Momany et al., 2001). e funda-
mentally crucial understanding that shows fungal
developmental morphogenesis to be distinct from
both animals and plants is that fungal morphogen-
esis depends on the placement of hyphal branches.
To proliferate, a hypha must branch; and to form the
organized structure of a tissue, the position at which
the branch emerges and its direction of growth must
Origin of Kingdom Fungi
Arranging organisms into kingdoms is a matter of
systematics; an agreed-upon scheme of categoriz-
ing the estimated 13–14 million species currently
thought to be alive on this planet. Yet the three-
Kingdoms arrangement of animals, fungi, and plants
is a natural classiﬁ cation that reﬂ ects the current
thinking about the early evolution of eukaryotes
(Margulis, 2004). is is an interesting story that
bears repetition, if only to provide some context for
the discussion that follows. e solar system formed
about 4.5 × 10⁹ years ago. ere are microbial fos-
sils in terrestrial rocks that are 3.5 × 10⁹ years old.
Life might have evolved even before that time, but
calculations based on study of craters on the Moon
suggest that the Earth/Moon system was subjected
to gigantic asteroid impacts up to about 3.8 × 10⁹
years ago. ese impacts were suﬃ ciently massive to
release enough energy to heat-sterilize the Earth’s
surface. Any life that had evolved in those more
distant times would have been destroyed by the
Volume 7, Issues 1&2, 2005 81
MUSHROOM DEVELOPMENT BIOLOGY
Once these cataclysmic impacts stopped and
the Earth’s surface stabilized suﬃ ciently for life
to evolve, the ﬁ rst bacteria-like fossils would have
been laid down (Knoll, 2003). After this, there
was a period of 1.5 × 10⁹ years during which early
bacteria continued to evolve before the higher or-
ganisms emerged. Eukaryotes and eubacteria last
shared a common ancestor about 2 × 10⁹ years ago
(Knoll, 1992; Gupta and Golding, 1996). In the
present day about 60 lineages of eukaryotes can be
distinguished on the basis of cellular organization
(Patterson, 1999). Most of these are traditionally
classiﬁ ed as protists, but one lineage comprises
green algae and plants and two others animals and
fungi, and these three major eukaryotic kingdoms
diverged from one another about 1 × 10⁹ years after
the appearance of the eukaryotic cell (Knoll, 1992;
Philippe et al., 2000).
Our understanding of eukaryote phylogenetic
relationships is not yet complete (Knoll, 1992;
Cavalier-Smith, 1993; Kuma et al., 1995; Kumar
and Rzhetsky, 1996; Sogin et al., 1996; Katz, 1998;
Sogin and Silberman, 1998; Katz, 1999; Roger,
1999). Recent discussion has stressed the importance
of the symbiotic partnership between phototrophs
and fungi in early colonization of the land, protein
sequence comparisons indicating that major fungal
and algal lineages were present one billion years
ago (Heckman et al., 2001). Animals and fungi
are more directly related, however. It is generally
agreed that the Metazoa and choanoﬂ agellates
(collar- ﬂ agellates) are sister groups, and that these,
together with the fungi and chytrids, form a single
lineage called the opisthokonts. is name opistho-
kont (Copeland, 1956) refers to the posterior (opis-
tho) location of the ﬂ agellum (kont) in swimming
cells. e term was applied to the (animals + fungi)
clade (Cavalier-Smith and Chao, 1995) because
comparative molecular analysis has indicated that
fungi and animals are each other’s closest relatives
(Baldauf and Palmer, 1993; Wainright et al., 1993;
Sogin and Silberman, 1998; Baldauf, 1999; Patterson
and Sogin, 2000).
So it seems that plants diverged ﬁ rst, and the pro-
gression that emerges is that plants arose from the
common eukaryotic ancestor 1 × 10⁹ years ago, then
a joint fungal/animal line continued for another 200
million years until that lineage diverged 800 million
years ago (Berbee and Taylor, 1993; Doolittle et al.,
1996; Sugiyama, 1998; Berbee and Taylor, 1999).
Recognizable fungi must have been around as
long ago as that, because from rocks only a few
hundred million years younger—about 570 million
years old—there is evidence in the form of fossil
spores for all the major groups of fungi that exist
today (Pirozynski, 1976a,b; Kalgutkar and Sigler,
1995). And it is quite clear that fungi were crucially
important in the shaping of ancient ecosystems. e
oldest fossils found to date (which are about 650
million years old) have been suggested to be lichens
rather than worms or jellyﬁ sh (Retallack, 1994).
Although this is a hotly disputed interpretation,
intimate associations between fungi and plants oc-
curred very early in evolution (Pirozynski, 1981).
Almost all land plants of today form cooperative
mycorrhizal associations with fungi, which con-
tribute to the mineral nutrition of the plant and
can beneﬁ t plants in a variety of other ways. is
cooperation would have eased, if not solved, some
of the most diﬃ cult problems the ﬁ rst land plants
faced as they emerged from the primeval oceans.
Some of the oldest (about 400 million year old)
plant fossils contain mycorrhizal structures almost
identical to those that can be seen today (Harvey et
al., 1969; Wright, 1985; Hass et al., 1994; Taylor et
al., 1995; Heckman et al., 2001). It is now generally
thought that the initial exploitation of dry land by
plants about 430 million years ago depended on the
establishment of cooperative associations between
fungi and algae on the one hand (as lichens), and
between fungi and emerging higher plants (forming
mycorrhizas) on the other.
An even more radical interpretation is that the
oldest terrestrial fossils were actually saprotrophic
fungi. e oldest terrestrial fossils we have are made
up of masses of thread-like and tube-like structures.
ey are called nematophytes, the name being derived
from the Greek nema, which means thread, com-
bined with phyte because of the belief when they
were originally found that they were plants in origin.
Nematophyte fossils started in rocks more than 450
million years old, and, in terms of both abundance
and diversity, they were important components of
the Earth’s terrestrial ecosystems for the best part
82 International Journal of Medicinal Mushrooms
of 100 million years, from the Ordovician to the
early Devonian geological periods. ey included
by far the largest organisms in early terrestrial
ecosystems; some specimens of a nematophyte
genus called Prototaxites have been reported to be
over one meter wide and to reach heights of 2–9
meters. ese fossils are now being reinterpreted,
following developments in chemical analysis that
suggest that their walls were not composed of the
sorts of chemicals you would expect in plant cell
walls. As a result, it has been claimed that some
of the nematophytes (including Prototaxites) were
terrestrial fungi or lichens, creating the possibility
that the earliest terrestrial organisms were fungal,
some being far larger than any known today (Gray,
1985; Wellman, 1995; Selosse and Le Tacon, 1998;
Wellman and Gray, 2000; Hueber, 2001; Selosse,
2002; Southwood, 2003).
Origins of Developmental Biology
Whatever the nature of these extremely early organ-
isms, it is evident that the major kingdoms separated
from one another at some unicellular level of orga-
nization. is being the case, it follows that plants,
animals, and fungi became distinct from one another
long before the multicellular grade of organization
was established in any of them. ey will, of course,
share all those features that clearly categorize them
as eukaryotes, but there is no logical reason to
expect that these three Kingdoms will share any
aspect of their multicellular developmental biology.
