Lichens: the Interface Between Mycology and Plant Morphology Author(S): WILLIAM B

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 Stable URL: http://www.jstor.org/stable/10.1641/0006- 3568%282001%29051%5B1025%3ALTIBMA%5D2.0.CO%3B2 . Accessed: 22/05/2013 17:34

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This content downloaded from 143.107.247.159 on Wed, 22 May 2013 17:34:00 PM All use subject to JSTOR Terms and Conditions Articles Lichens: The Interface between Mycology and Plant Morphology

WILLIAM B. SANDERS

here do the lichens belong in the biological Wsciences? They are composed of fungus and alga, but WHEREAS MOST OTHER FUNGI LIVE AS AN neither mycologists nor phycologists have been eager to claim them. In most lichens, it is the fungus that builds the struc- ABSORPTIVE MYCELIUM INSIDE THEIR tural tissues of the thallus (body), as well as the characteris- FOOD SUBSTRATE, THE LICHEN FUNGI tic fungal fruiting structures. Its predominance is such that we often speak loosely of a “species of lichen,” when we mean CONSTRUCT A PLANT-LIKE BODY WITHIN more precisely a species of lichen fungus; the lichen algae, of course, have their own separate scientific names. WHICH PHOTOSYNTHETIC ALGAL SYM- The lichen-forming fungi represent nearly one-fifth of all known species of fungi (Hawksworth et al. 1995), yet they are BIONTS ARE CULTIVATED 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 Lichens must first be appreciated in the context of other botany secure. Although lichens, as photosynthetic living fungi. As absorber heterotrophs, the primeval fungi evolved things, fit within the broad biological concept of “plant,”this a simple and enormously successful growth form: the term has been increasingly co-opted for use in a narrower, phy- mycelium. This loosely organized network of branching, fil- logenetic context that excludes all but green algae and their amentous cells (hyphae) is ideally suited to an organism that embryophyte (“land plant”) descendants. The lichens do re- lives inside its food source. The hypha’s exclusively linear ceive brief consideration as a classic example of symbiosis. But growth generates a vast absorptive surface area with very in treating them solely as a community-level ecological phe- modest increases in cell volume. nomenon, we overlook their organismal-level features and Only at the reproductive phase, when spores must be pro- their significance in mycology and botany. duced in quantity and borne away to fresh substrate, do cer- For the fungi, symbiosis with microalgae represents an tain fungi organize tissues and build complex structures that important nutritional innovation, one that evolved inde- emerge from the substrate, such as mushrooms. Such fruit- pendently in a number of different lineages (Wainio 1890, ing structures have diversified tremendously, as reproduction Gargas et al. 1995). These fungi have distinguished themselves and means of dispersal became specialized for exploitation of by a notable accomplishment: their transformation into very different food sources under diverse ecological conditions. “plants.” This metamorphosis is particularly visible in the But it is almost entirely within these reproductive phases 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 William B. Sanders ([email protected]) is a research as- tissues are usually fungal, thallus form and function are emer- sociate at the University Herbarium, University of California, Berke- gent properties that have no real parallels among nonlichen ley, CA 94720-2465. He has combined his training in mycology and fungi. These properties the lichen thallus shares instead with in developmental plant morphology to focus on studies of lichen struc- plants. Thus, the lichens are not only of great significance in ture and development. He has lived and carried out research in Cal- the evolution of fungi; they can also offer important insights ifornia, Spain, and Brazil. © 2001 American Institute of Biological into fundamental principles of plant morphology. Sciences.

