Lichens: The Interface between Mycology and Plant Morphology
Author(s): WILLIAM B. SANDERS
Source: BioScience, Vol. 51, No. 12 (December 2001), pp. 1025-1036
Published by: University of California Press on behalf of the American Institute of Biological Sciences
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Articles
Lichens: The Interface
between Mycology
and Plant Morphology
WILLIAM B. SANDERS
W
here do the lichens belong in the biological
sciences? They are composed of fungus and alga, but
neither mycologists nor phycologists have been eager to claim
them. In most lichens, it is the fungus that builds the structural tissues of the thallus (body), as well as the characteristic fungal fruiting structures. Its predominance is such that we
often speak loosely of a “species of lichen,” when we mean
more precisely a species of lichen fungus; the lichen algae, of
course, have their own separate scientific names.
The lichen-forming fungi represent nearly one-fifth of all
known species of fungi (Hawksworth et al. 1995), yet they are
rarely given adequate attention in mycology. It seems their behavior is too different from that of other fungi for many mycologists to feel comfortable with them. Nor is their place in
botany secure. Although lichens, as photosynthetic living
things, fit within the broad biological concept of “plant,” this
term has been increasingly co-opted for use in a narrower, phylogenetic context that excludes all but green algae and their
embryophyte (“land plant”) descendants. The lichens do receive brief consideration as a classic example of symbiosis. But
in treating them solely as a community-level ecological phenomenon, we overlook their organismal-level features and
their significance in mycology and botany.
For the fungi, symbiosis with microalgae represents an
important nutritional innovation, one that evolved independently in a number of different lineages (Wainio 1890,
Gargas et al. 1995). These fungi have distinguished themselves
by a notable accomplishment: their transformation into
“plants.” This metamorphosis is particularly visible in the
more conspicuous macrolichens, in which fungus and alga are
generally well-integrated in an often strikingly plant-like, superorganismal thallus (Figure 1). Although the structural
tissues are usually fungal, thallus form and function are emergent properties that have no real parallels among nonlichen
fungi. These properties the lichen thallus shares instead with
plants. Thus, the lichens are not only of great significance in
the evolution of fungi; they can also offer important insights
into fundamental principles of plant morphology.
WHEREAS MOST OTHER FUNGI LIVE AS AN
ABSORPTIVE MYCELIUM INSIDE THEIR
FOOD SUBSTRATE, THE LICHEN FUNGI
CONSTRUCT A PLANT-LIKE BODY WITHIN
WHICH PHOTOSYNTHETIC ALGAL SYMBIONTS ARE CULTIVATED
Lichens must first be appreciated in the context of other
fungi. As absorber heterotrophs, the primeval fungi evolved
a simple and enormously successful growth form: the
mycelium. This loosely organized network of branching, filamentous cells (hyphae) is ideally suited to an organism that
lives inside its food source. The hypha’s exclusively linear
growth generates a vast absorptive surface area with very
modest increases in cell volume.
Only at the reproductive phase, when spores must be produced in quantity and borne away to fresh substrate, do certain fungi organize tissues and build complex structures that
emerge from the substrate, such as mushrooms. Such fruiting structures have diversified tremendously, as reproduction
and means of dispersal became specialized for exploitation of
very different food sources under diverse ecological conditions.
But it is almost entirely within these reproductive phases
William B. Sanders ([email protected]) is a research associate at the University Herbarium, University of California, Berkeley, CA 94720-2465. He has combined his training in mycology and
in developmental plant morphology to focus on studies of lichen structure and development. He has lived and carried out research in California, Spain, and Brazil. © 2001 American Institute of Biological
Sciences.
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Figure 1. Leafy (foliose) and shrubby (fruticose) lichens
of the genera Parmotrema, Ramalina, Teloschistes, and
Heterodermia colonizing a tree branch behind dunes on
Santa Catarina Island, Brazil.
that morphological evolution of nonlichen fungi has occurred (Poelt 1986). The vegetative mycelium, by contrast, has
been very highly conserved throughout hundreds of millions of years of evolution. It characterizes most of the saprotrophic, parasitic, and mycorrhizal Eumycota (true fungi). The
mycelium also evolved independently in phylogenetically
distinct organisms traditionally treated as fungi, such as the
oomycetes. These are impressive indications of the mycelium’s
ideal suitability to the “endotrophic” absorber lifestyle.