If evolutionary separation between the major King-
doms occurred at a stage prior to the multicellular
grade of organization, then these Kingdoms must
have “learned” how to organize populations of cells
independently. e fungal hypha diﬀ ers in so many
important respects from animal and plant cells that
signiﬁ cant diﬀ erences in the way cells interact in the
construction of organized tissues must be expected.
Inevitably, in many cases these very diﬀ erent
organisms needed to solve the same sorts of mor-
phogenetic control problems and may have found
some common strategies. Comparison of the way
similar functions are controlled can reveal whether
and how diﬀ erent cellular mechanisms have been
used to solve common developmental demands
(Meyerowitz, 1999), although, of course, fungi are
not discussed. However, there are now suﬃ cient
ﬁ lamentous fungal genomes in the public sequence
databases to warrant direct sequence comparisons
with animal and plant genomes, and a recent search
of ﬁ lamentous fungal genomes with gene sequences
generally considered to be essential and highly
conserved components of normal development in
animals failed to reveal any homologies (Moore et
Data Mining Fungal Genomes
is initial survey attempted to establish whether
fungal multicellular development shows any closer
relationship to that of animals than to that of plants
by searching ﬁ lamentous fungal genomic databases
for sequences demonstrating similarity to develop-
mental gene sequences. e phylogenetic logic of
this approach is that it is not unreasonable to argue
that the opisthokonts evolved basic strategies for
dealing with cellular interactions prior to their di-
vergence, and that evidence of this might be found
in present day genomes in the form of similarities
between sequences devoted to tasks that can be
deﬁ ned broadly as “developmental.” is survey
concentrated on cell/cell signaling because it is es-
sential for many morphogenetic processes ranging
from developmental patterning to the regulation of
cell proliferation and cell death.
Sequences of the animal signaling mechanisms
Wnt, Hedgehog, Notch, and TGF-β were used to
search the Basidiomycetes Coprinus cinereus (syn. Co-
prinopsis, Redhead et al., 2001) and Ustilago maydis
(Anon, 2003a,b) at the Whitehead Institute’s Centre
for Genome Research; Cryptococcus neoformans (up-
date of 29/4/03) at TIGR; Phanerochaete chrysospo-
rium at the Department of Energy’s (DOE) Joint
Genome Institute; and the ascomycetes Aspergillus
nidulans (Anon, 2003c) and Neurospora crassa (Ga-
lagan et al., 2003), also at the Whitehead Institute’s
Centre for Genome Research; and Aspergillus fu-
migatus at TIGR. ese form a representative and
accessible collection of tissue-making ascomycete
and basidiomycete ﬁ lamentous fungal genomic
Volume 7, Issues 1&2, 2005 83
MUSHROOM DEVELOPMENT BIOLOGY
databases that are ﬁ nished or nearing completion.
ese genomes were searched for homologues of
Caenorhabditis elegans sequences involved in the sig-
naling mechanisms Notch, TGF-β, Wnt (including
the MOM and POP genes), and also a Hedgehog
sequence from Drosophila melanogaster (as C. elegans
lacks a Hedgehog homologue), but all were found
to be absent from the seven query fungi, just as they
are absent from plants (Moore et al., 2005).
Plants have their own highly developed signaling
pathways, one of which is the ethylene perception
and signal transduction system, which is carried out
by a family of membrane-bound receptors of which
ETR1 and ESR1 are members (Muller-Dieckmann
et al., 1999; Zhao et al., 2002; Stearns and Glick,
2003). Again, however, no substantive similarities
were returned by a search of fungal genomes using
the Arabidopsis thaliana ETR1 and ESR1 sequences,
suggesting that fungi also lack anything related to
the plant hormone ethylene-signaling pathway
(Moore et al., 2005).
Lack of homologies leads to the conclusion that
fungal and animal lineages diverged from their com-
mon opisthokont line well before the emergence of
any multicellular arrangement, and that the unique
cell biology of ﬁ lamentous fungi has caused control
of multicellular development in fungi to evolve in a
radically diﬀ erent fashion from that in animals and
plants. I must emphasize that this was an initial
survey. e conclusion must be moderated by the
recognition that the sequence databases are not yet
comprehensive. e fact that 41% of the predicted
proteins of the Neurospora crassa genome have been
shown to lack signiﬁ cant matches to known proteins
from public databases (Galagan et al., 2003) indi-
cates that the database deﬁ ciencies are not minor.
Nevertheless, we have embarked upon what we
intend to be a fully comprehensive data-mining ex-
ercise using Internet web robots (Meškauskas, 2005).
Preliminary results indicate that of 547 polypeptide
sequences assigned to the category “development”
(deﬁ ned as biological processes speciﬁ cally aimed
at the progression of an organism over time from
an initial condition—e.g., a zygote, or a young
adult—to a later condition—e.g., a multicellular
animal or an aged adult—only 37 sequences are
shared among all three kingdoms, 14 are shared
only between fungi and animals, two sequences are
shared between plants and fungi, and one sequence
was fungus speciﬁ c (Meškauskas, personal com-
munication). ese observations contribute to the
idea that fungi have more aﬃ nity with the animal
kingdom than with the plants.
We plan to extend the comprehensive search into
DNA genome databases. However, it must be ap-
preciated that the scales of some of the diﬀ erences
reﬂ ect the relative amounts of research done with
the three kingdoms. It will be many years before the
library of available genomes is suﬃ ciently representa-
tive for the sort of survey described above to be truly
complete. Until we achieve this, we have to proceed
with the incompletely supported proposition that
molecular control of fungal developmental biology
is fundamentally diﬀ erent from that of animals or
plants, and enquire into the rules that may apply. I
will start consideration of this aspect by describing a
recent mathematical model of hyphal growth, called
the Neighbour-Sensing model, and a Java™ com-
puter program realization of it that together gener-
ate extremely realistic visualizations of ﬁ lamentous
hyphal growth (Meškauskas et al., 2004a,b).
Computer Simulations with Cyberfungi
e Neighbour-Sensing model brings together
the basic essentials of hyphal growth kinetics into
a vector-based mathematical model in which the
growth vector of each virtual hyphal tip is calculated
at each iteration of the algorithm by reference to
the surrounding virtual mycelium. Kinetic hyphal
growth equations relate hyphal length, number of
branches, and growth rate, and incorporation of
the inﬂ uence of external factors on the direction
of hyphal growth and branching (i.e., tropisms)
provides us with a cyberfungus that can be used for
experimentation on the theoretical rules governing
e Neighbour-Sensing model employs a variety
of tropisms by incorporating mathematical represen-
tations of the nature of the signal, its propagation
through the medium, and its attenuation; the math-
ematical model deals with these as abstractions.