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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 Figure 1. Leafy (foliose) and shrubby (fruticose) lichens Coccocarpia palmicola (Spreng.) L.Arvidss. and D.Gall. of the genera Parmotrema, Ramalina, Teloschistes, and Scale bar = 20 µm. Heterodermia colonizing a tree branch behind dunes on Santa Catarina Island, Brazil. autonomous lichen colonizes inorganic or indigestible sub- that morphological evolution of nonlichen fungi has oc- strates and often occurs in extreme microhabitats with little curred (Poelt 1986). The vegetative mycelium, by contrast, has to offer the hunter–gatherer of ephemeral food resources. been very highly conserved throughout hundreds of mil- Agriculture has profound effects on the crop as well as on lions of years of evolution. It characterizes most of the sapro- the cultivator. Many of our most important crop plants trophic, parasitic, and mycorrhizal Eumycota (true fungi). The have been genetically selected for so long that they no longer mycelium also evolved independently in phylogenetically resemble any “natural” species, nor could they survive as distinct organisms traditionally treated as fungi, such as the such. Maize (corn), for example, is a crop whose exact ori- oomycetes. These are impressive indications of the mycelium’s gin is controversial, and one that cannot effectively perpet- ideal suitability to the “endotrophic” absorber lifestyle. uate itself outside human cultivation (Mangelsdorf 1974). But when a fungus establishes a symbiosis with a mi- Some lichen algae may be in a comparable situation. Species croalga, the usual spatial relationship of fungus to food source of the unicellular green alga Trebouxia (Figure 3) are the most is turned inside out. Surrounding the diminutive photosyn- common algal symbionts in lichens of temperate and boreal thetic cells, the fungus now finds itself on the outside (Figure climates. Yet Trebouxia’s immediate affinities among non- 2). To maintain and display the incorporated algae effec- lichen algae are unclear, and the genus has been only spo- tively, the fungus must build a protective, functional green- radically reported to occur outside lichen thalli (Tscher- house, usually emergent from the substratum. The hyphal mak-Woess 1978, Bubrick et al. 1984). It has been asserted building block is metamorphosed to produce a variety of that reportedly free-living Trebouxia cells represent transient tissue types, and a complex thallus replaces the mycelium. populations liberated from damaged or degenerated thalli or thallus fragments (Ahmadjian 1988). Such liberated al- Farmers of the fungal kingdom gal cells might then be likened to volunteer plants that es- Symbiosis with microalgae engenders a whole new fungal cape from cultivation. Whatever their origin or degree of sta- lifestyle: It represents nothing less than the advent of agri- bility, free-living Trebouxia populations can play an culture (see also Goward et al. 1994, p. 10). While their non- important role in lichen establishment. They can offer po- symbiotic brethren continue as hunter–gatherers of tran- tential symbionts available to compatible lichen fungi ger- sient carbon sources, the lichen fungi have become indoor minating from spores in the vicinity (Beck et al. 1998). gardeners, cultivating and perpetuating their internalized But not all lichen algae have been so thoroughly domesti- source of food. This agrarian control over food resources cated by the lichen fungus. Examples include algae of the confers both stability and the potential to occupy entirely new closely related genera Trentepohlia, Phycopeltis, and Cephaleu- ecological niches. In human development, agriculture per- ros, which are very important lichen symbionts in tropical and mitted the rise of populous, sedentary, highly complex civi- warm-temperate regions. These algae commonly occur free- lizations by providing a resource base far larger and more re- living as well as lichenized, not infrequently within the same liable than that available from the unmanipulated habitat. On a single leaf (an important substratum for trop- environment (Schwanitz 1966, Heiser 1990). For the fungi,“al- ical