But when a fungus establishes a symbiosis with a microalga, the usual spatial relationship of fungus to food source
is turned inside out. Surrounding the diminutive photosynthetic cells, the fungus now finds itself on the outside (Figure
2). To maintain and display the incorporated algae effectively, the fungus must build a protective, functional greenhouse, usually emergent from the substratum. The hyphal
building block is metamorphosed to produce a variety of
tissue types, and a complex thallus replaces the mycelium.
Farmers of the fungal kingdom
Symbiosis with microalgae engenders a whole new fungal
lifestyle: It represents nothing less than the advent of agriculture (see also Goward et al. 1994, p. 10). While their nonsymbiotic brethren continue as hunter–gatherers of transient carbon sources, the lichen fungi have become indoor
gardeners, cultivating and perpetuating their internalized
source of food. This agrarian control over food resources
confers both stability and the potential to occupy entirely new
ecological niches. In human development, agriculture permitted the rise of populous, sedentary, highly complex civilizations by providing a resource base far larger and more reliable than that available from the unmanipulated
environment (Schwanitz 1966, Heiser 1990). For the fungi,“algaculture” has led to the development of structurally elaborate, self-sufficient, long-lived thalli. The nutritionally
Figure 2. Lobe of a foliose lichen in longitudinal section.
The algal symbiont (Scytonema sp.) is confined to a
discrete layer surrounded by tissues of the lichen fungus
Coccocarpia palmicola (Spreng.) L.Arvidss. and D.Gall.
Scale bar = 20 µm.
autonomous lichen colonizes inorganic or indigestible substrates and often occurs in extreme microhabitats with little
to offer the hunter–gatherer of ephemeral food resources.
Agriculture has profound effects on the crop as well as on
the cultivator. Many of our most important crop plants
have been genetically selected for so long that they no longer
resemble any “natural” species, nor could they survive as
such. Maize (corn), for example, is a crop whose exact origin is controversial, and one that cannot effectively perpetuate itself outside human cultivation (Mangelsdorf 1974).
Some lichen algae may be in a comparable situation. Species
of the unicellular green alga Trebouxia (Figure 3) are the most
common algal symbionts in lichens of temperate and boreal
climates. Yet Trebouxia’s immediate affinities among nonlichen algae are unclear, and the genus has been only sporadically reported to occur outside lichen thalli (Tschermak-Woess 1978, Bubrick et al. 1984). It has been asserted
that reportedly free-living Trebouxia cells represent transient
populations liberated from damaged or degenerated thalli
or thallus fragments (Ahmadjian 1988). Such liberated algal cells might then be likened to volunteer plants that escape from cultivation. Whatever their origin or degree of stability, free-living Trebouxia populations can play an
important role in lichen establishment. They can offer potential symbionts available to compatible lichen fungi germinating from spores in the vicinity (Beck et al. 1998).
But not all lichen algae have been so thoroughly domesticated by the lichen fungus. Examples include algae of the
closely related genera Trentepohlia, Phycopeltis, and Cephaleuros, which are very important lichen symbionts in tropical and
warm-temperate regions. These algae commonly occur freeliving as well as lichenized, not infrequently within the same
habitat. On a single leaf (an important substratum for tropical lichens), one can sometimes find Cephaleuros both freeliving and in various stages of incorporation into a thallus of
the lichen genus Strigula (Figure 4).
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Figure 3. Thallus tissue of Neuropogon sp., showing dividing cells of the green algal symbiont Trebouxia. Scale bar = 20 µm.
Figure 4. Surface of leaf with epiphyllic alga Cephaleuros, both free-living (C) with erect trichomes and sporangiophores,
and incorporated into smooth white and yellow thalli of the lichen fungus Strigula smaragdula Fr. (S) at the margins (see
also Ward 1884). Scale bar = 1 mm.
Figure 5. (a) Crustose lichen Cryptothecia rubrocincta (Ehrenberg) Thor on tree branch and (b) crustose red alga on
intertidal reef.
