Endophytic fungi: natural insecticide?

dwheeler at teleport.com dwheeler at teleport.com
Sat Oct 10 14:30:57 EST 1998

The following is posted as a courtesy, and first appeared in The Oregonian,
Oct. 20, 1998 p E1

IN SEARCH OF FRIENDLY FUNGI By ROB MARVIN -- Special Writer, The Oregonian   
  Japanese cedar, a tree loved for its beauty and valued for its timber, is
being injured by gall-forming flies on Japan’s southernmost island of Kyushu.
	On other Japanese islands, the cedar trees are hardly bothered by the
fly that produces the abnormal growths. Their good fortune may be due to
little endophytes, friendly fungi living inside their needles.	 George
Carroll thinks that may be the case. He will spend a year in Japan to find
out and to learn how the unfortunate Kyushu trees may be protected.   Carroll
is a mycologist, a scientist who studies fungi, at the University of Oregon. 
  His lab equipment is simple: a few microscopes, stains, and glass tubes for
growing fungi. Thick bundles of yellow mountaineering rope for climbing
Douglas fir are stacked on a shelf, but Carroll is leaving those behind. What
he is taking to Japan are his skills at locating and identifying endophytes. 
Carroll met his first endophyte in the 1970s while studying the canopy high
in the Douglas fir forests. There was a surge of money then for studying
habitats in the belief that if enough information was gathered, the biology
of habitats could be described by predictable equations such as those in
classical physics.    That dream was never realized, but a number of things
were learned, among them the value of fungi.	  At the time Carroll was
studying epiphytes, fungi growing on the outside of needles. To make sure no
fungi were on the inside to skew his results, he sterilized the outside of
some needles, cut them in slices and put them on a dish of V-8 uice, Wheatena
and oatmeal, a diet fungi thrive on. To his surprise, fungus colonies grew
out of the needles. The fungi were endophytes, organisms living inside
needles or leaves.	Carroll could have thrown the batch out and
considered the experiment ruined, but as a good scientist he began asking
himself what the fungi were doing in healthy needles.	  Fungus-infected
needles should be sick-looking, discolored or wilting, but these were plump
and healthy. Was it an isolated fluke?	    To find out, he collected and
cultured 10,000 needle sections sliced from 3,500 needles taken from 200
sites throughout Oregon.	 He discovered that in most Western Oregon,
most Douglas fir had endophytes. The most common was an unknown species and
Carroll named it Rhabdocline parkeri, in honor of Canadian mycologist A.K.
Parker for his work on the genus Rhabdocline.	      But the discovery of
that endophyte was only the beginning. R. parkeri raised more questions than
it answered such as, “What is it doing there?” and “How did it get there?”   
Plants are not defenselless, so why, Carroll wondered would a tree allow a
fungus to live inside its needles unmolested? He suspected some kind of
mutualism, a situation where both the tree and fungus benefited. The fungus
had a home, but how did the tree benefit?	 Mutualism was a good guess
because in biology, parasites are seldom neutral: they either cause disease
or offer a benefit. Carroll first suspected the fungus might be pulling
organic nitrogen out of raindrops fo the host to use. Some fungi on leaves
capture nitrogen from rainwater. Other fungi on the roots break down minerals
for the tree to use. Could Carroll have discovered a fungus that obtained
nitrogen for the tree? It was an exciting prospect, but the fungus was inside
the needle and had no access to rainwater. Carroll had to find another
explanation.	 Mutualism also can suggest toxins, poisons that defend the
tree against something, so his next step was to look at what ate Douglas fir
needles.	One such pest is a tiny fly called a gall midge, whose larvae
form galls on Douglas fir needles. Carroll find a higher death rate of larvae
in trees infected with R. parkeri than in trees without the endophyte.	   
Gall midges emerge from their pupae in the early summer and lay their eggs in
the newly forming bud at the ends of branches. As the bud grows into a
needle, the fly larva hatches and produces plant hormones that cause needle
cells to build a gall, providing the larva with food and shelter. In the fall
the larva flips itself off the needle and spends the winter in the ground as
a pupa. If the larva is still in the needle when the autumn rains spread R.
parkeri spores, the larva usually dies. Toxins produced by the fungus are
presumed to kill the larva.   Carroll thinks R. Parkeri toxins kill the
larva. A collegue in Canada is looking for them, but so far the toxins have
not been found.   R. parkeri grows rapidly when the larvae die, probably
nourished by nutrients released from the ruptured larvae cells, and produces
spores in three days. In needles without larvae, R. parkeri waits until the