In the Neighbour-Sensing program, each hyphal
84 International Journal of Medicinal Mushrooms
tip is an active agent, described by its 3D position,
length, and growth vector, that is allowed to vector
within 3D data space using rules of exploration
that are set (initially by the experimenter) within
the program. ose Neighbour-Sensing rules are
the biological characteristics. ey start with the
basic kinetics of in vivo hyphal growth, include
branching characteristics (frequency, angle, posi-
tion), and, through the tropic ﬁ eld settings, involve
interaction with the environment. A graphical user
interface (GUI) written into the Java™ realization
of the Neighbour-Sensing model makes adjustment
of the parameters an easy operation for even the
casual user of the program, but the experimenter
does not deﬁ ne the geometrical form of the outcome
of a Neighbour-Sensing program run—it is not a
painting program. Rather, the ﬁ nal geometry must
be reached by adapting the biological characteris-
tics of the active agents during the course of their
growth—exactly as in life.
e program starts out with just one hyphal tip,
which is equivalent to the fungal spore. Each time
the program runs through its algorithm, the tip ad-
vances by a growth vector (initially set by the user)
and may branch (with an initial probability set by
the user). e Neighbour-Sensing model “grows” a
simulated mycelium in the computer using branch-
ing rules decided by the user and calculates every-
thing else it needs to generate a mycelium. As the
cyberhyphal tips grow out into the modeling space,
the model tracks where they’ve been, and those
tracks become the hyphal threads of the cybermy-
celium. ese simple features (or parameters), in
which direction of growth is random, are suﬃ cient
to result in a spherical colony (circular if growth is
restricted to a ﬂ at plane). So the ﬁ rst conclusion of
the modeling experiments is that the characteristi-
cally circular colony of fungi does not need to be
contrived; it is a natural outcome of the exploratory
apical growth of fungi.
Real fungi, however, do not grow in random di-
rections. Real hyphal tips grow in accordance with
their reactions to the eﬀ ects of one or more tropisms.
In this mathematical model of hyphal growth, the
growth vector of each virtual hyphal tip depends
upon values derived from its surrounding virtual
mycelium. Eﬀ ectively, the mathematics allows
the virtual hyphal tip to sense the neighbouring
mycelium, which is why it is called the Neighbour-
Sensing model. Tropisms are implemented using
the concept of a ﬁ eld to which growing hyphal tips
react. In the real physical world, the ﬁ eld might be
an electrical ﬁ eld for a galvanotropism, the Earth’s
gravitational ﬁ eld for a gravitropism, or a chemi-
cal diﬀ usion gradient for a chemotropism. In the
mathematical model, the same basic ﬁ eld equations
can be used for all, the diﬀ erent tropisms being dis-
tinguished by the diﬀ erent physical characteristics
ascribed to the ﬁ eld.
e published model features seven tropisms: (1)
negative autotropism, based on the hyphal density
ﬁ eld; (2) secondary long-range autotropism (that
attenuates with either direct or inverse proportional-
ity to the square root of distance); (3) tertiary long-
range autotropism, which attenuates as rapidly as
the negative autotropism but can be given a large
impact value; (4) and (5) two galvanotropisms based
on the physics of an electric ﬁ eld produced by the
hypha that is parallel to the hyphal long axis; (6) a
gravitropism, which orients hyphae relative to the
vertical axis of the user’s monitor screen; and (7)
a horizontal plane tropism, which provides a way
of simulating colonies growing in or on a substra-
tum such as agar or soil by imposing a horizontal
geometrical constraint on the data space the cyber-
hyphal tips can explore. e user can determine how
strongly the hyphal tips are limited to the horizontal
plane and the permissible layer thickness.
ese features form the parameters of the model,
and all are under the control of the user via the
GUI. e Neighbour-Sensing model provides the
user with a set of abstract mathematical tools that
amount to a culture of a newly arrived fungus. e
rate of growth of the cyberfungus is user decided,
depending only on the power of the user’s com-
puter. It is possible to do more experiments in an
afternoon’s computing than can be done in a year
in the laboratory.
e Neighbour-Sensing model has been used in
a series of experiments (Meškauskas et al., 2004b) to
show that complex fungal fruit body shapes can be
simulated by applying the same regulatory functions
to all of the growth points active in a structure at any
speciﬁ c time—the shape of the fruit body emerges
Volume 7, Issues 1&2, 2005 85
MUSHROOM DEVELOPMENT BIOLOGY
as the entire population of hyphal tips respond to-
gether, in the same way, to the same signals.
e signiﬁ cant observation here is that no global
control of fruit body geometry is necessary, so the
important phrase in the previous sentence is that
“the shape of the fruit body emerges.” is is entirely
an outcome of the apical growth pattern of fungal
hyphae. All of the parameter sets that generate
shapes reminiscent of fungal fruit bodies feature
an organized series of changes in parameter settings
applied to all of the hyphal tips in the simulation.
In the real biological system, such morphogenetic
programs could be based on internal clocks of some
sort that synchronize behavior across a developing
structure on the basis of time elapsed since some
ese computer simulations demonstrate that
because of the kinetics of hyphal tip growth, very
little regulation is required to generate fungal fruit
body structures. Our next challenge is to establish
whether observations of living fungi can provide
guidance about the biological processes that might
Observations of Real Fungi
e ﬁ rst important point to make is that fungi
are modular organisms, like clonal corals and
vegetatively propagated plants, in which growth is
repetitive and a single individual will have local-
ized regions at very diﬀ erent stages of development
(Harper et al., 1986; Andrews, 1995). e general
developmental rules may be applicable to all multi-
cellular structures (indeed, that is the basis on which
the comparison is made), but it is important to keep
this fundamental nature of the organisms in mind
when attempting to apply the principles of pattern
formation and morphogenesis derived from animal
models, where the embryos are individual whole or-
ganisms rather than fruit bodies.
It is also essential to emphasize that most re-
search concerning observations on fungal anatomy
and development has been done in order to clarify
taxonomic diﬀ erences (Watling and Moore, 1994;
Clémençon, 1997, 2004). is has been necessary
because fungal classiﬁ cation has been based on the
shape and form of the spore-producing tissue—the
hymenium—and on the hymenophore—the struc-
ture on which the hymenium was borne—since the
classiﬁ cation was ﬁ rst developed at the beginning
of the 19 century (Persoon, 1801; Fries, 1821).