Figure 6. (a) Foliose thallus of the lichen Flavoparmelia caperata (L.) Hale, growing on a cactus stem at the University of
California, Berkeley, Botanical Garden and (b) thallose bryophyte Anthoceros (hornwort) on soil bank at Puerto Blest,
Argentina.
Figure 7. (a) Pendulous fruticose thallus of the lichen Usnea repens Motyka (an epiphytic form) at Ibitipoca, Minas Gerais,
Brazil. (b) Unidentified moss on branches at Puerto Blest.
When lichenized, Cephaleuros grows much more slowly and
may not form reproductive structures. Indeed, lichenization
can reduce or eliminate the pathogenic effects of this alga’s vigorous growth on cultivated plants (Joubert and Rijkenberg
1971). Thus, lichenization can have different ecological implications for different algal symbionts. For some algae, like
Trebouxia, the symbiosis can be essentially obligatory for
survival in many habitats. For others, such as Cephaleuros, lichenization might be a nuisance, at least under conditions in
which the alga could otherwise survive and reproduce without supporting a fungus.
These ecological considerations, beyond the nutritional interaction of the symbionts, can determine whether one
chooses to view the lichen symbiosis as mutualistic (Honegger 2001) or parasitic (Ahmadjian 1993). For a highly
coevolved and dependent lichen alga such as Trebouxia, recognizing advantage or disadvantage in the symbiosis might
be as difficult as attempting to judge whether maize has
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niscent of a plant leaf or a thallose
bryophyte (Figure 6). Still others
form fruticose thalli with erect or
pendent branching axes, usually
with radial or bilateral symmetry
(Figure 7). Some of these fruticose
lichens can even show differentiation into stem-like supportive axes
of structural tissue bearing leaf-like
assimilative squamules that contain
the algal cells (Figure 8). Erect, fruticose lichens with highly branched
axes can resemble miniature shrubs
(Figure 9). A few species are actually
marketed commercially to represent trees in model railroads and
architectural scale models (Figure
10). The numerous convergences
suggest that these growth forms are
universally practical designs for displaying photosynthetic surfaces, using cell walls—of any origin—as
Figure 8. Fruticose thallus of Cladonia sphacelata Vain. with stem- and leaf-like
structural building material.
components. The brownish vertical axes consist entirely of fungal tissue; the algal cells
An examination of the thallus
are localized within the greenish lobed squamules borne along the axes. Scale
anatomy of macrolichens often reapproximately twice actual size.
veals further plant-like features. A
transverse section through the thalFigure 9. Shrub-like thallus of fruticose lichen Cladonia subreticulata Ahti, shown
lus of a typical foliose lichen shows
about actual size.
a tissue organization analogous in
Figure 10. Dyed lichens (Cladina sp.) representing trees in a scale model. The
many respects to that of a leaf (Figcommercially packaged lichen was purchased in the hobby section of a hardware store
ure 11). The algal cells are usually
in Berkeley, California. Scale is about one-quarter actual size. (Model designed and
arranged in a discrete layer just beconstructed by architecture students Elano Collaço, Patrícia Izabel, and Wallace
low the upper cortex of fungal tissue,
Amorim, Jr., at Universidade Federal de Pernambuco, Recife, Brazil.)
like a densely packed, chloroplastrich palisade parenchyma tissue. Efficient
gas
exchange
in
this
photosynthetically active stra“benefited” from its agricultural association with humans.
tum
is
facilitated
by
the
air
spaces
in the loosely organized
However, there is little justification for viewing lichenization
medullary
region
below,
as
occurs
in
the spongy mesophyll
as disadvantageous to Trebouxia (cf. Ahmadjian 1993, pp.
of
the
plant
leaf.
A
thin
coating
of
hydrophobic
protein and
3–4) if one maintains that this alga cannot really exist freeinsoluble
secondary
substances
over
the
medullary
hyphae and
living (Ahmadjian 1988).
associated algal cells can serve to maintain these spaces free
of water, as well as to seal a conduit between fungus and alga
Lichens as “plants”
(Honegger 1997).