needle dies of old age before sporulating. Needles live for about five years.
  Why should R. parkeri wait for years in a needle instead of colonizing it
immediately and producing spores?     In nature there are always tradeoffs.
R. parkeri’s strategy gives it a predictable resource. It trades a chance of
rapid reproduction for security. Its close relatives are pathogenic, trading
the security of a reliable resource for high reproduction if they can
successfully colonize a needle. In human terms it is like having a long-term
certificate of deposit at a fixed rates of interest vs. a volatile investment
that can make a person very rich -- or very poor.      A tree can make
chemical defenses to protect itself from fungi. But like the disease it tries
to fight, chemical defenses also can weaken a tree by taking resources from
branches, leaves and seeds. Fungi face a similar problem: getting the tree’s
resources at the least expense to themselves. Over the ages, the fungus and
tree evolved for their mutual benefit.	     Sexual reproduction produces new
gene combinations, turning out slightly different combinations of proteins in
the age-old attempt to out-compete, or eat thy neighbor. Carroll calls the
result of gene shuffling “chemical variability,” and the “gene for gene
hypothesis” may explain how it works. The predator combines a gene, allowing
some of its offspring to overcome the tree’s defenses; the tree in turn
recombines a gene, allowing some of its offspring to meet the challenge.     
   This concept of chemical variability poses a riddle for biologists: If a
Douglas fir’s genes were fixed when its seed was conceived 600 years ago, and
insects reproduce one or more times a year, what keeps a particular group of
insects from specializing on a particular tree and doing it in?     How can a
long-cycle plant like a tree hope to defend itself aginast rapid chemical
variability of short-cycle insects?	    Carroll believes the answer may
be endophytes, which reproduce as quickly as insects and provide a rapidly
changing defense against the hordes of creatures that want to eat trees.    
He believes that different strains of endophytes may live together even
within the same tree, each producing such a range of toxins that the insect
can’t cope with them all at once.   For the Douglas fir, R. parkeri appears
to be a bargain. It kills a single epidermal cell to live in. Epidermal cells
are a protective covering on the needle, and killing some does no apparent
damage. Because many of the older needles are infected with R. parkeri, the
tree has plenty of spores to kill the larvae in the fall. The endophyte
consumes little of the tree’s energy and seems to wait patiently for the
needle to die. But other Douglas fir trees succeed without the endophyte, so
there may be costs that simply haven’t been discovered yet.  R. parkeri
spends most of its life waiting in the living needles, reproducing rapidly
after the needle dies.	  When the fall rains come, raindrops hit spores in
dead needles that have lodged in branches, spider webs and chinks of bark.
The raindrops splash the fungus spores from the dead needles onto living
needles.  On the living needle, the spore divides and sends a penetrating peg
into the epidermal cell of the needle. The single epidermal cell is killed
and becomes filled with fungal cells.	 Then a curious thing happens.
Instead of taking over the leaf the way mold multiplies on an over-ripe
cantaloupe, the fungus cells stop and rest until the needle dies of old age. 
    Fungal cells grow quickly inside a dead needle, filling with a network of
fungal cells. When the needle falls, the fungus is ready to send out
thousands of spores to infect living needles. “That is the beauty of it,”
Carroll says.  The strategy allows R. parkeri to get a head start on
competing fungi and to reproduce while it is still close to young healthy
needles. Rain splashes the spores onto nearby needles and another generation
of R. parkeri begins.	   Some endophytes produce toxins whose tiny amounts
can kill insects and livestock. They create plant hormones to produce a more
robust plant. They protect the plant from extinction, but R. parkeri seems to
do none of that. The gall midge is not a serious threat. Why then, is there
an interest in a conifer’s endophyte of no apparent economic value?    The
interest lies in the powerful role endophytes have in other plants and the
discovery that they also exist in conifers.	 R. parkeri’s value is as a
teacher. It may provide clues to controlling insects like spruce budworm,
responsible for heavy economic losses in Canadian timber, and wester budworm
in Central Oregon.    R. parkeri may prove to be a good instructor. Carroll
is taking its lessons and his mycological skills to Japan, where he hopes to
locate and identify endophytes in the Japanese cedar.

Posted by:
Daniel B. Wheeler

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