Shape was not a factor in driving plant or animal
classiﬁ cation during the 20 century, but it remained
dominant in fungal classiﬁ cation until the last quar-
ter of the 20 century. e traditional classiﬁ cation
scheme is now being challenged by use of molecular
methods to establish relationships and, it must be
said, by more detailed microscopical analyses started
by Reijnders (1948, 1963) and now hugely contrib-
uted to by Clémençon (2004).
e traditional classiﬁ cation scheme is the one
that most of us know. We know about agarics that
have gills (vertical plates) beneath an umbrella-
shaped cap (pileus), as in the ordinary cultivated
mushroom. But it has emerged that this single group
is actually a collection of organisms with very diverse
evolutionary origins. e feature that unites them
(the fact that their spore forming tissues are ampli-
ﬁ ed by being distributed over the plate-like gills)
is one to which there are several evolutionary and
e function of the mushroom fruit body (ba-
sidiome) is to produce as many basidiospores as the
structure will allow. Reijnders’ (1948, 1963) careful
observation of developing basidiomes revealed that
there are at least ten ways by which the familiar
mushroom shape can be formed, a shape that is ex-
cellently designed to give protection to the develop-
ing hymenia in exposed environments (Watling and
Moore, 1994). ese vary from those with naked
development, which includes the majority of the
bracket fungi developing from a concentration of
tightly bound hyphae forming a rounded structure
(known to foresters as a conk) to those with a com-
plete enclosing membrane or membranes that only
break just before maturity. Importantly, relationships
between species based on the type of development
conform to classiﬁ cation schemes based on other
features (Reijnders and Stalpers, 1992; Watling and
e veils formed by agarics are considered to be
protective; they allow the hymenia to develop in
a sheltered environment that is controlled by the
86 International Journal of Medicinal Mushrooms
organism itself. e shape of the gills is strongly
tied to the constraints of this environment within
the developing basidiome and has led to the use
in identiﬁ cation of gill attachment, which is how
the gill is attached to the stem (stipe) apex. At
least eight types of attachment have been used
and are now undergoing analytical examination
ere is a large group of fungi that have their
basidiospores enclosed in the basidiome, even when
mature. ey are generally called Gasteromycetes and
include puﬀ balls, earthstars, and earth-balls, all
adapted into the form of an epigeous or hypogeous
sack of spores. Basidiomycetous hypogeous fungi,
as with their ascomycete cousins the truﬄ es, have
a distinctive odor to attract animals to excavate the
buried fruit body and distribute spores while eating
it. Indeed, hypogeous fungi form a major propor-
tion of the nutrition of many small mammals and
consequently make a crucial contribution to food
webs in nature (an example is described by Molina
et al., 2001). e stinkhorns are also included along-
side the gasteromycetes. ese parallel the agarics
in gross morphology, although their hymenium is
adapted for insect dispersal as opposed to wind
dispersal, and they also produce penetrating odors
to attract insects. e shape of the stinkhorns is
highly specialized, with similarities to the bizarre
shapes and strong smells of insect-attracting ﬂ ow-
e similarities in shapes found in these groups
are again, as in the agarics, derived from convergent
evolution from several diﬀ erent ancestral positions.
e similarity in shape and ecological function does
not signify unity of relationship; rather, it represents
an evolutionary goal at which diverse lineages have
arrived (Reijnders, 2000).
A similar conclusion is reached when the detailed
cellular structure involved in growth to maturity is
considered. Fruit body structure can be expanded in
several ways to optimize spore production. For ex-
ample, in the Russulales, this is achieved as columns
and rosettes of hyphae expanding in an orchestrated
way are accompanied in Coprinus (= Coprinopsis)
by narrow, uninﬂ ated hyphae (Reijnders, 1976;
Hammad et al., 1993a,b). In their distribution
these narrow hyphae resemble the inducer hyphae
of Russula and Lactarius (Reijnders, 1976; Watling
and Nicoll, 1980). In the Amanitas, the mode of
gill formation is unusual (being schizohymenial),
and this diﬀ erence correlates with the unusual way
that individual cells of hyphae of the ﬂ esh undergo
massive inﬂ ation to cause the fruit body to expand
is description of tissue construction in mush-
rooms and toadstools, called hyphal analysis, was
introduced by Corner (1932a,b, 1966) (Redhead,
1987; Ryvarden, 1992). Hyphal analysis is entirely
descriptive, and the only quantitative study pub-
lished is that done by Hammad et al. (1993a,b),
who showed that enumerating cell types at diﬀ erent
stages of development (in the fruit bodies of Copri-
nopsis cinereus) is a powerful way of revealing how
fruit body structure emerges during morphogenesis
as a result of changes in hyphal type and distribution.
Previous to this study, mushroom structure has been
measured in terms of fruit body height, cap diameter,
and diameter of the stem.
Ingold (1946) and Bond (1952) used published
illustrations of a wide range of agarics to extract
graphical relationships between these features, ar-
riving at the conclusion that smaller fruit bodies
have proportionately longer and more slender stems.
Watling (1975) established a diﬀ erent graphical rep-
resentation for the Bolbitiaceae, using measurements
from fresh specimens. He pointed out faults with
the earlier work, which depended on selective use
of published collections of illustrations.
We should be wary of generalizations from
combined measurements of diﬀ erent species. But
morphological measurements are valuable and have
practical value. ey have been used to deﬁ ne the
“normal” mushroom for the Agaricus bisporus crop
(Flegg, 1996), and image analysis of shape, form, and
color of A. bisporus can be related statistically to crop
development (van Loon et al., 1995). e practical
value of such approaches is that they contribute to
the design of control methods for machine automa-
tion of crop picking.
From the conceptual point of view, measuring
and counting cells in diﬀ erent regions of fruit bodies
at diﬀ erent stages of development reveals speciﬁ c
patterns of cell diﬀ erentiation (particularly inﬂ a-
tion), which mechanically generate the ﬁ
Volume 7, Issues 1&2, 2005 87
MUSHROOM DEVELOPMENT BIOLOGY
of the fruit body. A common feature that emerges
is that in most fungal tissues there is a repetitive
substructure comprising a central hypha (which
remains hyphal) and an immediately surround-
ing family of hyphae that diﬀ erentiate in concert.
ese hyphal aggregations were identiﬁ ed and
termed hyphal knots by Reijnders (1977, 1993). e
indications are that the central hypha induces the
diﬀ erentiation of its surrounding family. If this is
the case, then any control exerted by morphogens
must be imposed on the central induction hypha
that may not diﬀ erentiate itself, but simply relay
the message to its dependent family. is two-stage
process may inﬂ uence the physical characteristics of
the morphogen(s), but it might also inﬂ uence their
number. If the induction hyphae determine the
terminal diﬀ erentiation of their surrounding fam-
ily, the morphogen(s) may simply need to instruct
a diﬀ erentiation process to occur, without deﬁ ning
the nature of that diﬀ erentiation. e latter might
be determined by local environmental, physical, or
e patterns revealed show that positional infor-
mation is regulated in time and space and strongly
suggest that patterning in fungal tissues is organized
by signaling molecules. Attempts to determine the
nature of the signals used in fungi have been initi-
ated (Novak Frazer, 1996); oddly enough, with very
few exceptions, compounds detected on the basis of
morphogenetic bioassays prove to be unexceptional
components of normal intermediary metabolism
when puriﬁ ed. It is a moot point whether this ex-
perience indicates that fungi actually make use of
metabolic intermediates as morphogens, or whether
fungal morphogens are so exquisitely sensitive that
they are lost during all the puriﬁ cation procedures
so far attempted.
Plasticity in Form
Clearly, fungal systematists are now appreciating
that fruit body shape should not hold the central
position it once did. One reason it is less useful is
that it is proving to be a more ﬂ exible character
than previously thought. Variation in basidiomycete
fruit body morphology in response to environmental
change is easily demonstrated. Bondartseva (1963)
was the ﬁ rst to warn against placing too much taxo-
nomic emphasis on a single character for this reason.
In fact, plasticity in the shape and form of fruit
bodies arising on a particular strain can be caused
by a variety of events.
