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BEN # 177



                                                   
BBBBB    EEEEEE   NN   N             ISSN 1188-603X
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BBBBB    EEEEE    NN N N             BOTANICAL
BB   B   EE       NN  NN             ELECTRONIC
BBBBB    EEEEEE   NN   N             NEWS

No. 177                              November 21, 1997

aceska@freenet.victoria.bc.ca        Victoria, B.C.
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 Dr. A. Ceska, P.O.Box 8546, Victoria, B.C. Canada V8W 3S2
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SEQUESTRATE BEN - IT STARTED WITH MACOWANITES

On October 11 and 12, 1997, the South Vancouver Island Mycologi-
cal  Society  organized  a mushroom foray to the Pacific Rim Na-
tional Park near Tofino, British  Columbia.  With  the  help  of
mushroom  experts  (Bryce  Kendrick,  Paul Kroeger, Ian Gibbson,
Oluna Ceska, Tony Trofimow, et al.) we compiled a list of  about
140  mushroom  species.  One  of  the most interesting finds, at
least for me, was Macowanites chlorinosmus.

Macowanites looks like Russula that has never made  it:  an  un-
opened  ball  with  contorted  gills  inside. Dr. Bryce Kendrick
explained to us that Macowanites is a member  of  the  so-called
sequestrate  fungi  (also  called  secotioid or gastroid fungi),
mushrooms that follow the example of truffles and remain  buried
underground,  or  grow  close  to  the  soil surface. They don't
release their spores, but rely on animals  for  spreading  their
spores around.

I  asked  Dr.  Bryce  Kendrick to write me a short note on these
mushrooms for BEN, and he sent me two articles that he published
in McIlvainea. I read these articles and realized that  a  short
note  would  not  do  justice to those interesting fungi. I have
decided to post them in full and the next three  issues  of  BEN
(177, 178, and 179) will be fully devoted to this topic.

I  apologize  to all of you who believe that mushrooms really do
not belong to the botanical realm. I will post these BEN  issues
in  short  intervals of two or three days. This will ensure some
degree of continuity, and at the same time, it won't  fill  your
mail  boxes  entirely.  I  hope  you will enjoy this sequestrate
diversion. - Adolf Ceska


EVOLUTION IN ACTION: FROM MUSHROOMS TO TRUFFLES? PART 1
From: Dr. Bryce Kendrick <mycolog@pacificcoast.net>

[Kendrick, B. 1994.  Evolution  in  action:  from  mushrooms  to
   truffles. I. McIlvainea 11 (2): 34-38.]

The  fungi  are very old. Their history extends over hundreds of
millions of years. Yet their origins, and the major evolutionary
pathways they have followed, are still cloaked in mystery.  This
is largely because the fossil record of the fungi is fragmentary
and  disconnected. Organisms that live on land, and particularly
such ephemera as most  fungal  fructifications,  are  much  less
likely  to  be  fossilized  than  are marine organisms with hard
parts. The paucity of  fossil  evidence  has  not  deterred  the
cognoscenti  among  mycologists from a little judicious specula-
tion, inevitably based largely on what we know about fungi  that
are  alive  today.  This  speculation  is probably wrong in many
respects and is usually heavily laced with the prejudices of its
authors, but it is not necessarily a bad thing: students of  the
fungi  need  a conceptual framework on which to cut their teeth,
and at which to aim their more mature  criticisms.  But  we  are
still  on shaky ground when we try to look into the evolutionary
history of most modern fungi.

It is, then, all the more  exciting  to  encounter  an  area  of
mycology  in  which  not only the results of evolution, but also
the starting points, and the steps in the process, can still  be
seen  in  living  organisms.  And  all this has happened, not in
obscure microscopic fungi, but in conspicuous and fairly  common
mushrooms that can be held in the hand and compared. We now know
that  some  mushrooms  have  given rise to radically changed but
still viable descendants: relatives which, although often  look-
ing  very  different  from their forebears, clearly betray their
ancestry at the microscopic and molecular level. Let us see  how
this  has happened in the well-known and easily recognized mush-
room genus  Lactarius  (the  "milky-caps":  family  Russulaceae,
order Agaricales).

But  before I describe the exciting changes we have seen, I must
establish a base-line or starting point by describing how  mush-
rooms  usually  develop,  and  what  they do: how their form and
function are  interrelated.  First,  the  thread-like  mycelium,
which  permeates  the  soil and is often involved in an intimate
and mutually beneficial mycorrhizal association with tree roots,
must accumulate  considerable  reserves  of  food  energy.  Then
conditions  of  temperature  and  moisture  must  be favourable.
Finally, the mushroom begins its development underground,  form-
ing  a  clump  of mycelium which differentiates into a "button,"
then rapidly expands upward and emerges  from  the  earth  as  a
characteristic  structure with a central stalk or stipe, bearing
an expanding circular cap or pileus.  The  top  of  the  cap  is
covered  by  a skin or cutis. The thin, plate-like gills of Lac-
tarius normally develop in  a  neat  radial  pattern  (like  the
spokes  of  a wheel) on the under side of the expanding cap. The
basidiospores will form on these gills. As  the  cap  opens  out
like  an  umbrella, the gills assume a precise vertical orienta-
tion and are now ready to make and liberate spores.