lichens), one can sometimes find Cephaleuros both free- gaculture” has led to the development of structurally elabo- living and in various stages of incorporation into a thallus of rate, self-sufficient, long-lived thalli. The nutritionally 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 which the alga could otherwise survive and reproduce with- may not form reproductive structures. Indeed, lichenization out supporting a fungus. can reduce or eliminate the pathogenic effects of this alga’s vig- These ecological considerations, beyond the nutritional in- orous growth on cultivated plants (Joubert and Rijkenberg teraction of the symbionts, can determine whether one 1971). Thus, lichenization can have different ecological im- chooses to view the lichen symbiosis as mutualistic (Honeg- plications for different algal symbionts. For some algae, like ger 2001) or parasitic (Ahmadjian 1993). For a highly Trebouxia, the symbiosis can be essentially obligatory for coevolved and dependent lichen alga such as Trebouxia,rec- survival in many habitats. For others, such as Cephaleuros, lich- ognizing advantage or disadvantage in the symbiosis might enization might be a nuisance, at least under conditions in 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 dis- playing photosynthetic surfaces, us- ing 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 re- approximately twice actual size. veals further plant-like features. A Figure 9. Shrub-like thallus of fruticose lichen Cladonia subreticulata Ahti, shown transverse section through the thal- about actual size. lus of a typical foliose lichen shows 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 (Fig- commercially 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 be- constructed 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, chloroplast- rich palisade parenchyma tissue. Ef- “benefited” from its agricultural association with humans. ficient gas exchange in this photosynthetically active stra- However, there is little justification for viewing lichenization tum is facilitated by the air spaces in the loosely organized as disadvantageous to Trebouxia (cf. Ahmadjian 1993, pp. medullary region below, as occurs in the spongy mesophyll 3–4) if one maintains that this alga cannot really exist free- of the plant leaf. A thin coating of hydrophobic protein and living (Ahmadjian 1988). insoluble secondary substances over the medullary hyphae and associated algal cells can serve to maintain these spaces free Lichens as “plants” of water, as well as to seal a conduit between fungus and alga The fungus must provide its algal symbiont with an envi- (Honegger 1997). ronment that makes effective use of physiologically favorable Like an epidermis, the upper cortex of the lichen protects conditions. It must display the photosynthetic cells advanta- the photosynthetic cells below, slowing evaporation and fil- geously to the light while filtering excessive or harmful radi- tering harmful or excessive radiation with the assistance of pig- ation. It must facilitate adequate hydration while permitting ments and secondary substances (Rikkinen 1995). Unlike carbon dioxide to diffuse into the thallus during photosyn- the cutinized plant epidermis, however, the lichen cortex pre- thetically active periods. In short, the lichen faces the same ba- sents no impermeable barrier to water diffusion. On the con- sic functional challenges as do terrestrial plants. trary, the corticated thallus surfaces must serve in absorption The structural solutions, in turn, are remarkably similar of water as well as light, as do the leaves of mosses and at- (Jahns and Ott 1997). Many lichens produce a simple crus- mospheric vascular epiphytes (Figure 12). tose thallus intimately attached to the substratum, as do cer- In certain lichens occurring in habitats that receive high lev- tain species of red and brown marine algae (Figure 5). Oth- els of light, the lichen cortex can form a thick optical filter ers have foliose, dorsiventral forms, with a discrete lower through which light diffuses downward and laterally to ver- surface attached to the substratum at specific points, remi- tically arranged tiers of photosynthetic cells (Figure 13), as in