Many morphological mutants or genetic vari-
ants have been induced or isolated from nature,
especially in Coprinus (= Coprinopsis) cinereus and
Schizophyllum commune (Raper and Krongelb,
1958; Takemaru and Kamada, 1972; Kanda and
Ishikawa, 1986; Kanda et al., 1989). Such mutants
can be used to establish developmental pathways
(Esser et al., 1977; Moore, 1981) and to make
detailed studies of particular phenotypes (Ka-
mada and Takemaru, 1977a,b; Kanda et al., 1990;
Boulianne et al., 2000; Lu et al., 2003). Fruiting
is a complex multigene process in these fungi (De
Groot et al., 1997), which is further modulated by
environmental factors (Leslie and Leonard, 1979,
1984; Manachère et al., 1983; Meinhardt and Esser,
1983; Prillinger and Six, 1983; Raudaskoski and
Salonen, 1984; Manachère, 1985, 1988; Leatham
and Stahmann, 1987; Moore, 1998; Kües, 2000;
Kües and Liu, 2000; Kües et al., 2002; Han et al.,
2003; Sánchez, 2004).
ere is some evidence for genetic mosaics in
Armillaria fruit bodies (Peabody et al., 2000), for
genetically diﬀ erent multiple initiation pathways
(Leslie and Leonard, 1979) and, conversely, for
diﬀ erent structures (speciﬁ cally sclerotia and ba-
sidiomes) sharing a common initiation pathway
(Moore, 1981). Fruiting in haploid, primary ho-
mothallic species, such as Volvariella bombycina and
V. volvacea (Chang and Yau, 1971; Chiu and Chang,
1987; Royse et al., 1987) and in homokaryons in het-
erothallic species (Uno and Ishikawa, 1971; Elliott,
1972, 1985; Stahl and Esser, 1976; Dickhardt, 1983;
Graham, 1985) shows that fruiting is independent
of the sexual cycle regulated by the incompatibility
system in heterothallic species (Kües and Casselton,
1992; Kronstad and Staben, 1997; Casselton and
Olesnicky, 1998; Kües et al., 1998; Chiu and Moore,
1999; Kües and Liu, 2000; Brown and Casselton,
2001; Kothe, 2002). Basidiome variants must be in-
terpreted against this background of quite diverse
genetic control mechanisms.
88 International Journal of Medicinal Mushrooms
Epigenetic plasticity is possibly more interesting
from the developmental point of view. ese are
instances where, for some reason, the development of
a normal genotype is disturbed, but without change
to that genotype (Steimer et al., 2004).
is sort of plasticity in fruiting morphogenesis
may be a strategy for adaptation to environmen-
tal stress. e rose-comb disease of the cultivated
mushroom, Agaricus bisporus, in which convoluted
growths of hymenium develop over the outer surface
of the cap, seems to be caused by mineral oil volatiles
in mushroom farms (Lambert, 1930; Flegg, 1983;
Flegg and Wood, 1985). Viral infections have been
implicated in some instances—e.g., in Laccaria, Ar-
millaria, and Inocybe (Blattny et al., 1971, 1973), and
fungal attack in others. For example, Buller (1922)
showed that gill-less fruit bodies of Lactarius pipera-
tus were caused by parasitism by Hypomyces lactiﬂ uo-
rum, and Watling (1974) showed that primordia of
Entoloma abortivum can be converted to a puﬀ -ball
structure by interaction with Armillaria mellea.
Fruit body polymorphism or developmental plas-
ticity like this has been reported in various fungal
species (Buller, 1922, 1924; Keyworth, 1942; Singer,
1975; van der Aa, 1997), but thorough studies have
only been made on Psilocybe merdaria (Watling, 1971;
Reijnders, 1977), Agaricus bisporus (Worsdell, 1915;
Atkins, 1950; Reijnders, 1977; Flegg and Wood,
1985) and Volvariella bombycina (Chiu et al., 1989).
e developmental variants reported include ster-
ile fruit bodies (carpophoroids), forked fruit bodies
(where a single stem carries two or more caps), ad-
ditional secondary caps arising from the cap tissues
(= proliferation), bundles of joined basidiomes (=
fasciation), and fruit bodies bearing supernumerary
hymenia on the upper surface of the pileus.
In Volvariella bombycina, these teratological forms
arose spontaneously in two diﬀ erent strains and
were found in cultures bearing normal fruit bod-
ies, regardless of the composition of the substrate.
Importantly, all hymenia in these forms were func-
tional in the sense that they produced apparently
normal basidiospores. e function of the plasticity
in fruiting morphogenesis seems to be to maximize
spore production and favor dispersal of spores, even
under environmental stress. e spore production
pathway can tolerate major errors in other parts of
the developmental process.
Tropic responses can be considered, quite rea-
sonably, to be an aspect of epigenetic plasticity.
Tropisms involve directed growth. eir study is
consequently relevant to developmental biology
because they can show how particular shapes can
arise and how growth can be regulated by varying
the expression of the genotype. More importantly,
tropisms allow experimental study of these develop-
mental processes. e tropic signal can be repeated
as often as needed to accumulate statistically valid
observations. Equally, the tropic signal can be at-
tenuated or ampliﬁ ed to study the sensitivity of
perception and reaction, and the experiment can
be adapted to any observational technique.
Hymenomycete mushroom fruit bodies (polypore
and agaric) exhibit a number of tropisms, of which
anemotropism, gravitropism, phototropism, and
thigmotropism have been clearly demonstrated
(Moore, 1991, 1996). At any one time, one tropism
usually predominates, but the inferior tropisms can
be demonstrated, and during the course of develop-
ment of a fruit body diﬀ erent tropisms predominate
at diﬀ erent times. Gravitropism is the easiest of these
to work with. e gravitational ﬁ eld is all pervasive
and penetrates everything, so detailed growth ex-
periments can be done with the experimental tissue
without damage (Moore et al., 1996).
e stem of Coprinopsis cinereus became gravi-
receptive after completion of meiosis, implying ei-
ther some communication between cap and stem
or a synchronized timing mechanism (Kher et al.,
1992). Stem bending began within 30 minutes of
being placed horizontal, although experiments
with clinostats showed that the minimum time of
stimulation required to elicit a gravitropic reaction
was 9.6 min (Hatton and Moore, 1992, 1994). Re-
moval of large segments of the apical part of the
stem of Coprinopsis cinereus (extending to about
half its length) did not diminish the ability of the
stem to show gravitropic bending, but response
time was directly proportional to the amount of
stem removed, which might imply that the apex
produces a morphogenetic signal needed for the
Volume 7, Issues 1&2, 2005 89
MUSHROOM DEVELOPMENT BIOLOGY
Mechanical stress is unlikely to contribute to
gravi tropic bending because application of lateral
loads of up to 20 g had no adverse eﬀ ects on ad-
justment of the stem to the vertical (Greening et
al., 1993). In both Flammulina and Coprinopsis,
gravity perception seems to be dependent on the
actin cytoskeleton because cytochalasin treatment
suppresses gravitropic curvature in Flammulina, and
in Coprinus signiﬁ cantly delays curvature without
aﬀ ecting stem extension. is, together with altered
nuclear motility observed in living hyphae during
reorientation, suggests that gravity perception in-
volves statoliths (probably nuclei) acting on the
actin cytoskeleton and triggering speciﬁ c vesicle/
microvacuole release from the endomembrane sys-
tem (Moore et al., 1996).