The flat surfaces of the gills are covered by  a  fertile  layer
called  a  hymenium. This contains huge numbers of special cells
called basidia, which produce and liberate astronomical  numbers
of  spores.  Each  basidium  bears  four spores (sometimes more,
occasionally fewer). These develop asymmetrically, in an  offset
manner,  at  the tips of four sterigmata, which are tiny projec-
tions from the mother cell. When ripe, the spores are delicately
but deliberately launched into the air between the  gills.  They
float  slowly  and  gently  downward  until they emerge from the
gills, and are then carried away like dust by air  movement.  In
this  way  the  fungus  broadcasts  its spores far and wide. The
different genera and  families  of  agarics  often  follow  sig-
nificantly  different  developmental  pathways,  some with gills
exposed from the beginning, others with  gills  enclosed  almost
until  maturity, but they all eventually arrive at the same end-
point, with vertical, exposed gills  dropping  spores  into  the
air.

One of the ways in which we identify agarics is by placing a cap
on  a piece of white paper in a draft- free place and letting it
drop millions of spores onto the paper  overnight.  The  deposit
will  form  a  visible radiating pattern, which reflects the ar-
rangement of the gills from which the spores  came.  This  spore
print  may  be  white, cream, pink, brown or black, according to
the mushroom genus which produces it. The spore  print  of  Lac-
tarius is white or cream coloured.

Everything I have said so far applies not just to Lactarius, but
also  to  many  other genera of mushrooms. So how does Lactarius
differ from the rest? That's easy: it has a  unique  combination
of  three  features  which  are  not found together in any other
genus of agarics.

      [1] The cap and gills of Lactarius contain  special  cells
filled  with  a  milky  juice or latex (white, yellow, orange or
red) that oozes out in visible drops when the  tissues  are  cut
(and sometimes change colour after exposure to air).
      [2]  The  flesh  of  Lactarius  contains  large numbers of
swollen, thin-walled cells called sphaerocysts: these  make  the
flesh extremely and characteristically brittle and granular.
      [3]  The  spores  of  Lactarius  are  ornamented with con-
spicuous warts and spines, lines and ridges, which often join up
to form a network. These ornamentations are chemically different
from the rest of the  spore  wall,  because  they  stain  darkly
(grey,  blue,  purple  or black) in iodine, while the spore wall
itself remains unstained, or stains only slightly. Ornamentation
that gives this colour reaction is often  described  as  iodine-
positive, or amyloid.

Even  beginners can easily identify Lactarius by the milky juice
it exudes when the brittle flesh is broken:  no  other  ordinary
mushroom has anything like it.

But  in  addition  to  specimens  of  Lactarius  as  I have just
described it,  we  occasionally  find  extraordinary  specimens.
Specimens  which have a few important differences from the milky
caps we are used to seeing. They are similar (and  theoretically
could  therefore be included in the genus) because they have all
three  characters  listed   above:   brittle   flesh   full   of
sphaerocysts;  latex  exuded  when the tissues are ruptured; and
spores with ornamentation that is iodine-positive. Yet they  are
different because their cap develops in such a way as to enclose
their  gills,  and  the gills are no longer vertical plates, but
have become crumpled or convoluted to form a  spongy,  chambered
mass.  Since the cap remains closed, the spores obviously cannot
escape. This sounds as if it would be a serious problem for  the
fungus: after all, have not mushrooms evolved to be spore-making
and spore-launching machines? And if the spores are not released
into  the  atmosphere,  how  will  they  be dispersed? Yet if we
remember that the lungs of land  vertebrates  evolved  from  the
swim-bladders  of  their  fish ancestors, and the wings of birds
from the forearms of their earthbound  reptilian  ancestors,  we
will  appreciate that evolution, guided by environmental forces,
often drives organisms in unforeseen  directions.  Something  of
this  kind appears to be happening to the Lactarius, and we must
assume that some other way of dispersing  the  spores  has  been
evolved.

If we now cut away the edge of the unopened cap which is obscur-
ing  the  gills,  and  try  to  make  a spore print, we will not
succeed. No spores will be deposited. This is  not  because  the
mushroom  is  either unripe or overmature. If we examine some of
the basidia under a microscope,  we  will  see  that  they  have
produced  mature  basidiospores.  But  the  basidia  have subtly
changed. The four spores  tend  to  develop  symmetrically  (not
offset)  on  the sterigmata, and they tend to remain attached to
the sterigmata: they are never forcibly discharged, as they were
in normal Lactarius fruit bodies.

