Growth, Differentiation and Sexuality

126 N.L. Glass and A. Fleissner
1888, Marshall Ward published his work on
a Botrytis species found on lily (Ward 1888). He
described how hyphae were attracted to each other
at a distance, and showed directed growth followed
by fusion. In N. crassa and other filamentous
ascomycete species, the frequency of hyphal
fusion within a vegetative colony varies from the
periphery to the interior of the colony, and also
within the interior of the colony itself (Hickey et al.
2002). Hyphal tips at the periphery of the colony
are refractory to hyphal fusion. At the periphery,
hyphae grow straight out from the colony and
show subapical branching. The leading hyphae
as well as the subapical branches show avoidance
(negative autotropism), presumably to maximize
the outward growth of the colony (Trinci 1984).
Even in cases of contact between hyphae at the
periphery of the colony, fusion is not observed
(Hickey et al. 2002).
Intheinnerportionofacolony,hyphaeshow
a different behavior. They branch and begin to
fill the spaces between individual hyphae. Instead
of avoidance, certain hyphae show attraction, directed
growth and hyphal anastomoses (Köhler
1929; Buller 1933; Hickey et al. 2002). Within the
colony, microscope observations suggest that competency
plays a role in vegetative hyphal fusion,
that is, not all hyphae within a colony are equally
competent to respond to fusion signals. The nature
of the difference in competency among hyphal
types and position within a colony is unknown. It
is clear that different morphologies of hyphae occur
within the interior of a colony, also in N. crassa
(for terminology, see Bistis et al. 2003). Thus, the
various hyphal types within a colony may be in
different physiological states with respect to hyphal
fusion. The spatial frequency of anastomosis
within the fusion-competent regions of a colony
can also vary, although parameters that affect this
process are unclear.
Similarly to germling fusion, studies on
filamentous fungi have shown that the ability
to undergo hyphal fusion is highly influenced
by growth conditions. Investigations of nutritional
conditions affecting hyphal anastomosis
frequency in the basidiomycete species Rhizoctonia
solani and Schizophyllum commune also
showed a negative correlation between nutrient
concentration and fusion frequency (Ahmad and
Miles 1970; Yokoyama and Ogoshi 1988). Nitrogen
levels affected hyphal fusion frequency in the
basidiomycetes R. solani (Yokoyama and Ogoshi
1988) and R. oryzae (Bhuiyan and Arai 1993). The
addition of nitrogen to nutrient-poor media led to
the largest decrease in hyphal fusion frequency,
compared to the addition of other compounds
such as carbon, potassium, phosphate, magnesium
or iron.
The formation of interconnected networks
and the pooling of existing storage compounds
may favor the survival of a fungal individual
under suboptimal environmental conditions.
While this theory assumes that anastomosis is
beneficial, other authors speculate that fusion
could be somehow connected with parasitism
and pathogenicity (Laibach 1928). In this scenario,
one fusion partner would benefit from the
nutrient sources of the other, a type of resource
plundering. A resemblance between hyphal fusion
and infection of plant hosts by pathogenic fungi
has also been reported (Chen and Wu 1977;
Yokoyama and Ogoshi 1988). In addition, some
aspects of mycoparasitism show similarity to the
hyphal fusion process. Mycoparasites recognize
a diffusible signal produced by the host, which
results in the reorientation of a hyphal growth
trajectory (Evans and Cooke 1982; Jeffries 1985).
In the host–parasite system of Absidia glauca and
Parasitella parasitica (bothmembersoftheZygomycota),
fusion bridges were observed between
mycelia of the two species (Kellner et al. 1993). The
interaction between Absidia and Parasitella was
mating-type dependent; only + mating-type A.
glauca were infected by – mating-type P. parasitica,
andviceversa.Theseobservationsledtothe
hypothesis that this parasitic interaction might be
an abortive attempt at sexual conjugation (Satina
and Blakeslee 1926; Jeffries 1985), representing an
interesting example of how basic mechanisms such
as mating and cell fusion could evolve to serve new
purposes. Similarly, in nematode-trapping fungi,
such as Arthrobotrys oligospora, trap formation
requires a hyphal fusion event (Nordbring-Hertz
et al. 1989). Fusion occurs between a small
branch growing initially perpendicular to the
leading hyphae and the parental hypha; the
self-communication and signaling processes that
regulate the formation of the trap must occur at
a very fine spatial and temporal scale.
IV. Mechanistic Aspects of Anastomosis
In 1933, Buller outlined morphological aspects
of anastomosis in detail (Buller 1933). Based on