Stem bending in Coprinopsis cinereus results
from diﬀ erential enhancement of growth rate
in the cells in the outer ﬂ ank of the bend. ere
were no signiﬁ cant diﬀ erences in hyphal diameter,
distribution, or populations of cell types, but cells
of the outer ﬂ ank were 4–5 times longer than those
of the inner. us tropic bending requires only an
increase in length of preexisting hyphal cells in
the outer ﬂ ank tissue (Greening et al., 1997). An
interesting observation is that large voids, up to
85 µm in diameter, occurred only in bent stems.
It is thought that such voids may prevent the
propagation of cracks through the stem tissue
during bending (Greening et al., 1997). eir
occurrence, however, shows that the gravitropic
morphogenetic program is rather more complex
than simply arranging that cells at the bottom grow
more rapidly than those at the top. In itself, that
may be diﬃ cult enough to arrange, but in addition
the program includes features that preserve the
structural integrity of the tissue as the stresses to
which it is subjected change drastically (Moore et
Basidiome developmental variants can be used to
comment on the ontogenetic program. Because they
are actually or potentially functional as basidiospore
production and dispersal structures, they have been
interpreted as indicating that normal fruit body
development comprises a sequence of independent
but coordinated morphogenetic subroutines, each of
which can be activated or repressed as a complete en-
tity (Moore, 1988, 1998; Chiu et al., 1989; Watling
and Moore, 1994; Moore et al., 1998).
For example, there is a “hymenium subroutine”
that, in an agaric, is normally invoked to form the
“epidermal” layer of the hymenophore (gill lamella);
but if it is invoked aberrantly on the upper surface
of the cap, it forms not a chaotic travesty of a hy-
menium but a functional proliferated hymenium.
Similarly, the “hymenophore subroutine” produces
the classic agaric form when invoked on the lower
surface of the pileus, but if wrongly invoked on the
upper surface, it produces not a tumorous growth
but a recognizable inverted cap.
Normal development of fungal structures in gen-
eral is thought to depend upon organized execution
of such subroutines. e sequence and location in
which they are invoked determines the normal
developmental pattern (ontogeny) and normal
morphology of the fruiting structure. Invocation of
these developmental subroutines may be logically
equivalent to the “code switches” between diﬀ erent
mycelial states discussed by Gregory (1984) and
Rayner and Coates (1987). Some of the subrou-
tines can be identiﬁ ed with speciﬁ c structures, such
as basal bulb, stem, cap, hymenophore, hymenium,
and veil, but others are rather subtle, aﬀ ecting posi-
tional or mechanical morphogenetic features. One
such might be a “grow to enclose” capability, pos-
sibly associated primarily with the veil subroutine
but perhaps expressed in the stipe base to generate
so-called “pilangiocarpic” basidiomes.
Essentially the same subroutines could give rise
to morphologically very diﬀ erent forms, depend-
ing on other circumstances. For example, the agaric
gill hymenophore subroutine seems to be expressed
with the rule “where there is space, make gill” (Chiu
and Moore, 1990a,b). When this is combined with
mechanical anchorages the contortions initially
produced by this rule are removed as the gills are
stretched along the lines of mechanical stress when
the fruit body expands during maturation (Moore,
1998). It is this mechanical process that produces
the ﬁ nal morphology.
90 International Journal of Medicinal Mushrooms
Regional Patterns and Commitment
Fungi, like animals and plants, have a basic “body
plan,” which is established very early in development.
Tissues are demarcated in even the earliest fruit
body initials. e processes of regional speciﬁ cation,
cell diﬀ erentiation, and cell coordination essentially
establish the pattern sequentially. It is likely that
all of these are orchestrated by morphogens and/or
growth factors, although there is no direct evidence
for the existence of morphogens in the diﬀ erentiat-
ing fruit body primordium.
However, the distributions of cystidia and gills
in Coprinus cinereus have been interpreted as being
dependent on the interplay between activating and
inhibiting “morphogen” factors (Horner and Moore,
1987; Moore, 1988) in a pattern-forming process
similar to the model developed by Meinhardt and
Gierer (1974, 1980) and Meinhardt (1984, 1998).
Successful application of this morphogenetic ﬁ eld
model to fungi as well as to plants and animals con-
centrates attention on the fact that the distribution
of stomata on a leaf, bristles on an insect, and cystidia
on a fungal hymenium have a great deal in common
at a fundamental mechanistic level. In other words,
these examples are expressions of general rules of
pattern formation that will apply similarly to all
Other similarities emerge when a search for
commitment is made. e classic demonstration of
commitment used in animal embryology involves
transplanting a cell into a new environment. If the
transplanted cell continues the developmental path-
way characteristic of its origin, then it is said to have
been committed prior to transplantation. On the
other hand, if the transplanted cell embarks upon the
pathway appropriate to its new environment, then it
was clearly not committed at the time of transplant.
Most fungal tissues produce vegetative hyphae very
rapidly when disturbed and “transplanted” to a new
“environment” or medium. is is a regenerative
phenomenon that itself creates the impression that
fungal cells express little commitment to their state
of diﬀ erentiation.
Very little formal transplantation experimenta-
tion has been reported with fungal multicellular
structures. e clearest examples of commitment
to a developmental pathway has been provided by
Bastouill-Descollonges and Manachère (1984) and
Chiu and Moore (1988), who demonstrated that
basidia of isolated gills of Coprinus congregatus and
Coprinopsis cinereus, respectively, continued develop-
ment to spore production if removed to agar medium
at early meiotic stages. Other hymenial cells, cystidia,
paraphyses, and tramal cells immediately reverted
to hyphal growth, but this did not often happen to
immature basidia. Evidently, basidia are speciﬁ ed ir-
reversibly as meiocytes, and they become determined
to complete the sporulation program during meiotic
prophase I. Once initiated, the maturation of basidia
is an autonomous, endotrophic process that is able
to proceed in vitro.
Clearly, then, these experiments demonstrate
commitment to the basidium diﬀ erentiation path-
way some time before the diﬀ erentiated phenotype
arises in these fungi. It is also important to stress
that other cells of the hymenium do not show
commitment. Rather, they immediately revert to
hyphal growth on explantation as though they
have an extremely tenuous grasp on their state of
diﬀ erentiation. at these cells do not default to
hyphal growth in situ implies that some aspect of
the environment of the tissue that they normally
inhabit somehow continually reinforces their state
of diﬀ erentiation. ese uncommitted cells must
be considered to be totipotent stem cells. It is this
uncommitted state of diﬀ erentiation of most of the
cells in mushroom fruit bodies that accounts for the
readiness of ﬁ eld-collected mushrooms to revert to
vegetative growth when fragments are inoculated
to culture medium.
Mycologists expect as a matter of common rou-
tine to be able to make cultures in this way, using
the simplest media, from fruit bodies they collect.