The fungus must provide its algal symbiont with an enviLike an epidermis, the upper cortex of the lichen protects
ronment that makes effective use of physiologically favorable
the
photosynthetic cells below, slowing evaporation and filconditions. It must display the photosynthetic cells advantatering
harmful or excessive radiation with the assistance of piggeously to the light while filtering excessive or harmful radiments
and secondary substances (Rikkinen 1995). Unlike
ation. It must facilitate adequate hydration while permitting
the
cutinized
plant epidermis, however, the lichen cortex precarbon dioxide to diffuse into the thallus during photosynsents
no
impermeable
barrier to water diffusion. On the conthetically active periods. In short, the lichen faces the same batrary,
the
corticated
thallus
surfaces must serve in absorption
sic functional challenges as do terrestrial plants.
of
water
as
well
as
light,
as
do the leaves of mosses and atThe structural solutions, in turn, are remarkably similar
mospheric
vascular
epiphytes
(Figure 12).
(Jahns and Ott 1997). Many lichens produce a simple crusIn
certain
lichens
occurring
in
habitats that receive high levtose thallus intimately attached to the substratum, as do cerels
of
light,
the
lichen
cortex
can
form a thick optical filter
tain species of red and brown marine algae (Figure 5). Oththrough
which
light
diffuses
downward
and laterally to verers have foliose, dorsiventral forms, with a discrete lower
tically
arranged
tiers
of
photosynthetic
cells
(Figure 13), as in
surface attached to the substratum at specific points, remi1028 BioScience • December 2001 / Vol. 51 No. 12
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These pores most likely facilitate gas exchange (Green et al.
1981), as do plant stomata, but unlike the stomata they cannot be actively regulated by closure to conserve water. Nor
would their closure effectively conserve water, because evaporation occurs over the entire thallus surface. The lichen
thallus is poikilohydric: It survives drought by physiological
tolerance of desiccation rather than by maintaining thallus hydration. For many lichens that colonize exposed sites, rapid
water loss under full sunlight limits daily photosynthetic activity to brief periods (such as early mornings); in the dessicated state, the lichen can survive extreme conditions over long
periods of time (Lange et al. 1975).
The typical foliose lichen thallus is attached to the substrate
by rhizines, which are short hyphal bundles of determinate
(limited) growth that emerge from the lower surface. HowFigure 11. Transverse section through foliose thallus of
ever, some lichens produce more elaborate, branching fungal
the lichen Pseudocyphellaria aurata (Ach.) Vainio. U,
structures of indeterminate growth that penetrate the substrate
upper cortex; A, algal layer; M, medulla; L, lower cortex;
extensively. These structures, known as rhizomorphs, can reP, pore (pseudocyphella) in lower cortex facilitating gas
semble the roots of conventional plants (Figure 14). They do
exchange. The medulla shows extensive deposits of
not contain algae. Lichen rhizomorphs can penetrate both calbrownish secondary substances. Scale bar = 250 µm.
careous and siliceous rock substrates (Figure 15) as well as soil,
apparently by both mechanical and chemical means (Sanders
the so-called window leaves of South African succulent plants
et al. 1994). Their development is often much more extensive
such as Lithops (Vogel 1955, Malcolm 1995). This system
than would be expected of a structure that merely fixes the
permits the display of considerable photosynthetic tissue to
thallus to the substrate.
the light while greatly reducing the external surfaces exposed
Rhizomorphic excavation may increase the substrate’s cato evaporative water loss. When the lichen cortex is satupacity
to store capillary water available to the thallus. Howrated with water, diffusion of carbon dioxide through the thalever,
the
rhizomorphs themselves do not show distinctive
lus to the algal layer is impeded (Lange and Tenhunen 1981).
specializations
for transport (Sanders and Ascaso 1997), such
Thus, most of the larger lichens have some type of cortical peras
the
vessel
hyphae
observed in rhizomorphs of certain nonforation, such as cyphellae, pseudocyphellae (Figure 11), or
lichen
fungi
(Duddridge
et al. 1980). Where rhizomorphs
epicortical micropores (Hale 1981).
occur superficially, thallus squamules can arise secondarily
from them (Figure 14). This situation occurs when rhizomorphic
hyphae capture compatible algae
encountered in the substratum,
initiating development of the lichenized thallus component (Figure
16). Thus, the lichen rhizomorphs
can have a colonizing function
comparable to that of rhizomes
and shoot-bearing roots of many
conventional plants (Sanders
1994). By producing a rhizomorphic system, the lichen can maintain its presence within the substratum even as erosion continues
to expose new surfaces for pioneer
colonization by competitors.
