FUNGAL ECOLOGY
(sometimes with special regard to macromycetes)
Fungi and their environment • Life strategies and interactions of fungi • Ecological groups of
fungi, saprotrophs (terrestrial fungi, litter and plant debris, wood substrate, etc.) • Fungal
symbioses (ectomycorrhiza, endomycorrhiza, endophytism, lichenism, bacteria, animal relationships)
• Parasitism (parasites of animals and fungi, phytopathogenic fungi, types of parasitic relations)
• Fungi in various habitats (coniferous forests, broadleaf forests, birch stands and non-forest
habitats, fungal communities)
• Fungal dispersal and distribution • Threat and protection of fungi
(the study material has not been corrected by native speaker)
PF_72_100_grey_tr ubz_cz_black_transparent
MASARYK UNIVERSITY, FACULTY OF SCIENCE
DEPARTMENT OF BOTANY AND ZOOLOGY

ENDOMYCORRHIZA
The vast majority of plants develop endotrophic mycorrhiza; about 75% of species are reported,
including ferns, lycophytes and some bryophytes.
The most common type is arbuscular mycorrhiza (AM); in this case, the mycorrhizated roots do not
differ from the others, the root hairs remain here.
The extraradical mycelium extends outside the rhizosphere, the hyphae are forming appressoria on
the root surface and penetrate the cells of the inner cortex (on the other hand, they never
penetrate the endodermis, vascular bundles or root caps).
• At first the hyphae form branched arbuscules – it is a metabolically active part of the fungus,
there is a bilateral transfer of substances across the membranes (initially there is no penetration
of the plasmalemma of the plant cell, but invagination – the transfer of substances is still
realised across two membranes).
tz0511
Sinauer Associates, Inc., 1998

Presence of the fungus affects life of the cell – a solid cell wall is not formed in the place of
contact, or remains in the form of a fibrillar net; there is also evidence that the fungus may
cause limited lysis of the pectin component of the cell wall. After a certain time (days to weeks),
the arbuscules are „digested“ by the cell.
C:\Documents and
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• Later, spherical vesicles are formed on terminal or inter-calary positions of intraradical
hyphae; these are long-lasting structures, which do not have absorbent but storage function – there
are lipid particles inside and solid chitinous wall on the surface.
In some plant species, vesicles are not created (family feature in
some cases – it is also used in classification, in addition to molecular analyses), therefore, the
abbreviated term „arbuscular mycorrhiza“ is recently preferred instead of the well-established
„vesicular-arbuscular mycorrhiza“ (VAM).
In plants of the families Zingiberaceae and Burmanniaceae, arbuscular structures are also formed in
the tissues of leaves, rhizomes or xylem.
http://invam.caf.wvu.edu/fungi/taxonomy/Glomineae/glomves.JPG

Two basic morphological types of arbuscular mycorrhiza:
– Arum-type (linear AM): in the intercellular spaces of the root cortex, a hyphal network grows,
the lateral protrusions of which invaginate cortical cells and form arbuscules (usually „digested“
in 4–20 days); vesicles are usually intercellular;
C:\Documents and Settings\Hrouda\Dokumenty\S_Vyuka\stazeno\ekolhub_symbiot\44_arum-linear-type.jpg
C:\Documents and Settings\Hrouda\Dokumenty\S_Vyuka\stazeno\ekolhub_symbiot\41_arbuscule.jpg
Big lateral arbusculus
(typical for Arum-type)
of Glomus mosseae in the root of Fragaria vesca
http://www.sci.muni.cz/~mykorrhi/html/arbuscule.htm
Bottom: Longitudinal growth of Glomus versiforme hyphae
with formation of arbuscules; their number increases with distance from the growing hyphal apex.
http://mycorrhizas.info/vam.html

– Paris-type (coiling AM; type widespread even in non-green plants): extensive development of
intracellular hyphae in the cortex, which are surrounded by plasmalemma of the plant cells; they
often form coils (different size and density in different plants), which can branch inside the
cells and form lateral arbuscules.
Some Gentianaceae (Centaurium) have a specific type: a single plant is not able to germinate, but
needs to be accompanied by other individuals, with which it is connected by fungal hyphae, through
which it draws nutrients from the other ones; in addition, the cytoplasm of fungal cells is
„digested“ within a few days, hence the plant needs to be repeatedly colonised for successful
germination.
C:\Documents and
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C:\Documents and
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rbuscules.jpg
Left: Growth of hyphae in the root cortex of Erythronium americanum (E – entry into the root,
A – arbuscules, arrows show coiled hyphae growing through the cells; scale bar 100 µm).
Right: Arbuscules (A) growing from irregularly coiled hyphae (C) into the inner cortex cells of the
Asarum canadense root (scale bar 10 µm). http://mycorrhizas.info/vam.html