These differences are important enough for taxonomists  to  con-
clude  that  the fungus can no longer be called a Lactarius, and
it has been placed in a different  genus,  named  Arcangeliella.
This  genus  has  sometimes  been  excluded from the family Rus-
sulaceae and even from the order  Agaricales,  and  has  instead
been  put in a separate order, the Hymenogastrales. But there is
no doubt that it has evolved from Lactarius in relatively recent
times, that it is still closely related to that genus, and  that
it  should  be  retained in the Agaricales, and even in the Rus-
sulaceae.

Arcangeliella still looks very like  a  mushroom,  even  if  its
behaviour is a little strange. But we have found other specimens
which  have  evolved  even  further  away  from Lactarius. These
specimens develop, and remain, just below  the  surface  of  the
ground,  looking  rather  like truffles. They are rounded or ir-
regular in shape. The skin that covered the Lactarius  now  com-
pletely  surrounds  the  truffle-like  specimens.  They  have no
stalk. There are  no  gills:  the  hymenium  lines  labyrinthine
chambers.  And  the  basidiospores,  now sitting straight on the
sterigmata of the basidia, are not actively shot away.

Note that the outer skin and often the walls of the labyrinthine
spore-bearing tissues contain sphaerocysts; latex oozes from the
cut surfaces of fresh specimens; and the spores  have  spiny  or
ridged ornamentation that stains dark in iodine. Once again, the
three  diagnostic  characters of Lactarius. A vestige of a stalk
may even occur in the form of a pad of sterile tissue inside the
base of the fruit body; the walls of the  labyrinthine  chambers
could  be  derived  from  crumpled  gills;  and  the presence of
sterigmata on the basidia is a reminder  that  these  structures
were  originally evolved as part of a mechanism to launch spores
into the air.

Yet it would be stretching the concept of Lactarius  beyond  the
breaking  point  to include these specimens in it: surely no-one
would call them agarics. It is also clear  that  they  are  con-
siderably  more  "reduced"  even  than  those  placed  in Arcan-
geliella. So mycologists put them in another new  genus,  called
Zelleromyces.

Although  Zelleromyces  differs from both Arcangeliella and Lac-
tarius  in  important  ways,  the  fact  that  it   has   latex,
sphaerocysts  and  iodine-positive (amyloid) spore ornamentation
is a compelling argument for  keeping  it  in  the  family  Rus-
sulaceae  of  the  order Agaricales. After all, this disposition
seems to best reflect its true relationships. Arcangeliella  and
Zelleromyces  are  what  we  now  call sequestrate (see the note
below) derivatives of the original agaric. The word  sequestrate
implies  that they sequester or retain their spores, rather than
broadcasting them into the air. This retentive habit,  diagnosed
by  spores  sitting  symmetrically  on  the  sterigmata  of non-
shooting basidia, is clearly characteristic of both genera.

Before drawing the first part of this discussion to a  close,  I
must  address one final issue. If these sequestrate genera share
all the essential diagnostic features of Lactarius, how  are  we
to  distinguish  the  Lactarius we all know from its sequestrate
derivatives? It is apparent that the three diagnostic characters
I described earlier must  be  supplemented  by  three  more,  as
follows:

      [4]  the  cap  of a true Lactarius expands at maturity and
the gills are exposed.
      [5] its gills are vertically oriented.
      [6] its basidiospores are asymmetrically  mounted  on  the
sterigmata and are forcibly discharged at maturity.

If  the  Lactarius -> Arcangeliella -> Zelleromyces sequence was
the only case in which this strange  evolutionary  sequence  had
been  observed,  we  might  be  able to dismiss it as a quirk of
evolution, a freak. But we have evidence that  similar  pathways
have evolved in other mushroom genera. These will be explored in
the second part of this article, in the next two issues of BEN.

The  term  "sequestrate"  has recently been introduced (Kendrick
1992) to describe all these closed  or  hypogeous  offshoots  of
regular  fungi.  It  means  that  the  spores are sequestered or
hidden away, kept from contact with the outside world, at  least
until  the  fruit  body decays or is eaten. The term sequestrate
appears to be a more useful and more widely applicable term than
such frequently-used words as `gastroid' (which  inappropriately
implies close relationship with gasteromycetes) and `secotioid,'
an  arcane  word  suggesting  similarity with the genus Secotium
(which is a sequestrate derivative of  Agaricus).  Most  amateur
and  many  professional mycologists have never seen Secotium, so
the term derived from that name conveys little or no meaning.

[Continuation in BEN # 178]

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