Figure 12. Tree branch colonized by a fruticose lichen (Ramalina sp.) at left and
atmospheric bromeliad (Tillandsia sp.) at right, near Caruaru in Pernambuco, Brazil.
Role of apices and
In both epiphytes the photosynthetic surfaces are also used for absorption of water.
margins
The structural convergences with
Figure 13. Transverse section through thallus of lichen Psorinia conglomerata (Ach.)
plants show further parallels when
G. Schneider, with an undulating layer of green algal cells arranged below a deep,
the patterns of lichen growth and
translucent optical filter of fungal cortical tissue (C). Scale bar = 50 µm.
development are considered. Lichen
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cortex can proceed more rapidly on one surface relative to the other, producing an inrolling of the apex
comparable to that of the fern leaf crozier (Figure 21).
Diffuse growth processes
Even when morphogenetic and histogenetic events
are clearly localized at apices and margins, overall thallus growth may not necessarily be limited to these
zones. Diffuse or nonapical growth of the thallus can
also occur and might be common in fruticose lichens
in which attachment to the substratum is limited to the
base, leaving the rest of the thallus free. Diffuse growth
is sometimes referred to as intercalary growth, although the latter term is more correctly applied to
growth zones that occur intercalated between regions
where growth has ceased (Fritsch 1935, Esau 1965). The
reticulate thallus of the lace lichen provides the most
dramatic example of diffuse growth. Although new perforate tissue and apical branches are formed excluFigure 14. Toninia sp., a soil-inhabiting lichen with a thallus
sively at the apical margin of the thallus nets (Figure
composed of inflated squamules (S) interlinked by root-like
20), considerable tissue expansion occurs diffusely
rhizomorphs within the substrate. Young squamules (arrows) are
throughout the reticulum (Sanders 1989, 1992). Some
forming on the rhizomorphs. Scale bar ≈ 1 mm.
umbilicate lichens (i.e., foliose lichens attached to rock
by a single central “umbilicus”) also appear to show difFigure 15. Rhizomorphic hyphae of Acarospora scotica Hue (arrow)
fuse growth (Hestmark 1997). Diffuse growth probawithin siliceous rock substrate; a fragment of the substrate (F) is
bly occurs in other species as well (Honegger 1993), but
being incorporated into the rhizomorph. The embedded, polished,
at present lichen growth patterns remain largely unand stained surface of the cleaved substrate is imaged with SEM in
studied.
The presence of diffuse growth in at least some
backscattered electron mode (Sanders et al. 1994). Scale bar = 8 µm.
lichens raises fundamental questions about the mechFigure 16. Young squamule forming on rhizomorphs of Aspicilia
anisms of thallus growth at the cellular level. Can these
crespiana Rico from capture of compatible algal cells contacted
growth processes be compared with those exhibited by
nonlichen
fungi or even those of conventional plants?
within the substrate. Scale bar = 50 µm.
Because thallus structural tissue is fungal in most
lichens, it might be expected that the component fungal cells
thallus growth is polar, occurring at localized, usually peare behaving essentially as hyphae. However, growth of the vegripheral, zones of growth. As in conventional plants, growth
etative fungal hypha occurs exclusively at the tip. In this zone,
is potentially indeterminate and development open. Open dethe wall exhibits plasticity, and new cell wall components are
velopment allows the continued production of new lobes,
added to the existing structure during growth (Wessels 1986).
branches, or other units of construction in a modular fashExclusively apical growth of component fungal cells canion (Figure 17). Generation of form (morphogenesis) and ininot
account for diffuse growth of the lichen thallus. The metiation of certain thallus structures (organogenesis) are often
chanical
tissue of R. menziesii, for example, is constructed
localized at apices or margins that function analogously to the
of
elongate
fungal cells forming an anastomosing network
apical meristems of plants. Examples include the initiation of
embedded
in
thick deposits of cell wall material (Figure
apical branching (Figure 18), the formation of appendages
22).