43_Thysanotus_FringedLilyRoot
The process of fungal root colonisation can be primary and secondary.
Primary phase: hyphae germinate from the individual diaspore, grow along the root and form
appressoria when contacting its surface => usually the penetration hypha (growing between cells or
into rhizodermis cells) grows from only one appressorium, while the others die.
Subsequent colonisation depends on a positive response from the host plant => the hyphae penetrate
through the hypodermis cells (through „short“ cells, while „long“ cells are suberised) or through
the intercellular spaces.
Thysanotus root, cross section: distinct darker line between cells of the epidermis and the outer
cortex; hyphal growth is limi-ted to this layer only.
http://bugs.bio.usyd.edu.au/learning/resources/Mycology/Plant_Interactions/Mycorrhizas/Atypical/aty
pical.shtml
thysanotus1
http://mycorrhizas.info/ozplants.htm
Another example of an atypical mycorrhiza is the
tropical Thysanotus (Anthericaceae) – the fungi also connect newly germinating plants with the
older ones as in the previous type; in addition, the fungal tissue forms a „sheath“ between the
cortex and epidermis, which resembles mantle of ectomycorrhizal fungi after detachment of the
epidermis.

In the Arum-type, hyphae spread through the intercellular spaces => at first the arbuscules are
formed near the point of penetration into the root, then further => as the colony grows, many
arbuscules are formed, but their formation decreases over time; little is known about the course of
their formation in the Paris-type.
Vesicles are usually formed at certain stage of the life cycle at certain places in the root – this
is likely due to the genetic information of the fungus and the plant.
Secondary colonisation: from the outer hypha (outside the root surface) a lateral protrusion grows
near the appressorium => the hypha grows along the root and after a certain time (10–14 days) it
colonises (again appressorium => penetration) the same root or it can grow through soil to another
root. The rate of secondary colonization depends on the ability of the fungus to spread (it depends
on environ-mental conditions and available sources, but fungi with rapid growth of hyphae forming
large colonies have an advantage over species spreading mainly by individual spores).
In terms of time (if fungal diaspores are present in the soil), colonisation occurs within a few
days after root formation; initially it proceeds quite quickly until it reaches a certain
„coverage“ of the root with the fungus and stabilises the state. The course and rate of
colonisation depends on the fungal species, number of diaspores and their distribution in the soil
profile.
In annuals, the death of mycorrhiza foreshadows the plant death; in perennials it depends on the
condition of individual roots – new roots are quickly colonised, while in old ones the fungus
retreats, what is connected with the depletion of organic carbon reserves in the dying root.

The success and extent of colonisation are influenced by environmental factors:
– amount of phosphorus in the soil: generally an indirect proportion (if there is enough available
phosphorus, the plants do not need fungi), but at a certain level the mycorrhizal relationship is
maintained even in phosphorus-rich soils;
– light: at low light (PhAR) the loss of organic carbon in favour of the fungus exceeds its gain
from photosynthesis => plants attenuate the mycorrhizal relationship to reduce losses (this works
well experimentally, but in nature, where different fungi can interconnect the roots of different
plants and mutual provision of substances occurs, the results are not so clear);
– soil structure/texture and associated oxygen availability: the fungi need oxygen, so hyphae grow
well only in oxygenated layer of the soil; in anoxic soil (deeper layers, very compact, clayey or
flooded soil) they are able to grow only close to the roots from which they can obtain oxygen.
Other factors (water availability, pH, temperature) rather affect the mycorrhizal relationship
indirectly through the condition of the plant.

Endomycorrhizal fungi release the glycoprotein glomalin (in tropical soil up to 5% of nitrogen and
carbon can be present in this compound), which forms a hydrophobic layer on the surface of soil
particles and can connect them => together with a network of hyphae and plant roots it can connect
soil micro-aggregates (<250 µm) to macroaggre-gates (> 250 µm) => in some cases a „conglomerate“ is
formed with an anaerobic environment inside, while the outer surface is aerobic => thus creating an
environment for both aerobic and anaerobic microbes.
Soil „conglomerate“ with hyphae on the surface.
Source: Ritz & Young 2004; taken from http://botany.natur.cuni.cz/koukol/ekologiehub/EkoHub_4.ppt
Glomalin
There is a direct relationship between the stability of macroaggregates and the amount of hyphae of
mycorrhizal fungi in the soil (from 0.5 m/g in cultivated soils /it corresponds to about 3 m of
hyphae per 1 cm of root/ to about 5 m/g in stable stands, in extreme up to 20 meters of hyphae per
gram of soil). Due to the mechanical binding of soil particles and the production of exudates,
there is higher stability in soils under stable stands than in disturbed or cultivated stands; if
the soil is degraded, recovery of the stability is a rather slow process.