No animal or plant ecologist can expect to be able to
do this. e diﬀ erence denotes a signiﬁ cant quality
of fungal cell diﬀ erentiation.
Cell Form, Function, and Lineage
In the hymenium of Agaricus the “epidermal pave-
ment” that provides the structural support for basidia
is made up of basidioles (= young basidia) in an ar-
Volume 7, Issues 1&2, 2005 91
MUSHROOM DEVELOPMENT BIOLOGY
rested meiotic state. Even after many days’ existence,
when the fruit body is close to senescence, 30–70%
of the basidioles were in meiotic prophase (Allen
et al., 1992). is is not wastage of reproductive
potential but use of one diﬀ erentiation pathway to
serve two distinct but essential functions.
Coprinus (as Coprinopsis) illustrates the other
extreme by using a highly diﬀ erentiated cell type,
which is called a “paraphysis,” to construct the epi-
dermal pavement. ese cells arise after the numeri-
cally static basidiole population commits to meiosis.
Paraphyses arise as branches from beneath the ba-
sidia and force their way into the hymenium (Rosin
and Moore, 1985). At maturity, individual basidia
are surrounded by about ﬁ ve paraphyses; thus, more
than 80% of the hymenial cells in Coprinus serve a
structural function. Agaricus and Coprinus hymeno-
phore tissues reach essentially the same structural
composition by radically diﬀ erent routes.
Other cell lineages reach the same ﬁ nal morphol-
ogy through diﬀ erent routes. Both Coprinus cinereus
and Volvariella bombycina have facial (pleuro-) and
marginal (cheilo-) cystidia. Both types of cystidium
in V. bombycina are established when the hymenium
is ﬁ rst laid down on the folded gills, and, apart from
location, their diﬀ erentiation states and ontogeny
appear to be identical. Facial cystidia in Coprinus
cinereus are also established as components of the
very ﬁ rst population of dikaryotic hyphal tips, which
form hymenial tissue and are mostly binucleate as a
result (Rosin and Moore, 1985; Horner and Moore,
1987). Marginal cystidia in C. cinereus are the apical
cells of branches from the multinucleate gill trama,
which become swollen to repair the injury caused
when primary gills pull away from the stipe; mar-
ginal cystidia retain the multinucleate character of
their parental hyphae (Chiu and Moore, 1993).
e “decisions” made during development be-
tween diﬀ erent pathways seem to be made with
a degree of uncertainty, as though they are based
on probabilities rather than absolutes. For example,
facial cystidia of C. cinereus are generally binucle-
ate, reﬂ ecting their origin and the fact that they are
sterile cells, yet occasional examples can be found
of cystidia in which karyogamy has occurred or of
cystidia bearing the sterigmata usually found only
on basidia (Chiu and Moore, 1993). is suggests
that entry to the cystidial pathway of diﬀ erentiation
does not totally preclude expression of at least part
of the diﬀ erentiation pathway characteristic of the
basidium. Equally, the fact that a large fraction of the
basidiole population of Agaricus bisporus remains in
arrested meiosis indicates that entry to the meiotic
division pathway does not guarantee sporulation
(Allen et al., 1992). ere are many other examples
in the literature.
ese many examples suggest that fungal cells
behave as though they assume a diﬀ erentiation
state even when all conditions for that state have
not been met. Rather than rigidly following a pre-
scribed sequence of steps, diﬀ erentiation pathways in
fungal fruit bodies generally appear to be based on
application of rules that allow considerable latitude
in expression. It is another aspect of the tolerance of
imprecision referred to above (Moore et al., 1998).
It has been described as a system showing opera-
tion of “fuzzy logic” (Moore, 1998), an extension of
conventional (Boolean) logic that can handle the
concept of partial truth, that is truth values between
“completely true” and “completely false.” It is the
logic underlying modes of decision making that are
approximate rather than exact, being able to handle
uncertainty and vagueness and has been applied to
a wide variety of problems. Decision making in the
real world is characterized by the need to process
incomplete, imprecise, vague or uncertain informa-
tion—the sort of information provided by error-
prone sensors, inadequate feedback caused by losses
in transmission, excessive noise, etc. e importance
of fuzzy logic derives from the fact that the theory
provides a mathematical basis for understanding
how decision making seems to operate generally in
nature (Zadeh, 1996; Leondes, 1999).
Degeneration, Senescence, and Death
In the other two major eukaryotic Kingdoms it is
clear that death is an important aspect of biology.
Removal of old individuals makes way for the young
and allows populations to evolve, and in recent years
programmed cell death (PCD) has been recognized
as a crucial contributor to morphogenesis in both
animals and plants.
92 International Journal of Medicinal Mushrooms
PCD is the removal of tissue in a manner con-
trolled in time and position. ere are two types of
cell death: traumatic or necrotic death and apoptosis
or programmed cell death. In higher animals, PCD
involves a sequence of well-regulated processes, in-
cluding synthetic ones, which lead to internal cell
degeneration and eventual removal of the dying
cell by phagocytosis. It is important that apoptotic
elimination of cells is intracellular in higher ani-
mals to avoid escape of antigens and the consequent
danger of an immune response to components of
the animal’s own cells (autoimmunity). is is not
a consideration in plants and fungi. e most obvi-
ous example of fungal PCD is the autolysis that
occurs in the later stages of development of fruit
bodies of many species of Coprinus, which Buller
(1924, 1931) interpreted as an integral part of fruit
body development (autolysis removes gill tissue
from the bottom of the cap to avoid interference
with spore discharge from regions above). Autolysis
involves production and organized release of a range
of lytic enzymes (Iten, 1970; Iten and Matile, 1970),
so autolytic destruction of these tissues is clearly a
programmed cell death.
Umar and Van Griensven (1997b, 1998) have
found that cell death is a common occurrence in
various structures starting to diﬀ erentiate—for
example, the formation of gill cavities in Agaricus
bisporus. e authors emphasize that speciﬁ c tim-
ing and positioning deﬁ nitely imply that cell death
is part of the diﬀ erentiation process. Fungal PCD
could play a role at many stages in development
of many species (Umar and van Griensven, 1998).
In several examples detailed by these authors, the
program leading to cell death involves the sacriﬁ ced
cells overproducing mucilaginous materials, which
are then released by cell lysis. In autolysing Copri-
nus gills, the cell contents released on death contain
heightened activities of lytic enzymes. Evidently, in
fungal PCD, the cell contents released when the
sacriﬁ ced cells die could be specialized to particular
functions as well. Individual hyphal compartments
can be sacriﬁ ced to trim hyphae to create particular
tissue shaping. It seems, therefore, that PCD in fungi
is used to sculpture the shape of the fruit body from
the raw medium provided by the hyphal mass of the
fruit body initial and primordium.