With
extensive
diffuse growth of the thallus, these funsuch as apical cilia (Figure 19), and the generation of the
gal
cells
must
somehow
maintain plasticity along their
perforated tissue that gives rise to the reticulate thallus of Ralength.
Such
diffuse
plasticity
is indeed known in certain spemalina menziesii, the lace lichen (Figure 20).
cialized
cells
of
nonlichen
fungi,
such as those of the mushAt the anatomical level, cell differentiation and organizaroom
stipe
(Craig
and
Gull
1977,
Mol and Wessels 1990) or
tion into thallus layers frequently occur in a gradation remzygomycete
sporangiophore
(Burnett
1979). The specialized
iniscent of histogenesis at plant apices. At the thallus apex or
hyphae
of
these
nonlichen
fungi
have
been shown experimargin, fungal and algal cells are interspersed in an undifferentiated mixture (Figure 21a). With distance from the tip,
mentally to incorporate structural components into a cell
the two symbionts become stratified into distinct thallus laywall extending along its entire length, allowing the wall to
ers, the rate of algal cell division declines (Greenhalgh and Anmaintain its integrity while elongating diffusely. Unfortuglesea 1979), and the fungal cells of the cortex acquire their
nately, similar experiments cannot be readily performed
final shape and typically thickened walls. Differentiation of the
with lichen thalli.
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Figure 17. Open development by repetition of a determinate module. (a) The lichen Cladonia penicillata (Vain.) Ahti and
Marcelli. The verticillate thallus is formed of lobed, chalice-shaped modules that proliferate mainly from the center (for
contrasting developmental interpretations, cf. Goebel 1928, pp. 71–73, and Hammer 1996). (b) The cactus Opuntia
palmadora; the plant body is formed of flattened, succulent, determinate stem segments that proliferate along their upper
edge.
Figure 18. Initiation of dichotomous branching. (a) Apex of lichen Pseudephebe sp. (whole-mounted in water). Scale bar =
40 µm. (b) Apex of Lycopodium sp., a vascular plant (stained and sectioned). Scale bar = 250 µm.
Figure 19. Apex of lichen Teloschiste flavicans (Swartz) Norman showing cilium (C) produced at point of dichotomy of
apical branches. The inrolled branches (arrows) continue to grow and rebranch with successive production of cilia (Sanders
1993). Scale bar = 50 µm.
Figure 20. Development of the lichen Ramalina menziesii Tayl. in the field; four stages of development of the same thallus
net shown at the same scale. Letter “a” identifies the same perforation in all four stages. Note development of new perforated
tissue and lobations at the apical margin.
Nonetheless, ultrastructural examination of thallus tissue
in R. menziesii suggests that the cells behave very differently
from the diffusely growing hyphae studied in mushroom
stipes or sporangiophores. Unlike those hyphae, a fungal
cell in the structural tissue of R. menziesii does not possess
a precisely delimited cell wall that maintains its integrity
throughout thallus expansion. Instead, new wall layers are
continually produced to the cell interior as older layers are
disrupted by the continued diffuse growth of the thallus
(Figure 23). Remnants of the older wall layers accumulate in
massive quantities between neighboring cells, forming a
dense intercellular matrix. New branch cells grow through this
wall material and produce their own series of wall layers
within it (Figure 23), profoundly altering the usual adjaDecember 2001 / Vol. 51 No. 12 • BioScience 1031
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Figure 21. (a) Longitudinal section through the apex of
Ramalina menziesii. The dividing spheroidal algal cells
and interpenetrating fungal cells are present as an
undifferentiated mixture at the apical margin; the algal
cells become stratified into a distinct central layer with
distance from the margin. The accelerated differentiation and expansion of the cortex (arrows) on one surface
relative to the other produces the inrolling of the margin.