C:\user\Houba\Škola-www\stazeno\ekolhub_symbiot\gryndler010_klicici-spora-glomus.JPG C:\Documents
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Settings\Hrouda\Dokumenty\S_Vyuka\stazeno\ekolhub_symbiot\40_mature_spores_gigaspora_gigantia.jpg
http://www.wynboer.co.za/recentarticles/200705miko.php3
Photo André Meyer
Mature spores of Gigaspora gigantia
300 µm
C:\Documents and
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Glomus microcarpus, sporocarps


right scale bar by 1 mm
http://tartufi-online.com/2008/01
Individual blastospores are mostly formed by species growing in disturbed soils, sporocarps mostly
by species of undisturbed soils.
In the soil, fungi survive and spread through hyphae or spores – they either grow directly on the
hyphae of the extraradical mycelium (terminally or subterminally) as blastospores or are formed in
sporocarps.
Simple sporocarps are only a tangle of hyphae
surrounding the spores, complex ones have a
distinct external peridium and possibly a stem
with which they can be attached to the surface
of soil particles; the number of spores in the
sporocarps varies from units to thousands.

While spore formation depends mainly on the amount of available storage substances and energy, and
root colonisation is roughly the same throughout the soil profile, the density of hyphae growing
freely in the soil is highest just below the surface and decreases downward – as already mentioned,
the hyphae prefer less compact and more oxygenated soil.
Mycorrhizal fungi have a different ability to survive in the soil even if the plant symbiont dies
(some do not survive, others up to several years); they survive best in undisturbed and dry soils
(in moist soil there is higher probability that the fungus germinates and wastes its reserves in
the absence of any symbiont).
Internal dormancy (several months, it does not allow germination in unfavourable periods)
facilitates spore survival in some genera (mainly of the family Acaulo-sporaceae), while in fungi
adapted to extreme temperatures, external dormancy (developed as adaptation to environmental
conditions) is applied in high heat or cold (when no symbiont is available).
The possibility of survival in the form of mycelium is reduced by influences such as soil
disturbance, invertebrate eating, bacteria; the hyphae survive better in soil full of organic
residues than in the mineral fraction. Although arbuscular species have long been considered fungi
with minimal saprotrophic abilities, dependent on their hosts, a nitrogen transport (15N isotope
from decaying leaves; Hodge et al., Nature, 2006) has been experimentally demonstrated in Glomus
hoi – the question remains whether it is able to participate in the leaf decay (saprotrophy in
principle) or just took the decomposition products from other microorganisms.

(Vesiculo-)arbuscular mycorrhiza is formed exclusively by fungi of the order Glomerales s. l.
(formerly Zygomycota, now Glomeromycota; recently this order has been split into up to four orders)
– conversely, Glomerales s. l. are solely mycorrhizal fungi (except for Geosiphon pyriforme, which
has symbiosis with cyanobacteria).
There is a very low specificity – species of several fungal genera (about 150 species are
morphologically recognised; the question is how much the number of species changes based on DNA
studies) form arbuscular mycorrhiza with thousands of different plant species including ruderal
(Chenopodium), aquatic (Isoëtes) or salt marsh plants (Spartina cynosuroides).
Compared to ectomycorrhiza, we find arbuscular representatives predominantly in herbal communities
and abundantly in tropical regions (moreover there are, and will be, considerable reserves in
exploration for a long time to come).
Ecto- and endomycorrhizae do not exclude each other – for example, in acacias, a connection with
fungi of the genera Thelephora or Pisolithus (Basidiomycota) and the order Glomerales has been
found (bacteria can also stimulate the success of a mycorrhizal relationship here, see below).