Only one experimental study of fungal fruit body
longevity has appeared. Umar and Van Griensven
(1997a) grew the cultivated mushroom in artiﬁ cial
environments that protected the culture from pests
and diseases, and under these conditions they found
that the life span of fruit bodies of Agaricus bisporus
was 36 days. Aging was ﬁ rst evident in fruit bodies
about 18 days old, when localized nuclear and cyto-
plasmic lysis was seen. Remnants of lysed cells ag-
gregated around and between the remaining hyphal
cells. Eventually, most of the stem hyphae became
empty cylinders, although other cells within the fruit
body collapsed irregularly. Electron microscopy of
specimens 36 days old and older showed most of
the cells in the fruit body to be severely degenerated
and malformed. Nevertheless, a number of basidia
and subhymenial cells were alive and cytologically
intact even on day 36.
Post-harvest physiology and morphology of
mushrooms is a prime marketing concern and has
been extensively studied. Post-harvest behavior
is usually described as senescence or as an aging
process, but Umar and Van Griensven (1997a) em-
phasize that the morphological changes that occur
in naturally senescent and post-harvest fruit bodies
of A. bisporus are diﬀ erent. e harvested mushroom
has suﬀ ered a traumatic injury, and its post-harvest
behavior derives from that. In harvested A. bisporus
fruit bodies (stored under various conditions), dif-
fuse cell wall damage was observed ﬁ rst and was only
later accompanied by cytoplasmic degeneration. A
major factor must be inability to replace water lost
by evaporation. Exposed surfaces become desiccated
and are damaged ﬁ rst. us, in what might be called
a “post-harvest stress disorder,” further damage is
inﬂ icted on the cell inwards, from the outside.
In complete contrast, during the senescence
that accompanies normal aging, the damage starts
inside the cell and proceeds outwards. e nuclear
and organelle genomes suﬀ er ﬁ rst, then cytoplasmic
integrity, and ﬁ nally cell wall damage occurs as an
aspect of the eventual necrosis suﬀ ered as the cell
Even in severely senescent fruit bodies Umar and
Van Griensven (1997a) found healthy, living cells,
and these are presumably the source of origin of an
unusual phenomenon known as “renewed fruiting.”
Volume 7, Issues 1&2, 2005 93
MUSHROOM DEVELOPMENT BIOLOGY
Fıeld-collected fruit body tissues of a mushroom
usually generate abundant vegetative hyphae when
inoculated onto nutrient agar plates. But there ap-
pears to be some sort of “memory” of the diﬀ eren-
tiated state in these vegetative cells. Initial hyphal
outgrowth from gill lamellae usually at ﬁ rst mimics
the densely packed branching and intertwined hyphal
pattern of the gill tissues from which it is emerging,
and is quite unlike the pattern of normal vegetative
hyphae in culture. e idea of some sort of memory
is not necessarily very exotic in cell biological terms.
It need be no more than the residual expression of
diﬀ erentiation-speciﬁ c genes (such as the hydropho-
bins, Wessels, 1994a,b, 1996) before their products are
diluted out by continued vegetative growth.
Renewed fruiting, though, is more than just a
diﬀ erent vegetative mycelium. Entirely new crops of
fruit bodies may appear on the remains of the old.
Formation of fruit bodies directly on fruiting tissue
is not uncommon, and it can occur at various loca-
tions (cap, stem, and/or gills) in improperly stored
excised fruit bodies. Experiments in vitro show
that numerous primordia can arise on excised fruit
body tissues and can mature into normal, although
miniature, fruit bodies. In comparison to vegetative
cultures, the excised fruit body tissues form fruit
bodies very rapidly. For example, in Coprinopsis
cinereus, renewed fruiting occurred within 4 days,
compared with 10–14 days for cultures inoculated
with vegetative dikaryon (Chiu and Moore, 1988;
Brunt and Moore, 1989).
Renewed fruiting may have an important role in
survival, consuming and immediately recycling the
resource in the dying fruit body tissue to disperse
further crops of spores. For experimentalists it may
be more important that renewed fruiting provides an
excellent experimental system for the study of fruit
body morphogenesis (Bourne et al., 1996), especially
for bioassay of fruiting modulators such as heavy
metal pollutants like cadmium (Chiu et al., 1998).
PRINCIPLES OF MUSHROOM
In many fungi hyphae diﬀ erentiate from the veg-
etative form that ordinarily composes a mycelium
and aggregate to form tissues of multihyphal struc-
tures. ese may be linear organs (that emphasize
parallel arrangements of hyphae) such as strands,
rhizomorphs, and fruit body stems; or globose
masses (that emphasize interweaving of hyphae)
such as sclerotia, fruit bodies, and other sporulating
structures of the larger Ascomycota and Basidiomy-
cota. Fungal morphogenesis depends on a series of
principles, most of which diﬀ er from both animals
• Principle 1. e fundamental cell biology of
fungi on which development depends is that
hyphae extend only at their apex, and cross walls
form only at right angles to the long axis of the
• Principle 2. Fungal morphogenesis depends on
the placement of hyphal branches. Increasing the
number of growing tips by hyphal branching is
the equivalent of cell proliferation in animals and
plants. To proliferate, the hypha must branch,
and to form an organized tissue, the position of
branch emergence and its direction of growth
must be controlled.
• Principle 3. e molecular biology of the man-
agement of cell-to-cell interactions in fungi is
completely diﬀ erent from that found in animals
• Principle 4. Fungal morphogenetic programs are
organized into developmental subroutines, which
are integrated collections of genetic information
that contribute to individual isolated features of
the program. Execution of all the developmental
subroutines at the right time and in the right
place results in a normal structure.
• Principle 5. Because hyphae grow only at their
apex, global change to tropic reactions of all the
hyphal tips in a structure is suﬃ cient to generate
basic fruit body shapes.
• Principle 6. Over localized spatial scales coordi-
nation is achieved by an inducer hypha regulating
the behavior of a surrounding knot of hyphae
94 International Journal of Medicinal Mushrooms
and/or branches (these are called Reijnders’
• Principle 7. e response of tissues to tropic
signals and the response of Reijnders’ hyphal
knots to their inducer hyphae, coupled with
the absence of lateral contacts between fungal
hyphae analogous to the plasmodesmata, gap
junctions and cell processes that interconnect
neighbouring cells in plant and animal tissues
suggest that development in fungi is regulated
by morphogens communicated mainly through
the extracellular environment.
• Principle 8. Fungi can show extremes of cell
diﬀ erentiation in adjacent hyphal compart-
ments even when pores in the cross wall appear
to be open (as judged by transmission electron
• Principle 9. Meiocytes appear to be the only
hyphal cells that become committed to their
developmental fate. Other highly diﬀ erentiated
cells retain totipotency—the ability to gener-
ate vegetative hyphal tips that grow out of the
diﬀ erentiated cell to reestablish a vegetative
• Principle 10. In arriving at a morphogenetic
structure and/or a state of diﬀ erentiation, fungi
are tolerant of considerable imprecision (= ex-
pression of fuzzy logic), which results in even the
most abnormal fruit bodies (caused by errors in
execution of the developmental subroutines) still
being able to distribute viable spores, and poorly
(or wrongly-) diﬀ erentiated cells still serving a
• Principle 11. Mechanical interactions inﬂ uence
the form and shape of the whole fruit body as
it inﬂ ates and matures, and often generate the
shape with which we are most familiar.
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