(b) Leaf tip of Sadleria cyatheoides Kaulf., a leptosporangiate fern. Precocious expansion of cells on the abaxial
surface of the leaf apex produces the characteristic
inrolling of the tip that may serve to protect its delicate
growing tissues.
cent wall boundary relationship between neighboring cells
(Sanders and Ascaso 1995). Cell behavior in this type of tissue is neither like that of nonlichen fungi nor like that of conventional plants. It is an example of the significant structural
and functional transformations that a fungus can undergo
in forming a lichen thallus.
From mycelium to integrated tissue:
Ontogeny of the lichen thallus
The plant-like features of lichens become all the more remarkable when one considers that the ontogeny of the lichen
is profoundly different from that of conventional plants. A
spore produced by the lichen fungus germinates to produce
hyphae that will have to contact and capture a compatible alga
Figure 22. Detail of a longitudinal section through tissue
of the reticulate thallus of Ramalina menziesii. Within the
dense cortical tissue, lumina of fungal cells embedded in
an intercellular matrix run lengthwise, interweave, and
anastomose (fuse). Scale bar = 40 µm.
Figure 23. Ramalina menziesii. Transmission electron
micrograph of fungal tissue in transverse section. Note
concentric electron-dense and electron-transparent cell
wall layers and their remnants, which accumulate as an
extensive matrix between cell lumina. New branch cells
(arrows) penetrate through the matrix of old wall layers,
producing new wall layers of their own. Scale bar = 5 µm.
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(Figure 24). Alternatively, the fungus and alga can be dispersed
together, in thallus fragments or in various types of specialized vegetative propagules (Figure 25). In either case, the
fungus grows out hyphally, and the alga, unicellular or filamentous, grows and divides initially without much apparent
coordination with the fungal hyphae. The algal cells are encircled and are gradually enveloped by the fungus, which, radiating out over the substrate, can also encompass other
compatible algae as well as fuse with other protothalli forming from similar propagules (Figure 26; Schuster et al. 1985).
The initially independent cellular growth eventually becomes integrated, giving rise to a thallus with emergent properties of form and development that bear little resemblance
to those exhibited by its components previously. A key process
in this transition appears to be the secretion of abundant
cell wall substances that bind the fungal cells together in a common cortical matrix (Ahmadjian and Jacobs 1983, Jahns
1988). Usually, this material is of fungal origin (Figures 22 and
23), but in the so-called gelatinous lichens, whose thalli are
composed mainly of blue-green algal cells, the thick intercellular matrix consists of copious algal sheath material (Figure 27). The formation of secondary cytoplasmic connections
(anastomoses) between laterally adjacent fungal cells is also
of fundamental importance in integrating the fungal cells into
tissues (Poelt 1986). These integrative processes facilitate a
transfer of growth properties from formerly independent
cellular elements to the newly constructed surfaces and volumes of the thallus.
Relationship of cells to the plant body
The lichen thallus is constructed of cellular elements of initially independent growth that are secondarily integrated
into a coherent, unified body. This kind of ontogeny exemplifies the principles that the cell theory promoted by Schleiden (1838) and Schwann (1839) attributed to multicellular
plants and animals. According to this theory, cells are primary
elemental organisms that build up the multicellular organism
by surrendering their individuality and autonomy to form an
integrated federation (Schleiden 1838). The basis of nutrition
and growth is attributed to the individual cellular elements
rather than to the organism as a whole (Schwann 1839).
Although the cell theory has been extremely influential,
most plants are actually much better described by the opposing organismal theory (Kaplan and Hagemann 1991). The
organismal view emphasizes that plant cellularity is a secondary phenomenon, arising from a compartmentalization
process that subdivides an organism that is integral from inception. Growth and morphogenesis are manifestations of the
organism, not its cellular compartments. Autonomous cell
properties and cell specializations are features that are acquired only at a later stage of tissue development in plants
(Kaplan 1992). By contrast, the lichen fits the tenets of the
cell theory quite well: The thallus is unquestionably composed
of distinct elemental organisms. Individual fungal hyphae and
algal cells exhibit autonomy at the earliest stages of lichen
ontogeny.
Figure 24. Germination of a fungal spore (S). Numerous
germination hyphae are growing out radially and
associating with algae encountered on the substrate
(arrows). Scale bar = 50 µm.