Ericoid mycorrhiza is formed by imperfect fungi (Oidiodendron) or ascomycetes (probably only of the
orders Helotiales and Leotiales, chiefly Pezoloma ericae, also classified in the genera Pezizella,
Rhizoscyphus or Hymenoscyphus) or some basidiomycetes (Clavaria, Tulasnella, Sebacinales). These
fungi have a wide range of enzymes, including proteases, chitinases and phenol oxidases, which
allow them to decompose organic matter in humus at low pH and draw nutrients from complex organic
sources inaccessible to plants (peptides, proteins, chitin from fungal mycelia or dead insects,
etc.).
Their partners are plants of the families Ericaceae and Epacridaceae (family from the southern
hemisphere, recently also included in Ericaceae), usually growing on strongly acidic and
nutrient-poor soils (heath vegetation, tundra and undergrowth of some northern hemisphere forests;
in the southern hemisphere they occur in Australia and South Africa – simply put, plants with
ericoid mycorrhiza are distributed more to the north/south and also in higher elevations than
ectomycorrhizal or arbuscular plants).
The greatest problem of plants, which symbiosis with fungi helps to solve, is the difficult
availability of nitrogen and phosphorus – the latter is bound mainly in organic form, often in
complexes with iron and aluminum. The fungi must be tolerant to these metals – the mechanism of
tolerance has not yet been elucidated, perhaps they can enclose them in the cell wall or in
vacuoles; they can also regulate uptake of these metals by the plant.

Characteristic anatomical structure of ericoid mycorrhiza are thin ephemeral roots of ericoid
plants, the so-called hair roots.
These roots are very primitive, the stele is surrounded by only 1–3 layers of cells without root
hairs (unlike arbuscular mycorrhiza).
From the colonised roots, a network of extraradical mycelium penetrates into the surrounding
substrate (another difference compared to AM: hyphae of the above-mentioned fungi are septate).
Extraradical mycelium and hyphal coils in hair root cells of Leucopogon verticillatus
http://mycorrhizas.info/ozplants.html#ericoid
gryndler12_rhododendron-erikoid-mykorh Leucodon
Milan Gryndler et al.: Mykorhizní symbióza, Academia, Praha, 2004.
Hyphae penetrate only into the cells of the outer cortical layer of the roots – hypodermis
(preferably at the tips, where the plants form hairy roots in the extreme with only one layer of
cortical cells).

ericoid conf Vacco15
During the colonisation (it is important to recognise specific partners) an appressorium is pressed
on the plant cell surface => hyphae invaginate into the cell => their loops and coils, where the
exchange of substances
Over 70% of the cells are colonised; only one species of fungus colonises each individual cell, but
different fungal symbionts may be present in neighbouring cells of the same root – however, due to
their difficult cultivability, it is difficult to identify them.
46_erikoidni_mykorhiza_Leucopogon_verticillatus_detail 46_erikoidni_mykorhiza_Ledum_palustre
Different hyphae colonising root cells of Ledum palustre
Photo Anna Lepšová, http://botanika.bf.jcu.cz/mykologie/galerie/mycorhiza/Ledumpalustre.jpg
ericoid drawing colour detail cortical cell
Detail of mycelium and hyphal coils in hair root cells of Leucopogon verticillatus
http://mycorrhizas.info/ozplants.html#ericoid
between the fungus and the plant takes place, finally fill almost entire cells.
Drawing and photo Hugues Massicotte, http://web.unbc.ca/forestry/Hugues
/Images/

The mycorrhizal connection is physio-
logically active for a short time (3–4
weeks), then the fungus penetrates
into new cells, which is related to
formation of new roots.
It was observed that the hyphae of
some ericoid mycorrhiza forming fungi
contact the tests of testate amoebae.
In regions with distinct
alternation of dry and rainy periods, plant growth and their mycorrhizal symbiosis has a seasonal
character – hair roots, whose cells are colonised by fungi, are formed when the wet period is
coming, and die again with the onset of drought.
The fungus can survive either in the form of spores in the soil or in specialised plant cells – in
the tissues of some species (Woolsia pungens etc., Australia) thick-walled cells containing viable
hyphae have been found; the hyphae can survive drought in these cells and grow again into newly
formed roots, when the wet period is coming.
The fungi forming ericoid mycorrhiza are another group in which the ability to saprotrophic
nutrition has been found – Pezoloma ericae has this ability even stronger than ectomycorrhizal
species. In general, these fungi can survive for a long time without a partner plant, which is
obviously related to the above-mentioned enzymatic equipment.
Pezoloma (Rhizoscyphus) ericae colonising the test.
Source: Vohník et al. 2008; taken from http://botany.natur.cuni.cz/koukol/ekologiehub/EkoHub_5.ppt