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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 ac- tivity to brief periods (such as early mornings); in the dessi- cated 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. How- Figure 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 re- P, 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 cal- brownish secondary substances. Scale bar = 250 µm. careous and siliceous rock substrates (Figure 15) as well as soil, the so-called window leaves of South African succulent plants apparently by both mechanical and chemical means (Sanders such as Lithops (Vogel 1955, Malcolm 1995). This system et al. 1994). Their development is often much more extensive permits the display of considerable photosynthetic tissue to than would be expected of a structure that merely fixes the the light while greatly reducing the external surfaces exposed thallus to the substrate. to evaporative water loss. When the lichen cortex is satu- Rhizomorphic excavation may increase the substrate’s ca- rated with water, diffusion of carbon dioxide through the thal- pacity to store capillary water available to the thallus. How- lus to the algal layer is impeded (Lange and Tenhunen 1981). ever, the rhizomorphs themselves do not show distinctive Thus, most of the larger lichens have some type of cortical per- specializations for transport (Sanders and Ascaso 1997), such foration, such as cyphellae, pseudocyphellae (Figure 11), or as the vessel hyphae observed in rhizomorphs of certain non- epicortical micropores (Hale 1981). lichen fungi (Duddridge et al. 1980). Where rhizomorphs 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 per- forate tissue and apical branches are formed exclu- Figure 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 dif- Figure 15. Rhizomorphic hyphae of Acarospora scotica Hue (arrow) fuse growth (Hestmark 1997). Diffuse growth proba- within 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 un- and stained surface of the cleaved substrate is imaged with SEM in studied. backscattered electron mode (Sanders et al. 1994). Scale bar = 8 µm. The presence of diffuse growth in at least some lichens raises fundamental questions about the mech- Figure 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 within the substrate. Scale bar = 50 µm. nonlichen fungi or even those of conventional plants? Because thallus structural tissue is fungal in most thallus growth is polar, occurring at localized, usually pe- lichens, it might be expected that the component fungal cells ripheral, zones of growth. As in conventional plants, growth are behaving essentially as hyphae. However, growth of the veg- is potentially indeterminate and development open. Open de- etative fungal hypha occurs exclusively at the tip. In this zone, velopment allows the continued production of new lobes, the wall exhibits plasticity, and new cell wall components are branches, or other units of construction in a modular fash- added to the existing structure during growth (Wessels 1986). ion (Figure 17). Generation of form (morphogenesis) and ini- Exclusively apical growth of component fungal cells can- tiation of certain thallus structures (organogenesis) are often not account for diffuse growth of the lichen thallus. The me- localized at apices or margins that function analogously to the chanical tissue of R. menziesii, for example, is constructed apical meristems of plants. Examples include the initiation of of elongate fungal cells forming an anastomosing network apical branching (Figure 18), the formation of appendages embedded in thick deposits of cell wall material (Figure such as apical cilia (Figure 19), and the generation of the 22). With extensive diffuse growth of the thallus, these fun- perforated tissue that gives rise to the reticulate thallus of Ra- gal cells must somehow maintain plasticity along their malina menziesii, the lace lichen (Figure 20). length. Such diffuse plasticity is indeed known in certain spe- At the anatomical level, cell differentiation and organiza- cialized cells of nonlichen fungi, such as those of the mush- tion into thallus layers frequently occur in a gradation rem- room stipe (Craig and Gull 1977, Mol and Wessels 1990) or iniscent of histogenesis at plant apices. At the thallus apex or zygomycete sporangiophore (Burnett 1979). The specialized margin, fungal and algal cells are interspersed in an undif- hyphae of these nonlichen fungi have been shown experi- ferentiated mixture (Figure 21a). With distance from the tip, mentally to incorporate structural components into a cell the two symbionts become stratified into distinct thallus lay- wall extending along its entire length, allowing the wall to ers, the rate of algal cell division declines (Greenhalgh and An- maintain its integrity while elongating diffusely. Unfortu- glesea 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 continually produced to the cell interior as older layers are in R. menziesii suggests that the cells behave very differently disrupted by the continued diffuse growth of the thallus from the diffusely growing hyphae studied in mushroom (Figure 23). Remnants of the older wall layers accumulate in stipes or sporangiophores. Unlike those hyphae, a fungal massive quantities between neighboring cells, forming a cell in the structural tissue of R. menziesii does not possess dense intercellular matrix. New branch cells grow through this a precisely delimited cell wall that maintains its integrity wall material and produce their own series of wall layers throughout thallus expansion. Instead, new wall layers are within it (Figure 23), profoundly altering the usual adja-