Figure 25. Germination of soredia, lichenized propagules
containing both fungal and algal symbionts. The fungal
hyphae grow out over the substrate surface, and the algal
cells divide. Scale bar = 20 µm.
Figure 26. Contact and merging of neighboring lichen
protothalli during early ontogeny. Scale bar = 50 µm.
December 2001 / Vol. 51 No. 12 • BioScience 1033
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Thus, lichens and conventional plants differ profoundly
in their ontogenetic relationship of cell to body (Figure 28).
Yet their morphological convergences are so striking that
one cannot help but conclude that the form of the plant
body really has no necessary relationship to the manner in
which it is composed of—or subdivided into—cells. Rather,
it appears that cell shape and patterns of cell division are
determined by mechanical and biophysical constraints
that have little relationship to the overall form of the vegetative structure (Cooke and Lu 1992). The lichen thallus
provides convincing evidence that plant form is a property
that resides not in cells, but rather in body surfaces and volumes, regardless of whether these surfaces and volumes are
present from inception or secondarily assembled in the
course of development. The lichen thallus extends the
province of plant morphology from the organismal to the
superorganismal level.
Just as the phylogeny of lichen fungi cannot be understood without mycology, their form and function cannot be
appreciated without botany. They have the genes of a fungus, but they have adopted the lifestyle of a plant. Of course,
with phylogenetic reconstruction being the overwhelming concern of so many organismal biologists nowadays,
some may find it unacceptable to refer to lichens as “plants”
(Honegger 1993) in the broad, nonphylogenetic sense of
this ancient word. But it is not merely out of respect for
Figure 28. Relationship of cell to body in conventional plants
versus lichens. (a) Shoot apex of the flowering plant Coleus,
longitudinal section. Cells arise by the continued partitioning or
subdividing of the organism during growth (see Kaplan and
Hagemann 1991). Scale bar = 100 µm. (b) Branching isidium
(thallus surface appendage) of the lichen Sticta fuliginosa
(Hoffm.) Ach. Component cells of two different organisms, fungus
(vertical arrows) and alga (horizontal arrows), originate from
separate filaments that coalesce and organize secondarily to
produce a thallus that functions as an integrated plant. Scale
bar = 25 µm
tradition that contemporary botany texts still treat a hopelessly
polyphyletic array of “plants,” including the seaweeds and
the lichens. There is good biological justification—
structural, functional, and ecological—for considering all
these organisms together. Highlighting these convergences
need not and should not mean neglect of phylogenetically relevant characteristics and their central significance in biosystematics. The two perspectives are fully complementary and
are equally necessary for a complete understanding of the
courses that evolutions follow in generating biodiversity.
Figure 27. Section through a lobe of a foliose gelatinous
lichen. The bulk of the thallus consists of filamentous
chains of the blue-green alga Nostoc (vertical arrow),
whose thick sheaths compose the structural matrix of the
thallus. Scattered hyphae (horizontal arrow) of the
lichen fungus (Collema sp.) penetrate through this
material. Note the lack of organization into layers
(compare with Figures 2 and 11). The gelatinous lichens
are exceptional in that the algal symbiont is the
predominant, structural component of the thallus.
Despite these fundamental differences in anatomical
construction, the gelatinous lichens do not markedly
differ morphologically from many lichens with a
stratified, fungus-dominated construction. Scale bar =
60 µm.
Acknowledgments
I thank the Federal University of Pernambuco, Recife, for
the opportunity to serve as visiting professor at that institution from October 1998 to October 2000, during which time
this article was written and presented in various forms. I am
indebted to Dr. Isabelle I. Tavares for her counsel and generosity. The manuscript benefited from critical reading by
Isabelle I. Tavares, Donald R. Kaplan, Richard L. Moe, William
Stein, and two anonymous reviewers. Facilities at the Scientific Visualization Center (University of California, Berkeley)
were utilized in composition of the figures. T. Ahti, I. Tavares,
and E. Timdall provided determinations of some of the lichen
material illustrated.
1034 BioScience • December 2001 / Vol. 51 No. 12
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Articles
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