Orchid mycorrhiza is formed by orchids (probably all species of the family Orchidaceae) with
basidiomycetes of the genera Sebacina, Tulasnella, Thanatephorus, Ceratobasidium (species of the
anamorphic genus Rhizoctonia), observable in the form of anasto-
mosing extraradical mycelium,
on which they can form inflated
„moniliform“ cells; their clustering
creates sclerotia, in which the
fungi survive worsened conditions.
Other orchid mycobionts are fungi
of the genera Armillaria, Mycena,
Marasmius, Russula, Hymeno-
chaete, Xerotus, Fomes, Coriolus,
Thelephora, Tomentella and even
the ascomycete Tuber; these fungi
represent ectomycorrhizal or
phytopathogenic species, which
redirect the substances gained from other plants and „feed“ the orchids (it is typical for
non-green orchid species).
The species that form OM in nature are referred to as „ecological symbionts“; however, other fungi
are also able to support seed germination in laboratory conditions („physiological symbionts“).
C:\user\Houba\Škola-www\stazeno\ekolhub_symbiot\gryndler024_hyfy+monilioidni-b.JPG
Gryndler et al.: Mykorhizní symbióza, 2004
diameter of monilioid cells = cca 20 µm

At least in the first phase of ontogenesis, orchids are dependent on the supply of nutrients from
the fungus, because their small seeds lack enough nutrients for successful germination – the
germination is therefore conditioned by presence of a symbiotic mycobiont. Their „encounter“ can
happen in three ways: either there is a successful recognition => mycorrhizal relationship, or they
do not „know each other“ => the seed does not start to germinate, or the fungus becomes a parasite
=> death of the plant. A possible prevention by the plant is the excretion of phytoalexin orchinol
– in this case it is important for the plant to survive the initial phase of „infestation“ before
it creates enough defensive substances and
C:\user\Houba\Škola-www\stazeno\ekolhub_symbiot\47_young-embryo+hyphae-longitudinal-section.jpg
so-called physiological compensation occurs (in the next phase mycorrhiza can also protect the
plant against other soil fungi).
Germination process (in the case of successful recognition):
the seed absorbs water, at the same time the hyphae penetrate its testa and grow into the embryo =>
invagination of the plasmalemma => formation of hyphal loops in plant cells => septate hyphae in
the cells are „digested“ after a certain time.
Heinz Clémençon: Cytology and Plectology of the Hymenomycetes. Bibliotheca Mycologica 199.
J. Cramer, Berlin-Stuttgart, 2004.

Thus, the fungus colonizes the embryo before formation of plant organs => during the plant
development, the basal part remains colonised, from which the roots develop, while base of the
shoot grows away of the colonisation. While in terrestrial orchids terminal part of the roots is
the most colonised, in epiphytic ones it may be different, the fungus is mostly beneficial in
places of contact with the substrate.
C:\user\Houba\Škola-www\stazeno\ekolhub_symbiot\48_neottia-protocorm+fungus.jpg
C:\user\Houba\Škola-www\stazeno\ekolhub_symbiot\gryndler08_ophrys+rhizoctonia-prunik-hyf.jpg
Hyphae penetrate into the roots through „passage cells“ in the exodermis (or mesodermis) =>
further, the fungus can spread through neighbouring cells, it does not penetrate between the cells
(similar to Paris-type endomycorrhiza or ectendomycorrhiza).
          Heinz Clémençon:           Cytology and Plectology of the Hymenomycetes.
Berlin-Stuttgart, 2004.
Milan Gryndler et al.: Mykorhizní symbióza,
Academia, Praha, 2004.

The exchange of nutrients takes place mainly in trophocytes („host cells“) in the primary cortex
(neither endodermis nor tissues of the middle cylinder are colonised). Transfer of compounds is
started after hyphal invagination into the plant cell, where clusters of branched hyphae (pelotons)
are formed; subsequently, the hyphae can grow into other cells.
After a certain time, the plant cell enters the phase of phagocyte („digestive cell“) – enzymatic
digestion of the hyphal content
C:\user\Houba\Škola-www\stazeno\ekolhub_symbiot\gryndler026_mlady-peloton.JPG
occurs => coils of dead hyphae can then be observed in the cells, or the cell „digests“ the hyphal
walls; over time it can be colonised again by new hyphae. (However, the „digestion“ of mycelia that
has penetrated the cells is not a specialty of orchid mycorrhiza; a similar process takes place,
for example, in lycophytes, ferns or Pyrolaceae.)
Milan Gryndler et al.: Mykorhizní symbióza, Academia, Praha, 2004.