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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 leptospor- angiate 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 tis- Figure 22. Detail of a longitudinal section through tissue sue is neither like that of nonlichen fungi nor like that of con- of the reticulate thallus of Ramalina menziesii. Within the ventional plants. It is an example of the significant structural dense cortical tissue, lumina of fungal cells embedded in and functional transformations that a fungus can undergo an intercellular matrix run lengthwise, interweave, and in forming a lichen thallus. anastomose (fuse). Scale bar = 40 µm. From mycelium to integrated tissue: Figure 23. Ramalina menziesii. Transmission electron Ontogeny of the lichen thallus micrograph of fungal tissue in transverse section. Note The plant-like features of lichens become all the more re- concentric electron-dense and electron-transparent cell markable when one considers that the ontogeny of the lichen wall layers and their remnants, which accumulate as an is profoundly different from that of conventional plants. A extensive matrix between cell lumina. New branch cells spore produced by the lichen fungus germinates to produce (arrows) penetrate through the matrix of old wall layers, µ hyphae that will have to contact and capture a compatible alga producing new wall layers of their own. Scale bar = 5 m.

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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 en- circled and are gradually enveloped by the fungus, which, ra- diating 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 be- comes 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 (Fig- ure 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 exem- plifies the principles that the cell theory promoted by Schlei- den (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 op- Figure 24. Germination of a fungal spore (S). Numerous posing organismal theory (Kaplan and Hagemann 1991). The organismal view emphasizes that plant cellularity is a sec- germination hyphae are growing out radially and ondary phenomenon, arising from a compartmentalization associating with algae encountered on the substrate process that subdivides an organism that is integral from in- (arrows). Scale bar = 50 µm. ception. Growth and morphogenesis are manifestations of the organism, not its cellular compartments. Autonomous cell Figure 25. Germination of soredia, lichenized propagules properties and cell specializations are features that are ac- containing both fungal and algal symbionts. The fungal quired only at a later stage of tissue development in plants hyphae grow out over the substrate surface, and the algal (Kaplan 1992). By contrast, the lichen fits the tenets of the µ cell theory quite well: The thallus is unquestionably composed cells divide. Scale bar = 20 m. of distinct elemental organisms. Individual fungal hyphae and Figure 26. Contact and merging of neighboring lichen algal cells exhibit autonomy at the earliest stages of lichen µ ontogeny. protothalli during early ontogeny. Scale bar = 50 m.

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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 under- Figure 28. Relationship of cell to body in conventional plants stood without mycology, their form and function cannot be versus lichens. (a) Shoot apex of the flowering plant Coleus, appreciated without botany. They have the genes of a fun- longitudinal section. Cells arise by the continued partitioning or gus, but they have adopted the lifestyle of a plant. Of course, subdividing of the organism during growth (see Kaplan and with phylogenetic reconstruction being the overwhelm- Hagemann 1991). Scale bar = 100 µm. (b) Branching isidium ing concern of so many organismal biologists nowadays, (thallus surface appendage) of the lichen Sticta fuliginosa some may find it unacceptable to refer to lichens as “plants” (Honegger 1993) in the broad, nonphylogenetic sense of (Hoffm.) Ach. Component cells of two different organisms, fungus this ancient word. But it is not merely out of respect for (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 rel- evant characteristics and their central significance in biosys- tematics. 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 Acknowledgments chains of the blue-green alga Nostoc (vertical arrow), I thank the Federal University of Pernambuco, Recife, for whose thick sheaths compose the structural matrix of the the opportunity to serve as visiting professor at that institu- thallus. Scattered hyphae (horizontal arrow) of the tion from October 1998 to October 2000, during which time lichen fungus (Collema sp.) penetrate through this this article was written and presented in various forms. I am material. Note the lack of organization into layers indebted to Dr. Isabelle I. Tavares for her counsel and gen- (compare with Figures 2 and 11). The gelatinous lichens erosity. The manuscript benefited from critical reading by are exceptional in that the algal symbiont is the Isabelle I. Tavares, Donald R. Kaplan, Richard L. Moe, William predominant, structural component of the thallus. Stein, and two anonymous reviewers. Facilities at the Scien- Despite these fundamental differences in anatomical tific Visualization Center (University of California, Berkeley) construction, the gelatinous lichens do not markedly were utilized in composition of the figures. T.Ahti, I. Tavares, differ morphologically from many lichens with a and E. Timdall provided determinations of some of the lichen stratified, fungus-dominated construction. Scale bar = material illustrated. 60 µm.

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