Although the plant also obtains substances from the fungal body in this way, the elimination of
hyphae in plant cells is rather considered to be a defense mechanism against excessive development
of the symbiont, which could potentially become a pathogen (however, a simple autolysis of aging
hyphae is also possible).
A common tolypophagous form of orchid mycorrhiza is described above.
In several non-green tropical species, the ptyophagous form is known – in this case hyphal coils
are not formed in the cells, but individual hyphae grow into the cells (from a rhizomorph outside
the root), which are lysed here and their content is poured into vesicles (ptyosomes).
C:\user\Houba\Škola-www\stazeno\ekolhub_symbiot\50_orchid-endomycorrhiza.jpg
C:\user\Houba\Škola-www\stazeno\ekolhub_symbiot\gryndler025_tolypofag-ptyofag.JPG
Heinz Clémençon: Cytology and Plectology of the Hymenomycetes. Bibliotheca Mycologica 199.
J. Cramer, Berlin-Stuttgart, 2004.
Milan Gryndler et al.: Mykorhizní symbióza, Academia, Praha, 2004.

Orchid mycorrhiza is the only symbiotic relationship with the participation of fungi, in which the
flow direction of carbon compounds is from the fungus to its partner. During the initial
development of a non-green young plant, it is a fungus that produces cellulases, which contribute
to the degradation of cellulose (in epiphytic species it is also important in adulthood) => the
plant then takes the obtained oligosaccharides from the fungus (some plants also draw other
nutrients from the fungi – they serve as a source of nitrogen and phosphorus, vitamins, amino acids
or growth hormones) – in this phase of plant ontogenesis it is basically parasitism until the plant
fully begins photosynthesis (later the metabolism is probably mycorrhizal, but carbon transfer from
plant into the fungus still remains unconfirmed, although some experiments suggest it).
Permanently non-green orchids thus remain parasites on „their“ fungus for the whole life (the fungi
can also form ectomycorrhizal connections with other plants in the vicinity and then it can
actually be phytoparasitism through the fungus, see above).
Some orchids are perennial, others survive in underground organs (tubers) – at this stage the
fungus is excluded outside, it can be isolated from the root or tuber surface, but does not
penetrate into the tissues.
Fungi entering orchid mycorrhiza also have saprotrophic abilities, in addition to the
above-mentioned cellulases they also possess pectinases or polyphenol oxidases.

In anamorphic fungi of the genus Rhizoctonia (mentioned in orchids) with teleo-morphs in the orders
Ceratobasidiales, Platygloeales, Exidiales, Tulasnellales and Sebacinales, we find a wide range of
relationships with various plants.
Teleomorphic genus Sebacina (including anamorphs in the genus Rhizoctonia) is a genus with the
largest known number of mycorrhizal associations – it forms orchid mycorrhiza (Neottia nidus-avis),
ericoid mycorrhiza (Gaultheria shallon), endomycorrhiza in liverworts, ectomycorrhiza (Dryas
octopetala), eventually both ectendomycorrhiza and ectomycorrhiza (Pinus, Salix, Tilia or
Eucalyptus).
Rhizoctonia_mikro
Hyphae of the genus Rhizoctonia are characterized by more or less rectangular branching.
http://www.forestpests.org/nursery/rhizoctoniablight.html
Sebacina_incrustans
Sebacina incrustans
http://users.skynet.be/bs133881/champis/sebacina_incrustans_%28yd%29_2.htm
Photo Yves Deneyer

As already mentioned, mycorrhiza is not limited to vascular plants – some ascomycetes and
basidiomycetes (again mainly Sebacinaceae) enter a symbiosis with frondose liverworts and form
jungermannioid mycorrhiza. Hyphae of fungi grow into rhizoids of liverworts; these hyphae can also
form ectomycorrhiza with surrounding plants. Purely mycotrophic is the non-green liverwort Aneura
mirabilis (Cryptothallus mirabilis, right photo), nourished by a fungus (Tulasnella sp.), in which
a connection to birch or pine has been found.
Cryptothallus_mirabilis
Aneura (Cryptothallus) mirabilis
C:\Documents and
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pg
http://rbg-web2.rbge.org.uk
/bbs/Resources/gallery
/cryptothallus%20mirabilis%203.jpg
Hyphae of Tulasnella sp.
in rhizoid of Aneura mirabilis
Photo Martín Bidartondo,
http://plantbio.berkeley.edu
/~bruns/tour/monotrope.html
C:\user\Houba\Škola-www\stazeno\ekolhub_symbiot\79_fungi+mosses-and-liverworts.jpg
Heinz Clémençon: Cytology and Plectology of the Hymenomycetes. Bibliotheca Mycologica 199.
J. Cramer, Berlin-Stuttgart, 2004.
Not every connection with the fungus is mycorrhizal, in the right photo it is obviously a parasitic
penetration.

These are not only non-green orchids or species using monotropoid mycorrhiza – mycoheterotrophy has
already been found in at least 400 species of plants belonging to various groups (liverworts,
ferns, Orchidaceae, Ericaceae, Pyrol-aceae, Monotropaceae, Gentianaceae or Fabales); their
symbionts are mostly Basidiomycota and they are quite strictly bound to the species of fungal host.
Epipactis_microphylla GaleolaSeptentrionalis
Besides other mycorrhizal relationships, it is worth mentioning the mycoheterotrophic plants (the
term epiparasitic might be more accurate, because in principle they parasitise on fungi and thus
through them on other plants). So far accepted view that they are saprotrophic perennial herbs is
clearly wrong – these plants are not able to decompose organic matter. Some plant species are
non-green for the whole life, others only initially; in some species we find even photosynthetic
and non-photosynthetic individuals.
Epipactis microphylla is nourished by truffles (so far the only known ascomycetes).
Galeola septentrionalis
draws nutrients from Armillaria, parasitising on woody plants.
http://www.aho-nrw.de/Arten/Arten_Ep-micr.htm
http://www.parasiticplants.siu.edu/Mycotrophs/images/Orchids/GaleolaSeptentrionalis1.jpg

ENDOPHYTIC AND EPIPHYTIC FUNGI
A special case is fungi living endophytically in the intercellular spaces of plant tissues, which
are neither parasites nor symbionts directly connected to plant cells; usually there are no
apparent external manifestations of colonisation – we are talking about asymptomatic colonisers.
Plants probably provide them with a suitable niche for growth, as they represent a stable
environment and source of organic carbon; on the contrary, fungal metabolites can protect plants
against herbivorous insects, pathogenic fungi, bacteria and other organisms (antibiotics, alkaloid
production in Clavicipitaceae, etc.).
C:\user\Houba\Škola-www\stazeno\ekolhub_symbiot\56_endophytic_xylaria_in_bazzania.gif
Hyphae of Xylaria growing through and braiding rhizoids of the Bazzania liverwort (orig. 1000x).
Inset: stolon with fascicles of rhizoids (orig. 40x).

Source: Davis et al. 2003, http://www.amjbot.org/cgi/content/full/90/11/1661
In almost all plants recently tested for the presence of endophytes, the result was positive, so
this is probably a widespread phenomenon; endophytic fungi are recruited from practically all
divisions of fungi (mostly ascomycete anamorphs, also some Xylariales, endophyticism was also
observed in Coprinus group!) …

and have been recorded in tissues (especially in leaves) of many species of terrestrial and aquatic
plants, as well as red and brown algae). Hundreds to thousands of strains belonging to dozens of
species are commonly found in vari-ous parts of the plant.
Colonisation can vary in size from single cells (Rhabdocline) to ingrowth of the entire shoot,
stems and leaves (Chaetomium), as well as root endophytes (Phialocephala); likewise, among
endophytes there are species widely distributed ecologically and geographically …
Source: Müller et al. 2004; taken from http://botany.natur.cuni.cz/koukol/ekologiehub/EkoHub_8.ppt

... and, conversely, species with a narrow host specificity and a rare and limited occurrence.
Spread of fungal diaspores takes place in air, but also by insects (even a few entomopathogenic
fungi have been found to be endophytes).
It is assumed that this is a mutually beneficial relationship – plants provide the fungi with a
stable environment and source of nutrients; on the other hand, in order for endophytic fungi not to
grow uncontrollably, plants must have developed mechanisms by which they can limit their growth.
These mechanisms are usually physical and chemical (production of phenolic compounds etc.) and
their application can also increase the resistance (stimulate the response) of plants against
other, pathogenic fungi.
Plants also benefit from endophytic symbiosis: fungal metabolites are a source of  nutrients, the
already mentioned stimulation of defense against pathogens (e.g. Chaetomium), protection against
herbivores (Phomopsis, Lecanicillium;
animal toxic substances are distributed
throughout the plant body, even if the
fungus colonises only part of the tissue)
and increase in tolerance to drying was
noted (perhaps by changing the osmotic
conditions in the tissue).
Thermotolerance of Dichanthelium lanuginosum –right plants colonised by an endophytic fungus of the
genus Curvularia, left without endophytes.
Dichanthelium Dichanthelium_D
http://wfrc.usgs.gov/research/aquatic%20ecology/STRodriguez3.htm
Source: Redman et al. 2002

Plants may also have developed mechanisms that facilitate fungal colonisation in the next
generation – for example, the genus Neotyphodium on grasses, where there is a „vertical transfer“
(in the seeds to the next generation). Neotyphodium (teleomorph: parasitic genus Epichloë) belongs
to the specific grass endophytes of the order Hypocreales; in this genus, it was well observed that
the proportion of individuals with endophytes increased over time compared to non-colonised ones,
which were grazed by herbivores, while colonised plants did not. The negative effect on herbivores,
as well as invertebrate parasites of plants, is due to the formation of alkaloids that repel these
animals and can be toxic to them – clavine alkaloids repel mammals (tested on rabbits, but can also
bother cattle), while ergovalines and lysergic acid amides have negative effect to insects.
Left: teleomorph stroma of Epichloë typhina, centre: Neotyphodium sp. hyphae in seed, right: in
leaf.

Source: Mueller & Krauss 2005;
Taken from http://botany.natur.cuni.cz
/koukol/ekologiehub/EkoHub_8.ppt
(In addition to this effect, the osmoregulatory function of alkaloids is also considered, but
results of different studies are contradictory.)

Epiphytic fungi differ somewhat from endophytic fungi; these fungi rather only use leaf exudates
and do not penetrate into the tissues. They are usually melanised (UV resistant) and some are able
to break down fats and thus utilise a wax layer on the leaf surface.
Endophytes (or also epiphytes) do not damage the healthy tissue of their „hosts“, but they can also
be latent pathogens – either physiological changes in the host tissue (they can be caused by fungal
activity, or even natural tissue aging) can lead to the change of symbiont into pathogen, or
changes in the environment that increase the stress on the plant (e.g. Alternaria becomes a
pathogen in potassium deficiency).
Latent infection (can last for days or even years) can then change into a disease that manifests
itself externally. The direct cause of its outbreak is the action of fungal metabolites or
depletion of nutrients available for the host; it must also not be forgotten that there are a
number of fungi in plant tissues, so in many cases the action of one weakens the plant and the
other fungus kills it.
After fall of the colonised part of the plant, the endophytes and epiphytes are the first
colonisers to start the decomposition process.

Besides typical endophytes, we can mention „pseudomycorrhizal“ fungi forming DSE-associations (dark
septate endophytes), manifested by asymptomatic colonisation of conifer roots, herbs (grasses) or
ericoid plants. These are ana-morphs of saprotrophic ascomycetes with melanised hyphae (e.g.
Phialocephala fortinii, Meliniomyces variabilis, Cadophora finlandica). In their case, slight
„harmless“ parasitism of the fungus on the plant was previously considered, but it appears that the
connection could be neutral or mutually beneficial (it seems that the relationship may vary
depending on environmental conditions).
Thick melanized septate hyphae form a dense network around the host root. They often form
appressoria, penetrate the root tissues and grow along the stele.

C:\Documents and
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um_vyrez.jpg C:\Documents and
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g
Vaccinium corymbosum root colonised by unknown DSE fungus.
http://www.ibot.cas.cz/mykosym
/mykorhiza.html#pseudo
Photo (C) Martin Vohník, Instutute of Botany AS CR

This type of symbiosis predominates in cold nutrient-poor areas (where it dominates over arbuscular
fungi), but also in semi-arid steppes; the occurrence of pseudomycorrhizal fungi is still probably
underestimated.
It is limited by extreme environmental conditions, DSE fungi do not occur in aquatic or waterlogged
ecosystems, but have been found, for example, in soil samples collected on the Antarctic Peninsula.

Inside individual (most often rhizodermal) cells, these fungi form typical structures, so-called
mikrosclerotia.
C:\Documents and
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yrez.jpg
50 µm
Photo (C) Martin Vohník, Institute of Botany AS CR
Hyphae with appressoria and microsclerotia on the root surface of a plant of the family Ericaceae.
Formation of microsclerotia
in the plant cells.
Source: Schadt et al. 2000;
taken from http://
botany.natur.cuni.cz
/koukol/ekologiehub
/EkoHub_8.ppt